UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO 
POSGRADO EN CIENCIAS BIOLÓGICAS 
INSTITUTO DE BIOLOGÍA  
BIOLOGÍA EVOLUTIVA Y SISTEMÁTICA 
 
 
PATRONES BIOGEOGRÁFICOS Y COFILOGENÉTICOS DE MARGOTREMA SPP. (DIGENEA: 
ALLOCREADIIDAE), PARÁSITOS DE PECES DULCEACUÍCOLAS DE LA SUBFAMILIA 
GOODEINAE (CYPRINODONTIFORMES: GOODEIDAE) EN EL CENTRO DE MÉXICO 
  
 
TESIS 
QUE PARA OPTAR POR EL GRADO DE: 
DOCTOR EN CIENCIAS 
 
 
PRESENTA: 
ANDRÉS MARTÍNEZ AQUINO 
 
TUTOR PRINCIPAL: DR. GERARDO PÉREZ PONCE DE LEÓN (INSTITUTO DE BIOLOGÍA)  
 
COMITÉ TUTOR: DR. LUIS ENRIQUE EGUIARTE FRUNS (INSTITUTO DE ECOLOGÍA) 
                               DRA. ELLA GLORIA VÁZQUEZ DOMÍNGUEZ (INSTITUTO DE ECOLOGÍA) 
 
MÉXICO, D.F.                                                                        JUNIO, 2013. 
 
UNAM – Dirección General de Bibliotecas 
Tesis Digitales 
Restricciones de uso 
  
DERECHOS RESERVADOS © 
PROHIBIDA SU REPRODUCCIÓN TOTAL O PARCIAL 
  
Todo el material contenido en esta tesis esta protegido por la Ley Federal 
del Derecho de Autor (LFDA) de los Estados Unidos Mexicanos (México). 
El uso de imágenes, fragmentos de videos, y demás material que sea 
objeto de protección de los derechos de autor, será exclusivamente para 
fines educativos e informativos y deberá citar la fuente donde la obtuvo 
mencionando el autor o autores. Cualquier uso distinto como el lucro, 
reproducción, edición o modificación, será perseguido y sancionado por el 
respectivo titular de los Derechos de Autor. 
 
  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO 
POSGRADO EN CIENCIAS BIOLÓGICAS 
INSTITUTO DE BIOLOGÍA  
BIOLOGÍA EVOLUTIVA Y SISTEMÁTICA 
 
 
PATRONES BIOGEOGRÁFICOS Y COFILOGENÉTICOS DE MARGOTREMA SPP. (DIGENEA: 
ALLOCREADIIDAE), PARÁSITOS DE PECES DULCEACUÍCOLAS DE LA SUBFAMILIA GOODEINAE 
(CYPRINODONTIFORMES: GOODEIDAE) EN EL CENTRO DE MÉXICO 
  
 
TESIS 
QUE PARA OPTAR POR EL GRADO DE: 
DOCTOR EN CIENCIAS 
 
 
PRESENTA: 
ANDRÉS MARTÍNEZ AQUINO 
TUTOR PRINCIPAL: DR. GERARDO PÉREZ PONCE DE LEÓN (INSTITUTO DE BIOLOGÍA)  
 
COMITÉ TUTOR: DR. LUIS ENRIQUE EGUIARTE FRUNS (INSTITUTO DE ECOLOGÍA) 
                               DRA. ELLA GLORIA VÁZQUEZ DOMÍNGUEZ (INSTITUTO DE ECOLOGÍA) 
 
 
MÉXICO, D.F.                                                                        JUNIO, 2013. 
 
 
 
UN M 
POSG} DO 
Ci,"oi .. 1;0161;<0' 
• 
Dr_I. .... _ 
_ _ • __ bcGIor . U~"" 
"f ...... 
COORDINACiÓN 
"-_ ........... __ .... _...- ... CarnoIOM ,_ ... .....,_ 
..,c-..-... .. _, ,,ulJ,,",...,..oo ;¡O¡ IJ . .. _ .. _ ........ 
.... .. • , ""'"" <lo .,_ "" DOCTDI! OH C."" ....................... ~ __ O 
""" -. <lO -.. •• ,. ... , "'" lo _ ........ "'''''0'''' """",,,,,,,,",oco. y 
COI'L<XKNnICOa,. ....... __ , .......... .o.uOC" · _'f ~ ~_OI OI! " CU 
DULCl.OCtlIccIu.I DI: u. .......... _Od·· ¡c •• % "'T~, . __ , IN 
ti. _110 01111_. _ _ lO _ ... DI!. 0E1tAROO PEREZ I'OOOC( DI! -
• ----
0I'l CW<oI L -.coa l'\Ii(IIO 001.-. 
DI! .--JOIE~""'" 
".,. EU.o 01.0Il100. v.lZOllU ~ 
DI! OOOEUO """-"<NI _ 
"" oowo DOIoIlNOUEZ ooonlr'O"n 
80> .... _ . ... ___ "" __ 
A'l NI •• Ulft 
_""" .. ll,O,U, -.. lL [..ru" 
co "' .... _ .. D F . .... _ .. l."J 
DIlO. .... RIA O ... COItO ... "ltIItNt> ......... G ... 
COOfUIINAOORA OI!L ""<XI .... . 
~ ... '->do ·c_,jd .......... C"_' "~s [oI;_8., ... _c..- ... ,....· CIlU ... _ 
()oIop< ... c..,....c. 001,' 101",,_0 r ,el ~l1Q01'" pdIooI¡ • __ .. , 
• 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
AGRADECIMIENTOS INSTITUCIONALES 
 
> Al Posgrado en Ciencias Biológicas (PCB) de la Universidad Nacional Autónoma de México 
(UNAM) por el apoyo logístico brindado para la realización de este proyecto. 
 
> Al Consejo Nacional de Ciencia y Tecnología (CONACyT) por la beca otorgada (202632) para 
realizar estudios de Doctorado (Febrero 2009-2013). 
 
> A los Proyectos de Investigación a cargo del Dr. Gerardo Pérez Ponce de León que financiaron mi 
estudio doctoral: a) CONACyT 83043 (enero 2009-diciembre 2011) “Diversidad y riqueza de 
helmintos parásitos de peces dulceacuícolas mexicanos: un enfoque sistemático y biogeográfico desde 
las moléculas hasta los ecosistemas; b) PAPIIT IN202111 (enero 2009-diciembre 2011) “Evolución y 
biogeografía histórica de helmintos parásitos de peces dulceacuícolas de la Zona de Transición 
Mexicana”. 
 
> Al Programa de Apoyo de Estudios de Posgrado (PAEP) de la UNAM por las siguientes becas 
otorgadas: 
- Beca PAEP-2012, para Estancia Internacional; Universitat de Barcelona, Barcelona, España. 
Marzo-Julio, 2012. 
- Beca PAEP-2011, para Congreso Internacional; XIII International Symposium of Fish 
Parasites, Viña del Mar, Chile. Septiembre, 2011. 
- Beca PAEP-2010, para Estancia Nacional; Instituto de Ecología, A.C., Xalapa, Veracruz, 
México. Septiembre, 2010.  
 
> A la Swiss Systematics Society (SSS) por la Beca de condenación de pago de inscripción para el 
curso de especialización “Model-based methods in biogeography”, y por la Beca de condenación de 
pago de inscripción para la participación dentro del “5. Scientific meeting of the Swiss Systematics 
Society”, Porrentruy, Suiza. Noviembre, 2012. 
 
> A la Universitat de Barcelona por la Beca de condenación de pago de inscripción para curso de 
especialización; Filogenias y Genealogías de DNA: Reconstrucción y Aplicaciones, celebrado en la 
Universitat de Barcelona, Barcelona, España. Julio, 2012. 
 
> Al CONACyT por la beca otorgada de Recursos Humanos de Alto Nivel de CONACyT (CONACyT-
MIXTA), para Estancia Internacional; Universitat de Barcelona, Barcelona, España. Marzo-Julio, 2012.  
 
> Al PCB por la beca otorgada de Condenación de pago de inscripción para curso de especialización; 
WHS Twelfth International Workshop in Phylogenetics Methods, celebrado en el Instituto de Ecología 
A.C., Xalapa, México. Mayo 2011. 
 
> Al Dr. Gerardo Pérez Ponce de León por fungir como mi tutor principal de tesis doctoral. 
 
> A la Dra. Ella Gloria Vázquez y al Dr. Luis Enrique Eguiarte Fruns por fungir como mi Comité 
Tutorial del proyecto doctoral. 
 
 
 
 
AGRADECIMIENTOS PERSONALES 
 
> Al Dr. Gerardo Pérez Ponce de León por dirigir de manera directa mi proyecto doctoral. 
 
> A la Dra. Ella Vázquez por evaluar el desarrollo de mi proyecto doctoral, mi examen de candidatura 
de grado a doctor, así como de mi desempeño dentro de su curso de Filogeografía, impartido dentro del 
Programa del PCB. 
 
> Al Dr. Luis E. Eguiarte por evaluar el desarrollo de mi proyecto doctoral y mi desempeño dentro de 
su curso de Evolución Molecular, impartido dentro del Programa del PCB. 
 
> Al Dr. Daniel Piñero por evaluar mi tesis doctoral, mi examen de candidatura de grado a doctor, así 
como mi desempeño dentro del Taller Latinoamericano de Evolución Molecular (TLEM-2010), 
impartido dentro del Programa del PCB. 
 
> Al Dr. Juan José Morrone por evaluar mi tesis doctoral y mi examen de candidatura de grado a 
doctor, así como por proporcionarme información biogeográfica y académica de manera incondicional. 
 
> Al Dr. Rogelio Aguilar por evaluar mi tesis doctoral, así como por proporcionarme ayuda de campo y 
colaborar en distintos proyectos de manera incondicional.  
 
> Al Dr. Omar Domínguez por evaluar mi tesis doctoral y mi examen de candidatura de grado a doctor, 
así como proporcionarme información especializada referente a la historia natural de los goodeinos. 
 
> Al la Dra. Sara Ceccarelli por la ayuda incondicional en el laboratorio de biología molecular, análisis 
de datos y para la estancia de investigación en el Instituto de Biogeografía, Basel, Suiza.    
 
> Al Dr. Julio Rozas, por permitirme realizar una estancia de investigación en su laboratorio de 
Genómica Evolutiva; Universitat de Barcelona, Barcelona, España así como por permitirme el libre 
acceso de uso de la supercumpotadora HERCULES. 
 
> Al Dr. Alejandro Sánchez-Gracia, por guiarme en mis estudios de filogenias intraespecíficas durante 
mi estancia en el laboratorio de Genómica Evolutiva. 
 
> Al PhD student Pablo Librado, por guiarme en mis estudios de su softwere DnaSP V5.10.1 durante 
mi estancia en el laboratorio de Genómica Evolutiva y por la ayuda incondicional con Linux para el 
manejo de HERCULES. 
 
> A la Dra. Martha Barluenga, por financiar mi visita al Museo Nacional de Ciencias Naturales de 
Madrid, España. 
 
> Al Dr. Efraín de Luna, por permitirme realizar una estancia de investigación en su laboratorio de 
Morfometría Geométrica y Filogenia, Instituto de Ecología, A.C., Xalapa, Veracruz, México.  
 
> A la Dra. Blanca Hernández por evaluar mi examen de candidatura de grado a doctor. 
 
> A los colegas del laboratorio de Genómica Evolutiva, Barça; Cristina, Pablo, Roser, Juanma y Alex, 
por la excelente camaradería catalana!  
 
> A la Dra. Eva Puerna y a su esposo Tonys, por acogerme en su casa con una ejemplar fraternidad 
catalana ¡Viva el FCB! 
 
> A los colaboradores del laboratorio de Sistemática Molecular III; Sara Ceccarelli, EcoLiliana y Javo 
Alcantár, por los miles de ensayo y error directamente publicados en PhDComics! 
 
> A los colegas de las bastas expediciones de campo; Rodo Pérez, David Pandilla, Javo Alcantá y 
Roger Aguilar. 
 
> A los M. en C. Berenit Mendoza y Luis García por toda su ayuda incondicional durante mi estancia 
en el laboratorio de la Colección Nacional de Helmintos (CNHE), del Instituto de Biología, UNAM. 
 
> A los compañeros del laboratorio de la Colección Nacional de Helmintos (CNHE), a los del Instituto 
de Biología, a los de la Facultad de Ciencias y de otras corporaciones educativas en el mundo; Rodo 
Pérez, Noemí Matías, Javo Alcantár, Aldo Merlo, Tania Merlo, Vladimir de Jesús Bonilla, George 
Kimba, Ana Cecilia, Rogelio Rosas, Lorena Garrido, Lupita Velarde, Ángeles de Charlie, Jorge López, 
Paty Rosas, Nadhieli, Lya Aguilar, Luiza Camargo, Tom, Sean Rovito, Juanjo Martínez, Carlitos 
Pedraza, Paty Ornelas, Isabel Santos, Christoph Liedtke, Simon Loader y Carlitos Mendoza.  
 
> A mis amigos Fernando Camacho, Ulises Muty, Esteban Benítez y Karlita Butterfly Nájera.  
 
> La base para consolidar este trabajo se encuentra en mis padres y mis hermanos.  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
Phylogeny as a cloud of gene histories. 
Phylogeny is more like a statistical distribution  
than a simple tree of discrete thin branches.  
It has a central tendency,  
but it also has a variance because  
of the diversity of gene trees.  
Gene trees that disagree  
with the central tendency are not wrong;  
rather, they are part of the  
diffuse pattern that is the genetic history. 
  
W.P. Maddison. 1997. Gene Tree in Species Tree.  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
ÍNDICE 
 
RESUMEN ……………….…………………………………………………………….………….………………………...………….……………. 1 
ABSTRACT …………………………………………………………………………………………….…………………………...……………….. 3 
INTRODUCCIÓN GENERAL ………………..……………………..……..…………………….…………………………………………….... 5 
 
CAPÍTULO I. REGISTROS DE MARGOTREMA SPP. PARA PECES DULCEACUÍCOLAS DE MÉXICO: 
TAXONOMÍA E INVENTARIOS …………………………………………………………………………….……………….……………… 12 
 
1) HELMINTH PARASITES OF XEONOTAENIA RESOLANAE (OSTEICHTHYES: CYPRINODONTIFORMES: 
GOODEIDAE) FROM THE CUZALAPA HYDROLOGICAL SYSTEM, JALISCO, MEXICO ……....……….. 15 
 
2) HELMINTH FAUNA OF TWO CYPRINID FISH (CAMPOSTOMA ORNATUM AND CODOMA ORNATA) 
FROM THE UPPER PIAXTLA RIVER, NORTHWESTERN MEXICO .….…………………………………….....… 19 
 
3) ENDOHELMINTH PARASITES OF THE FRESHWATER FISH ZOOGONETICUS PURHEPECHUS 
(CYPRINODONTIFORMES: GOODEIDAE) FROM TWO SPRINGS IN THE LOWER LERMA RIVER, 
MEXICO ……………………………………………………………………………………………………………………….……..… 26 
 
4) ENDOHELMINTH PARASITES OF SEVEN GOODEIN SPECIES (CYPRINODONTIFORMES: 
GOODEIDAE) FROM LAKE ZACAPU, MICHOACÁN, CENTRAL MEXICO PLATEAU …………..…...… 33 
 
5) A NEW SPECIES OF MARGOTREMA (DIGENEA, ALLOCREADIIDAE) FROM THE LEOPARD SPLITFIN 
XENOTAENIA RESOLANAE (CYPRINODONTIFORMES, GOODEIDAE) FROM WEST-CENTRAL 
MEXICO ……………………………………………………………………………………………………………………………...… 39 
 
6) COMPOSICIÓN TAXONÓMICA DE HELMINTOS PARÁSITOS DE GOODEINAE (OSTEICHTHYES:  
CYPRINODONTIFORMES: GOODEIDAE) EN MÉXICO ……………………………………………….…………...… 43 
 
CAPÍTULO II. MOLECULAR PHYLOGENY OF THE GENUS MARGOTREMA (DIGENEA: ALLOCREADIIDAE), 
PARASITIC FLATWORMS OF GOODEID FRESHWATER FISHES ACROSS CENTRAL MEXICO: SPECIES 
BOUNDARIES, HOST-SPECIFICITY, AND GEOGRAPHICAL CONGRUENCE …............................................………... 110 
  
 
CAPÍTULO III. DOES THE HISTORICAL BIOGEOGRAPHY AND COPHYLOGENY OF THE DIGENEAN 
MARGOTREMA SPP. ACROSS CENTRAL MEXICO MIRRORS THAT OF THEIR FRESHWATER FISH HOSTS 
(GOODEINAE)? …..………………………………………………………………………………………………………………………….... 152 
 
DISCUSIÓN GENERAL ………………………………………………………….................................................................................... 206 
CONCLUSIONES GENERALES …………………………..…………...………………………………..………………………………... 213 
LITERATURA CITADA …………………………………………………………………………...…………………….……………..…..... 215 
 
APÉNDICE. HELMINTH PARASITES OF FRESHWATER FISHES FROM CUATRO CIÉNEGAS, COAHUILA, IN  
THE CHIHUAHUA DESERT OF MEXICO: INVENTORY AND BIOGEOGRAPHICAL IMPLICATIONS …….… 224
RESUMEN 
El género Margotrema, contiene digéneos parásitos que forman parte de la helmintofauna 
principal (core helminth fauna) de Goodeinae, un grupo monofilético de peces dulceacuícolas 
endémico del centro de México, debido a que comparten patrones de distribución geográfica y los 
digéneos exhiben altos niveles de especificidad. Los procesos de diversificación de Goodeinae 
son el resultado de los cambios hidrogeomorfológicos que modificaron la configuración de la 
superficie del centro de México. Margotrema representa un modelo excelente para realizar 
análisis filogenéticos, biogeográficos y cofilogenéticos en el sentido de dilucidar, en primera 
instancia, la historia evolutiva de las dos especies putativas de Margotrema: M. bravoae y M. 
guillerminae. 
Los objetivos de esta tesis fueron los siguientes: a) Realizar la reconstrucción filogenética 
intraespecífica de las dos especies del género Margotrema: M. bravoae y M. guillerminae. b) 
Establecer la validez taxonómica de las dos especies del género Margotrema (M. bravoae y M. 
guillerminae), a través de análisis filogenéticos, basados en coalescencia, para datos moleculares. 
c) Detectar si la estructura filogenética de Margotrema spp. coincide con el patrón de distribución 
geográfico de las cuatro tribus de Goodeinae. d) Poner a prueba la hipótesis de “La 
diversificación de los goodeinos, resultado de los eventos de vicarianza-dispersión del centro de 
México, influye de igual modo en la evolución de las poblaciones de Margotrema spp.”. Para 
ello, se realizaron análisis biogeográficos para detectar el patrón de distribución de Margotrema 
spp., en función del tiempo y del espacio, y contrastarlo con la estructura filogenética de 
Goodeinae y con la historia geológica del centro de México. 
  Entre agosto de 2008 y julio de 2010 se muestreo en 57 localidades, a lo largo de siete 
sistemas hidrológicos del centro de México. Se obtuvieron secuencias de dos marcadores 
moleculares: mitocondrial (COI; 118 secuencias) y nuclear (ITS1; 98 secuencias). Se realizaron 
análisis filogenéticos con inferencia bayesiana para bases de datos de genes independientes y 
combinados. Los árboles con probabilidad posterior más alta fueron utilizados para análisis de 
delimitación de especies usando modelos de coalescencia (v. gr. General Mixed Yule Coalescent; 
Species Tree by multispecies coalescent). La reconstrucción biogeográfica y los procesos 
cofilogeneticos fueron detectados a través de análisis biogeográficos paramétricos (v.gr. 
Dispersal-Extinction-Cladogenesis). 
 2 
Con base en el numero de linajes detectado a través de la combinación de los análisis 
filogenéticos, usando los marcadores COI (cuatro linajes) e ITS1 (dos linajes), se puede 
evidenciar la distinta tasa de evolución molecular que existe entre ambos marcadores. El Linaje I, 
apoyado por la resolución filogenética de ambos marcadores más caracteres morfológicos 
taxonómicamente delimitados, representa una nueva especie para Margotrema: M. resolanae. Las 
poblaciones restantes de Margotrema pertenecen a M. bravoae, y muestran una estructura 
genealógica que incluye tres linajes con evolución independiente que se refleja en sus patrones de 
distribución geográfica y especificidad. 
  Con base en la integración de los resultados de los análisis biogeográficos y 
cofilogenéticos se detecta que la relación Goodeinae-Margotrema representa tres niveles de 
asociaciones históricas distintas que reflejan que los procesos de divergencia de Margotrema, en 
primera instancia, se deben a eventos vicariantes seguidos de los procesos de diversificación de 
los grupos monófileticos de goodeinos a los que están asociados. Los tres niveles son: a) Especie-
Especie. Representado por la asociación histórica Xenotaenia resolanae-Margotrema resolanae, 
exclusivo del Río Cuzalapa. b) Especie-Linaje (Codivergencia Tipo I). Representado por la 
asociación histórica Characodon audax-Margotrema bravoae Linaje III, exclusivo del Río 
Mezquital Medio-Alto. c) Tribu-Linaje (Codivergencia Tipo II). Representado, a su vez, por dos 
tipos de asociaciones históricas distintas: 1) Ilyodontini-Margotrema bravoae Linaje I, 
distribuido sobre los sistemas hidrológicos de los Ríos Ayuquila y Balsas y 2) Girardinichthyini / 
Chapalichthyini-Margotrema bravoae Linaje II, distribuido sobre el Río Lerma. Por tanto, la 
historia evolutiva de los parásitos Margotrema spp. es congruente con la historia filogenética y 
biogeográfica de sus huéspedes goodeinos.   
 
 
 
 
 
 
 3 
ABSTRACT 
Margotrema is a genus of helminth parasites that form part of the core parasite helmithfauna of 
goodeines, a group of freshwater cyprinodontiform fish endemic to central Mexico. The 
diversification of these fish is the result of complex hydrogeomorphological changes that took 
place in central Mexico. This raises the question of the evolutionary history and biogeography of 
their parasites, in the case of this study, two putative species of Margotrema: M. bravoae and M. 
guillerminae.  
The objectives of the present thesis were: a) To describe the molecular intraspecific 
phylogenetic history of M. bravoae and M. guillerminae. b) To establish species boundaries 
based on novel phylogenetic species delimitation analyses. c) To test the hypothesis that each 
subgroup of goodeines (tribes) possesses their own species of Margotrema as a result of a similar 
history of vicariance and dispersal. d) To use recently published phylogenies of Goodeinae and 
those of their digenena parasite (Margotrema spp.) to uncover biogeographical and 
cophylogenetic patterns and to describe the processes that determined them over 6.5 million years 
ago. The key question addressed in this study is: Was the evolution of Margotrema spp. 
influenced by the complex geographical scenario of central Mexico, through the close association 
with their goodeinae hosts, or both? 
Between August 2008 and July 2010, samplings were made in 57 localities distributed 
along seven hydrological systems of Central Mexico. Sequences of two molecular markers –COI 
and ITS1– were obtained, and a phylogenetic tree per marker was reconstructed by Bayesian 
Inference, subjecting them to species delimitation analyses using the General Mixed Yule 
Coalescent algorithm. Subsequently, a Species Tree analysis was performed. A dispersal-
extinction-cladogenesis model was used to describe the historical biogeography of digeneans and 
their cophylogenetical process with goodein hosts.  
The difference in numbers of lineages obtained from phylogenetic trees using COI and 
ITS1 can be explained by the relative evolutionary rates of these molecular markers (fast and 
slow, respectively). Lineage I, delimited using both markers plus morphological characters, 
represents a new species of Margotrema: M. resolanae. The remaining populations of 
 4 
Margotrema are postulated to belong to one species (M. bravoae), whose populations however 
display a certain degree of geographic restriction and host specificity.  
The biogoegraphical and cophylogenetical results in this study show a response in a geographical 
context followed by host specificity at three distinct levels of historical association: a) Species-
Species; historical association represented by Xenotaenia resolanae-Margotrema resolanae and 
exclusive to the Cuzalapa River. b) Species-Lineage (Codivergence Type I);  historical 
association represented by Characodon audax-Margotrema bravoae Linaje III, exclusive of the 
Mezquital Medium-Hight River Basin. c) Tribe-Lineage (Codivergence Type II); represented, in 
turn, by two different types of historical associations: 1) Ilyodontini-Margotrema bravoae 
Lineage I, distributed on hydrological systems of the Ayuquila River and Balsas River. 2) 
Girardinichthyini / Chapalichthyini-Margotrema bravoae Lineage II, distributed on the Lerma 
River. Therefore, the parasite Margotrema evolutionary history is congruent with the 
phylogenetical and biogeographical history and of their goodein hosts. 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 5 
INTRODUCCIÓN GENERAL 
La biología evolutiva de los organismos parásitos puede ser explorada sobre tres tipos de 
asociaciones históricas distintas; i.e. a) Organismo-Gen, b) Área-Organismo y c) Huésped-
Parásito (Page & Charleston, 1998) (Figura 1). 
 
En este contexto, es válido interpretar de manera equitativa la evolución de estas tres 
asociaciones históricas realizando analogías entre los distintos fenómenos, mecanismos y 
procesos evolutivos que teóricamente ocurrieron entre ellas; i.e. codivergencia, duplicación, 
transferencia horizontal y sorteo de linajes (Page, 1994a; Page & Charleston, 1998; Cuadro 1). 
De este modo, es plausible comparar dos árboles filogenéticos de taxones distintos pero que 
representan una asociación intrínseca (v. gr., parasitismo), para inferir su historia evolutiva sobre 
un mismo escenario espacio-temporal capaz de detectar eventos evolutivos que se reflejen en 
patrones biogeográficos y concordancias filogenéticas (cofilogenéticas) (Page & Holmes, 1998; 
Charleston, 2011). Estos patrones pueden analizarse sobre las aristas de la teoría coevolutiva 
(Darwin, 1859; Ehrlich & Raven, 1964; Page, 2003) y, específicamente, reflejarse sobre un 
mosaico geográfico en el que las poblaciones de los asociados (parásitos) difieren de sus 
características y especializaciones en función a las especies con las que se asocian (huéspedes) 
(ver Thompson, 1994, 2005). 
 
 6 
Cuadro 1. Fenómenos, mecanismos y procesos equivalentes entre diferentes asociaciones 
históricas. Tomado y modificado de Page & Charleston, 1998.  
Asociación 
histórica 
Codivergencia Duplicación Transferencia 
horizontal 
Eventos de sorteo 
Organismo-Gen Coalescencia 
interespecífica 
Duplicación de 
genes, sorteo 
incompleto de linajes  
Transferencia de 
genes 
Pérdida de genes, 
sorteo de linajes 
Huésped-Parásito Coespeciación  Especiación dentro 
de un mismo huésped 
Duplicación de 
huésped (host-
switch) 
Extinción de parásitos 
–missing the boat–  
Áreas-Organismos Vicarianza Simpatría Dispersión Extinción 
 
Glosario 
Asociado. Un linaje que sigue a otro linaje, o un conjunto de entidades históricamente relacionadas.  
Codivergencia. Divergencia conjunta tanto del huésped como del asociado. 
Duplicación. Divergencia independiente del asociado, con ambos descendientes remanentes asociados con el 
huésped. 
Eventos de sorteo. La ausencia total o aparente de un asociado en los descendientes de un huésped que previamente 
habían tenido esa asociación. 
Transferencia horizontal. La transferencia de un linaje asociado de un huésped ("origen") a otro huésped 
("colonizado"), que no es en sí mismo un descendiente inmediato del huésped de origen. 
Teoría de la coalescencia. Enfoque matemático que modela la profundidad de árboles de genes de una o varias 
poblaciones cercanamente relacionadas.  
Coalescencia interespecífica. Concordancia topológica para múltiples linajes.   
Tiempo de coalescencia. Tiempo para que dos genes homólogos o un conjunto de genes pueda llegar a un ancestro 
común más reciente (MRCA, por sus siglas en inglés Most Recent Common Ancestor). 
Sorteo de linajes. Perdida de linajes específicos por cambios debidos a la deriva génica a través del tiempo. 
Sorteo incompleto de linajes. Es el fracaso de linajes de haplotipos entre individuos de una misma población para 
coalescer, permitiendo que al menos uno de los linajes coalezca primero con un linaje de una población menos 
estrechamente relacionada. 
Genealogía de genes. El patrón de similitudes entre secuencias de ADN que contiene información en común 
acerca de su historia evolutiva. 
Transferencia de genes. Proceso en el que un organismo transfiere material genético a otra célula que no es 
descendiente.  
Host switching. Proceso donde el parásito diverge por el cambio o duplicación para colonizar y establecerse en otro 
linaje de huéspedes. 
Missing the boat. Proceso en donde si un asociado se distribuye solo en una parte de la distribución del huésped 
(por ejemplo, un parásito con distribución irregular), la divergencia dentro de los linajes de huéspedes puede 
producir  descendientes que carezcan de esta asociación. Por tanto, la asociación nunca se extinguió en esos 
huéspedes sino que nunca estuvo presente.  
 
 
 7 
 Los avances en la obtención y métodos de análisis de datos moleculares (secuencias de 
ADN) han permitido interpretar e integrar la historia evolutiva de los organismos parásitos, 
misma que es influenciada por las complejas asociaciones que establecen con sus huéspedes 
(Huelsenbeck et al., 2001; Rosenberg & Nordborg, 2002; Morrison, 2006). Por ejemplo, en 
algunas especies de helmintos parásitos que presentan especificidad se ha registrado variación 
genealógica codiferenciada por la historia biogeográfica y filogenética de sus huéspedes (Zietara 
& Lumme, 2002; Plaisance et al., 2007; Nieberding et al., 2008). Además, recientemente se han 
propuesto medios de análisis para la reconstrucción biogeográfica usando inferencia filogenética 
capaz de incorporar de manera directa a la base de datos de análisis la variable tiempo a través del 
uso de árboles de genes, reloj molecular y la relativización de las longitudes de las ramas entre 
dos árboles filogenéticos de especies (Ree et al., 2005; Edwards, 2009; Ronquist & Sanmartin, 
2011). En este contexto, es posible poner a prueba hipótesis evolutivas entre asociaciones 
históricas de tipo huésped-parásito, sobre un espacio geográfico particular a través del tiempo 
(Sanmartin et al., 2008; Crisp et al., 2011; Sanmartin, 2012). 
 En México, un espacio geográfico complejo es la Zona de Transición Mexicana (ZTM) 
debido a que es una zona de contacto entre dos regiones biogeográficas: Neártica y Neotropical 
(Luna-Vega et al., 2005; Morrone, 2010; Luna-Vega & Contreras-Medina, 2012). La ZTM se 
ubica en el centro de México, se extiende de costa a costa desde el Océano Pacífico hasta el 
Golfo de México, entre los paralelos 18º 30-24º 30´ N y los meridianos 98º 30´-105º 00´ W, 
cubriendo un área de 267 000 km2 con altitudes que oscilan desde 100-200 m.s.n.m. hasta los 
5000 m.s.n.m. (Challenger, 1998; Ferrusquía-Villafranca, 1998; Figura 2). La ZTM es 
considerada como un área de endemismo para múltiples taxones dulceacuícolas debido a su 
historia hidrogeomorfologíca compleja. A la fecha se han registrado más de 100 taxones de agua 
dulce  exclusivos de esta área (Miller & Smith, 1986; Huidobro et al., 2006; Martínez-Aquino et 
al., 2007a).  
Un modelo biológico de asociación histórica para poner a prueba hipótesis de 
codivergencia en función al escenario geográfico (como por ejemplo la ZTM) y a la historia 
evolutiva de los huéspedes, puede ser estudiado a través de la denominada fauna principal (core 
species) de helmintos parásitos de peces dulceacuícolas de México (ver Pérez-Ponce de León & 
Choudhury, 2005), debido a que presenten alta especificidad sobre áreas geográficas restringidas 
 8 
(sistemas hidrológicos epicontinentales), en las que naturalmente no se dispersan por el agua y, 
por tanto, no tienen flujo génico entre las especies de huéspedes a las que están asociadas o bien, 
entre los sistemas hidrológicos en los que se distribuyen (Martínez-Aquino et al., 2013). 
Particularmente, la asociación entre Goodeinae-Margotrema, grupos biológicos que 
presumiblemente presentan una estrecha relación evolutiva sobre el centro de México (ver 
detalles más delante; Pérez-Ponce de León & Choudhury, 2005), es un modelo para poner a 
prueba hipótesis de codivergencia sobre un escenario geográfico particular.  
 
  La subfamilia Goodeinae (Osteichthyes: Cyprinodontiformes: Goodeidae) es un grupo 
monofilético de peces dulceacuícolas endémico del centro de México (Doadrio & Domínguez-
Domínguez, 2004). La subfamilia contiene 41 especies incluídas en cuatro tribus: 
Girardinichthyini, Chapalichthyini, Ilyodontini y Characodontini; todas presentan un patrón de 
distribución claramente asociado al escenario geográfico del centro de México (Domínguez-
Domínguez et al., 2010). Dicho escenario resultado de los cambios hidrogeomorfológicos que 
modificaron la configuración del área y provocaron procesos de vicarianza, y en algunos casos 
vicarianza-dispersión, en los distintos linajes de peces (Gesundheit & Macías-García, 2005; 
Domínguez-Domínguez et al., 2006; 2010). 
 9 
Estudios sobre la helmintofauna de algunas especies de goodeinos (v. gr. Pérez-Ponce de 
León et al., 2000; Martínez-Aquino et al., 2004, 2007b, 2009, 2011, 2012; Mejía-Madrid et al., 
2005), han detectado especies de helmintos parásitos que alcanzan la madurez sexual en los peces 
y que, al parecer, presentan una estrecha relación evolutiva con sus huéspedes (Pérez-Ponce de 
León & Choudhury, 2005). Entre otros helmintos, los digéneos del género Margotrema Lamothe-
Argumedo, 1972 (Digenea: Allocreadiidae) evidencian esta relación. 
  El género Margotrema fue descrito originalmente para incluir a M. bravoae Lamothe-
Argumedo, 1972 como parásito de Girardinichthys multiradiatus en La Lagunilla, Estado de 
México (Lamothe-Argumedo, 1972). Previo a este trabajo, dos especies de este género fueron 
descritas: M. bravoae y M. guillerminae Pérez-Ponce de León, 2001 como parásito de los peces 
Notropis calientis (Cyprinidae) y Alloophorus robustus (Goodeinae) en el Lago de Zacapu, 
Michoacán (Pérez-Ponce de León, 2001). Los caracteres morfológicos diagnósticos que 
diferenciaron a estas especies fueron la extensión de los ciegos intestinales a lo largo del cuerpo, 
la distribución de las glándulas vitelógenas y la posición del receptáculo seminal (Pérez-Ponce de 
León, 2001). Algunos autores cuestionaron la validez taxonómica de M. guillerminae sugiriendo 
que existe una alta variación morfológica en Margotrema (Pineda-López et al., 2005); sin 
embargo, no presentaron datos que corroboren tal cuestionamiento, ni plantearon una alternativa 
metodológica para demostrarlo. Por otra parte, el género Margotrema se ha registrado asociado a 
las cuatro tribus de goodeinos, en 21 especies de peces, y es considerado como restringido para el 
centro-occidente de México en las cuencas de los ríos Lerma, Santiago, Balsas, Ayuquila y 
algunos cuerpos de agua del norte de México (Martínez-Aquino et al., 2007b, 2011, 2012; Pérez-
Ponce de León et al., 2007a; 2009, 2013; Aguilar-Aguilar et al., 2010). Algunos autores han 
inferido que Margotrema presenta una estrecha relación evolutiva con la de sus huéspedes 
(Goodeinae), constituyendo parte de su fauna principal (Pérez-Ponce de León & Choudhury, 
2005), debido al área de distribución y a la especificidad registrada para peces de esta subfamilia 
(Mejía-Madrid et al., 2005; Pérez-Ponce de León & Choudhury, 2005; Martínez-Aquino et al., 
2007a, 2007b). Se ha sugerido también que Margotrema es un género de afinidad Neártica con 
base en su posición filogenética y a la historia evolutiva de sus huéspedes (Pérez-Ponce de León 
et al., 2007b; Curran et al., 2011). En este sentido, debido a su distribución geográfica 
fragmentada es posible que exista variación fenotípica interespecífica en Margotrema resultado 
del polimorfismo genético causado por aislamiento geográfico y a la supresión del flujo génico 
 10 
entre sus poblaciones. Además, dicho polimorfismo podría estar relacionado a una asociación 
específica con los grupos monofiléticos de huéspedes (Tribus) a los que parasitan. De este modo, 
las poblaciones de Margotrema pudieran mostrar un patrón de codistribución y codiferenciación 
filogenética asociada a la historia evolutiva de las cuatro tribus de goodeinos, reflejado en la 
historia hidrogeomorfológica del centro de México. En este contexto, analizar la asociación 
Goodeinae-Margotrema, con evidencia de marcadores moleculares, permitirá proponer hipótesis 
biogeográficas y contrastarlas con hipótesis cofilogenéticas para detectar si existe congruencia o 
no entre ellas. Así, Margotrema es un excelente modelo para analizar la biología evolutiva de 
parásitos de México sobre tres niveles distintos de asociaciones históricas como se refirió 
anteriormente:  a) Organismo-Gen, genealogía intra e interspecífica de Margotrema, b) Área-
Organismo, biogeográfica comparada tanto con el escenario geográfico del centro de México 
como con sus huéspedes y c) Huésped-Parásito, a través del contraste cofilogenético de 
Goodeinae y Margotrema (Page & Charleston, 1998). Por tanto, para realizar estos análisis, en el 
presente estudio se plantearon las siguientes hipótesis y objetivos (general y particulares): 
Hipótesis 
1. Margotrema bravoae y M. guillerminae representan dos especies válidas cuya 
distinción morfológica está sustentada en su estructura filogenética con base en árboles de 
genes. 
2.  La estructura filogenética de Margotrema spp. coincide con el patrón de la distribución 
geográfica de las cuatro tribus de Goodeinae. 
3.  La diversificación de los goodeinos, resultado de los eventos de vicarianza-dispersión 
del centro de México, influye de igual modo en la evolución de las poblaciones de 
Margotrema spp. 
Objetivo general 
Detectar los patrones biogeográficos y cofilogenéticos que influyeron en la asociación 
histórica de Goodeinae-Margotrema en sistemas hidrológicos del centro de México. 
 
 11 
Objetivos particulares 
1. Establecer la validez taxonómica de las dos especies del género Margotrema (M. 
bravoae y M. guillerminae), a través de análisis filogenéticos con base en coalescencia, 
utilizando un marcador molecular mitocondrial (COX1) y uno nuclear (ITS1). 
  2.  Determinar la estructura genética intra e interpoblacional de Margotrema spp. 
  3.  Estimar los tiempos de divergencia filogenética de Margotrema spp. 
4.  Contrastar los tiempos de divergencia filogenética de Margotrema spp. con aquellos de 
los cuatro linajes (tribus) de Goodeinae. 
5.  Detectar los eventos y procesos biogeográficos espacio-temporales de las poblaciones 
de Margotrema spp. en su área de distribución. 
6. Proponer una hipótesis biogeográfico-cofilogenética que explique el patrón de 
distribución de Margotrema spp., en función tanto de los patrones filogenéticos de 
Goodeinae como de la historia hidrogeomorfológica del centro de México.    
  Con base en este planteamiento del problema y el modo de abordarlo, se presenta este 
estudio en tres capítulos. El primero incluye una recopilación de todos los registros 
helmintológicos para Goodeinae publicados a la fecha, además de algunos que se generaron en 
este trabajo, con el objetivo de tener un listado lo mas completo posible de todas las localidades 
donde se han registrado ejemplares de Margotrema lo que, en sumatoria, representa su área de 
distribución actualizada. Los registros efectuados durante el transcurso de este estudio doctoral se 
presenta en cinco artículos publicados como parte de los primeros resultados derivados de esta 
investigación. El capítulo dos muestra los resultados filogenéticos de Margotrema, el cual 
representa la primera asociación histórica de tipo Organismo-Gen. El capítulo tres, se muestra en 
formato de manuscrito para ser sometido para su publicación y, finalmente, este trabajo incorpora 
una discusión general y conclusiones. Además, con base en el apoyo recibido por el Posgrado en 
Ciencias Biológicas, UNAM y con la colaboración con distintos grupos de trabajo, se presentan 
un manuscrito más aceptado para su publicación que se coloca a modo de Apéndice en la parte 
final del presente trabajo y que se realizó de manera paralela durante este estudio doctoral. 
 12 
 
 
 
 
 
 
 
 
 
 
CAPÍTULO I 
REGISTROS DE MARGOTREMA SPP. PARA PECES DULCEACUÍCOLAS DE MÉXICO:  
TAXONOMÍA E INVENTARIOS 
 
 
 
 
 
 
 
 
 
 
 
 13 
Para realizar este proyecto el primer objetivo particular fue generar un listado lo mas completo 
posible de todas las localidades donde se registro Margotrema spp., lo que en sumatoria, 
representa su área de distribución actualizada. Los registros taxonómicos de Margotrema spp. 
aportados durante el transcurso de este proyecto doctoral se presentan en cinco artículos 
publicados formalmente, como parte de los primeros resultados derivados de esta investigación. 
Para ello, realizamos muestreos propios que permitieron visitar 30 localidades en donde fueron 
registrados individuos de Margotrema como parásitos asociados a 22 especies de Goodeinae, y 
en cuatro y una especie más de peces dulceacuícolas de las familias Cyprinidae y 
Cyprinodontidae, respectivamente. Además, se visitaron 27 localidades nuevas para explorar la 
posibilidad de recolectar y determinar el área de distribución actual de Margotrema. Por último, 
como resultado de esta exploración de campo se presenta un manuscrito (pág. 43) que será 
sometido para su publicación en una revista indizada referente al inventario helmintológico más 
actualizado para Goodeinae – incluyendo el área de distribución de Margotrema – el cual 
representa el grupo de vertebrados mejor estudiado para México en términos de su 
helmintofauna.  
  A continuación se presenta una versión de cada documento en orden según la secuencia 
cronológica en la que cada artículo fué publicado y, por último, un manuscrito en formato de 
articulo en extenso el cuál será sometido para su publicación en una revista arbitrada e indizada 
(ISI / SCI). 
1) Helminth parasites of Xenotaenia resolanae (Osteichthyes: Cyprinodontiformes: 
Goodeidae) from the Cuzalapa hydrological system, Jalisco, Mexico (Martínez-
Aquino et al., 2009). 
2) Helminth fauna of two cyprinid fish (Campostoma ornatum and Codoma ornata) 
from the upper Piaxtla River, Northwestern Mexico (Aguilar-Aguilar et al., 2010). 
3) Endohelminth parasites of the freshwater fish Zoogoneticus purhepechus 
(Cyprinodontiformes: Goodeidae) from two springs in the Lower Lerma River, 
Mexico (Martínez-Aquino et al., 2011). 
4) Endohelminth parasites of seven goodein species (Cyprinodontiformes: Goodeidae) 
from Lake Zacapu, Michoacán, Central Mexico Plateau (Martínez-Aquino et al., 
2012). 
 14 
5) A new species of Margotrema (Digenea, Allocreadiidae) from the leopard splitfin 
Xenotaenia resolanae (Cyprinodontiformes, Goodeidae) from west-central Mexico 
(Pérez-Ponce de León et al., 2013). 
6) Composición taxonómica de helmintos parásitos de Goodeinae (Osteichthys: 
Cyprinodontiformes: Goodeidae) en México. 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 15 
 
 
 
 
 
 
 
 
 
 
1) HELMINTH PARASITES OF XEONOTAENIA RESOLANAE (OSTEICHTHYES: 
CYPRINODONTIFORMES: GOODEIDAE) FROM THE CUZALAPA HYDROLOGICAL SYSTEM, 
JALISCO, MEXICO 
 
 
 
 
 
 
 
 
 
 
 
 
 
J. Parasitol., 95(5), 2009, pp. 1221-1223 
O American Society of Parasitologists 2009 
Helminth Parasites of Xenotaenia resolanae (Osteichthyes: Cyprinodontiformes: 
Goodeidae) From the Cuzalapa Hydrological System, Jalisco, Mexico 
Andrés Martínez-Aquino, Rogelio Aguilar-Aguilar, Rodolfo Pérez-Rodríguez, and Gerardo Pérez-Ponce de León*, Departamento de 
Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, C.P. 04510, Apartado Postal 70-153, México, D.F., Mexico; *To whom 
correspondence should be addressed. e-mail: ppdleonBibiología. unam.mx 
ABSTRACT: Six helminth species were recorded during the helmintholo- 
gical examination of 35 specimens of the goodeid Xenotaenia resolanae 
from Arroyo Durazno, Jalisco, Mexico, a tributary of the Cuzalapa River. 
Helminth species identified included: 4 species of digeneans, ¡e., 
Posthodiplostomum minimum (metacercariae), Clinostomum companatum 
(metacercariae), Dendrorchis sp. (adult), and Margotrema guillerminae 
(adult); and 2 species of nematodes, i.e., Spiroxys sp. (larvas) and 
Rhabdochona ahuehuellensis (adult). A very low number of individual 
larvae were found. The observed species richness, individual parasite 
abundance, and diversity were low at both component community and 
infracommunity levels. The values of similarity between infracommunities 
were relatively high because of the predominance of the digenean M. 
guillerminae, the species that reached the higher values of both prevalence 
and abundance. High water flow of the collecting site is suggested as the 
main factor determining the depauperate helminth assemblage in this fish 
species. 
Xenotaenia resolanae Turner 1946, (Cyprinodontiformes: Goodeidae) 
ranges in small rivers in Central Mexico's Pacific Slope (Domínguez- 
Domínguez et al., 2005). It is not recorded as an endangered species 
(Froese and Pauly, 2008), even though some authors have suggested that 
this fish species is very susceptible to environmental degradation (Lyons 
and Navarro-Pérez, 1990) and should be regarded as vulnerable 
(Domínguez-Domínguez et al., 2005). The helminth fauna of this 
freshwater fish is poorly known. The only published record for X. 
resolanae includes the intestinal nematode Rhabdochona ahuehuellensis 
(Mejía-Madrid et al., 2005). However, this record was established for the 
Rio Tecolote, Jalisco, a locality different from the one examined in the 
present study. The aim of this research note is to present the 
helminthological record of X. resolanae from Arroyo Durazno, a tributary 
of the Cuzalapa River which drains into the Marabasco River Basin in the 
state of Jalisco, Mexico; to describe the helminth infracommunity 
structure; and to briefly discuss the possible causes that determine that 
structure. 
On August 2008, 35 specimens of X. resolanae were collected by 
electrofishing from Arroyo Durazno (19"30'32.1"N, 104*17'45.6"W), 
which is a small affluent of the Cuzalapa River, a tributary of the 
Marabasco River Basin in Jalisco State, southwestern Mexico. Hosts were 
taken alive to the laboratory, pithed, and examined individually for 
intestinal helminths. Other organs (gills, liver, gall, swim and urinary 
bladders, and spleen) were examined using a stereomicroscope in separate 
Petri dishes with 0.65% saline. Worms were fixed with 4% hot (steaming) 
formalin. Platyhelminths were stained with Mayer's paracarmine. 
Nematodes were cleared with glycerin for light microscopy and stored in 
70% ethanol. Voucher specimens of all taxa were deposited in the 
Colección Nacional de Helmintos (CNHE), Instituto de Biología, 
Universidad Nacional Autónoma de México, Mexico City. Use of 
prevalence (% infected), mean intensity (mean number of parasites per 
infected fish), and abundance (mean number of parasites of a single 
species per analyzed host) follows Bush et al. (1997). Helminth species 
were classified from an ecological point of view as dominant (high 
prevalence and abundance) and rare (low prevalence and abundance) after 
an Olmstead-Tukey corner test of association (Steel and Torrie, 1981). 
Infracommunities were described by the mean number of parasite species, 
the mean number of individual helminths, and the mean value of the 
Brillouin diversity index that is commonly used in parasitological studies 
for fully censured communities. To demonstrate numerical dominance, the 
Berger-Parker index was used (the closer the value to 1.00, the greater the 
dominance). Similarity among infracommunities was estimated by using 2 
indices: the Jaccard index and the Morisita-Horn index, for qualitative 
and quantitative similarity, respectively, as calculated in Magurran (1988). 
DOL: 10.1645/GE-1925,1 
A total of 154 individual helminths was collected. Six helminth species 
were recovered, 4 digeneans and 2 nematodes (Table I). Three species were 
recovered as larval stages: Clinostomum complanatum, Posthodiplostomum 
minimum, and Spiroxys sp.; the remaining 3 helminth species were adults. 
The digenean Margotrema guillerminae was the most abundant species, 
accounting for about 85% of the collected worms, followed by R 
ahuehuellensis, which accounted for 10.4%. The digenean Dendrorchis sp. 
was the least numerous, with a prevalence of 5.7% and a mean intensity of 
1.5 worms per infected host. "This digenean was not identified to species 
level because it appears to represent an undescribed species. Additional 
samples are necessary to present a proper description. Infection site, 
number of infected fish, prevalence, abundance, and mean intensity of 
each helminth species are shown in Table 1. 
Thirty of the 35 individual hosts were infected with at least 1 species of 
helminth. Eight of these harbored 2 or more helminth species. The total 
number of individual helminths of all species per host varied from 1 to 24, 
with a mean number of 4.4 + 5.4 individuals per host. The Olmstead- 
Tukey test showed that only the intestinal digenean M. guillerminae was 
frequent (prevalence >80%) and abundant (abundance >3.7 worms per 
analyzed host). The other intestinal species, ¡.e., R. ahuhuellensis, exhibited 
a relatively high prevalence, but it was not abundant, while the 
Dendrorchis sp. was actually a rare species. The remaining species 
exhibited low prevalence and abundance values (Table D) and were also 
considered as rare. 
The helminth infracommunities were species-poor. Most infracommu- 
nities were composed of a single species, 7 of them had 2 helminth species, 
and only 1 had the maximum of 4 species. The mean number of species per 
host was 1.1 + 0.8. Five of the 7 infracommunities with 2 or more species 
were composed of the intestinal adult worms M. guillerminae and R. 
ahuehuellensis. The Brillouin index for all infracommunities varied from 0 
to 0.915, with a mean diversity value of 0.113 + 0.218, while the Berger- 
Parker dominance index values varied from 0.444 to 1, with a mean of 
0.918 + 0.16. For comparative purposes, we calculated the Brillouin index 
for the 8 infracommunities with at least 2 species, which varied from 0.23 
to 0.915 with a mean diversity value of 0.425 + 0.215; the Berger-Parker 
dominance index values varied from 0.444 to 0.900 with a mean of 0.693 + 
0.167. Most of these assemblages were dominated by the digenean M. 
guillerminae. The helminth infracommunities showed a relatively high level 
of similarity. The corresponding Jaccard index varied from 0 to 1 (mean of 
0.654 + 0.353), and the Morisita-Horn index varied from 0 to 1 (mean of 
0.765 + 0.342). 
Three of the 6 helminth species parasitizing X. resolanae were larval 
stages. However, even though they have been previously reported 
parasitizing other goodeids in Central and Northern Mexico (Peresbar- 
bosa-Rojas et al., 1994; Martínez-Aquino et al., 2004; Mejía-Madrid et al., 
2005; Martínez-Aquino et al., 2007), their prevalence and abundance were 
very low. The remaining 3 taxa have also been reported for other goodeid 
species and are members of the core endohelminth fauna of this fish family 
(Mejía-Madrid et al., 2005), particularly M. guillerminae and R. 
ahuehuellensis, while congeneric species of Dendrorchis have been recorded 
as parasites of characids in the Neotropical region (Volonterio and Ponce 
de León, 2005). The record of 3 adult endohelminth species in X. 
resolanae, along with the finding of Salsuginus (monogeneans) on the gills 
(Martínez-Aquino, 2005), conform a particular parasite assemblage where 
adult native species are predominant. The helminth parasite species 
composition herein reported for X. resolanae is similar to that found in 
other goodeid fishes in central and northern Mexico (Peresbarbosa-Rojas 
et al., 1994; Pérez-Ponce de León et al., 2000; Martínez-Aquino et al., 
2004; Sánchez-Nava et al., 2004; Mejia-Madrid et al., 2005; Salgado- 
Maldonado, 2006; Martínez-Aquino et al., 2007; Romero-Tejeda et al., 
2008). However, the prevalence and abundance of individual larval forms 
is very low. This can be explained as a result of the physical conditions of 
the locality where fishes were collected, particularly water flow. The brook 
where we conducted our sampling belongs to a small, exoreic river basin 
1221
 16 
 
 
1222 THE JOURNAL OF PARASITOLOGY, VOL. 95, NO. 5, OCTOBER 2009 
TaBLE I. Helminth parasites of Xenotaenia resolanae (n = 35) in Arroyo Durazno, Jalisco, Mexico. 
Number of Prevalence Mean intensity CNHE 
Helminth Infection site(s)* infected hosts (%) Abundance + SD catalog no. 
Adult Digenea 
Margotrema guillerminae I 28 80 3.74 4.68 + 5.6 6880 
Dendrorchis sp. U 2 5.711 0.09 1.5 + 0.71 6881 
Larval Digenea 
Clinostomum complanatum Bc 1 2.86 0.03 1 6882 
Posthodiplostomum minimum M 1 2.86 0.03 1 6883 
Adult Nematoda 
Rhabdochona ahuehuellensis I 7 20 0.46 2.29 + 1.49 6884 
Larval Nematoda 
Spiroxys sp. M 1 2.86 0.06 2 6885 
* L, intestine; U, urinary bladder; Bc, body cavity; M, mesentery. 
where water flows very rapidly and, apparently, there are no piscivorous 
birds nesting in the area because no aquatic vegetation can be established 
under this permanent water flow and, as a result, the presence of these 
birds (definitive hosts for several larvae) is not common. This condition is 
different than that found in endorreic springs, and even in lakes, where 
most of the goodeid species occur and where a larger number of allogenic 
parasite species, usually exhibiting high abundance levels, are dispersed by 
fish-eating reptiles and birds that feed upon goodeids (see Pérez-Ponce de 
León et al., 2000; Martínez-Aquino et al., 2004, 2007; Martinez-Aquino 
and Aguilar-A guilar, 2008; Romero-Tejada et al., 2008). 
The data we present here suggest that the helminth parasite species 
composition and the helminth infracommunity structure in X. resolanae 
are slightly different than those found in freshwater fishes occurring in 
other water bodies of central and northern Mexico. Our data may indicate 
that physical conditions in the locality, particularly rapid water flow, 
could be responsible for determining the helminth community structure. 
Likewise, the helminth assemblage is consistent with the pattern that 
shows a depauperate parasite fauna in freshwater fishes inhabiting 
epicontinental waters in the Nearctic part of Mexico (Espinosa-Huerta 
et al., 1996; Rojas et al., 1997; Choudhury and Dick, 2000; Pérez-Ponce de 
León et al., 2000; Martínez-Aquino et al., 2004; Sánchez-Nava et al., 2004; 
Martínez-Aquino et al., 2007; Martínez-Aquino and Aguilar-Aguilar, 
2008; Romero-Tejeda et al., 2008). Another characteristic shared among 
the helminth community of X. resolanae and helminth communities of 
other freshwater fishes occurring in central and northern Mexico is the 
numerical dominance exacted by a single species of parasite; in this case, 
the digenean M. guillerminae is the dominant species. Furthermore, the 
helminth community of X. resolanae exhibits low species richness values at 
both the component community and infracommunity levels; this has been 
reported for other goodeid fishes in the Nearctic part of Mexico such as 
Alloophorus robustus, Goodea atripinnis, Allotoca diazi, Chapalichthys 
encaustus, Characodon audax, Skiffia lermae, Girardinychthys multi- 
radiatus, Xenotoca variata, and Zoogoneticus quitzeoensis (Astudillo- 
Ramos and Soto-Galera, 1997; Rojas et al., 1997; Pérez-Ponce de León 
et al., 2000; Sánchez-Nava et al., 2004; Martínez-Aquino et al., 2004, 2007; 
Romero-Tejeda et al., 2008). 
This work is a result of a prospective study of the doctoral dissertation 
of A.M.A. The authors wish to thank Rogelio Rosas Valdez for his 
comments on an earlier draft of this manuscript. This project was partially 
funded by grants from the program PAPITT-UNAM IN209608 and 
CONACyT No. 83043 to G.P.P.L. Most of this paper was written during 
the sabbatical leave of G.P.P.L. to the Department of Nematology, 
University of California, Davis. Thanks are due to Steve Nadler for his 
support and also to the program UCMEXUS-CONACyT (University of 
California Institute for Mexico and the United States-Consejo Nacional 
de Ciencia y Tecnología) for the fellowship awarded. 
LITERATURE CITED 
ASTUDILLO-RAMOS, L., AND E. Soro-GALERA. 1997. Estudio helmintoló- 
gico de Chirostoma humboldiianum y Girardinichthys multiradiatus 
capturados en el Lerma. Zoología Informa 35: 53-59. 
Bush, A. O., K. D. LarrerTY, J. M. Lorz, AND A. W. ShHosTAKk. 1997, 
Parasitology meets ecology on its own terms: Margolis et al. revisited. 
Journal of Parasitology 65: 667-669. 
CHOUDHURY, A., AND T, Dick. 2000. Richness and diversity of helminth 
communities in tropical freshwater fishes: Empirical evidence. 
Journal of Biogeography 27: 935-956. 
DominGuEz-DomiNGUEZ, O., N. MERCADO-SILVA, J. LyoNs, AND H. J. 
GRIER. 2005. The viviparous goodeid fishes. In Viviparous fishes, M. 
C. Uribe and H. J. Grier (eds.). New Life Publications, Homestead, 
Florida, p. 525-569, 
EsPINosA-HUÉERTA, E., L. GARCcÍA-PRIETO, AND G. PÉREZ-PONCE DE LEÓN. 
1996. Helminth community structure of Chirostoma attenuatum 
(Osteichthyes: Atherinidae) in two Mexican lakes. Southwestern 
Naturalist 41: 288-292, 
FROESE, R., AND D. PAuLy. 2008. FishBase. World Wide Web electronic 
publication. www.fishbase.org, version (07/2008). 
Lyons, J., AND S. NAVARRO-PÉREZ. 1990. Fishes of the Sierra de Manantlán, 
West-Central Mexico. Southwestern Naturalist 35: 3246. 
MAGURRAN, A. 1988. Ecological diversity and its measurement, Croom 
Helm, London, U.K., 179 p. 
MARTÍNEZ-ÁQUINO, A. 2005. Biogeografía de helmintos parásitos de peces de 
la familia Goodeidae (Pisces: Cyprinododntiformes) del centro de 
México. B.S. Thesis. Facultad de Ciencias, UNAM, México D.F., 129p. 
, AND R. AGUILAR-AGUILAR. 2008. Helminth parasites of the 
pupfish Cyprinodon meeki (Pisces: Cyprinodontiformes), an endemic 
freshwater fish from North-Central Mexico. Helminthologia 45: 
48-51. 
, G. SALGADO-MALDONADO, R. AGUILAR-ÁGUILAR, G. CABAÑAS- 
CARRANZA, AND C. MENDOZA-PALMERO. 2007. Helminth parasite 
communities of Characodon audax aud C. lateralis (Pisces: Good- 
eidae), endemic freshwater fishes from Durango, Mexico. Southwest- 
ern Naturalist 52: 125-130, 
  
  
  ——=, ——=, —=, , AND M. P. ORTEGA-OLIVARES. 2004. 
Helminth parasites of Chapalichthys encaustus (Pisces: Goodeidae), 
an endemic freshwater fish from Lake Chapala, Jalisco, Mexico. 
Journal of Parasitology 90: 889-890. 
Mería-MabproD, H. H., O. DominGuEz-DOMÍNGUEZ, AND G. PÉREZ-PONCE 
DE LEóN. 2005. Adult endohelminth parasites of Goodeinae 
(Cyprinodontiformes: Goodeidae) from Mexico with biogeographical 
considerations. Comparative Parasitology 72: 200211. 
PERESBARBOSA-ROJAS, E., G. PÉREZ-PONCE DE LEÓN, AND L. GARCÍA-PRIETO. 
1994. Helmintos parásitos de tres especies de peces (Goodeidae) del Lago 
de Pátzcuaro, Michoacán. Anales del Instituto de Biología, Universidad 
Nacional Autónoma de México, Serie Zoología 65: 201-204. 
PÉREZ-PONCE DE LEóN, G., L. GARcÍA-PRIETO, V. LEÓN-REGAGNON, AND A. 
CHoubHurY. 2000. Helminth communities of native and introduced 
fishes in Lake Pátzcuaro, Michoacán, México. Journal of Fish 
Biology 57: 303-325, 
Rojas, E., G. PÉREZ-PONCE DE LEÓN, AND L. GARcía-PRIETO. 1997. 
Helminth community structure of some freshwater fishes from 
Patzcuaro, Michoacan, Mexico. Tropical Ecology 38: 129-131.
 17 
 
 
Romero-TeJeDA, M. L., L. GARcÍA-PRIETO, L. GARRIDO-OLVERA, AND 
G. PÉREZ-PONCE DE LEóN. 2008. Estimation of the endohelminth 
parasite species richness in freshwater fishes from La Mintzita 
Reservoir, Michoacán, Mexico. Journal of Parasitology 94: 288- 
292. 
SALGADO-MALDONADO, G. 2006. Checklist of helminth parasites of 
freshwater fishes from Mexico. Zootaxa 1324: 1-357. 
SANCHEzZ-NAVa, P., G. SALGADO-MALDONADO, E. SoTo-GALERA, AND B. 
JAmes-CRUZ. 2004. Helminth parasites of Girardinichthys multi- 
RESEARCH NOTES — 1223 
radiatus (Pisces: Goodeidae) in the upper Lerma River sub-basin, 
Mexico. Parasitology Research 93: 396-402. 
STEEL, R. G. D., AND J. H. TorrIE. 1981. Principles and procedures of 
statistics: A biometrical approach, 2nd ed. McGraw-Hill Interna- 
tional Book Company, London, U.K., 633 p. 
'VOLONTERIO, O., AND R. PoNcE DE León. 2005. Description of Dendrorchis 
retrobiloba n. sp. (Digenea; Gorgoderidae) from Astyanax fasciatus 
(Teleostei; Characidae) from southern Uruguay, with an emended diag- 
nosis of the genus Dendrorchis. Journal of Parasitology 91: 1204-1207.
 18 
 
 
 19 
 
 
 
 
 
 
 
 
 
 
2) HELMINTH FAUNA OF TWO CYPRINID FISH (CAMPOSTOMA ORNATUM AND CODOMA 
ORNATA) FROM THE UPPER PIAXTLA RIVER, NORTHWESTERN MEXICO 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 20 
 
©2010 Parasitological Institute of SAS, Košice  
DOI  10.2478/s11687-010-0039-2 
 
 
                                                                                                                                                                                             251 
 
 
 
Summary 
 
The helminth parasite fauna of 2 species of freshwater 
fishes from the upper Piaxtla River in northwestern Mexi-
co was studied. A total of 41 cyprinids, corresponding to 
20 Campostoma ornatum and 21 Codoma ornata were 
analyzed. Six species of platyhelminths were recorded, 
including 2 species of monogeneans (Gyrodactylus sp. and 
Dactylogyrus sp.), 3 species of digeneans (Posthodip-
lostomum minimum, Clinostomum complanatum, and 
Margotrema sp.), and 1 species of tapeworm (Bothrio-
cephalus acheilognathi). Helminth parasite infracommuni-
ties were depauperate, showed low richness and diversity 
values, and were dominated by 1 or 2 helminth species. 
This pattern is consistent with that observed for the 
helminth parasite communities in other freshwater fishes in 
central and northern Mexico.  
 
Keywords: Platyhelminthes; Digenea; Monogenea; Cesto-
da; parasite communities; Cyprinidae; Mexico 
 
Introduction 
 
The freshwater fish species Campostoma ornatum Girard, 
1856 and Codoma ornata Girard 1856 (Cypriniformes: 
Cyprinidae) have a widespread distribution in northern 
Mexico (Espinosa-Pérez et al., 1993; Miller et al., 2005; 
Froese & Pauly, 2009). Both species are relatively com-
mon among the freshwater fish fauna of the upper Piaxtla 
River, which flows from the highlands of the Sierra Madre 
Occidental to the Pacific Ocean in northwestern Mexico. 
The helminth fauna of these cyprinids along its distribu-
tional range is poorly known. The only available records 
were recently published by Pérez-Ponce de León et al. 
(2009, 2010) from the upper-Mezquital and the Nazas river 
basins, respectively. The main objectives of this work are 
....  
 
to record the helminth parasite fauna of both species of 
cyprinids in the upper Piaxtla River by presenting the list 
of species, and to describe the helminth parasite commu-
nity structure of each host species through the species 
richness and diversity atributtes. We briefly compare our 
findings with data reported by Pérez-Ponce de León et al. 
(2009, 2010) for the same fish species in the Nazas and 
upper-Mezquital river basins. 
 
Materials and methods 
 
In December, 2008, 20 specimens of Campostoma or-
natum and 21 of Codoma ornata were collected by elec-
trofishing in the upper Piaxtla River (24º 21' 59'' N, 105º 
31' 7.8'' W, altitude 2391 m), located at Municipio San 
Dimas, Durango State, Northern Mexico. Hosts were taken 
alive to the laboratory. Once there, hosts were pithed, and 
examined individually for helminths. Gills and fins were 
separated in Petri dishes with tap water, and then examined 
under a stereomicroscope. Other organs (intestine, liver, 
gall, swim and urinary bladders, and spleen) were exa-
mined in separate Petri dishes with 0.65% saline. Platy-
helminths were fixed with 4% hot (steaming) formalin, 
stained with Mayer's paracarmine and mounted as perma-
nent slides in Canada balsam. Several individual monoge-
neans were fixed in glycerin ammonium-picrate (GAP), to 
study their sclerotized structures. Voucher specimens of all 
taxa were deposited in the Colección Nacional de 
Helmintos (CNHE), Instituto de Biología, Universidad 
Nacional Autónoma de México, Mexico City (see Table 
1). Prevalence (% of infected hosts in a sample), and abun-
dance (mean number of parasites of a single species in the 
sample) follows definitions by Bush et al. (1997). To de-
termine if sample size was sufficient to produce an accu-
HELMINTHOLOGIA, 47, 4: 251 – 256, 2010 
 
 
Helminth fauna of two cyprinid fish (Campostoma ornatum and Codoma ornata) 
from the upper Piaxtla River, Northwestern Mexico 
 
 
R. AGUILAR-AGUILAR1*, R. ROSAS-VALDEZ2, A. MARTÍNEZ-AQUINO3,4, R. PÉREZ-RODRÍGUEZ3,4,  
O. DOMÍNGUEZ-DOMÍNGUEZ5, G. PÉREZ-PONCE DE LEÓN2 
 
 
1*Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México, Apartado 
Postal 70-399, C. P. 04510, México D.F., Mexico, E-mail: raguilar@ibiologia.unam.mx; 2Departamento de Biología 
Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Apartado Postal 70-399, C. P. 04510, 
México D.F., Mexico; 3Laboratorio de Helmintología, Instituto de Biología, Universidad Nacional Autónoma de 
México. Apartado Postal 70-153. C. P. 04510, México D.F., Mexico; 4Posgrado en Ciencias Biológicas, Universidad 
Nacional Autónoma de México; 5Laboratorio de Biología Acuática, Universidad Michoacana de San Nicolás de 
Hidalgo, Edificio R planta Baja, Ciudad Universitaria, Morelia, Michoacán, Mexico 
 
rate estimate of the pool of parasites using both host spe- 
cies in the sampled locality, an accumulation species curve 
and the species richness estimators Chao 1 and Chao 2 
were used for each component community. Helminth spe- 
cies were classified from an ecological point of view as 
dominant (high prevalence and abundance) and rare (low 
prevalence and abundance) after an Olmstead-Tukey cor- 
ner test of association (Steel and Torrie, 1981). Infracom- 
munities include all the helminth species in an individual 
host, and were described by using the mean number of 
parasite species per host, the mean number of individual 
helminths, and the mean value of the Brillouin diversity 
index. Infracommunities were compared qualitatively 
within the locality using the Jaccard similarity index, and 
quantitatively using the Morisita-Horn index, as calculated 
in Magurran (1988). 
Results 
A total of 148 individual helminths belonging to four spe- 
cies were collected from Campostoma ornatum. Helminth 
species recovered include a fins monogenean Gyrodactylus 
sp., the metacercariae of the digeneans Posthodiplostomum 
minimum from the mesentery and Clinostomum com- 
planatum from the body cavity, and the adults of an intro- 
duced cestode Bothriocephalus acheilognathi from the 
intestine. The Olmstead-Tukey test for this fish species 
showed that the monogenean Gyrodactylus sp and the 
metacercariae of P. minimum were most frequent (preva- 
lence 95 and 85 %, respectively) and abundant (abundance 
from 3.1 to 3.25 helminths per analyzed host), while C. 
complanatum and B. acheilognathi reached low values for 
these parameters. Infection site, number of infected fish, 
prevalence, and abundance for each helminth species are 
shown in Table 1. 
In contrast, a total of 3292 individual helminths belonging 
to five species were collected from Codoma ornata. 
Helminth species recovered include a gills monogenean of 
the genus Dactylogyrus sp., the adult digenean Margot- 
rema sp. from the intestine, the metacercariae of Post- 
hodiplostomum minimum and Clinostomum complanatum, 
and the cestode Bothriocephalus acheilognathi. “The 
Olmstead-Tukey test showed that only the metacercariae of 
P. minimum was most frequent (prevalence 100 %) and 
abundant (143.29 worms per analyzed host). The monoge- 
nean Dactylogyrus sp. and the metacercariae of C. com- 
planatum exhibited a high prevalence (100 % and 81%, 
respectively), but they were not abundant, while Margot- 
rema sp. and B. acheilognathi showed low prevalence and 
abundance values (Table 1), and were considered as rare. 
Infection site, number of infected fish, prevalence, and 
abundance for each helminth species are shown in Table 1. 
In Campostoma ornatum, most of the parasite infracom- 
munities (85 %) harbored 2 or more helminth species. In 
terms of abundance, the total number of individual 
helminths of all species per analyzed host varied from 1 to 
15, with a mean number of 7 + 3.47. Similarly, parasite 
infracommunities in Codoma ornata harbored 2 or more 
252 
helminth species, however, the presence of gill monogene- 
ans in 5 hosts was not determined because fish died several 
hours before examination. For this reason, values of 
prevalence and abundance for those particular helminth 
taxa were calculated only for 16 individual hosts (Table 1). 
The number of helminths of all species per analyzed host 
was much higher, and varied from 3 to 365, with a mean 
number of 157 + 92,39, 
Even though, individual hosts of both fish species were 
infected at least with 1 helminth species, the helminth 
parasite infracommunities in both host species were rela- 
tively species-poor. Most of the infracommunities found in 
Campostoma ornatum (55 %), were composed by three 
species, and only 2 of them reached a maximum of four 
species. In terms of species richness, the mean number of 
species per host was 3 + 0.88. The Brillouin index for the 
infracommunities varied from O to 0.976, with a mean 
diversity value of 0.537 + 0.261, while the Berger-Parker 
dominance index values varied from 0.333 to 1, with a 
mean of 0.624 + 0.194, The helminth infracommunities in 
C. ornatum showed a relatively high level of similarity; the 
corresponding Jaccard index varied from O to 1 (mean of 
0,59 + 0,235) while the Morisita-Horn index varied from O 
to 1 (mean of 0.729 + 0.215). 
In the case of Codoma ornata, 42.85% of the infracommu- 
nities were also composed by 3 species, and only 2 had a 
maximum of 5 species. The mean number of species per 
host was 3.09 + 0,94, The Brillouin index for the infra- 
communities varied from 0.043 to 0.571, with a mean 
diversity value of 0.299 + 0.163, while the Berger-Parker 
dominance index values varied from 0.667 to 0.991, with a 
mean of 0.902 + 0.078. The helminth infracommunities 
showed a comparatively higher level of similarity; the 
corresponding Jaccard index varied from 0.2 to 1 (mean of 
0.629 + 0.224) and the Morisita-Horn index varied from 
0.43 to 1 (mean of 0.943 = 0.15). 
Discussion 
Helminth taxa 
The helminth parasite fauna of the cyprinids Campostoma 
ornatum and Codoma ornata in the upper Piaxtla River 
includes 6 helminth species, 2 monogeneans, 3 digeneans 
and 1 cestode. The taxonomic composition of the helminth 
parasite fauna of Campostoma ornatum comprises 3 gener- 
alist species, which are widely distributed among fresh- 
water fishes in several localities in Mexico (Pérez-Ponce 
de León et al., 2007; Rojas-Sánchez $ Garcia-Prieto, 
2008). Species of the monogenean Gyrodactylus sp., col- 
lected from the fins of their hosts, have been recently re- 
corded from diverse freshwater fishes in central and north- 
ern Mexico, where apparently a high species richness of 
this parasite group is found (Mendoza-Palmero, 2007; 
Mendoza-Palmero et al., 2009; Pérez-Ponce de León el al., 
2010); further studies will allow us to establish the taxo- 
nomic identity and potential host specificity of Gyrodac- 
tylus species occurring in Mexican freshwater fishes. The 
specimens we collected might be conspecific with an un-
 21 
 
 
2
2
  
 
 
 
 
253
Table 1. Helminth parasites of Campostoma ornatum and Codoma ornata in the upper Piaxtla River, Durango, Mexico 
 
 Campostoma ornatum (n = 20) Codoma ornata (n = 21) 
Helminth taxa Infection 
site 
Infected 
Hosts (n) 
Prevalence 
(%) 
Abundance 
± SD 
CNHE No. Infected 
Hosts (n) 
Prevalence 
(%) 
Abundance 
± SD 
CNHE No. 
Monogenea  
   Gyrodactylus sp. Fins 19 95 3.1 ± 1.85 7465 - - - - 
   Dactylogyrus sp. * Gills - - - - 16 100 11.2 ± 9.69 7466 
Digenea  
   Margotrema sp. Intestine - - - - 6 28.57 0.33 ± 0.58 7473 
   Posthodiplostomum 
minimum 
Mesentery 17 85 3.25 ± 2.47 7467 21 100 143.29 ± 
85.8 
7468 
   Clinostomum 
complanatum 
Body cavity 8 40 0.45 ± 0.6 7469 17 80.95 4.33 ± 4.49 7470 
Cestoda  
   Bothriocephalus 
acheilognathi 
Intestine 8 40 0.5 ± 0.76 7471 5 23.81 0.29 ± 0.58 7472 
      * Values based on16 host 
253
 23 
 
 
 
 
 
254 
described species, Gyrodactylus sp. 4, reported by Pérez-
Ponce de León et al. (2010) as a parasite of the fins of 
Campostoma ornatum in the Nazas River Basin, however, 
this species has not yet been described.  
Furthermore, the helminth parasite fauna of Codoma or-
nata includes 3 species that were also found in Cam-
postoma ornatum; in addition, the adult digenean Margot-
rema sp. and the monogenean Dactylogyrus sp. were also 
found. Currently, 2 species of Margotrema spp., an alleg-
edly parasite of goodeid fishes, have been described in 
freshwater fishes from central Mexico (Pérez-Ponce de 
León et al., 2007). The distinctive morphological character 
that distinguishes these species is the extent of the ceca. 
Unfortunately, the specimens we collected from cyprinids 
in the Piaxtla River had the uteri full of eggs, impeding the 
observation of the extent of the ceca.  Monogeneans of the 
genus Dactylogyrus have also been found parasitizing 
freshwater fishes in central and northern Mexico (Men-
doza-Palmero, 2007; Pérez-Ponce de León et al., 2010). In 
particular, in cyprinids from a nearby river basin (the 
Nazas River), 6 species of Dactylogyrus have been re-
ported (Pérez-Ponce de León et al., 2010), 3 of them com-
mon parasites of introduced species of cyprinids, and 1 
typically found in cichlids. Other 2 species from cyprinids 
were considered to represent a new species for which no 
description has been made. As in the case of the fin mono-
genean, Gyrodactylus sp., we may claim conspecificity to 
some of these undescribed species, however, we preferred 
to take a conservative position pending proper description 
of the undescribed species. 
Interestingly, the taxonomic composition of the helminth 
parasite fauna herein reported for both cyprinid species 
included only platyhelminthes. No nematodes or acantho-
cephalans were found in present study. This might be due 
to a relatively small sample size, even though 20 individual 
hosts are considered a sufficient sample size to detect para-
site species richness in a particular locality, and, in addi-
tion to that, there are no missing species according with the 
information provided by the accumulation species curves 
and the non-parametric species richness estimators Chao 1 
and Chao 2. The absence of such parasite groups contrasts 
with findings we recently made describing the helminth 
parasite fauna in of freshwater fishes from the Nazas and 
the upper-Mezquital river basins, including Campostoma 
ornatum (Pérez-Ponce de León et al., 2009, 2010). These 
river basins are located at relatively short distance from the 
upper Piaxtla River, even though the former runs west-
wards from high elevation areas of Durango State, through 
Nayarit State, to the Pacific coast, while the Nazas River 
represents an endhorreic basin that runs from the Sierra 
Madre Occidental eastward, through the states of Durango 
and Coahuila, into the now-dry Laguna del Mayran 
(Castañeda-Gaytán et al., 2005; Návar et al., 2006). In the 
upper-Mezquital River only 4 individuals of Campostoma 
ornatum were sampled, and 2 helminth species were re-
corded, the cestode Bothriocephalus acheilognathi, and the 
nematode Rhabdochona canadensis. We also sampled 23 
individuals of Codoma ornata and only the tapeworm B. 
acheilognathi was found (see Pérez-Ponce de León et al., 
2009).  
In contrast, in the Nazas River a much larger sample size 
was analyzed for both cyprinid species (Pérez-Ponce de 
León et al., 2010). Eighty individuals of Campostoma 
ornatum were studied, and the helminth species recorded 
were: the digeneans P. minimum and Uvulifer sp., the 
cestode B. acheilognathi, the nematodes Spiroxys sp., and 
Rhabdochona canadensis and two species of 
monogeneans, an undescribed species of Gyrodactylus 
(recorded as Gyrodactylus sp. 4) and Urocleidoides 
strombicircus. In 101 analyzed specimens of Codoma 
ornata only 3 helminth species were recorded, the dige-
nean P. minimum, the cestode B. acheilognathi, and the 
nematode R. canadensis (Pérez-Ponce de León et al., 
2010). The absence of R. canadensis in cyprinids from the 
Piaxtla River is noteworthy, since this is a common para-
site of cyprinids in North America (see Hoffman, 1999). 
Likewise, the larval digeneans P. minimum and C. com-
planatum are commonly found parasitizing freshwater 
fishes in México (Pérez-Ponce de León et al., 2007), while 
the species of the genus Margotrema are allegedly to be 
members of the helminth parasite core fauna of goodeid 
fishes in central Mexico (Pérez-Ponce de León & Choud-
hury, 2005; Mejía-Madrid et al., 2005). The adult cestode 
B. acheilognathi is an autogenic and generalist species 
whose life cycle is completed in the aquatic ecosystem 
(Hoffman, 1999). This species was introduced into Mexico 
along with its hosts, grass carps, from Asia. It possesses a 
large dispersal capability and as a result, it is now found 
not only in introduced hosts but also in the native fresh-
water fish fauna (Rojas-Sánchez and García-Prieto, 2008). 
No carps (Cyprinus carpio, Ctenopharyngodon idella), 
which are commonly used for aquaculture purposes and 
are disseminated to natural environments on regular basis, 
were found during our samplings in the Piaxtla River. It 
could be possible that the endemic cyprinids we studied 
became infected with the Asian tapeworm through an 
ecological host extension from other host species, such as 
poeciliids, but still this needs to be determined with further 
samplings in the locality.  
 
Helminth communities 
Parasite communities of both species of cyprinids are de-
pauperate and are dominated by one helminth species; this, 
and the fact that a low species richness values at both, the 
component community and infracommunity levels, were 
detected, is consistent with the parasite community struc-
ture in a diverse array of freshwater fishes inhabiting in 
epicontinental waters in central and northern Mexico, cor-
responding with the Nearctic region (Peresbarbosa-Rojas 
et al., 1994; Espinosa-Huerta et al., 1996; Rojas et al., 
1997; Pérez-Ponce de León et al., 2000; Martínez-Aquino 
et al., 2004, 2007; Martínez-Aquino & Aguilar-Aguilar, 
2008; Romero-Tejeda et al., 2008). Helminth parasite 
communities in the 2 cyprinids we studied herein also 
show a numerical dominance by a single or a few helminth 
species. In the case of Codoma ornata, dominance is 
 24 
 
 
 
 
 
255
mainly exerted by the metacercariae of Posthodiplostomum 
minimum, which shows a high abundance. In Campostoma 
ornatum, two helminth species were dominant, the dige-
nean P. minimum and the monogenean Gyrodactylus sp. 
Based on the results of the species accumulation curves 
and the species richness estimators, we are confident about 
the accuracy of species richness and community structure 
patterns herein described. Both methods were used as indi-
cators of species richness as a function of sample size, 
even though it is well-known that addressing sample size is 
a common problem when dealing with prevalence data (see 
Jovani & Tella, 2006); likewise, our analysis corroborated 
that the number of analyzed hosts represents a sufficient 
sample size to recover most members of the parasite com-
munity. Since the number of hosts we analyzed in this 
study fall within the category of “medium sample size” as 
proposed by Jovani and Tella (2006), it is possible that the 
prevalence of infection for each parasite species might 
have been affected, but not the species richness. We are 
certain that, by gathering a larger dataset on different 
helminth parasite communities in freshwater fishes, we 
will be able to establish a correlation between the sample 
size and the parasite fauna. As a comparison, the 80 
specimens of Campostoma ornatum and 101 of Codoma 
ornata that were studied in the Nazas River basin by 
Pérez-Ponce de León et al. (2010), contained 7 (i.e., Uvu-
lifer sp., Posthodiplostomum minimum,, Gyrodactylus sp. 
4, Urocleidoides strombicircus, Bothriocephalus acheilog-
nathi, Rhabdochona canadensis, and Spiroxys sp.) and 3 
helminth species (i.e., P. minimum, B. acheilognathi and R. 
canadensis, respectively. The data we provide in the pre-
sent paper represents an additional piece of information on 
the parasite species composition, and patterns of commu-
nity structure of the helminth parasites of freshwater fishes 
in Mexico, particularly from lotic environments of the 
northwestern region. Still, more data needs to be gathered 
on these species of cyprinids along its distributional range, 
as well as on other freshwater fish species, in order to 
describe general patterns of host-parasite associations, and 
to fully understand the processes that shaped the historical 
biogeography and community structure of the freshwater 
fish parasite fauna in Mexico. 
 
Acknowledgements 
 
We thank to Carlos Mendoza Palmero for technical assis-
tence. This project was partially funded by grants from the 
Comisión Nacional para el Conocimiento y Uso de la Bio-
diversidad (CONABIO FM001), Consejo Nacional de 
Ciencia y Tecnología (CONACyT 83043), and Programa 
de Apoyo a Proyectos de Investigación e Innovación Tec-
nológica (PAPIIT-UNAM IN 209608) to G.P.P.L. AMA 
and RPR thank CONACYT for the scholarship provided to 
complete their PhD programs at the Posgrado en Ciencias 
Biológicas, UNAM. This paper was partially written dur-
ing the sabbatical leave of G.P.P.L. at the University of 
California-Davis under the support of a fellowship granted 
by the program UC MEXUS-CONACyT. Thanks are also 
due to Steve Nadler for facilities provided in his laboratory 
during sabbatical. 
 
References 
 
BUSH, A. O., LAFFERTY, K. D., LOTZ, J. M., SHOSTAK, A. 
W. (1997): Parasitology meets ecology on its own terms: 
Margolis et al. revisited. J. Parasitol., 65: 667 – 669 
CASTAÑEDA-GAYTÁN, G., GARCÍA-DE LA PEÑA, C., 
LAZCANO, D., SALAS-WESTPHAL, A. (2005): Notes on 
Herpetofauna 7: Herpetological Diversity of the Low Basin 
of the Nazas River, Durango, México. Bull. Chicago 
Herpetol. Soc., 40: 34 – 37 
ESPINOSA-PEREZ, H., GASPAR-DILLANES, M. T., FUENTES-
MATA, P. (1993): Listados faunísticos de México III. Los 
Peces Dulceacuícolas Mexicanos. México, D. F., Mexico: 
Instituto de Biologia, Universidad Nacional Autónoma de 
México, 98 pp. 
ESPINOSA-HUERTA, E., GARCÍA-PRIETO, L., PÉREZ-PONCE 
DE LEÓN, G. (1996): Helminth community structure of 
Chirostoma attenuatum (Osteichthyes: Atherinidae) in two 
Mexican lakes. Southwest. Nat., 41: 288 – 292 
FROESE, R., PAULY, D. (2009): Campostoma ornatum and 
Codoma ornata. In: FishBase. Retrieved June 26, 2009 
from http://www.fishbase.org. 
HOFFMAN, G. L. (1999): Parasites of North American 
freshwater fishes. 2nd Edition, Ithaca, New York, Cornell 
University Press, 539 pp. 
JOVANI, R., TELLA, J. L. (2006): Parasite prevalence and 
sample size: Misconceptions and solutions. Trends in 
Parasitology, 22: 214 – 218. DOI: 10.1016/j.pt.2006.02.011 
MAGURRAN, A. (1988): Ecological diversity and its meas-
urement. London, UK, Croom Helm, 179 pp. 
MARTÍNEZ-AQUINO, A., AGUILAR-AGUILAR, R. (2008): 
Helminth parasites of the pupfish Cyprinodon meeki (Pi-
sces: Cyprinodontiformes), an endemic freshwater fish 
from North-Central Mexico. Helminthologia, 45: 48 – 51. 
DOI: 10.2478/s11687-008-0008-1 
MARTÍNEZ-AQUINO, A., SALGADO-MALDONADO, G., 
AGUILAR-AGUILAR, R., CABAÑAS-CARRANZA, G., MEN-
DOZA-PALMERO, C. A. (2007): Helminth parasite com-
munities of Characodon audax and C. lateralis (Pisces: 
Goodeidae), endemic freshwater fishes from Durango, 
Mexico. Southwest. Nat., 52: 125 – 130. DOI: 10.1894/ 
0038-4909(2007)52[125:HPCOCA]2.0.CO;2 
MARTÍNEZ-AQUINO, A., SALGADO-MALDONADO, G., 
AGUILAR-AGUILAR, R., CABAÑAS-CARRANZA, G., 
ORTEGA-OLIVARES, M. P. (2004): Helminth parasites of 
Chapalichthys encaustus (Pisces: Goodeidae), an endemic 
freshwater fish from Lake Chapala, Jalisco, Mexico. J. 
Parasitol., 90: 889 – 890. DOI: 10.1645/GE-255R 
MEJÍA-MADRID, H. H., DOMÍNGUEZ-DOMÍNGUEZ, O., 
PÉREZ-PONCE DE LEÓN, G. (2005): Adult endohelminth 
parasites of Goodeinae (Cyprinodontiformes: Goodeidae) 
from Mexico with biogeographical considerations. Comp. 
Parasitol., 72: 200 – 211. DOI: 10.1654/4169. 
MENDOZA-PALMERO, C. A. (2007). Monogéneos parásitos 
de peces de la subfamilia Goodeinae (Pisces: Cyprinodon-
 25 
 
 
 
 
 
256 
tiformes) con un análisis de su distribución geográfica. 
MSc thesis, Mexico, Posgrado en Ciencias Biológicas, 
Universidad Nacional Autónoma de México, Mexico. 
MENDOZA-PALMERO, C. A., SERENO-URIBE, A. L., SALGA-
DO-MALDONADO, G. (2009): Two new species of Gyro-
dactylus Von Nordmann, 1832 (Monogenea: Gyrodac-
tylidae) parasitizing Girardinichthys multiradiatus (Cypri-
nodontiformes: Goodeidae), an endemic freshwater fish 
from central Mexico. J. Parasitol., 95: 315 – 318. DOI: 
10.1645/GE-1761.1. 
MILLER, R.R., MINCKLEY, M. L., NORRIS, S. M. (2005): 
Freshwater fishes of Mexico. Chicago, The University of 
Chicago Press, 490 pp. 
NÁVAR, J., HERNÁNDEZ, H., RÍOS, J. (2006): Temporal 
tendencies of river discharge of five watersheds of north-
ern Mexico. In: AGUIRRE -BRAVO, C., PELLICANE, J. P., 
BURNS, D. P., DRAGGAN, S. (Eds) Monitoring Science and 
Technology Symposium: Unifying Knowledge for Sustain-
ability in the Western Hemisphere. Forth Collins, U.S.: 
Department of Agriculture, Forest Service, Rocky Moun-
tain Research Station, pp. 710 – 714 
PERESBARBOSA-ROJAS, E., PÉREZ-PONCE DE LEÓN, G., 
GARCÍA-PRIETO, L. (1994): Helmintos parásitos de tres 
especies de peces (Goodeidae) del Lago de Pátzcuaro, 
Michoacán. An. Inst. Biol. Univ. Nac. Auton. Mex., Ser. 
Zool., 65: 201 – 204 
PÉREZ-PONCE DE LEON, G., CHOUDUHRY, A. (2005): Bio-
geography of helminth parasites of freshwater fishes in 
Mexico: the search for patterns and processes. J. Biogeogr., 
32: 645 – 659. DOI: 10.1111/j.13652699.2005.01218.x 
PÉREZ-PONCE DE LEÓN, G., GARCÍA-PRIETO, L., LEÓN-
RÈGAGNON, V., CHOUDHURY, A. (2000): Helminth com-
munities of native and introduced fishes in Lake Pátzcuaro, 
Michoacán, México. J. Fish Biol., 57: 303-325. DOI: 
10.1111/j.1095-8649.2000.tb02174.x 
PÉREZ-PONCE DE LEÓN, G., GARCIA-PRIETO, L., 
..................  
 
 
 
 
 
 
 
 
 
RECEIVED AUGUST 27, 2009 
 
 
 
 
 
 
 
 
 
 
 
MENDOZA-GARFIAS, B. (2007): Trematode parasites 
(Platyhelminthes) of wildlife vertebrates in Mexico. Zo-
otaxa, 1534: 1 – 247 
PÉREZ-PONCE DE LEÓN, G. , ROSAS-VALDEZ, R., AGUI-
LAR-AGUILAR, R., MENDOZA-GARFIAS, B., MENDOZA-
PALMERO, C., GARCÍA-PRIETO, L., ROJAS-SÁNCHEZ, A., 
BRIOSIO, R., PÉREZ-RODRÍGUEZ, R., AND DOMÍNGUEZ-
DOMÍNGUEZ, O. (2010): Helminth parasites of freshwater 
fishes of the Nazas River Basin, Northern Mexico. Check 
List, 6: 26 – 35 
PÉREZ-PONCE DE LEÓN, G., ROSAS-VALDEZ, R., 
MENDOZA-GARFIAS, B., AGUILAR-AGUILAR, R., FALCÓN-
ORDAZ, J., GARRIDO-OLVERA, L., PÉREZ-RODRÍGUEZ, R. 
(2009): Survey of the endohelminth parasites of freshwater 
fishes in the upper Mezquital River Basin, Durango State, 
Mexico. Zootaxa, 2164: 1 – 20 
ROJAS, E., PÉREZ-PONCE DE LEÓN, G., GARCÍA-PRIETO, L. 
(1997): Helminth community structure of some freshwater 
fishes from Patzcuaro, Michoacan, Mexico. Trop. Ecol., 
38: 129 – 131 
ROJAS-SÁNCHEZ, A., GARCÍA-PRIETO, L. (2008): Dis-
tribución actual del Céstodo Bothriocephalus acheilog-
nathi en México. In Memorias XXV Simposio sobre Fauna 
Silvestre. Mexico, D. F.: Universidad Nacional Autónoma 
de México, Mexico, 2008, pp. 89 – 93 
ROMERO-TEJEDA, M. L., GARCÍA-PRIETO, L., GARRIDO-
OLVERA, L., PÉREZ-PONCE DE LEÓN, G. (2008): Estima-
tion of the endohelminth parasite species richness in 
freshwater fishes from La Mintzita Reservoir, Michoacán, 
Mexico. J. Parasitol., 94: 288 – 292. DOI: 10.1645/GE-
1157.1 
STEEL, R. G. D., TORRIE, J. H. (1981): Principles and pro-
cedures of statistics: a biometrical approach. 2nd Edition. 
London, UK, McGraw-Hill International Book Company, 
633 pp. 
 
 
 
 
 
 
 
 
 
 
 
ACCEPTED  MARCH 26, 2010 
 26 
 
 
 
 
 
 
 
 
 
 
3) ENDOHELMINTH PARASITES OF THE FRESHWATER FISH ZOOGONETICUS PURHEPECHUS 
(CYPRINODONTIFORMES: GOODEIDAE) FROM TWO SPRINGS IN THE  
LOWER LERMA RIVER, MEXICO 
 
 
 
 
 
 
 
 
 
 
 
 
 
Revista Mexicana de Biodiversidad 82: 1132-1137, 2011 
 
Endohelminth parasites of the freshwater fish Zoogoneticus purhepechus 
(Cyprinodontiformes: Goodeidae) from two springs in the Lower Lerma River, 
Mexico 
Endohelmintos parásitos del pez dulceacuícola Zoogoneticus purhepechus (Cyprinodontiformes: 
Goodeidae) en dos manantiales de la cuenca del río Lerma bajo, México 
Andrés Martínez-Aquino!”, David Iván Hernández-Mena!”, Rodolfo Pérez-Rodríguez!”, Rogelio Aguilar- 
Aguilar? and Gerardo Pérez-Ponce de León! Y 
“Instituto de Biología, Universidad Nacional Autónoma de México, Apartado postal 70-153, 04510 México, D.F, Mexico. 
“Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México, Apartado postal 70-399, 04510 México, 
D.F, Mexico. 
¿Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México. 
9 ppdleonQibiologia.unam.mx 
Abstract. In order to establish the helminthological record of the viviparous fish species Zoogoneticus purhepechus, 
72 individuals were collected from 2 localities, La Luz spring (n= 45) and Los Negritos spring (n= 27), both in the 
lower Lerma River, in Michoacán state, Mexico. Twelve helminth taxa were recovered, 5 adults (the digeneans 
Margotrema bravoae and Phyllodistomum sp., the cestode Bothriocephalus acheilognathi, the nematode Rhabdochona 
lichtenfelsi and the acanthocephalan Pomphorhynchus cf. bulbocolli), and 7 larvae (the metacercarias of Clinostomum 
complanatum, the cysticercoid of Cyclophyllidea, the nematodes Rhabdochona sp., Eustrongylides sp., Contracaecum 
sp. and Spiroxys sp., and the cysthacanth of Polymorphus brevis). Of these, R. lichtenfelsi was the most prevalent and 
abundant species at La Luz spring with 15.6% and 0.33 individuals per analyzed host. The remaining species were 
relatively more rare and infrequent. The helminth parasite community of Z. purhepechus at Los Negritos spring was 
remarkably poor and abundance was very low. The omnivorous feeding habits, the position of the host species in the 
food web, and the environmental characteristics of each locality are suggested as the main factors determining the 
helminth parasite communities in this freshwater fish. 
Key words: Goodeidas, Zoogoneticus purhepechus, helminth parasites, community structure, Mexico. 
Resumen. Se examinaron 72 individuos del pez vivíparo Zoogoneticus purhepechus para establecer el registro 
helmintológico de la especie. Los huéspedes se recolectaron de los manantiales La Luz (n= 45) y Los Negritos (n= 27), 
ubicados en la porción baja del río Lerma, en el estado de Michoacán, México. El registro helmintológico consta de 12 
especies, incluyendo como adultos los digéneos Margotrema bravoae y Phyllodistomum sp., el céstodo Bothriocephalus 
acheilognathi, el nemátodo Rhabdochona lichtenfelsi, y el acantocéfalo Pomphorhynchus cf. bulbocolli. Además, como 
estadios larvarios, se encontraron las metacercarias de Clinostomum complanatum, el cisticercoide de Cyclophyllidea, 
los nemátodos Rhabdochona sp., Contracaecum sp., Eustrongylides sp. y Spiroxys sp., y el cistacanto de Polymorphus 
brevis. De éstas, R. lichtenfelsi fue la especie más frecuente y abundante en el manantial La Luz, en tanto que las 
restantes fueron relativamente más raras. La comunidad de helmintos de Z. purhepechus en el manantial Los Negritos 
fue pobre y poco abundante. Se sugiere que los principales factores que determinan la estructura de la comunidad de 
helmintos son los hábitos alimentarios omnívoros de los huéspedes, la posición que éstos ocupan en la red trófica y las 
características ambientales de cada localidad. 
Palabras clave: Goodeidae, Zoogoneticus purhepechus, helmintos parásitos, estructura de la comunidad, México. 
Introduction fishes, Z. quitzeoensis Bean, Z. tequila Webb and Miller, 
and the recently described Z. purhepechus Domínguez- 
The genus Zoogoneticus Meek (Cyprinodontiformes: Domínguez, Pérez-Rodríguez and Doadrio. These fish 
Goodeidae) includes 3 species of livebearing freshwater species are restricted to particular river drainages in 
central Mexico (Domínguez-Domínguez et al., 2008) and 
are considered as endangered or critically endangered 
Recibido: 18 agosto 2010; aceptado: 31 mayo 2011 (De la Vega-Salazar et al., 2003; Dominguez-Domínguez 
 27 
 
Revista Mexicana de Biodiversidad 82: 1132-1137, 2011 
et al., 2005, 2008). The helminth fauna of livebearing 
freshwater fishes of the family Goodeidae has been well 
documented and the depauperate nature of helminth 
parasite communities in these fishes has been suggested 
(Astudillo-Ramos and Soto-Galera, 1997; Rojas et 
al., 1997; Pérez-Ponce de León et al., 2000; Martínez- 
Aquino et al., 2004, 2007, 2009; Sánchez-Nava et al., 
2004; Martínez-Aquino, 2005; Mejía-Madrid et al., 
2005; Romero-Tejeda et al., 2008). However, the only 
species of Zoogoneticus that has been studied to a certain 
extent is Z. quitzevensis and no records of the helminth 
parasite fauna of the other 2 congeneric species had been 
established. The main objective of this work is to record 
the helminth parasite fauna of Z. purhepechus collected 
in 2 sites (Los Negritos and La Luz springs) located in the 
lower Lerma River Basin, and to describe the helminth 
community structure and the processes that determine 
such structure. 
Materials and methods 
On July 2009, 72 adult specimens of Z. purhepechus 
were collected using nets in 2 localities, La Luz spring (n= 
45) (19% 56” 10,4” N, 102? 17” 57,8” W; 1 616 m) and Los 
1133 
Negritos spring (n= 27) (20? 03” 23,1” N, 102? 36” 38.3” 
W; 1 539 m), in Michoacán state, central Mexico. Hosts 
were taken alive to the laboratory, pithed and examined 
individually for intestinal helminths. Other organs (eyes, 
gall bladder, liver, spleen, swim and urinary bladders) 
as well as body cavity and musculature, were examined 
under a stereomicroscope in separate Petri dishes with 
0.65% saline, Digeneans, nematodes and cestodes were 
fixed with 4% (steaming) formalin. Acanthocephalans 
were maintained at 4%C for 24 hrs. in distilled water, 
and then fixed in 100% ethanol. Platyhelminths and 
acanthocephalans were stained with Meyer”s paracarmine. 
Nematodes were cleared with glycerin for light microscopy 
and stored in 70% ethanol. Voucher specimens were 
deposited in the Colección Nacional de Helmintos (CNHE), 
Instituto de Biología, Universidad Nacional Autónoma de 
México, Mexico City (Table 1); when accession number 
is not provided, specimens were collected for DNA work 
or scanning electron microscopy. Use of prevalence (% 
infected) and abundance (mean number of parasites of a 
single species in the sample) follows Bush et al. (1997). 
The non-parametric species richmess estimators Chao 
1 and Chao 2, were calculated following Colwell and 
Coddington (1995) and Escalante (2003), and were 
Table 1. Endohelminth parasites of Zoogoneticus purhepechus in 2 springs of the Lower Lerma River, Mexico. CNHE= Accession 
number; HI= Number of infected hosts; %= Prevalence; Ab= Abundance; SD= Standard deviation; MI= Mean intensity 
Helminth (Infection site* / CNHE) La Luz spring (n= 45) 
HI/%/Ab+SD/MI+SD 
Los Negritos spring (n= 27) 
HI/%/Ab+SD/MI+SD 
Adult Digenea 
Margotrema bravoae (1) 
Phyllodistomum sp. (Ub / 7791) 
Larval Digenea 
Clinostomum complanatum (Bc, M / 7792) 
Adult Cestoda 
Bothriocephalus acheilognathi (1, 77793) 
Larval Cestoda 
Cyclophyllidea gen. sp. (Gb) 
Adult Nematoda 
Rhabdochona lichtenfelsi (1, 7794) 
Larval Nematoda 
Rhabdochona sp. (1, 7108) 
Contracaecum sp. (L, 7105) 
Eustrongylides sp. (L, 7106) 
Spiroxys sp. (M) 
Adult Acanthocephala 
Pomphorhynchus cf. bulbocolli (1, 7795) 
Larval Acanthocephala 
Polymorphus brevis (M, 7796) 
4/8.9/0.13%20.5/15+1 
1/2.2/0.02+0.15/1 
1/2.2/0.02+0.15/1 
5/11.1/0.13204/1.2%0.45 
2/7.4/0.07+0.27/1 
1/3.7/0.04+0.19/1 
7/15.6/0,33 + 0.98 / 2,14 + 1.57 
1/3.7/0.04+0.19/1 
1/3.7/0.07 + 0.38 / 2 
1/3.7/0.04%0.19/1 
1/3.7/0.11%0.58 /3 
6/13.3/0.13+0.34/1 
1/3.7/0.04+0.19/1 
*Infection site: Bc= Body cavity; Gb= Gall bladder; Ub= Urinary bladder; I= Intestine; L= Liver; M= Mesentery
 28 
 
 
1134 
used to estimate the number of missing species for each 
component community. Infracommunities include all the 
helminth species in an individual host, and were described 
by using the mean number of parasite species per host, the 
mean number of individual helminths, and the mean value 
of the Brillouin diversity index. The numerical dominance 
at the infracommunity level was determined using the 
Berger-Parker dominance index (Southwood, 1978). 
Infracommunities were compared qualitatively within the 
locality using Jaccard similarity index and quantitatively 
using the Morisita-Horn index, as calculated in Magurran 
(1988). 
Results 
Twelve  helminth taxa were  recovered from 
the 2 sampled localities. The helminthological record 
comprises 3 digenean species: Margotrema bravoae 
Lamothe-Argumedo, 1970, Phyllodistomum sp., and the 
metacercariae of Clinostomum complanatum (Rudolphi, 
1819); 2 cestodes: the cysticercoid of Cyclophyllidea gen. 
sp., and Bothriocephalus acheilognathi Yamaguti, 1934; 2 
acanthocephalans: the cystacanth of Polymorphus brevis 
(Van Cleave, 1916) and Pomphorhynchus cf. bulbocolli 
Van Cleave, 1919; the adult nematode Rhabdochona 
lichtenfelsi Sánchez-Álvarez, García-Prieto and Pérez- 
Ponce de León, 1998, and larval forms of Contracaecum 
sp., Spiroxys sp., Eustrongylides sp., and Rhabdochona sp. 
La Luz spring. Thirty-four individual helminths 
were collected from 45 hosts from La Luz spring. 
These helminths represent 6 species: M. bravoae, 
Phyllodistomum sp. (adult), C.  complanatum 
(metacercariae), R. lichtenfelsi (adult), Spiroxys sp. 
(larvae), and P. cf. bulbocolli (adult). Infection site, 
number of infected fish, prevalence, abundance, and 
mean intensity for each helminth taxa are shown in 
Table 1. The adult nematode R. lichtenfelsi was the most 
abundant helminth species, accounting for about 42.8% 
of the worms collected in this locality; this nematode 
reached a prevalence value of 15.6% and abundance of 
0.33 worms per analyzed host. The remaining species 
were rare, infrequent, and reached very low abundance 
values (Table 1). Of the 45 analyzed individual hosts, 
19 were infected with at least 1 species of helminth in 
La Luz spring. Only 5 of the 45 hosts harbored 2 or 
more helminth species. The total number of individuals 
of all species per host varied from 1 to 7, with a mean 
intensity of 0.82 + 1.41. The non-parametric species 
richness estimators (Chaol and Chao 2) reached a value 
of 6. The helminth infracommunities were species-poor. 
Mean number of species per host was 0.6 + 0.8. The 
Brillouin index for all infracommunities varied from 0 
Martínez-Aquino et al.- Helminth parasites of Zoogoneticus purhepechus 
to 0.599, with a mean diversity value of 0.099 + 0.21, 
while the Berger-Parker dominance index values varied 
from 0.33 to 1, with a mean of 0.91 + 0.2. The helminth 
infracommunities displayed a low level of similarity. 
The corresponding Jaccard index varied from 0 to 1 
(mean of 0.18 + 0,4) and the Morisita-Horn index varied 
from 0 to 1 (mean of 0.2 + 0.37). 
Los Negritos spring. Only 11 individual helminths were 
collected from Los Negritos spring. The 7 species recovered 
were B. acheilognathi (adult), 1 specimen of Cyclophyllidea 
(cysticercoid), the larval nematodes Rhabdochona sp., 
Contracaecum sp., Eustrongylides sp., and Spiroxys sp., and 
Polymorphus brevis (cystacanth). Infection site, number 
of infected fish, prevalence, abundance, mean intensity 
for each helminth species are shown in Table 1. Only B. 
acheilognathi was found in 2 hosts, while the remaining 
species were even more rare and infrequent (Table 1). The 
total number of individual helminths of all species per 
host varied from 1 to 7, with a mean number of 0.4 + 1.4 
individuals per host. The value obtained from the non- 
parametric species richness estimators (Chao 1= 11 and 
Chao 2= 25), shows that apparently several missing species 
remaining to be found at the component of community 
level. The helminth infracommunities were also species- 
poor; 2 infracommunities had just 1 species and 1 had a 
maximum of 4. Mean number of species per host was 0.29 
+ 0.87, The Brillouin index for all infracommunities varied 
from 0 to 0,86, with a mean diversity value of 0,3 + 0,41, 
while the Berger-Parker dominance index values varied 
from 0,43 to 1, with a mean of 0.73 + 0,31. The helminth 
infracommunities show a low level of similarity. The 
corresponding Jaccard index varied from 0 to 0.5 (mean of 
0.08 + 0.2) and the Morisita-Horn index varied from 0 to 
0.67 (mean of 0.11 + 0.27). 
The comparison between the helminth parasite fauna 
of both study sites, exhibits a very low similarity. Table 1 
shows that only 1 taxon (Spiroxys sp.) is shared between 
component communities, resulting in a Jaccard value of 
0.17, and a Morisita-Horn value of 0.23. However, it is 
possible that the larval stage of Rhabdochona found in Los 
Negritos might be conspecific with R. lichtenfelsi; although, 
we were unable to identify this larval satge up to species. 
Discussion 
Most of the helminth species found in this study have 
been previously recorded in diverse freshwater fish species 
in central and northern Mexico (Mejía-Madrid et al., 2005; 
Pérez-Ponce de León et al., 2007, 2009, 2010; Martínez- 
Aquino and Aguilar-A guilar, 2008; Romero-Tejeda et al., 
2008). Two of these species, the digenean M. bravoae 
and the nematode R. lichtenfelsi, are commonly found
 29 
 
 
Revista Mexicana de Biodiversidad 82: 1132-1137, 2011 
in goodeid fishes, and have been considered as a part of 
the core parasite fauna for this fish family (Mejía-Madrid 
et al., 2005; Pérez-Ponce de León and Choudhury, 2005; 
Martínez-Aquino et al., 2009). 
Other helminth species recorded herein as adults 
were Phyllodistomum sp., P. cf. bulbocolli, and B. 
acheilognathi. The finding of Phyllodistomum sp. in 
this study represents a new host record for fishes of the 
family Goodeidae, To date, 6 species of Phyllodistomum 
have been recorded as a parasite of marine and 
freshwater fishes in Mexico (Pérez-Ponce de León et 
al., 2007). In this work, we collected 1 single specimen 
of this digenean, which hinders the accurate taxonomic 
determination. Considering the host associations of 
species of Phyllodistomum in freshwater fishes of North 
America (Hoffman, 1999), we may speculate that this 
represents an undescribed species. Further analysis of 
this worm and those collected from other goodeids in 
central Mexico (Martínez-Aquino, unpublished data) will 
allow the proper taxonomic identification of this digenean 
by using both, morphological and molecular data. 
The acanthocephalan P. cf. bulbocolli is a parasite of 
freshwater fishes frequently recorded in North America 
(Hoffmann, 1999), and it was recently found in Mexico 
as a parasite of the catostomid Catostomus nebuliferus 
Garman and the cyprinid Gila conspersa Garman (Pérez- 
Ponce de León et al., 2009, 2010). The presence of this 
acanthocephalan in Z. purhepechus from La Luz spring 
represents the third published record for this species in 
Mexico, and the first record in freshwater fishes of the 
family Goodeidae. The cestode B. acheilognathi is an 
introduced species, which currently is widely distributed 
in freshwater fishes of Mexico (Rojas-Sánchez and 
García-Prieto, 2008), including several species of 
goodeids (Peresbarbosa-Rojas et al., 1994; Pérez-Ponce 
de León et al., 2000; Sánchez-Nava et al., 2004; Romero- 
Tejeda et al., 2008; Pérez-Ponce de León et al., 2009). 
The remaining 7 helminth species found in Z. 
purhepechus inboth localities were larval stages frequently 
recorded in the freshwater fish helminth fauna of Mexico 
and North America. These species were C. complanatum, 
the cysticercoid of Cyclophyllidea, Contracaecum sp., 
Eustrongylides sp. and P. brevis, all of them maturing 
in piscivorous birds, and the nematode Spiroxys sp., 
which reaches the maturity mainly in freshwater turtles. 
One single immature specimen of Rhabdochona sp. was 
found in Los Negritos spring. This nematode most likely 
belongs to the species R. lichtenfelsi, however, absence 
of reproductive structures prevent its accurate taxonomic 
determination. 
The data we present here suggest that the helminth 
parasite species composition, and the  helminth 
1135 
infracommunity structure in Z. purhepechus is consistent 
with the pattern that shows a depauperate parasite fauna in 
goodeid fishes inhabiting freshwaters in the Nearctic part 
of Mexico such as Alloophorus robustus Bean, Goodea 
atripinnis Jordan, Állotoca diazi Meek, Chapalichthys 
encaustus Jordan and Snyder, Characodon audax 
Smith and Miller, Skiffia lermae Meek, Girardinychthys 
multiradiatus Meek, Xenotoca variata Bean, Xenotaenia 
resolanae Turner, and Z. quitzeoensis Bean (Astudillo- 
Ramos and Soto-Galera, 1997; Rojas et al., 1997; 
Pérez-Ponce de León et al., 2000; Martínez-Aquino et al., 
2004, 2007, 2009; Sánchez-Nava et al., 2004; Martínez- 
Aquino, 2005; Romero-Tejeda et al., 2008). The factors 
that determine the helminth community structure herein 
described are concordant with those described in the 
aforementioned studies (the feeding habits, omnivorous 
in this case, and the position in the food web of this 
species of host), i.e., 11 of the 12 helminth species infect 
their host when it feeds upon some species of crustacean 
or insect. Likewise, 7 of the 12 helminth species are 
larval forms that complete their life cycle when the fish 
is consumed by a definitive host, either a fish-eating bird 
or a reptile. 
On the basis of the values obtained through the species 
richness estimators used in this study (Chao 1 and Chao 
2), 1t seems that we sampled all the helminth fauna in 
La Luz spring, since the observed and estimated richness 
value was very similar; however, values obtained for the 
same richness estimators in Los Negritos spring indicate 
that various helminth species apparently remain to be 
found. This result was surprising, since following the idea 
of Pérez-Ponce de León and Choudhury (2010) that the 
inventory of the freshwater fish helminth fauna in Mexico 
is nearing completion, and not many additional species are 
expected to be found, and particularly in goodeids, since 
this is a group of hosts that has been extensively studied 
for helminths in the last years. Thus, this apparently high 
number of species remaining to be found at Los Negritos 
spring, could be the result of an artifact derived from 
very low abundance and mean intensity values for each 
helminth taxa, Both nonparametric estimators Chao 1 
and Chao2 are sensitive to the presence of rare species 
(Escalante, 2003), and that is probably the reason of 
the apparently high number of missing species in that 
particular locality. 
The comparison between the 2 study sites showed 
that both helminth assemblages had very low numbers of 
individuals and consequently, remarkable low prevalence 
and abundance values. However, the helminth community 
of Z. purhepechus at La Luz spring included at least 2 
of the species considered specialists for the fish family 
Goodeidae, the digenean M. bravoae and the nematode R.
 30 
 
 
1136 
lichtenfelsi (Pérez-Ponce de León and Choudhury 2005). 
Likewise, the helminth assemblage of Los Negritos 
spring is comparatively species-poor, specialist species 
are lacking, and is conformed only by larval stages and 
the introduced tapeworm B. acheilognathi. This pattern 
results in very low levels of similarity between the 
component communities. It is noteworthy the absence 
of digeneans in Los Negritos spring in conjunction 
with extremely low abundance values for the helminth 
species found in that locality. On the other hand, in La 
Luz, helminth species composition includes at least 3 
species of digeneans, even though no tapeworms were 
found, and abundance values of the helminth parasite 
fauna are slightly higher than in Los Negritos. We may 
speculate that this is the result of different environmental 
conditions of the sampling sites, e.g., primary productivity 
and associated physicochemical parameters (personal 
observation), and it is possible that the absence of 
digeneans in Los Negritos could be the result of the lack 
of molluscs that are the first intermediate host in their 
life cycle, however this needs to be determined with the 
proper sampling in the locality. 
Of the 3 recognized species of Zoogoneticus, the 
helminth parasite fauna has been studied for 2 of them, 
Z. quitzeoensis, and now, Z. purhepechus. We compared 
the helminth parasite fauna of Z. purhepechus and its 
putative sister species, Z. quitzeoensis (see Dominguez- 
Domínguez et al., 2008), and some differences were 
found. The endohelminth fauna of both Zoogoneticus 
species comprises 16 taxa, including 7 digeneans (4 
adults and 3 metacercarias), 2 cestodes (1 adult and 1 
cysticercoid), 5 nematodes (1 adult and 4 larvae), and 2 
acanthocephalans (1 adult and 1 larvae) (see Martínez- 
Aquino, 2005; Mejía-Madrid et al., 2005; Romero-Tejeda 
et al., 2008). Only 3 of the 16 taxa (M. bravoae, B. 
acheilognathi, and R. lichtenfelsi) are shared between 
both species. Considering that they are sister species, 
and even though they do not occur in sympatry, the 
differences in helminth parasite fauna are a sampling 
artifact due to the fact that these species have not been 
studied along their entire distributional range, in the 
Lower and Middle Lerma River, respectively. We predict 
that the result of a detailed survey work in other localities 
along the distribution range for both species, will allow 
us to find the species that have not yet been documented, 
increasing as a result the levels of similarity among the 
parasite fauna, 
Acknowledgments 
We thank Lorena Garrido-Olvera for corroborating 
the identification of the nematodes. AMA and RPR were 
Martínez-Aquino et al.- Helminth parasites of Zoogoneticus purhepechus 
supported by a Research Doctoral Fellowships from the 
Consejo Nacional de Ciencia y Tecnología (CONACyT), 
Mexico. D.I.H.M. thanks CONACyT for scholarship to 
accomplish his MSc degree. The study was funded by 
grants from the Consejo Nacional de Ciencia y Tecnología 
(CONACyT, No. 83043), and the Programa de Apoyo a 
Proyectos de Investigación e Innovación Tecnológica 
(PAPITT-UNAM IN 202111) to G.P.P.L. 
Literature cited 
Astudillo-Ramos, L. and E. Soto-Galera. 1997. Estudio 
helmintológico de  Chirostoma  humboldtianum y 
Girardinichthys multiradiatus capturados en el Lerma. 
Zoología Informa 35:53-59, 
Bush, A. O., K. D. Lafferty, J. M. Lotz and A. W. Shostak. 1997. 
Parasitology meets ecology on its own terms: Margolis et al. 
revisited. Journal of Parasitology 65:667-669. 
Colwell, R. K. and J. A. Coddington. 1995, Estimating terrestrial 
biodiversity through  extrapolation. ln Biodiversity: 
measurement and estimation, D. L. Hawksworth, (ed.). 
Chapman and Hall, London. p. 101-118. 
De la Vega-Salazar, M. Y., E. Ávila-Luna and C. Macías-García. 
2003. Ecological evaluation of local extinction: the case 
of two genera of endemic Mexican fish, Zoogoneticus and 
Skiffia. Biodiversity and Conservation 12:2043-2056. 
Domínguez-Domínguez, O., N. Mercado-Silva, J. Lyons and H. 
J. Grier. 2005. The viviparous goodeid fishes. [n Viviparous 
fishes, M. C. Uribe and H. J. Grier (eds.). New Life 
Publications, Homestead, Florida. p. 525-569. 
Domínguez-Domínguez, O., R. Pérez-Rodríguez and Ll. 
Doadrio. 2008. Morphological and genetic comparative 
analyses of populations of Zoogoneticus quitzeoensis 
(Cyprinodontiformes: Goodeidae) from Central Mexico, 
with description of a new species. Revista Mexicana de 
Biodiversidad 79:373-383. 
Escalante, T. 2003. ¿Cuántas especies hay?: los estimadores no 
paramétricos de Chao. Elementos 52:53-56. 
Hoffman, G. L. 1999. Parasites of North American freshwater 
fishes. 2"* edition. Cornell University Press, California. 539 
p. 
Magurran, A. 1988. Ecological diversity and its measurement. 
Croom Helm, London. 179 p. 
Martínez-Aquino, A. 2005. Biogeografía de  helmintos 
parásitos de peces de la familia Goodeidae (Pisces: 
Cyprinodontiformes) del centro de México. Tesis, Facultad 
de Ciencias, Universidad Nacional Autónoma de México, 
México, D.F. 129 p. 
Martínez-Aquino, A. and R. Aguilar-Aguilar. 2008. Helminth 
parasites of the pupfish Cyprinodon meeki (Pisces: 
Cyprinodontiformes), an endemic freshwater fish from 
North-Central Mexico. Helminthologia 45:48-51.
 31 
 
 
Revista Mexicana de Biodiversidad 82: 1132-1137, 2011 
Martínez-Aquino, A., R. Aguilar-Aguilar, R. Pérez-Rodríguez 
and G. Pérez-Ponce de León. 2009. Helminth parasites of 
Xenotaenia resolanae (Osteichthyes: Cyprinodontiformes: 
Goodeidae) from the Cuzalapa hydrological system, Jalisco, 
Mexico. Journal of Parasitology 95:1221-1223. 
Martínez-Aquino, A., G. Salgado-Maldonado, R. Aguilar- 
Aguilar, G. Cabañas-Carranza and C. Mendoza-Palmero. 
2007. Helminth parasite communities of Characodon audax 
and C. lateralis (Pisces: Goodeidae), endemic freshwater 
fishes from Durango, Mexico. The Southwestern Naturalist 
52:125-130. 
Martínez-Aquino, A., G. Salgado-Maldonado, R. Aguilar- 
Aguilar, G. Cabañas-Carranza and M. P. Ortega-Olivares. 
2004. Helminth parasites of Chapalichthys encaustus (Pisces: 
Goodeidae), an endemic freshwater fish from Lake Chapala, 
Jalisco, Mexico. Journal of Parasitology 90:889-890, 
Mejía-Madrid, H., O. Dominguez-Domínguez and G. Pérez- 
Ponce de León. 2005. Adult endohelminth parasites 
of Goodeinae (Cyprinodontiformes: Goodeidae) from 
Mexico with biogeographical considerations. Comparative 
Parasitology 72:200-211. 
Peresbarbosa-Rojas, E., G. Pérez-Ponce de León and L. García- 
Prieto. 1994, Helmintos parásitos de tres especies de peces 
(Goodeidae) del Lago de Pátzcuaro, Michoacán. Anales del 
Instituto de Biología, Universidad Nacional Autónoma de 
México, Serie Zoología 65:201-204. 
Pérez-Ponce de León, G. and A. Choudhury. 2005. Biogeography 
of helminth parasites of freshwater fishes in Mexico: the 
search for patterns and processes. Journal of Biogeography 
32:645-659. 
Pérez-Ponce de León, G. and A. Choudhury. 2010. Parasite 
inventories and DNA-based taxonomy: Lessons from 
helminths of freshwater fishes in a megadiverse country. 
Journal of Parasitology 96:236-244. 
Pérez-Ponce de León, G., L. García-Prieto, V. León-Regagnon 
and A. Choudhury. 2000. Helminth communities of native 
1137 
and introduced fishes in Lake Pátzcuaro, Michoacán, Mexico. 
Journal of Fish Biology 57:303-325. 
Pérez-Ponce de León, G., L. García-Prieto and B. Mendoza- 
Garfias. 2007. Trematode parasites (Platyhelminthes) of 
wildlife vertebrates in Mexico. Zootaxa 1534:1-247, 
Pérez-Ponce de León, G., R. Rosas-Valdez, R. Aguilar-A guilar, 
B. Mendoza-Garfias, C. Mendoza-Palmero, L. García-Prieto, 
A. Rojas-Sánchez, R. Briosio-Aguilar, R. Pérez-Rodríguez 
and O. Domínguez-Domínguez. 2010. Helminth parasites 
of freshwater fishes, Nazas River basin, northern Mexico. 
CheckList 6:26-35, 
Pérez-Ponce de León, G., R. Rosas-Valdez, B. Mendoza-Garfias, 
R. Aguilar-A guilar, J. Falcón-Ordaz, L. Garrido-Olvera and 
R. Pérez-Rodríguez. 2009. Survey of endohelminth parasites 
of freshwater fishes in the upper Mezquital River basin, 
Durango state, Mexico. Zootaxa 2164:1-20, 
Rojas, E., G. Pérez-Ponce de León and L. García-Prieto. 1997. 
Helminth community structure of some freshwater fishes 
from Patzcuaro, Michoacan, Mexico. Tropical Ecology 
38:129-131. 
Rojas-Sánchez, A. and L. García-Prieto. 2008. Distribución 
actual del céstodo Bothriocephalus acheilognathi en México. 
Memorias XXV Simposio sobre Fauna Silvestre, Facultad de 
Medicina y Zootecnia, Universidad Nacional Autónoma de 
México, Mexico. p. 89-93, 
Romero-Tejeda, M. L., L. García-Prieto, L. Garrido-Olvera 
and G. Pérez-Ponce de León. 2008. Estimation of the 
endohelminth parasite species richness in freshwater fishes 
from La Mintzita reservoir, Michoacán, Mexico. Journal of 
Parasitology 94:288-292. 
Sánchez-Nava, P., G. Salgado-Maldonado, E. Soto-Galera and 
B. Jaimes-Cruz. 2004. Helminth parasites of Girardinichthys 
multiradiatus (Pisces: Goodeidae) in the upper Lerma River 
sub-basin, Mexico. Parasitology Research 93:396-402. 
Southwood, T. R. 1978. Ecological methods, 2nd ed. Chapman $ 
Hall, London. 524 p.
 32 
 
 
 
 33 
 
 
 
 
 
 
 
 
 
 
4) ENDOHELMINTH PARASITES OF SEVEN GOODEIN SPECIES (CYPRINODONTIFORMES: 
GOODEIDAE) FROM LAKE ZACAPU, MICHOACÁN, CENTRAL MEXICO PLATEAU 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
  
Hidrobiológica 2012, 22 (1): 89-93 NOTAS Abril 2012 
Endohelminth parasites of seven goodein species (Cyprmodontiformes: Goodeidae) from Lake 
Zacapu , Michoacán, Central Mexico Plateau 
Endohelmintos parásitos de siete especies de godeinos (Cyprinodontiformes: Goodeidae) del 
lago de Zacapu, Michoacán, en la Mesa Central de México 
Andrés Martínez-Aquino,'? Rodolfo Pérez-Rodríguez,!? David |. Hernández-Mena,!? Lorena Garrido-Olvera?4 Rogelio Aguilar- 
Aguilar* and Gerardo Pérez-Ponce de León! 
1 Instituto de Biología, Universidad Nacional Autónoma de México (UNAM), Apartado Postal 70-153, México, D.F. 04510. México 
2 Posgrado en Ciencias Biológicas, UNAM. México, D.F. México 
3 Instituto de Ecología, UNAM, México, D.F. México 
4 Departamento de Biología Comparada, Facultad de Ciencias, UNAM, México D.F. México 
e- mail: ppdleonGibiologia.unam.mx 
 
Martínez-Aquino A., R. Pérez-Rodríguez, D. |. Hernández-Mena, Lorena Garrido-Olvera, R. Aguilar-Aguilar and G. Pérez-Ponce de León. 2012. Endohelminth 
parasites of seven goodein species (Cyprinodontiformes: Goodeidae) from Lake Zacapu, Michoacán, Central Mexico Plateau. Hidrobiológica 22(1): 89-93. 
ABSTRACT 
A total of 11 parasitic endohelminth taxa were found in 7 fresh- 
water fish species of the subfamily Goodeinae in Zacapu Lake, 
Michoacan, Mexico. Six were adults (Margotrema cf. bravoae, 
Phyllodistomum sp., Saccocoelioides sogandaresi, Rhabdochona 
lichtenfelsi, Bothriocephalus acheilognathi and Caryophillidae 
gen. sp.), while the remaining 5 taxa (Clinostomum complanatum, 
Posthodiplostomum minimum, Tylodelphis sp., Eustrongylides sp. 
and Polymorphus brevis) were larvae. The taxa S. sogandaresi, 
Tylodelphis sp., and R. lichtenfelsi reached the highest levels of 
prevalence and mean abundance among all hosts, while the ces- 
todes B. acheilognathi and Caryophillidae gen. sp. showed the 
lowest values. This study contributes with the inventory of the 
freshwater fish helminth fauna in Central Mexico Plateau, and 
particularly with the previous work that has been done with Goo- 
deinae, a subfamily of freshwater fishes endemic to that part of 
the country. 
Key words: Central Mexico Plateau, Goodeinae, helminth para- 
sites. 
RESUMEN 
En este trabajo se registran 11 taxa de helmintos endoparásitos 
de 7 especies de peces de la subfamilia Goodeinae del lago de 
Zacapu, Michoacán, en la mesa central de México. Seis taxa se 
registraron en estado adulto (Margotrema cf. bravoae, Phyllodis- 
tomum sp., Saccocoelioides sogandaresi, Rhabdochona lichten- 
felsi, Bothriocephalus acheilognathi y Caryophillidae gen. sp.), en 
tanto que los 5 restantes correspondieron a larvas (Clinostomum 
complanatum, Posthodiplostomum minimum, Tylodelphys sp. 
y Eustrongylides sp. y Polymorphus brevis). Los taxa S. sogan- 
daresi, Tylodelphis sp. y R. lichtenfelsí presentaron los valores 
más altos de prevalencia y abundancia en los peces estudiados, 
mientras que los céstodos B. acheilognathi y Caryophillidae gen. 
sp. presentaron los valores más bajos. Este estudio contribuye al 
inventario de la fauna helmintológica de peces de agua dulce de 
la mesa central de México y en particular al que ha sido realizado 
con Goodeinae, una subfamilia de peces dulceacuícolas endémi- 
ca de esa parte del territorio nacional. 
Palabras clave: Mesa central de México, Goodeinae, helmintos 
parásitos. 
Goodeinae (Cyprinodontiformes: Goodeidae) represents a sub- 
family of viviparous freshwater fishes, which comprises 20 genera 
and 43 species, entirely endemic to river drainages and basins of 
central Mexico (Domínguez-Domínguez et al., 2012). The helminth 
fauna parasitizing these freshwater fishes has been intensively 
documented during the lasttwo decades. Some papers have ad- 
dressed the helminth assemblage in one single species of host
 34 
 
 
(i.e., Martínez-Aquino et al, 2004, 2007b, 2009; Sánchez-Nava et 
al, 2004), while some others described the helminth fauna of three 
or more goodein species within the same locality (e.g., Peresbar- 
bosa-Rojas et al, 1994; Pérez-Ponce de León et al, 2000; Mejía- 
Madrid et al, 2005; Romero-Tejeda et al., 2008). 
Zacapu Lake, located in Central Mexico Plateau, in the 
state of Michoacán, is a medium-size water body fed by sever- 
al springs, which shows a relatively low level of environmental 
degradation, and serves as habitat for diverse freshwater taxa. 
Because of this, it has been argued that this area is important 
from a conservational point of view (Medina-Nava et al, 2005; 
Domínguez-Domínguez et al., 2006; Martínez-Aquino et al, 2007a). 
The freshwater fish fauna of the lake includes 7 goodein species 
of which 6 have been partially studied for helminth parasites (Gali- 
cia-Guerrero, 2001; Pérez-Ponce de León, 2001; Mejía-Madrid et 
al, 2005). The aim of this work is to record the endohelminth para- 
site fauna of all the species of goodeins inhabiting Zacapu Lake, 
and provide the ecological infection parameters, such as preva- 
lence and abundance. 
On July 2009, a total of 161 adult specimens of goodeins 
belonging to the species Alloophorus robustus (Bean, 1892) (n 
= 17), Allotoca zacapuensis Meyer, Radda € Domínguez-Domín- 
guez, 2001 (n = 32), Goodea atripinnis Jordan, 1880 (n = 20), Hubb- 
sina turneri de Buen, 1940 (n = 20), Skiffia lermae Meek, 1902 (n 
= 19), Xenotoca variata (Bean, 1887) (n = 21), and Zoogoneticus 
quitzeoensis (Bean, 1898) (n = 32), were collected in Zacapu Lake 
(19%4935" N; 1014710” W), using seine nets and electrofishing. 
Fishes were taken alive to the laboratory, sacrificed by pithing, 
and individually examined for endohelminth parasites. After dis- 
section, gastrointestinal tract was removed and placed in a Petri 
dish with 0.65% saline. Other organs (eyes, liver, spleen, gall, swim 
and urinary bladders), and body cavity, were examined under a 
stereomicroscope in separate Petri dishes with saline 0.65%. Di- 
geneans, nematodes and cestodes were fixed with 4% (steaming) 
formalin. Acanthocephalans were placed during 24 hrs in distilled 
water at 4”C, and preserved in absolute ethanol. Plathyhelminths 
and acanthocephalans were stained with Mayers paracarmine. 
Nematodes were cleared with glycerin for light microscopy study. 
Voucher specimens of all taxa were deposited in the Colección 
Nacional de Helmintos (CNHE), Instituto de Biología, Universidad 
Nacional Autónoma de México, Mexico City. The use of preva- 
lence (% infected), and abundance (mean number of parasites of 
a single species in the sample) follows Bush et al. (1997). 
In total, 11 endohelminth parasite taxa were collected from 
the 7 analyzed host species. The endohelminth fauna includes 6 
taxa of digeneans (3 adults and 3 larval stages), 2 adult cestodes, 
2 nematodes (1 adult and 1 larvae), and 1 acanthocephalan (cys- 
tacanth). Rhabdochona lichtenfelsiSánchez-Álvarez, García-Prie- 
to € Pérez-Ponce de León, 1998, Tylodelphys sp., and Polymor- 
phus brevis (Van Cleave, 1916), were the most widely distributed 
Notas 
taxa among the host species. The adult nematode A. lichtenfelsi 
reached the highest levels of prevalence and mean abundance. 
Allotoca zacapuensis harbored 7 endohelminth taxa, whereas 
the remaining fish hosts were parasitized by 4-5 endohelminth 
taxa. Endohelminth parasite taxa, prevalence and abundance, as 
well as the new host and locality records herein established are 
shoven in Table 1. 
Four endohelminth taxa are reported in Zacapu Lake for the 
first time, and in addition to that, 21 new host records are estab- 
lished in this paper. The endohelminth fauna of Skiffia lermae ¡is 
reported for the first time, meanwhile for the goodeins Allotoca 
zacapuensis, Hubssina turneri, and Zoogoneticus quitezeoensis, 
the known endohelminth parasite fauna was duplicated with 
respect to previous records. Our study brings the total number 
of helminth parasites of goodeins in Zacapu Lake to 18 (Galicia- 
Guerrero, 2001; Pérez-Ponce de León, 2001; Mejía-Madrid et al, 
2005). Additionally, with 64.3% of the fish fauna studied thus far 
for helminth parasites, our data increase the knowledge about the 
freshwater fish parasite fauna of this locality in 30%. 
The endohelminth fauna of goodeins in Zacapu Lake include 
at least 2 species which have been considered as specialists to 
Goodeinae, ¡.e., Margotrema cf. bravoae Lamothe-Argumedo, 
1970, and Rhabdochona lichtenfelsi (Pérez-Ponce de León ef 
al., 2000; Mejía-Madrid et al, 2005, 2007; Pérez-Ponce de León 4 
Choudhury, 2005). The adult digenean Phyllodistomum sp., could 
represent a third specialist species; however, this need to be de- 
termined once the taxonomic identity ofthe species is established. 
Morphologically similar specimens were recently recorded in the 
goodein fish Zoogoneticus purhepechus Domínguez-Domínguez, 
Pérez-Rodríguez et Doadrio, 2008 from a relatively close locality 
in the lower Lerma River (Martínez-Aquino et al., 2011). These 
specimens, along with those reported as Dendrorchis sp. by Mar- 
tínez-Aquino et al. (2009) have been only recorded in goodeins in 
central Mexico and may be conspecific. Moreover, they could 
represent a new species; although until additional taxonomic 
work based on morphology and molecular markers is carried out, 
their identities remain uncertain. In contrast, 8 generalist helminth 
taxa were recorded in the analyzed hosts both as adult or larval 
stages: Saccocoelioides sogandaresí Lumsden, 1963, Clinosto- 
mum complanatum (Rudolphi, 1819), Posthodiplostomum mini- 
mum (MacCallum, 1921), Tylodelphys sp., Bothriocephalus achei- 
lognathi Yamaguti, 1934, Caryophyllidae gen. sp., Eustrongylides 
sp., and PF. brevis. 
For this survey, specimens were collected only in one period 
during the year, preventing us from establishing a robust com- 
parison of the parasite fauna among analyzed species of hosts, 
or even between the records we establish in this work, and those 
previously made for other authors. However, our data correspond 
with the general pattern described for most species of freshwater 
fishes occurring in different river basins in central Mexico, ¡.e., a 
Hidrobiológica
 35 
 
 
 
3
6
  
 
Y 
species-poor helminth fauna, highly dominated by one species of 
helminth (Pérez-Ponce de León et al, 2000). In particular, ecologi- 
cal parameters of the parasitic infections herein reported coin- 
cide with those previously reported for other species of goodeins, 
¡.e., the nematode Ahabdochona lichtenfelsís, as well as larval 
digeneans reach the highest prevalence and abundance values 
(Martínez-Aquino et a/., 2004, 2007b; Romero- Tejeda et al., 2008), 
The results we provide in this paper contribute to our un- 
derstanding of the helminth parasite fauna of goodeins in Central 
Mexico Plateau, but also further contribute with the inventory of 
the Mexican freshwater fish parasite fauna. 
ACKNOWLEDGEMENTS 
We thank the local people of Zacapu for providing access to 
Zacapu Lake, particularly we are gratefull with those in charge 
of "Balneario La Angostura” for access to the type locality of 
Allotoca zacapuensis. We appreciate the valuable comments of 
reviewers. A.M.A., R.P.R., L.G.0., and D.I.H.M. thank to CONACyT 
for the scholarship received to complete their graduate programs 
within the Posgrado en Ciencias Biológicas, UNAM. This work 
was partially supported by grants from the Consejo Nacional de 
Ciencia y Tecnología (CONACyT 83043), and Programa de Apoyo 
a Proyectos de Investigación e Innovación Tecnológica (PAPIIT- 
UNAM IN 209608 and IN202111) to G.P.P.L. 
REFERENCES 
Bush, A. 0., K. D. LarrERTY, L. L. Lorz 8 A. W. SHosTAKk. 1997. Parasitology 
meets ecology on its own terms: Margolis et al., revisited. Journal of 
Parasitology 83 (4): 575-583. 
Domíncuez-Domínuez, O., E. MARTÍNEZ-Mever, L. ZAMBRANO 8 G. PÉREZ- 
Ponce DE León. 2006. Using ecological-niche modeling as a conser- 
vation tool for freshwater species: live-bearing fishes in Central 
Mexico. Conservation Biology 20 (6): 1730-1739. 
Domincuez-DomínGuEz, O., C, PEDRAZA-LARA, N. GURROLA-SÁNCHEZ, R. PÉREZ- 
Robrícuez, |. ISRADE-ALCÁNTARA, V. H. GARDUÑO-Monroy, l. Doabrlo, G. 
PérEz-Ponce DE LEÓN él D. R. Brooks, 2012. Historical biogeography of 
the Goodeinae (Cyprinodontiforms). /n: Uribe-Aranzabal, M. C. 8 H. 
Grier (Eds.). Viviparous Fishes Vol II. New Life Publications, Home- 
stead, pp. 13-30. 
GALICIA-GUERRERO, S. 2001. Helmintos parásitos de algunas especies de 
peces en el Lago de Zacapu, Michoacán. Tesis de Maestría, Facul- 
tad de Ciencias, UNAM, México. 127 p. 
MARTÍNEZ-ÁQUINO, Á., G. SALGADO-MALDONADO, R. AGUILAR-ÁGUILAR, G. CABA- 
Ñas-CARRANZA QM. P. ORTEGA-OLIVARES. 2004. Helminth parasites of 
Chapalichthys encaustus (Pisces: Goodeidae), an endemic freshwa- 
ter fish from Lake Chapala, Jalisco, Mexico. Journal of Parasitology 
90 (4): 889-890. 
MAaRTÍNEZ-ÁQUINO, Á., R. AGUILAR-ÁGUILAR, H. O. SANTA ÁNNA DEL CONDE- 
JUÁREZ € R. CONTRERAS-MEDINA. 2007a. Empleo de herramientas pan- 
Notas 
biogeográficas para detectar áreas para conservar: un ejemplo con 
taxones dulceacuícolas. lr Luna, l., J. J. Morrone 8 D. Espinosa 
(Eds.). Biodiversidad de la Faja Volcánica Transmexicana. Facultad 
de Ciencias, Universidad Nacional Autónoma de México. México, 
D. F., pp. 449-460. 
MARTÍNEZ-ÁQUINO, Á., G. SALGADO-MALDONADO, R. AGUILAR-ÁGUILAR, G. CABA- 
Ñas-CARRANZA él C. A. MenDOZA-PALMERO. 2007b. Helminth parasite 
communities of Characodon audax and C. lateralis (Pisces: Goodei- 
dae), endemic freshwater fishes from Durango, Mexico. The South- 
western Naturalist52 (1): 125-130. 
MARrTÍNEZ-ÁQUINO, A., R. AGUILAR-AGUILAR, R. PérEz-RooríGuEz 8 G. PÉREZ- 
Ponce DE León. 2009. Helminth parasites of Xenotaenía resolanae 
(Osteichthyes: Cyprinodontiformes: Goodeidae) from the Cuzalapa 
Hydrological System, Jalisco, Mexico. Journal of Parasitology 95 (5): 
1221-1223. 
MARTÍNEZ-ÁQUINO, A., D. |. HerNÁNDEZ-MENA, R. PÉREz-RoDRÍGUEZ, R. ÁGUILAR- 
AGuILAR 8 G. Pérez-Ponce DE León. 2011. Endohelminth parasites ofthe 
freshwater fish Zoogoneticus purhepechus (Cyprinodontiformes: 
Goodeidae) from two springs in the lower Lerma River, Mexico. Re- 
vista Mexicana de Biodiversidad 82 (4): 1132-1137. 
Menina-Nava, M., J. Lyons, T. ZuBiera-RoJas, E. SOLORIO-ORNELAS, y. P. 
Ramírez-HeRREJÓN 8 R. GaLván-MoraLes, 2005. Conservation of two 
sites in Central Mexico with a high diversity of livebearing fishes. /n: 
Uribe, M. C. 8 H. Grier (Eds.). Viviparous Fishes, New Life Publica- 
tions. Homestead, pp. 499-504, 
MeJía-MabriD, H., O. DomíncuEZ-DOMÍNGUEZ él G. PÉREZ-PONCE DE León. 2005, 
Adult endohelminth parasites of Goodeinae (Cyprinodontiformes: 
Goodeidae) from Mexico with biogeographical considerations. Com- 
parative Parasitology 72 (2): 200-211. 
MeJía-Mabrio, H., E. Váquez-DomínGuEz €: G. Pérez Ponce DE Léon. 2007. 
Phylogeography and freshwater basins in central Mexico: recent 
history as revealed by the fish parasite Rhabdochona lichtenfelsi 
(Nematoda). Journal of Biogeography 34: 787-801. 
PERESBARBOSA-ROJAS, E., G. PÉREZ-PONCE DE LEÓN $, L. GARCÍA-PRIETO. 1994, 
Helmintos parásitos de tres especies de peces (Goodeidae) del lago 
de Pátzcuaro, Michoacán. Anales del Instituto de Biología, Universi- 
dad Nacional Autónoma de México, Serie Zoología 65 (1): 201-204, 
PEREZ-PONCE DE LEÓN, G. 2001. Margotrema guillerminae n. sp. (Trematoda: 
Macroderoididea) from two species of freshwater fishes in Lake 
Zacapu. Michoacan state, Mexico, and new records of Margotrema 
bravoae Lamothe, 1970. Journal of Parasitology 87 (5): 1112-1114, 
Pérez-PoNcE DE LEÓN, G., L. GARcÍA-PrIiETO, V. LEÓN-REGAGNON € A. CHOUD- 
HURY. 2000. Helminth communities of native and introduced fishes in 
Lake Pátzcuaro, Michoacán, Mexico. Journal of Fish Biology 51 (2): 
303-352. 
PérEz-PoNCcE DE LEÓN, G. 8: A. CHouDHURY. 2005. Biogeography of helminth 
parasites of freshwater fishes in Mexico: the search for patterns and 
processes. Journal of Biogeography 32: 645-659. 
Hidrobiológica
 37 
 
 
Notas 
ROMERO-TEJEDA, M. L., L. GARCÍA-PRIETO, L. GARRIDO-OLVERA 8 G. PÉREZ-PONCE 
DE LEÓN. 2008. Estimation of the endohelminth parasite species rich- 
ness in freshwater fishes from La Mintzita reservoir, Michoacán, 
Mexico. Journal of Parasitology 94 (1): 288-292. 
SáncHEz-Nava, P., G. SALGADO-MALDONADO, E. SOTO-GALERA 4 B. JAIMES- 
Cruz. 2004. Helminth parasites of Girardinichthys multiradiatus (Pi- 
Vol. 22 No. 1 + 2012 
Y 
sces: Goodeidae) in the upper Lerma River sub-basin, Mexico. Para- 
sitology Research 93 (5): 396-402. 
Recibido: 15 de abril de 2011. 
Aceptado: 19 de septiembre de 2011.
 38 
 
 
 39 
 
 
 
 
 
 
 
 
 
 
5) A NEW SPECIES OF MARGOTREMA (DIGENEA, ALLOCREADIIDAE) FROM THE LEOPARD 
SPLITFIN XENOTAENIA RESOLANAE (CYPRINODONTIFORMES, GOODEIDAE)  
FROM WEST-CENTRAL MEXICO 
 
 
 
 
 
 
 
 
 
 
 
 
 
 40 
 
94   Accepted by Norman Dronen: 17 May 2013; published: 11 Jun. 2013 
ZOOTAXA
ISSN 1175-5326  (print edition)
ISSN 1175-5334 (online edition)Copyright © 2013 Magnolia Press
Zootaxa 3670 (1): 094–096 
www.mapress.com/zootaxa/ Correspondence
http://dx.doi.org/10.11646/zootaxa.3670.1.10
http://zoobank.org/urn:lsid:zoobank.org:pub:7C2432D5-2C54-4426-B181-C52D9FA78C05
A new species of Margotrema (Digenea, Allocreadiidae) from the leopard 
splitfin Xenotaenia resolanae (Cyprinodontiformes, Goodeidae) 
from west-central Mexico 
GERARDO PÉREZ-PONCE DE LEÓN1, ANDRÉS MARTÍNEZ-AQUINO1, 2 & BERENIT MENDOZA-GARFIAS1
1Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México (UNAM), Ap. Postal 70-153 C.P. 
04510, México D.F., México
2Posgrado en Ciencias Biológicas, UNAM, C.P. 04360, México. D.F.  E-mail: ppdleon@ibiologia.unam.mx
A new species of Margotrema is herein described from the intestine of the freshwater fish Xenotaenia resolanae from the 
Cuzalapa River, Jalisco State, on the Pacific slope of west-central Mexico. The new species was first recognized after a 
molecular phylogenetic analysis which explored the genetic variation at the intraspecific level of Margotrema spp across 
central Mexico. Sequences of mitochondrial (COI) and nuclear (ITS1) genes were obtained for 125 individuals, and a 
general mixed Yule-coalescent analysis (GMYC) for species delimitation of both genes allowed the recognition of an 
independent evolutionary lineage, representing an undescribed species of Margotrema. Detailed morphological 
observations allowed the species description. The new species is easily distinguished from the other valid species of the 
genus, M. bravoae, by having vitelline follicles restricted to the region between the pharynx and the ventral sucker a 
wider and more prominent ventral sucker, larger eggs, and symmetrical testes.
 The genus Margotrema included two species, M. bravoae Lamothe-Argumedo, 1970, from the goodeid 
Girardinichthys multiradiatus Meek from La Lagunilla, Estado de México (Lamothe-Argumedo 1970), and M. 
guillerminae Pérez-Ponce de León, 2001 from the cyprinid Notropis calientis Jordan and Snyder, and the goodeid 
Alloophorus robustus (Bean) from Lake Zacapu, Michoacán (Pérez-Ponce de León 2001). These species were 
distinguished mainly on the basis of relative length of cecae. While exploring the genetic diversity of Margotrema spp. in 
their goodeid hosts across central Mexico (in 15 localities representing seven hydrological systems), Martínez-Aquino et 
al. (2013) found evidence to synonymize M. guillerminae with the type-species, M. bravoae, and to recognize an 
independent genetic lineage (Lineage I), parasitizing the endemic goodeid Xenotaenia resolanae in the Cuzalapa river, a 
tributary of the Marabasco River Basin. The helminth fauna of X. resolanae had been studied by Martínez-Aquino et al.
(2009); the species of Margotrema was erroneously determined as M. guillerminae based on the extension of the ceca 
along body, a character that results from intraspecific morphological variability and is not reliable, in these digeneans, as 
a taxonomically important trait to distinguish species. After the molecular analyses, a closer look at the morphology of 
specimens (museum and freshly collected material) was then undertaken for specimens allocated to Lineage I, 
concluding it represented a new species. We describe the new species in this paper.
Specimens were stained with Mayer´s paracarmine and Gomori´s thrichorome, mounted as permanent slides using 
Canada balsam and deposited at the CNHE (Colección Nacional de Helmintos). For SEM study, specimens were post 
fixed in 1 % OsO4 for 1 hr, dehydrated through a graded series of ethyl alcohol and then critical point dryied with CO2. 
Specimens were mounted on metal stubs, coated with gold, and examined in a Hitachi Stereoscan Model S-2469N at 15 
kV. Measurements are presented in micrometers, as range followed by the average and standard deviation in parentheses. 
Margotrema resolanae n. sp. 
(Fig. 1A–C)
Host. Xenotaenia resolanae Meek. 
Locality. Cuzalapa River, Jalisco State, west-central Mexico. 19°30’32.1” N, 104°17’45.6” W. 
Specimens deposition. CNHE, Holotype 6868, paratypes 6869; CNHE 6880.
Etymology. This species in named after the host species (Xenotaenia resolanae) to which the digenean exhibits a 
strong host-specificity.
 41 
 
 Zootaxa 3670 (1)  © 2013 Magnolia Press  ·  95MARGOTREMA RESOLANAE N. SP. FROM MEXICO
FIGURE 1. Margotrema resolanae n. sp., A. Line drawing of Holotype, ventral view. Scale Bar 200µm. B. Scanning Electron 
Microscopy micrograph of body. Scale Bar 50 µm, and C. Detail of the oral sucker showing the distribution of 11 dome-like 
papillae. Scale Bar 50 µm.
Description. Based on measurements of 14 specimens. Body elongate, unspined, with scattered eyespot remnants 
384–925 (595±135) long, maximum width attained at level of ventral sucker 167–481 (277±71). Oral sucker subterminal 
95–143 (114±15) long by 100–133 (115±10) wide. Scanning Electron Microscopy (SEM) micrograph of the oral sucker 
shows a pattern of 11 dome-like papillae, 4 anterior, 4 lateral (2 on each side), and 3 posterior (Fig. 1C). Mouth 36–77 
(56±12) long, 50–88 (66±12) wide. Prepharynx absent. Pharynx 32-59 (43 ± 8) long, 31-59 (44±7) wide. Esophagus 
relatively short, 46-101 (63 ± 16, n = 6) long. Cecal bifurcation at 156-308 (215±45) from anterior end. Short ceca 
extending posteriorly to surpass the posterior end of ventral sucker; in some specimens ceca extend into the anterior 
testis. Ventral sucker wide, very well-developed, located in equatorial area or slightly in posterior third of body 110–230 
(156±34) long, 146–296 (216±37) wide, with a pattern of 6 dome-like papillae, 4 lateral (2 on each side), 1 anterior, 1 
 42 
 
PÉREZ-PONCE DE LEÓN ET AL.96  ·  Zootaxa 3670 (1)  © 2013 Magnolia Press
posterior (Fig. 1B); average oral sucker/ventral sucker ratio 1:1.37 (length), 1: 1.88 (width). Testes relatively small, 
symmetrical (oblique in few specimens), subspherical. Anterior testis 34–99 (63±17) long, 35–85 (59±13) wide. 
Posterior testis 27–108 (62±21) long, 40–77 (64±12) wide. Cirrus sac straight, dorsal to ventral sucker 107–216 
(151±42) long, containing bipartite seminal vesicle and short cirrus. Genital atrium poorly developed. Genital pore 
anterior to cecal bifurcation, at esophagus level 143–261 (200±39) from anterior end of body. Ovary pretesticular, 
relativelly small, subspherical, dextral 24–60 (39±11) long, 49–91 (67±12) wide. Seminal receptacle immediately 
postovarian. Vitelline reservoir, Laurer´s canal, and Mehlis’ gland not observed because the large number of eggs in 
uterine loops. Vitellarium follicular; vitelline follicles in two lateral fields in anterior end of body, extending mostly 
between pharynx and anterior margin of ventral sucker or slightly surpassing in some specimens. Uterus highly coiled, 
occupying most of posterior half of body, ascending sinuously between testes, forming a short metraterm to reach genital 
atrium dorsally to ventral sucker. Eggs large, embryonated 50–79 (67±7, n = 10) long, 25–47 (35±5, n = 10) wide. 
Excretory vesicle tubular reaching testes level. 
Remarks. The new species closely resembles M. bravoae in general morphology of the body however, M. resolanae
n. sp. may be easily distinguished from the type species by possesing vitelline follicles restricted to the region between 
the pharynx and the anterior end of ventral sucker. In contrast, M. bravoae has vitelline follicles extending from the 
pharynx level posteriorly to ovary, surpassing ventral sucker. Additionally, the new species posseses a wider and more 
prominent ventral sucker, larger eggs (measuring 67 by 35 compared with 48 by 33) and symmetrical testes. The new 
species exhibits a close phylogenetic and biogeographical association with the host species, and can be regarded as a 
member of the helminth parasite core fauna of Xenotaenia resolanae (sensu Pérez-Ponce de León & Choudhury 2005). 
The description we present herein corroborates that a DNA-based taxonomic approach is necessary to uncover 
previously unrecognized biodiversity, greatly enhancing our chances to complete the inventory of the freshwater fish 
parasite fauna in Mexico (Pérez-Ponce de León & Choudhury 2010). The record of Martinez-Aquino et al (2009) of M. 
guillerminae as a parasite of X. resolanae should then be referred as the new species we described in this paper. The 
generic diagnosis should be amended to include the following traits: Vitelline follicles restricted, extending between 
ovary and pharynx; postovarian testes, oblique or symmetrical; intestinal ceca short (extending to the ventral sucker 
region), or long (extending to surpass the testes). 
We thank Rogelio Aguilar and Rodolfo Pérez for their help during field-work. AMA thanks the Consejo Nacional de 
Ciencia y Tecnología (CONACyT) for the scholarship granted for his PhD program. This work was supported by a grant 
from the Program PAPIIT-UNAM No. IN-202111. 
References
Lamothe-Argumedo, R. (1970) Tremátodos de peces VI. Margotrema bravoae gen. nov. sp. nov. (Trematoda: 
Allocreadiidae), parásito de Lermichthys multiradiatus Meek. Anales del Instituto de Biología de la Universidad 
Nacional Autónoma de México, Serie Zoología, 41, 87–92.
Martínez-Aquino, A., Aguilar-Aguilar, R., Pérez-Rodríguez, R. & Pérez-Ponce de León, G. (2009) Helminth parasites of 
Xenotaenia resolanae (Osteichthyes: Cyprinodontiformes: Goodeidae) from the Cuzalapa hydrological system, 
Jalisco, Mexico. Journal of Parasitology, 95, 1221–1223.  
http://dx.doi.org/10.1645/ge-1925.1
Martínez-Aquino, A., Ceccarelli, F.S. & Pérez-Ponce de León, G. (2013) Molecular phylogeny of the genus Margotrema
(Digenea: Allocreadiidae), parasitic flatworms of goodeid freshwater fishes across central Mexico: species 
boundaries, host-specificity, and geographical congruence. Zoological Journal of the Linnean Society, 168,1–16.  
http://dx.doi.org/10.1111/zoj.12027
Pérez-Ponce de León, G. (2001) Margotrema guillerminae n. sp. (Trematoda: Macroderoididae) from two species of 
freshwaters fishes in Lake Zacapu, Michoacan state, Mexico, and new records of Margotrema bravoae Lamothe, 
1970. Journal of Parasitology, 87, 1112–1114. 
http://dx.doi.org/10.1645/0022-3395(2001)087[1112:mgnstm]2.0.co;2
Pérez-Ponce de León, G. & Choudhury, A. (2005) Biogeography of helminth parasites of freshwater fishes in Mexico: 
the research for patterns and processes. Journal of Biogeography, 32, 645–649.  
http://dx.doi.org/10.1111/j.1365-2699.2005.01218.x
Pérez-Ponce de León, G. & Choudhury, A. (2010) Parasites inventories and DNA-based taxonomy: lessons from 
helminths of freshwater fishes in a megadiverse country. Journal of Parasitology, 96, 236–244.  
http://dx.doi.org/10.1645/ge-2239.1
 43 
 
 
 
 
 
 
 
 
 
 
6) COMPOSICIÓN TAXONÓMICA DE HELMINTOS PARÁSITOS DE GOODEINAE 
(OSTEICHTHYES:  CYPRINODONTIFORMES: GOODEIDAE) EN MÉXICO 
 
 
 
 
 
 
 
 
 
 44 
Manuscrito para ser sometido para su publicación en una revista arbitrada e indizada (ISI / 
SCI). 
Articulo en extenso 
Martínez-Aquino et al.- Helmintos parásitos de Goodeinae 
 
Composición taxonómica de helmintos parásitos de Goodeinae (Osteichthys: 
Cyprinodontiformes: Goodeidae) en México 
 
ANDRÉS MARTÍNEZ-AQUINO1,2*, CARLOS A. MENDOZA-PALMERO3, ROGELIO 
AGUILAR-AGUILAR4 and GERARDO PÉREZ-PONCE DE LEÓN1 
 
1Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, 
Apartado Postal 70-153, Ciudad Universitaria, México, D.F., México.   
2Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Av. Ciudad 
Universitaria 3000, C.P. 04360, Coyoacán, Distrito Federal, México. 
3Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, and 
Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Bude˘ějovice, 
Czech Republic. 
4Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional 
Autónoma de México, Apdo. Postal 70-374, C. P. 04510 México D.F., Mexico. 
Correspondencia. E-m maandres@ibiologia.unam.mx.  Teléfono. +52 55 56 22 82 22 Ext. 47 86 
9.  Fax. +52 55 55 50 01 64. 
 
 45 
Resumen. Este estudio es un inventario helmintológico actualizado que representa la 
composición taxonómica de helmintos parásitos para Goodeinae en el centro de México. El 
registro helmintológico incluye 19 taxones de digéneos (11 adultos y ocho metacercarias), siete 
de monogéneos, 12 de céstodos (tres adultos y nueve metacéstodos), 15 de nemátodos (ocho 
adultos y siete larvas) y dos de acantocéfalos (un adulto y un cistacanto). Se observa un 
predominio de digéneos, nemátodos y céstodos, respectivamente, así como una escasez de 
acantocéfalos y un numero relativamente bajo de monógenos. El número de taxones encontrados 
en estadios adultos (29 taxones, 55%) es ligeramente mayor que el de larvas (25 taxones, 45%). 
Existe un mayor número de taxones autogénicos (35 taxones, 64%) que alogénicos (20 taxones, 
36%). Margotrema bravoae, M. resolanae, Phyllodistomum sp., Saccocoeloides sp., 
Gyrodactylus lamothei, G. mexicanus, Gyrodactylus  sp. 1, Gyrodactylus  sp. 2, Rhabdochona 
ahuehuellensis y R. lichtenfelsi son taxones endémicos del centro de México y especialistas de la 
subfamilia Goodeinae. El dígeneo Centrocestus formosanus, el monogéneo G. cf. elegans, el 
nemátodo Pseudocapillaria tomentosa y el céstodo Bothriocephalus acheilognathi son especies 
introducidas a la región. Se reconocen dos características de la helmintofauna de goodeinos: 1) un 
predominio de digéneos, nemátodos y céstodos; 2) un mayor número de especies autogénicas. La 
segunda característica refleja una estrecha relación evolutiva durante el proceso de 
diversificación de los helmintos asociados a la ictiofauna dulceacuícola mexicana (i.e. faunas 
principales), asociada a Goodeinae. En total, como resultado del trabajo de muestreo realizado en 
los últimos 5 años se presentan 112 nuevos registros de helmintos, e incluyen 23 taxones de 
helmintos parásitos asociados a 28 especies de goodeinos, de las cuales seis son nuevos para este 
grupo de peces. Este inventario representa al grupo de vertebrados – Goodeinane – mejor 
estudiado en términos helmintoparasitofaunísticos para México, lo que permitirá a especialistas 
de distintas áreas integrar y expandir interpretaciones acerca de la biodiversidad parasitaria de 
México. 
Introducción 
La subfamilia Goodeinae (Osteichthyes: Cyprinodontiformes: Goodeidae), sin duda, es el grupo 
de vertebrados en México con el mayor número de trabajos donde se describe la fauna 
helmintológica que los parasita. Los estudios de la última década reconocen que de las 42 
especies que se incluyen actualmente en este grupo de peces dulceacuícolas, 33 de ellas cuentan 
 46 
con registros helmintológicos. Esto representa al 80% de esta subfamilia, por lo que Goodeinae, 
junto con Cichlidae e Ictaluridae, forma parte de los tres grupos de peces dulceacuícolas mejor 
estudiados en México en términos helmintológicos (Pérez-Ponce de León & Choudhury, 2010). 
Los trabajos publicados sobre la helmintofauna de goodeinos consisten en cinco categorías: 1) 
Registros esporádicos o aislados para la descripción de la helmintofauna (v. gr. Lamothe-
Argumedo & Cruz-Reyes, 1972; García-Prieto & Osorio-Sarabia, 1991; Guzmán-Cornejo & 
García-Prieto, 1999; Scholz & Salgado-Maldonado, 2000, 2001; Salgado-Maldonado & Pineda-
López, 2003; Alcántar-Escalera et al., 2013). 2) Registros derivados de inventarios 
helminofaunísticos para sistemas hidrológicos particulares (v. gr., Salgado-Maldonado et al., 
2001a; 2001b; 2004a; 2004b; Salgado-Maldonado, 2006; Pérez-Ponce de León et al., 2009). 3) 
Registros sistematizados en los que se estudia la ecología de comunidades en especies 
particulares de goodeinos (v. gr. Peresbarbosa-Rojas et al., 1994; Pérez-Ponce de León et al., 
2000; Sánchez-Nava et al., 2004; Mejía-Madrid et al., 2005; Mendoza-Palmero et al., 2007; 
Romero-Tejeda et al., 2008; Martínez-Aquino et al., 2004, 2007b, 2009a, 2011, 2012). 4) 
Descripciones taxonómicas (v. gr. Lamothe-Argumedo, 1970; Sánchez-Alvárez et al., 1998; 
Pérez-Ponce de León, 2001; Mejía-Madrid & Pérez-Ponce de León, 2003; Mendoza Palmero et 
al., 2009; Pérez-Ponce de León et al., 2013). 5) Interpretaciones evolutivas entre asociaciones 
Goodeinae-faunas principales (v. gr., Mejía-Madrid et al., 2007b; Martínez-Aquino et al., 2013).  
En sumatoria, de las 204 especies de peces dulceacuícolas de México que cuentan con 
registros para taxones de helmintos parásitos (Pérez-Ponce de León & Choudhury, 2010), las 
cinco categorías anteriormente mencionadas representan el 16% del conocimiento de la 
helmintofauna mexicana generada hasta el momento. Sin embargo, solo existen dos inventarios 
de taxones de helmintos parásitos para goodeinos: 1) Mejía-Madrid et al. (2005), donde 
presentan un listado de los helmintos en estadio adulto en él categorizan su composición 
taxonómica y realizan comentarios empírico-biogeográficos para infierir posibles procesos 
evolutivos entre Goodeinae y sus faunas principales (sensu Pérez-Ponce de León & Choudhury, 
2005). 2) Pineda-López et al., (2005: 462), intentaron usar los registros de helmintos tanto en 
estadios larvarios como de adultos para inferir historias evolutivas de tipo Goodeinae-faunas 
principales. Desafortunadamente, esos autores tuvieron una gran confusión al apoyar sus 
inferencias usando la historia evolutiva de peces no goodeinos, sino mas bien con aquellos del 
género Chirostoma (Atheriniformes), lo que vuelve aún más débiles sus especulaciones. En otro 
 47 
contexto, Mejía-Madrid et al. (2007b) y Martínez-Aquino et al. (2013), han logrado integrar la 
historia evolutiva de los goodeinos con la de sus helmintos parásitos e interpretarla sobre la 
historia hidrogeomorfológica del centro de México con base en evidencia morfológica, 
molecular, biogeográfica, genealógica y filogenética. Estos autores resaltan la importancia de 
generar una basta cantidad de información referente al área de distribución de los taxones de 
helmintos a usar como modelo de estudio para postular inferencias evolutivas entre asociaciones 
de tipo huésped-parásito. El área de distribución de una especie se define como el área que ocupa 
(Rapoport, 1975). Se determina a partir de las localidades donde se ha registrado, entendiendo 
por localidad de registro tanto su descripción de localización y coordenadas geográficas, como 
sus atributos de hábitat. En este contexto, contar con toda la información generada, publicada, 
actualizada, organizada de manera sistematizada y colocarla en documentos de acceso libre para 
la comunidad científica permite integrar e interpretar los procesos y patrones que ocurren en la 
biodiversidad de parásitos. Por tanto, el objetivo de este trabajo es recabar toda la información 
bibliográfica especializada y publicada para helmintos parásitos de peces de la subfamilia 
Goodeinae, así como aportar datos originales de nuestros propios muestreos, para elaborar un 
inventario actualizado que permita describir su composición taxonómica a modo de describir 
patrones de diversidad de la fauna parasitaria en el centro de México. 
Materiales y métodos  
Recolecta de huéspedes y de helmintos parásitos 
Entre agosto de 2008 y julio de 2010 se realizaron siete muestreos en 57 localidades ubicadas en 
siete sistemas hidrológicos del centro de México; Río San Pedro Mezquital, Río Ameca, Río 
Ayuquila, Río Coahuayana, Río Lerma, Río Cuzalapa y Río Balsas. En total se examinaron 1632 
peces de 28 especies de goodeinos (Apéndice 1). 
Los peces fueron recolectados con un chinchorro de 3 m de longitud y ½ pulgada de luz 
de malla, con equipo de electropesca de corriente directa y con trampas tipo nazas; se 
transportaron vivos al laboratorio para su examen helmintológico, el cuál se realizó dentro de las 
24 horas posteriores a su captura. La determinación taxonómica de cada uno de los huéspedes fue 
apoyada con base en claves taxonómicas directamente en el campo (Miller et al., 2005), y 
verificada posteriormente por especialistas con base en datos moleculares (v.gr. Pérez-Rodríguez 
et al., sometido). 
 48 
La obtención de helmintos se realizó mediante un examen general de los peces con 
microscopio estereoscópico. El examen externo incluyó la superficie general del cuerpo, ojos, 
orificios del cuerpo (boca y ano) y aletas (anal, caudal, dorsal, pectorales y pélvicas). Los peces 
se sacrificaron, inmediatamente se extrajeron los arcos branquiales y aletas y se colocaron en 
cajas de Petri con agua del medio, estos órganos se revisaron en busca de helmintos bajo 
microscopio esteroscópico con ayuda de pinceles finos y agujas de disección. El examen interno 
se realizó haciendo un corte longitudinal en el pez desde el ano hasta la altura de las aletas 
pectorales, prolongándose hasta la boca y separando los diferentes órganos de la cavidad del 
cuerpo, que después fueron colocados por separado en cajas de Petri con solución salina al 
0.75%. Todos los helmintos fueron contados y separados in situ con ayuda de pinceles; gran parte 
del material recolectado fue fijado en alcohol absoluto y guardado en criotubos para su posterior 
análisis molecular. 
Los digéneos, monogéneos y céstodos se fijaron en formol al 4% caliente, posteriormente 
se conservaron en viales con formol al 4% limpio. Además, con los monogéneos y metacéstodos 
se realizaron preparaciones semipermanentes fijadas de acuerdo al método descrito por Mendoza-
Palmero et al. (2009), lo que permitió el estudio de las estructuras esclerotizadas. Los ejemplares 
se colocaron entre porta y cubre objetos aplanando ligeramente y sellando las esquinas de los 
cubreobjetos con barniz, aplicando picrato-amonio por las orillas del cubreobjetos dejando que 
penetrara por capilaridad (Mendoza-Palmero et al., 2009).  
Los nemátodos se fijaron en formol salino al 4% caliente, después se colocaron en viales 
y se conservaron en este mismo fijador hasta su estudio. Después de ser identificados 
taxonómicamente se conservaron en alcohol al 70%.  
Los acantocéfalos se colocaron en agua destilada y se refrigeraron entre 12 a 24 hrs. para 
que evertieran la proboscis, después se fijaron en alcohol absoluto. Para su posterior 
procesamiento se lavaron en alcohol al 96%. Con excepción de los nemátodos, todos los 
helmintos recolectados se tiñeron con Paracarmín de Meyer, y con ellos se realizaron 
preparaciones permanentes para su estudio morfológico y determinación taxonómica según las 
técnicas de tinción descritas por Pérez-Ponce de León et al. (2009). Una vez teñidos los 
ejemplares, se deshidrataron en una serie de alcoholes graduales hasta alcohol etílico absoluto, se 
 49 
aclararon en salicilato de metilo y se montaron en bálsamo de Canadá para hacer preparaciones 
permanentes con las cuales se llevó a cabo el estudio morfológico.  
Los nemátodos se estudiaron mediante aclaramiento en preparaciones semipermanentes. 
Se aclararon en una serie progresiva de solución glicerina / agua destilada (1:20, 1:15, 1:10, 1:5, 
1:2) calentando en una platina de temperatura regulada a 44ºC hasta su evaporación, con dos 
cambios de glicerina en cada paso (Moravec, 1998).  
Los parámetros de infección parasitaria fueron descritos con base en los términos de 
prevalencia (porcentaje de huéspedes parasitados con una especie dada de parásito) e intensidad 
promedio (promedio aritmético del total de parásitos de una especie recolectados en una muestra 
entre el total de huéspedes parasitados) según el criterio de Margolis et al. (1982). De acuerdo 
con Esch et al. (1988) se distinguieron especies autogénicas (las que completan su ciclo de vida 
dentro del cuerpo de agua, en huéspedes acuáticos) y alogénicas (que completan su ciclo de vida 
fuera del cuerpo de agua, principalmente en aves). 
Clasificación del inventario faunístico 
Con base en los registros helmintológicos publicados para peces de la subfamilia Goodeinae y 
datos originales aportados en este trabajo, se preparó un listado organizado según el orden 
filogenético de cada grupo (Digenea, Monogenea, Cestoda, Nematoda y Acanthocephala). Las 
especies de huéspedes se ordenaron filogenéticamente siguiendo la propuesta de Domínguez-
Domínguez et al. (2010). 
La lista de especies de cada grupo de helminto se presenta de manera sistematizada por 
familia, en orden alfabético, antecediendo los representantes en estadio adulto y en segundo los 
de fase larvaria. Para cada taxones de parásito se indica el autor y el año de su publicación y, a su 
vez, se refiere a la (s) especie (s) de huésped (es) – en orden alfabético – a la (s) que esta (n) 
asociado (s) seguido del acrónimo de la (s) localidad (es) en donde se distribuye (n). Los registros 
se presentan en orden de tipo parásito-huésped-acrónimo de la localidad y corresponden a modo 
de filas y columnas. En el listado, cuando no se refiere el nombre de la especie huésped o al 
acrónimo de una localidad en la columna que le precede, se entiende que el registro corresponde 
a la misma especie de huésped o localidad, según sea el caso. Por último, se muestran los 
 50 
parámetros de infección para cada especie, incluyendo los registros previamente publicados y 
aquellos aportados por nuestros propios muestreos. 
Resultados 
Se registró un total de 55 taxones de helmintos parásitos para 36 de las 42 especies descritas a la 
fecha para Goodeinae (Cuadro 1, 2). En total, 57 cuerpos de agua (localidades) fueron 
muestreados y corresponden tanto a sistemas loticos (v.gr., ríos y arroyos) como lénticos (v.gr., 
manantiales, presas y lagos) (Cuadro 3). El registro helmintológico incluye 19 taxones de 
digéneos (11 adultos y ocho metacercarias), siete de monogéneos, 12 de céstodos (tres adultos y 9 
metacéstodos), 15 de nemátodos (ocho adultos y siete larvas) y dos de acantocéfalos (un adulto y 
un cistacanto). Se observa un predominio de digéneos, nemátodos y céstodos (en ese orden), así 
como una escasez de acantocéfalos y un relativo incremento en el numero de taxones de 
monogéneos en comparación con registros publicados previamente.  
De los 55 taxones de helmintos registrados, 20 (36%) fueron formas larvarias alogénicas 
cuyos adultos maduran principalmente en aves, en tanto que los 35 (64%) restantes son 
autogénicos adultos que en su mayoría maduran en peces. El número de estadios adultos (30 
taxones o 55%), es mayor que el de las fases larvarias (25 taxones o 45%). Las prevalencias más 
altas se registraron en tres taxones autogénicos y dos alogénicos, respectivamente: Margotrema 
bravoae, Salsuginus angularis y Rhabdochona lichtenfelsi y Posthodisplostomum minimum y 
Tylodelphys sp. El dígeneo M. bravoae y el nemátodo R. lichtenfelsi, fueron los parásitos en 
estadio adulto con mayor numero de registros asociados a goodeinos, presentándose en 22 y 19 
especies de huéspedes, respectivamente (Cuadro 1). Se reconocen once taxones endémicos de 
México y especialistas para la subfamilia Goodeinae: M. bravoae, M. resolanae, Phyllodistomum 
sp., Saccocoeloides sp., Gyrodactylus lamothei, G. mexicanus, Gyrodactylus  sp. 1, Gyrodactylus  
sp. 2, R. ahuehuellensis y R. lichtenfelsi. Se presenta al goodeino Allotoca goslinei como un 
nuevo huésped con registro helmintológico. 
En total, 112 registros son aportados por nuestros muestreos e incluyen 23 taxones de 
helmintos parásitos asociados a 28 especies de goodeinos, de los cuales seis son nuevos para 
Goodeinae. Asimismo, cinco taxones potenciales requieren ser descritos como especies nuevas 
para la ciencia (ver Notas en Cuadro 1). Se proporciona el registro helmintológico para nueve 
nuevas localidades (Cuadro 3). La metacercaria Centrocestus formosanus, el céstodo B. 
 51 
acheilognathi y el nemátodo Pseudocapillaria tomentosa son especies introducidas por causas 
antropogénicas. 
Discusión 
El inventario helmintológico incluye registros para 36 de las 42 especies de goodeinos. Las seis 
especies de goodeinos que no forman parte de este inventario se encuentra en categoría de en 
peligro de extinción, estrictamente extirpadas o en cautiverio; v.gr., Allodontichthys polylepis 
Rauchenberger, 1988; Chapalichthys peraticus Álvarez del Villar, 1963, Characodon garmani 
Jordan & Evermann, 1898, Ilyodon lennoni Meyer & Foerster, 1983, Skiffia francesae Kingston, 
1978 y Zoogoneticus tequila Webb & Miller, 1998 (Domínguez-Domínguez et al., 2005, 2008; 
de la Vega-Salazar, 2006). Con base en los registros helmintológicos publicados para Goodeinae 
y los aportados en este trabajo, es posible mencionar que la helmintofauna presente en estos 
peces ha sido documentada casi en tu totalidad. En este contexto, Goodeinae es prácticamente el 
primer grupo de vertebrados en México al que se le describe su helmintofauna en todas las 
especies de huéspedes potenciales actuales. De este modo, a continuación se describe brevemente 
los patrones descriptivos de la biodiversidad de helmintos parásitos de Goodeinae. 
Todas las especies de peces muestreadas presentaron por lo menos un taxón de helminto 
parásito. La riqueza más alta de helmintos registrada en goodeinos se encuentra en Goodea 
atripinnis con 28 taxones de helmintos, seguida de Xenotoca variata con 18, en tanto que 
Alloophorus robustus y Girardinichthys multiradiatus presentan 17 taxones. El 35% de los 
taxones de helmintos registrados en este inventario son digéneos; los monogéneos constituyen el 
13%, los céstodos el 22%, en tanto que los nemátodos y acantocéfalos el 27% y 4%, 
respectivamente. La riqueza de especies de digéneos, nemátodos y céstodos y el bajo número de 
especies de acantocéfalos coincide con los patrones descritos en peces dulceacuícolas para 
regiones neotropicales del país y para distintas cuencas hidrológicas de México (i.e., Aguilar-
Aguilar et al., 2008; Garrido-Olvera et al., 2012; Pérez-Ponce de Léon et al., 2012).  
Los digéneos son el grupo taxonómico más numerosos de helmintos para goodeinos. Los 
digéneos adultos y las metacercarias, Saccocoelioides cf. sogandaresi, Magnivitellinum simplex y 
Posthodiplostomum minimum, son especies de amplia distribución geográfica.  
 52 
A la fecha, siete taxones de monogéneos han sido registrados para Goodeinae. Se ha 
sugerido que esta aparente pobreza se debe a una deficiencia taxonómica de muestreo más que a 
una característica biológica de las comunidades de helmintos en peces dulceacuícolas de México, 
por lo que, los monogéneos pueden ser más comunes en México de lo que se ha registrado y su 
inventario esta aún lejos de completarse (Mendoza-Franco et al., 2003; Pérez-Ponce de León & 
Choudhury, 2010). Es evidente que, con base en los esfuerzos recientes de trabajos de inventarios 
sistematizados, la composición taxonómica en monogéneos en México ha incrementado 
notoriamente en los últimos 10 años, por lo que se espera en estudios próximos se contraste este 
aparente patrón de escasa riqueza específica. 
La mayor proporción de céstodos esta constituida por estadios larvarios; nueve de 12 
taxones registrados. En particular, los metacéstodos de la familia Dilepididae son parásitos 
relativamente frecuentes en peces dulceacuícolas del centro y sureste de México y se tienen 
registrados cinco en ocho especies de goodeinos (Cuadro 1). 
La composición taxonómica de los nemátodos presenta cierto grado de riqueza alta y 
equitativa en estadios adultos y larvarios, con una distribución geográfica relativamente extensa. 
Esto se debe a su amplia capacidad de infección, baja especificidad y a la amplia distribución de 
sus huéspedes intermediarios y definitivos. 
Dos especies de acantocéfalos fueron registrados: Pomphorhynchus cf. bulbocolli y 
Polymorphus brevis. La escasa presencia de acantocéfalos en Goodeinae constituye un patrón 
previamente registrado para otras regiones del país (ver García-Prieto et al., 2010; Pérez-Ponce 
de León & Chodhury, 2010; Pérez-Ponce de León et al., 2012). 
Los taxones autogénicos representan una mayor proporción (64%) que las alogénicas 
(36%). El alto porcentaje de taxones autogénicos registrados en este trabajo refleja 
implícitamente la relevancia ecológica y evolutiva que representan los helmintos parásitos de 
Goodeinae por tener aparentemente estrechas asociaciones históricas, en el que a su vez reflejan 
un amplio acervo genético presumiblemente especializado tanto para condiciones bióticas como 
para recursos abióticos, incluyendo ciclos de vida complejos, cierta calidad ambiental y 
supervivencia en ambientes acuáticos determinados tanto de huéspedes intermediarios 
invertebrados como de sus huéspedes definitivos vertebrados. 
 53 
Los taxones alogénicos registrados para goodeinos son generalistas y con una distribución 
geográfica relativamente amplia. El proceso de dispersión de los taxones alogénicos es debida a 
los hábitos alimentarios de sus huéspedes definitivos (aves ictiófagas) y, como efecto secundario, 
a su capacidad de vagilidad intrínseca. En este sentido, los taxones alogénicos registrados para 
Goodeinae son evidencia de que los peces goodeinos forman parte de la cadena trófica de las 
aves; esto puede reflejar a lo largo de la posición geográfica de cada uno de los registros de 
especies alogénicas, posibles rutas de migración de distintos grupos de aves, en particular 
Anatidae y Ardeidae. 
Algunos otros taxones de helmintos se pueden encontrar como adultos en anfibios, como 
el caso del dígeneo Apharyngostrigea sp. que se desarrolla en ranas (Locke et al., 2011). Otros 
taxones se han registrado en estadios adultos en reptiles, como la larva de digéneo Ochetosoma 
bravicaecum, el cuál madura en serpientes acuáticas del género Thamnophis (Jiménez-Ruiz et al., 
2002); o bien, las larvas de nemátodos Falcaustra sp., Serpinema trispinosum, Spiroxys sp., que 
maduran en tortugas (Garrido-Olvera et al., 2006; Pérez-Ponce de León et al., 2007). 
Cuatro de las especies de helmintos registradas fueron introducidas antropogénicamente a 
cuerpos epicontinentales de México: C. formosanus, B. acheilognathi y P. tomentosa. En este 
contexto, se denota que las comunidades de helmintos parásitos de goodeinos están sujetas a 
invasión por especies exóticas. 
La metacercaria de C. formosanus fue introducida a través del caracol Thiara tuberculata 
(Aguilar-Aguilar et al., 2009). Actualmente ésta especie presenta una capacidad de infección 
parasitaria amplia en los peces dulceacuícolas de México registrada en 67 especies de 13 familias 
de peces dulceacuícolas (Aguilar-Aguilar et al., 2009; 2013; Pérez-Ponce de León et al., 2010).  
La presencia de B. acheilognathi en peces nativos de México está relacionada con la 
introducción de la carpa herbívora Ctenopharyngodon idella en 1965 (López-Jiménez, 1981). A 
partir de entonces, se ha extendido su distribución a múltiples localidades infectando a un gran 
número de huéspedes, tanto de especies nativas como introducidas en México, debido a su gran 
capacidad de infección, baja especificidad y a la potencialidad de distribución de sus huéspedes 
intermediarios (ver Rojas-Sanchéz & García-Prieto, 2008). Sin embargo, a pesar de registrar este 
hecho en la literatura especializada a la fecha no se ha realizado una propuesta seria que 
promueva una estrategia política para tratamiento de parásitos silvestres introducidos para peces 
 54 
dulceacuícolas (Martínez-Aquino & Aguilar-Aguilar, 2008; Martínez-Aquino et al., 2011; 
Aguilar-Aguilar et al., 2013). Por tanto, es importante resaltar que los 52 registros de este céstodo 
exótico en 39 localidades para 14 especies de goodeinos, representan una amenaza biológica para 
los distintos programas de conservación de fauna silvestre (Domínguez-Domínguez et al., 2010). 
Evidentemente, un trabajo sistematizado e integrativo, con datos moleculares y con valores de los 
parámetros de infección para B. acheilognathi, permitirá hacer de manera más explícita la 
necesidad de promover estrategias de manejo de recursos naturales en aguas interiores 
mexicanas. 
El nemátodo P. tomentosa también fue introducido a México con un ciprínido, en este 
caso la carpa común Cyprinus carpio (Moravec et al., 2001). Pseudocapillaria tomentosa 
actualmente se encuentra registrada en México en 12 especies de huéspedes de tres familias 
(Garrido-Olvera et al., 2006).  
Salgado-Maldonado et al. (2001) y Sánchez-Nava et al. (2004) registraron a 
“Gyrodactylus cf. elegans” (Monogenea: Gyrodactylidae) en G. multiradiatus en el centro de 
México; sin embargo, no fue posible corroborar la validez taxonómica de este registro debido a 
que estos autores no depositaron ejemplares de referencia en ninguna colección científica 
nacional o internacional. Adicionalmente, en nuestros muestreos ningún monogéneo recolectado 
mostró similitud morfológica con esta especie de girodactílido, el cuál es específico para Abramis 
brama (Cypriniformes: Cyprinidae) que se distribuyen en Eurasia (Harris et al., 2004). Por esta 
razón, en este trabajo no consideramos el registro de “Gyrodactylus cf. elegans” como válido. 
El género Salsuginus Beverly-Burton, 1984 incluye 12 especies registradas en peces de 
cuatro familias pertenecientes al orden Cyprinodontiformes: Fundulidae, Cyprinodontidae, 
Poeciliidae y Goodeidae (Mendoza-Franco & Vidal-Martínez, 2001; Martínez-Aquino et al., 
2004, 2007b). El presente trabajo contiene 14 nuevos registros del género Salsuginus en 12 
especies de goodeinos: A. diazi, A. dugesi, A. splendens, G. atripinnis, I. furcidens, I. whitei, S. 
multipunctata, X. resolanae, X. melanosoma, X. variata y Z. quitzeoensis. Estos registros 
concuerdan con la especificidad propuesta para especies de Salsuginus para peces del orden 
Cyprinodontiformes y representan una afinidad biogeográfica Neártica. 
Se distinguen 13 taxones de helmintos como endémicos para sistemas hidrológicos del 
centro de México: los digéneos A. mexicanum, Allocreadim sp., M. bravoae, M. resolanae, 
 55 
Phyllodistomum sp. y Saccocoeloides sp.; los monogéneos G. lamothei, G. mexicanus, 
Gyrodactylus  sp. 1 y Gyrodactylus  sp. 2 y los nemátodos R. ahuehuellensis, R. lichtenfelsi y R. 
xiphophori. Estos taxones – a excepción de A. mexicanum, Gyrodactylus  sp. y R. xiphophori – se 
consideran como parásitos especialistas para Goodeinae y reflejan una estrecha relación con la 
historia evolutiva de estos peces. En este contexto, dichos taxones representan una parte de las 
faunas principales de helmintos en un sentido biogeográfico sensu Pérez-Ponce de León & 
Choudhury (2005). 
El nemátodo R. lichtenfelsi originalmente fue descrito en peces de la subfamilia 
Goodeinae (Sánchez-Álvarez et al., 1998) y su especificidad en peces de esta subfamilia ha sido 
bien documentada (Pérez-Ponce de León & Choudhury, 2005; Garrido-Olvera et al., 2006; 
Mejía-Madrid et al., 2005, 2007b). Los 16 registros aportados en este trabajo en 10 especies de 
goodeinos, más los 28 publicados previamente en 19 especies de goodeinos, se suman a la 
propuesta de especificidad de este nemátodo para Goodeinae. El nemátodo R. ahuehuellensis fue 
descrita como asociada a I. furcidens en un afluente del río Balsas (Mejía-Madrid y Pérez-Ponce 
de León, 2003). Los tres registros documentados en este estudio en tres especies de goodeinos, 
más los 10 publicados previamente en seis especies de goodeinos, apoyan la especificidad 
propuesta para este nemátodo asociado a Goodeinae (Mejía-Madrid et al., 2005, 2007b). 
El género Margotrema fue descrito originalmente para incluir a M. bravoae Lamothe-
Argumedo, 1970 como parásito de Girardinichthys multiradiatus en La Lagunilla, Estado de 
México (Lamothe-Argumedo, 1972). Treinta años después, se describió una segunda especie para 
este género,  M. guillerminae Pérez-Ponce de León, 2001 como parásito de los peces Notropis 
calientis (Cyprinidae) y Alloophorus robustus (Goodeinae) en el Lago de Zacapu, Michoacán 
(Pérez-Ponce de León, 2001). Martínez-Aquino et al. (2013) delimitaron ambas especies 
putativas con base en análisis filogenéticos moleculares a lo largo de su área de distribución, y 
propusieron la sinonimia de M. guillerminae con M. bravoae. Posteriormente, con base en un 
detallado estudio taxonómico, se describió a M. resolanae como parásito del goodeino 
Xenotaenia resolanae (Pérez-Ponce de León et al., en prensa).  
Con base en los avances de los registros helmintológicos publicados para Goodeinae, 
distintos autores han descrito patrones biogeográficos entre goodeinos y sus helmintofaunas 
principales, los cuales representan la integración de dicha acumulación de información (ver 
 56 
Pérez-Ponce de León & Choudhury, 2005; Martínez-Aquino et al., 2007; Garrido-Olvera et al., 
2012). Por otra parte, Mejía-Madrid et al. (2007a, b) y Martínez-Aquino et al. (2013) han usado 
de manera explícita los registros de helmintos parásitos específicos para Goodeinae para poner a 
prueba hipótesis evolutivas acerca de los eventos históricas que ocurrieron entre Goodeinae y sus 
faunas principales de parásitos, esto es M. bravoae, M. resolanae, R. ahuehuellensis y R. 
lichtenfelsi. En este contexto, se resalta la utilidad, tanto de los registros aislados como de los 
organizados de manera sistematizada, para la descripción de la helmintofauna de peces 
dulceacuícolas en México. Aún cuando algunos autores han sugerido que la diversidad de 
helmintos para peces dulceacuícolas en México presumiblemente esta próxima a ser completada 
(Pérez-Ponce de León & Choudhury, 2010), los eventos evolutivos que se involucran en los 
procesos de diversificación de los parásitos quedan aún por descubrir. Por ejemplo, de las 11 
especies que se infiere en este trabajo como helmintofaunas principales para Goodeinae, solo tres 
han sido analizadas detalladamente y se ha detectado diferencias genealógicas asociadas al 
escenario geográfico y a la historia evolutiva de sus huéspedes (Mejía-Madrid et al., 2007b, 
Martínez-Aquino et al., 2013). Los otros ocho taxones de helmintos son modelos biológicos 
potenciales para expandir el conocimiento referente a las asociaciones históricas exclusivas para 
goodeinos de México; v. gr A. mexicanum, Allocreadim sp., Phyllodistomum sp., Saccocoeloides 
sp., G. lamothei, G. mexicanus, Gyrodactylus sp. 1 y Gyrodactylus sp. 2. Futuros estudios en 
estos taxones ayudaran a comprender los patrones de diversificación parasitaria en peces 
dulceacuícolas que habitan en el territorio nacional.  
Agradecimientos 
Agradecemos a R. Pérez, D.I. Hernández., F.J. Alcántar y L. Escalera por la asistencia en el 
campo. A B. Mendoza y L. Garrido por su colaboración en el trabajo de gabinete. A H. Mejía por 
proporcionar información de sitios de recolecta. A Omar Domínguez por sus comentarios en una 
primera versión de este manuscrito. A Luis García, técnico administrador de la Colección 
Nacional de Helmintos (CNHE), por proporcionar parte de la literatura especializada. A.M-A 
agradece al Consejo Nacional de Ciencia y Tecnología (CONACyT), por el apoyo proporcionado 
mediante una beca para realizar estudios de doctorado dentro del Programa de Posgrado en 
Ciencias Biológicas, de la Universidad Nacional Autónoma de México. Este estudio contó con el 
apoyo financiero otorgado a G.P-PdL. a través de los proyectos 83043 del Consejo Nacional de 
 57 
Ciencia y Tecnología (CONACyT), e IN 202111 del Programa de Apoyo a Proyectos de 
Investigación e Innovación Tecnología (PAPIIT-UNAM).  
Literatura citada 
Aguilar-Aguilar R., G. Salgado-Maldonado R. Contreras-Medina & A. Martínez-Aquino (2008). 
Richness and endemism of helminth parasites of freshwater fishes in Mexico. Biological 
Journal of the Linnean Society, 94, 435–444. 
Aguilar-Aguilar, R., Martínez-Aquino, A., Pérez-Ponce de León G. y R. Pérez-Rodríguez. (2009) 
Digenea, Heterophyidae, Centrocestus formosanus metacercariae: Distribution extension 
for Mexico, new state record, and geographic distribution map. Check List 5, 357-359. 
Aguilar-Aguilar R., Rosas-Valdez R., Martínez-Aquino A., R. Pérez-Rodríguez, Domínguez-
Domínguez O. & G. Pérez-Ponce de León. (2010) Helminth fauna of two cyprinid fish 
(Campostoma ornatum and Codoma ornata) from the upper Piaxtla River, Northwestern 
Mexico. Helminthologia, 47: 251–256. 
Aguilar-Aguilar R., Martínez-Aquino A. H. Espinoza-Pérez & Pérez-Ponce de León. (en prensa)  
Helminth parasites of freshwater fishes from Cuatro Ciénegas, Coahuila, in the 
Chihuahuan desert of Mexico: Inventory and biogeographical implications. Integrative 
Zoology. 
Alcántar-Escalera F.J., M. García-Varela, E. Vázquez-Domínguez & G. Pérez-Ponce de León. 
(2013) Using DNA barcoding to link cystacanths and adults of the acanthocephalan 
Polymorphus brevis in central Mexico. Molecular Ecology Resources.  
Astudillo-Ramos L. & E. Soto-Galera. 1997. Estudio helmintológico de Chirostoma 
humboldtianum y Girardinichthys multirradiatus capturados en el Lerma. Zoología 
Informa 35: 53-59.  
De la Vega-Salazar M.Y. (2006) Estado de conservación de los peces de la familia Goodeinae 
(Cyprinodontiformes) en la mesa central de México. Revista de Biología Tropical, 54: 
163-177.  
 58 
Domínguez O. 2010. Conservación de goodeidos, familia en alto riesgo. En: J. Carabias, J. 
Sarukhán , J. de la Maza, & C. Gallindo. Patrimonio Natural de México: cien casos de 
éxito. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad pp. 48-49. 
Domínguez-Domínguez O., N. Mercado-Silva, J. Lyons y H.0 Grier. 2005. The viviparous 
goodeid fishes. En: Uribe M.C. y H. Grier (eds.). Viviparous Fishes. New Life 
Publications. Homestead, Florida. pp. 525-569. 
Domínguez-Domínguez O., C. Pedraza-Lara, N. Gurrola-Sánchez, R. Pérez-Rodríguez, I. Israde-
Alcántara, V. H. Garduño-Monroy, I. Doadrio, G. Pérez-Ponce de León & D.R. Brooks. 
(2010) Historical biogeography of the Goodeinae (Cyprinodontiforms). En: Uribe-
Aranzabal M. C. and H. Grier. (Eds.). Viviparous Fishes II, New Life Publications, 
Homestead, Florida, 33-74.  
Esch, G. W., C. R. Kennedy, A. O. Bush & J. M. Aho. (1988) Patterns in helminth communities 
in freshwater fish in Great Britain: Alternative strategies for colonization. Parasitology 
96: 519-532. 
García-Prieto, L. & D. Osorio-Sarabia. (1991) Distribución actual de Bothriocephalus 
acheilognathi en México. Anales del Instituto de Biología, Universidad Nacional 
Autónoma de México, Serie Zoología, 62, 523–526.  
García-Prieto L, García-Varela M, Mendoza-Garfias B, Pérez-Ponce de León G (2010) Checklist 
of the Acanthocephala in wildlife vertebrates of Mexico. Zootaxa, 2419, 1–50. 
Garrido-Olvera L, L. García-Prieto & G. Pérez-Ponce de León. 2006. Checklist of the adult 
nematode parasites of fishes in freshwater localities from Mexico. Zootaxa 1201: 1–45. 
Garrido-Olvera L, H. T. Arita & G. Pérez-Ponce de León. (2012). The influence of host ecology 
and biogeography on the helminth species richness of freshwater fishes in Mexico. The 
influence of host ecology and biogeography on the helminth species richness of 
freshwater fishes in Mexico. Parasitology 139, 1652–1665. 
Guzmán-Cornejo, M.C. & García-Prieto, L. (1999) Trematodiasis en algunos peces del lago de 
Cuítzeo, Michoacán, México. Revista de Biología Tropical, 47, 593–596. 
 59 
Jiménez-Ruiz, F.A., García-Prieto, L. & G. Pérez-Ponce de León. (2002) Helminth 
infracommunity structure of the sympatric garter snakes Thamnophis eques and 
Thamnophis melanogaster from the Mesa Central of Mexico. Journal of Parasitology, 88, 
454–460. 
Lamothe-Argumedo R. 1972. Tremátodos de peces VI. Margotrema bravoae gen. nov.sp. nov. 
(Trematoda: Allocreadiidae) parásito de Lermichthys multiradiatus Meek. Anales del 
Instituto de Biología, UNAM, Serie Zoología 41: 87-92. 
Lamothe-Argumedo, R. & Cruz-Reyes, A. (1972) Hallazgo de  Ligula intestinalis (Goeze, 1782) 
Gmelin, 1790 en  Lermichthys multiradiatus (Meek) (Pisces: Goodeidae).  Revista de la 
Sociedad Mexicana de Historia Natural, 33, 99–106. 
Littlewood D.T.J. & R.A. Bray. (2001) Interrelationships of the Platyhelminthes. Taylor and 
Francis Group, Londres y Nueva York. 356 p.  
López-Jiménez, S. (1981) Céstodos de peces I. Bothriocephalus  (Clestobothrium ) acheilognathi 
(Cestoda: Bothriocephalidae). Anales del Instituto de Biología, Universidad Nacional 
Autónoma de México, Serie Zoología, 51, 69–84. 
Locke S.A., J.D. McLaughlin, A.R. Lapierre, P. T. J. Johnson, & D.J. Marcogliese. 2011.  
Linking Larvae and Adults of Apharyngostrigea cornu, Hysteromorpha triloba, and 
Alaria mustelae (Diplostomoidea: Digenea) Using Molecular Data. Journal of 
Parasitology, 97(5):846-851. 2011. 
Margolis L., G. W. Esch, J. C. Holmes, A. M. Kuris & G. A. Schad. (1982) The use ecological 
terms in Parasitology (Report of and hoc committee of the American Society of 
Parasitologists). Journal of Parasitology 68:131-133. 
Martínez-Aquino A. & R. Aguilar-Aguilar. (2008) Helminth parasites of the pupfish Cyprinodon 
meeki (Pisces: Cyprinodontiformes), an endemic freshwater fish from North-Central 
Mexico. Helminthologia 45, 48-51. 
Martínez-Aquino A., G. Salgado-Maldonado, R. Aguilar-Aguilar, G. Cabañas-Carranza & M.P. 
Ortega-Olivares. (2004) Helminth parasites of Chapalichthys encaustus (Pisces: 
 60 
Goodeidae), an endemic freshwater fish from Lake Chapala, Jalisco, México. Journal of 
Parasitolology, 90: 889-890. 
Martínez-Aquino A., Aguilar-Aguilar R., Santa Anna del Conde Juárez H.O. & R. Contreras-
Medina. (2007a) Empleo de herramientas panbiogeográficas para detectar áreas para 
conservar: un ejemplo con taxones dulceacuícolas. En: Luna I., J.J. Morrone y D. 
Espinosa (Eds). Biodiversidad de la Faja Volcánica Transmexicana. Las Prensas de 
Ciencias, Universidad Nacional Autónoma de México. Pp. 449-460. 
Martínez-Aquino, A., G. Salgado-Maldonado, R. Aguilar-Aguilar, G. Cabañas-Carranza & C.A. 
Mendoza-Palmero. (2007b) Helminth parasite communities of Characodon audax and C. 
lateralis (Pisces: Goodeidae), endemic freshwater fishes from Durango, Mexico. The 
Southwestern Naturalist 52: 125-130. 
Martínez-Aquino A., Aguilar-Aguilar R., Pérez-Rodríguez R. & G. Pérez-Ponce de León. (2009) 
Helminth parasite of Xenotaenia resolanae (Osteichthyes: Cyprinodontiformes: 
Goodeidae) from the Cuzalapa hydrological system, Jalisco, México. Journal of 
Parasitology 95: 1221-1223. 
Martínez-Aquino A., D. Hernández-Mena, R. Pérez-Rodríguez, R. Aguilar-Aguilar & G. Pérez-
Ponce de León. (2011) Endohelminth parasites of the freshwater fish Zoogoneticus 
purhepechus (Cyprinodontiformes: Goodeidae) from two springs in the Lower Lerma 
River, Mexico. Revista Mexicana de Biodiversidad 82: 1132-1137. 
Martínez-Aquino A., R. Pérez-Rodríguez, D.I. Hernández-Mena, L. Garrido-Olvera, R. Aguilar-
Aguilar & G. Pérez-Ponce de León. (2012) Endohelminth parasites of seven goodein 
species (Cyprinodontiformes: Goodeidae) from Lake Zacapu, Michoacán, Central Mexico 
Plateau. Hidrobiológica. 22: 88-91. 
Martínez-Aquino A., F.S. Ceccarelli & G. Pérez-Ponce de León. (2013) Molecular phylogeny of 
the genus Margotrema (Digenea: Allocreadiidae), parasitic flatworms of goodeid 
freshwater fishes across central Mexico: species boundaries, host-specificity and 
geographical congruence. Zoological Journal of the Linnean Society, 168: 1-66. 
 61 
Mejía-Madrid, H. & Pérez-Ponce de León, G. (2003) Rhabdochona ahuehuellensis  n. sp. 
(Nematoda: Rhabdochonidae) from the balsas goodeid, Ilyodon whitei (Osteichthyes: 
Gooedeidae), in Mexico. Journal of Parasitology, 89, 356–361. 
Mejía-Madrid H., Domínguez- Domínguez O. & G. Pérez-Ponce de León. (2005). Adult 
endohelminth parasites of Goodeinae (Cyprinodontiformes: Goodeidae) from México 
with biogeographical considerations. Comparative Parasitology, 72, 200–211. 
Mejía-Madrid H., A. Choudhury & G. Pérez-Ponce de León. (2007a) Phylogeny and 
biogeography of Rhabdochona Railliet, 1916 (Nematoda: Rhabdochonidae) species from 
the Americas Systematic Parasitology, 67:1–18. 
Mejía-Madrid H., E. Vázquez-Domínguez & G. Pérez-Ponce de León (2007b) Phylogeography 
and freshwater basins in central Mexico: recent history as revealed by the fish parasite 
Rhabdochona lichtenfelsi (Nematoda). Journal of Biogeography, 34, 787–801. 
Mendoza-Franco, E. F. &V. Vidal-Martínez (2001) Salsuginus neotropicalis n. sp. (Monogenea: 
Ancyrocephalinae) from the pike killifish Belonesox belizanus (Atheriniformes: 
Poeciliidae) from Southeastern Mexico. Systematic Parasitology 48:41-45. 
Mendoza-Franco, E. F., T. Scholz y G. Cabañas-Carranza. 2003. Guavinella tropica n. gen., n. 
sp. (Monogenea: Dactylogyridae) from the Gills of the Bigmouth Sleeper, Gobiomorus 
dormitor (Perciformes: Eleotridae), from Mexico. Comparative Parasitology 70: 26-31. 
Mendoza-Palmero, C. A., H. Espinosa-Pérez, & G. Salgado-Maldonado. (2007). Helmintos 
parásitos de peces dulceacuícolas. En Guía Ilustrada de La Cantera Oriente: 
caracterización ambiental e inventario biológico. Lot A. (Ed.). Coordinación de la 
Investigación Científica, Secretaría Ejecutiva de la Reserva Ecológica del Pedregal de San 
Ángel de Ciudad Universitaria, UNAM, Ciudad de México, D.F., p. 179–191. 
Mendoza-Palmero C.A., A.L. Sereno-Uribe & G. Salgado-Maldonado. (2009). Two new species 
of Gyrodactylus von nordmann, 1832 (Monogenea: Gyrodactylidae) parasitizing 
Girardinichthys multiradiatus (Cyprinodontiformes: Goodeinae), an endemic freshwater 
fish from central Mexico. Journal of Parasitology, 95: 315–318.  
 62 
Miller R.R., W.L. Minckley  & S.M. Norris. (2005) Freshwater fishes of México. The University 
of Chicago Press. Chicago. 490 pp. 
Moravec, F. (1998) Nematodes of freshwater fishes of the Neotropical Region . Academia Praha, 
464 pp. 
Moravec, F., R. Aguilar-Aguilar y G. Salgado-Maldonado. (2001) Systematic status of Capillaria 
patzcuarensis Osorio-Sarabia, Pérez-Ponce de León et Salgado-Maldonado, 1986 
(Nematoda: Capillariidae) from freshwater fishes in Mexico. Acta Parasitologica 46:8-
11. 
Peresbarbosa-Rojas, E., Pérez, G. & García-Prieto, L. (1994) Helmintos parásitos de tres especies 
de peces (Goodeinae) del Lago de Pátzcuaro, Michoacán. Anales del Instituto de Biología, 
Universidad Nacional Autónoma de México, Serie Zoología, 65, 201–204. 
Pérez-Ponce de León G. 2001. Margotrema guillerminae n. sp. (Trematoda: Macroderoididae) 
from two species of freshwaters fishes in Lake Zacapu, Michoacan state, Mexico, and 
new records of Margotrema bravoae Lamothe, 1970. Journal of Parasitology 87: 1112-
1114. 
Pérez-Ponce de León G. & A. Choudhury. (2005) Biogeography of helminth parasites of 
freshwater fishes in Mexico: the research for patterns and processes. Journal of 
Biogeography 32: 645-649. 
Pérez-Ponce de León, G. & A. Choudhury. 2010. Parasite inventories and DNA-based taxonomy: 
Lessons from helminths of freshwater fishes in a megadiverse country. Journal of 
Parasitology 96: 236-244. 
Pérez-Ponce de León G., García-Prieto L., León-Régagnon V. & A. Choudhury. (2000). 
Helminth communities of native and introduced fishes in Lake Pátzcuaro, Michoacan, 
Mexico. Journal of Fish Biology 57: 303-325. 
Pérez-Ponce de León G., García-Prieto L. & B. Mendoza-Garfias. (2007) Trematode parasites 
(Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa 1534: 1-247. 
 63 
Pérez-Ponce de León G., R. Rosas-Valdez, B. Mendoza-Garfias, R. Aguilar-Aguilar, J. Falcón-
Ordaz, L. Garrido-Olvera & R. Pérez-Rodríguez. (2009). Survey of the endohelminth 
parasites of freshwater fishes in the upper Mezquital River Basin, Durango State, Mexico. 
Zootaxa 2164: 1–20. 
Pérez-Ponce de León G., Rosas-Valdez R., Aguilar-Aguilar R., Mendoza-Garfias B., Mendoza-
Palmero C., García-Prieto L., Rojas A., Briosio-Aguilar R., R. Pérez-Rodríguez & O. 
Domínguez-Domínguez. (2010). Helminth parasites of freshwater fishes, Nazas River 
basin, northern Mexico. Check List 6, 26-35. 
Pérez-Ponce de León G., L. García-Prieto & B. Mendoza-Garfias (2012) Describing Parasite 
Biodiversity: The Case of the Helminth Fauna of Wildlife Vertebrates in Mexico, 
Changing Diversity in Changing Environment, PhD. Oscar Grillo (Ed.), ISBN: 978-953-
307-796-3, InTech, Available from: http://www.intechopen.com/books/changing-
diversity-in-changing-environment/describing-parasitebiodiversity-the-case-of-the-
helminth-fauna-of-wildlife-vertebrates-in-mexico 
Pérez-Ponce de León G., Mendoza-Garfias B., Rosas-Valdez R. & A. Choudhury. (Sometido) 
New host and locality records of freshwater fish helminth parasites in river basins north of 
the Transmexican Volcanic Belt in northern Mexico: Another look at biogeographical 
patterns. Revista Mexicana de Biodiversidad. 
Pérez-Ponce de León G., A. Martínez-Aquino & B. Mendoza-Garfias. (Sometido) A new species 
of Margotrema (Digenea, Allocreadiidae) from the Leopard splitfin Xenotaenia resolanae 
(Cyprinodontiformes, Goodeidae) from west-central Mexico. Zootaxa 
Pineda-López R., Salgado-Maldonado G., Soto-Galera E., Hernández-Camacho N., Orozco-
Zamorano A., Contreras-Robledo S., Cabañas-Carranza G. & R. Aguilar-Aguilar. (2005). 
Helminth parasites of viviparous fishes in Mexico. En: H. Grier & M.C. Uribe (Eds.). 
Viviparous Fishes: Genetics, Ecology, and Conservation. New Life Publications 
Homestrad, Florida. pp. 437-456.  
Rapoport, E. (1975) Areografía. Estrategias geográficas de las especies. Fondo de Cultura 
Económica, México, D. F. 214 p.  
 64 
Rojas-Sánchez A. & L. García-Prieto. (2008). Distribución actual del cestodo Bothriocephalus 
acheilognathi en México. Memorias XXV Simposio sobre Fauna Silvestre. Universidad 
Nacional Autónoma de México, México. 89-93 pp. 
Romero-Tejeda, M.L., L. García-Prieto, L. Garrido-Olvera & G. Pérez-Ponce de León. (2008). 
Estimation of the endohelminth parasite species richness in freshwater fishes from La 
Mintzita reservoir, Michoacán, Mexico. Journal of parasitology 94, 288–292. 
Rosas-Valdez, R., A. Choudhury, & G. Pérez-Ponce de León, G. 2011. Molecular prospecting for 
cryptic species in Phyllodistomum lacustri (Platyhelminthes, Gorgoderidae). Zoologica 
Scripta 40: 296-305. 
Salgado-Maldonado, G. (2006). Checklist of helminth parasites of freshwater fishes from Mexico. 
Zootaxa 1324: 1–357. 
Salgado-Maldonado, G. & Pineda-López, R.F. (2003). The Asian fish tapeworm Bothriocephalus 
acheilognathi: a potential threat to native freshwater fish species in Mexico. Biological 
Invasions, 5, 261–268. 
Salgado-Maldonado, G., Cabañas-Carranza, G., Caspeta-Mandujano, J.M., Soto-Galera, E., 
Mayén-Peña, E., Brailovsky, D. & Báez-Valé, R. (2001a) Helminth parasites of 
freshwater fishes of the Balsas River drainage basin southwestern Mexico.  Comparative 
Parasitology, 68, 196–203. 
Salgado-Maldonado, G., Cabañas-Carranza, G., Soto-Galera, E., Caspeta-Mandujano, J.M., 
Moreno-Navarrete, R.G., Sánchez-Nava, P. & Aguilar-Aguilar, R. (2001b) A checklist of 
helminth parasites of freshwater fishes from the Lerma-Santiago river basin, Mexico. 
Comparative Parasitology, 68, 204–218. 
Salgado-Maldonado, G., Cabañas-Carranza, G., Soto-Galera, E., Pineda-López, R.F., Caspeta-
Mandujano, J.M., Aguilar-Castellanos, E. & Mercado-Silva, N. (2004a) Helminth 
parasites of freshwater fishes of the Pánuco river basin, east central Mexico. Comparative 
Parasitology, 71, 190–202. 
 65 
Salgado-Maldonado, G., Mercado-Silva, N., Cabañas-Carranza, G., Caspeta-Mandujano, J.M., 
Aguilar-Aguilar, R. & Iñiguez-Dávalos, L.I. (2004b) Helminth parasites of freshwater 
fishes of the Ayuquila river, Sierra de Manantlán Biosphere Reserve, west-central 
Mexico. Comparative Parasitology, 71, 67–72. 
Sánchez-Álvarez, A., García-Prieto, L. & Pérez, G. (1998) A new species of  Rhabdochona 
Railliet,1916 (Nematoda: Rhabdochonidae) from endemic goodeids 
(Cyprinodontiformes) from two Mexican lakes. Journal of Parasitology, 84, 840–845. 
Sánchez-Nava, P., Salgado-Maldonado, G., Soto-Galera, E. & Jaimes-Cruz, B. (2004) 
Helminthparasites of Girardinichthys multiradiatus (Pisces: Goodeidae) in the Upper 
Lerma River subbasin, Mexico. Parasitology Research, 93, 396–402. 
Scholz, T. & Salgado-Maldonado, G. (2000) The introduction and dispersal of Centrocestus 
formosanus (Nishigori, 1924) (Digenea: Heterophyidae) in Mexico: a review. American 
Midland Naturalist, 143, 185–200. 
Scholz, T. & Salgado-Maldonado, G. (2001) Metacestodes of the family Dilepididae (Cestoda: 
Cyclophyllidea) parasitising fishes in Mexico. Systematic Parasitology 49, 23–40. 
Vidal-Martínez, V.M., Aguirre-Macedo, M.L., Scholz, T., González-Solís, D. & Mendoza-
Franco, E.F. (2001a) Atlas of the helminth parasites of cichlid fish of Mexico . Academia, 
Praha pp. 165. 
 
 
 
 
 
 
 
 
Cuadro 1. Helmintos parásitos de Goodeinae. Los acrónimos y características de las localidades se refieren en el Cuadro 3. 
A = Acrónimo de cada localidad; N = Número de huéspedes examinados; P (%) = Prevalencia expresada en porcentaje; 
IP + de = Intensidad promedio + desviación estandar; ND = No hay datos disponibles; Au = Autogénica; Al= Alogénica; 
Gn = Generalista; Es = Especialista. Sitios de infección: A = Aletas; Aa = Aleta anal; B = Branquias; Cb = Cavidad branquial; 
Cc = Cavidad del cuerpo; Co = Corazón; G= Grasa; H = Hígado; 1 = Intestino; M= Mesenterio; Mu = Musculo; O = Ojos; 
P = Piel; Pi = Pared intestinal; Vb = Vesícula biliar; Vu = Vejiga urinaria; * = Cyprinidae; ** Cyprinodontidae. 
Taxa (Helminto) Huésped / Sitio de infección A N P(%)  IP=de Referencia 
Digenea 
Fam. Allocreadiidae Looss 1902 
Allocreadium lobatum "o" Állotoca zacapuensis / 1 Zaca 17 5.8 0.1 =0.5 Mejía-Madrid et al., 2005 
Wallin, 1909 Zoogoneticus quitzeoensis / 1 Zaca 15 13,3 0.4 =1.3 Mejía-Madrid et al., 2005 
Allocreadium mexicanum"  Characodon audax /1 Tobo 10 20 0.8+1.7 Mejía-Madrid et al., 2005 
Osorio-Sarabia, Characodon lateralis / 1 Amad 15 46.7 0.8+1.3 Mejía-Madrid et al., 2005 
Pérez-Ponce de León 
y Salgado-Maldonado, 1986 
. Au/? 
Allocreadium sp. Characodon audax / 1 Tobo 42 4.7 ND Pérez-Ponce de León et al., 2009 
Nota 1 27No 9 44 ND Pérez-Ponce de León et al., 2009 
Characodon lateralis / 1 Amad 9 27 ND Pérez-Ponce de León et al., 2009 
Fam. Macroderoididae 
McMullem, 1937 
Margotrema bravoae "ES Allodontichthys zonistius / 1 Siem 6 6 3 Salgado-Maldonado et al., 2004b 
Lamothe-Argumedo, 1970 Ahua 10 70 3+2.8 Mejia-Madrid et al., 2005 
Nota 2 11 100 7.18+5.9 Martínez-Aquino ef al., 2013 
Allodontichthys hubbsi / 1 Tule 6 33.3 0.5 0.8 Mejía-Madrid et al., 2005
 66 
 
Allodontichthys tamazulae / 1 
ÁAlloophorus robustus / 1 
Allotoca diazi / 1 
Állotoca dugesti / 1 
Allotoca maculata / 1 
Allotoca meeki / 1 
Állotoca zacapuensis / 1 
Chapalichthys pardalis / 1 
Characodon audax / 1 
Cyprinella lutrensis* /1 
Cyprinodon nazas ** / 1 
Girardinichthys multiradiatus / 
I 
Goodea atripinnis / 1 
Ilyodon cortesae / 1 
Ilyodon furcidens / 1 
Ilyodon white / 1 
Tama 
Mcha 
Mcha 
Luz 
Mint 
Zaca 
Mcha 
Mcha 
Marc 
Opop 
Zaca 
Zaca 
Tocu 
Tobo 
Tobo 
Abra 
Pin1 
Guad 
Buen 
Sofi 
Lagu 
Vict 
Porv 
Verd 
Cutz 
Tama 
Ahua 
Tocu 
Ahue 
67 
34 
27 
14 
ND 
40 
34 
21 
22 
15 
19 
17 
32 
11 
38 
10 
12 
34 
14 
38 
27 
64 
36 
25 
30 
11 
11 
37 
180 
42.9 
ND 
14.7 
7.4 
7.14 
ND 
ND 
14.7 
23.81 
33.33 
100 
ND 
66.8 
79 
75 
35.3 
25 
18.2 
10.53 
10 
25 
47 
14.2 
ND 
3.7 
ND 
40 
5.6 
12 
6.7 
9.1 
100 
2.70 
72.2 
1+1.4 
ND 
0.3+0.7 
1.6 
ND 
1=0.27 
ND 
ND 
0.3+0.7 
6.2 + 3.47 
7+5.59 
37+1.7 
ND 
2.1+2.8 
59.1 
15>+11.18 
0.6+1 
ND 
0.4+0.9 
10.31 
1.84 + 1.21 
0.3+0.9 
ND 
ND 
ND 
ND 
ND 
ND 
22.5 + 6.4 
1 
0.2+0,5 
0.25+0.5 
0.1+0,3 
4,55 +4,59 
3 +0.49 
2.754.6 
Mejía-Madrid et al., 2005 
Pérez-Ponce de León, 2001 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Romero-Tejada ef al., 2008 
Martínez-Aquino ef al., 2013 
Pérez-Ponce de León, 2001 
Pérez-Ponce de León, 2001 
Mejía-Madrid et al., 2005 
Martínez-Aquino et al., 2013 
Presente trabajo 
Mejía-Madrid et al., 2005 
Martínez-Aquino et al., 2013 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Martínez-Aquino et al., 2013 
Mejía-Madrid et al., 2005 
Martínez-Aquino et al., 2012 
Mejía-Madrid et al., 2005 
Martínez-Aquino ef al., 2013 
Martínez-Aquino et al., 2007b 
Mejía-Madrid et al., 2005 
Pérez-Ponce de León et al., 2001 
Pérez-Ponce de León et al., 2001 
Pérez-Ponce de León et al., 2001 
Pérez-Ponce de León et al., sometido 
Pérez-Ponce de León et al., 2009 
Lamothe-Argumedo, 1970 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Martínez-Aquino et al., 2013 
Martínez-Aquino et al., 2013 
Mejía-Madrid et al., 2005
 67 
 
 
Margotrema resolanae 
Pérez-Ponce de Léon, 
Martínez-Aquino 
y Mendoza-Garfías, sometido 
Au/Es? 
Margotrema sp. : 
Fam. Gorgoderiade (Loss, 1899) 
Loss, 1901 9 
Dendrorchis sp es 
Neoophorus regalis / 1 
Notropis calientis * / 1 
Xenotoca variata / 1 
Zoogoneticus purhepechus / 1 
Zoogoneticus quitzeoensis / 1 
Xenotaenia resolanae / 1 
Codoma ornata * / 1 
Characodon audax / 1 
Goodea atripinnis / 1 
Xenotaenia resolanae / 1 
Notropis sp. / 1 
Ilyodon furcidens / 1 
Xenotaenia resolanae | Vu 
Potg 
Marc 
Reye 
Rico 
Zaca 
Mint 
Luz 
Mint 
Zaca 
Cuza 
Piax 
Tobo 
Pinl 
Igna 
Cuza 
Tamo 
Sand 
Siem 
Cuza 
35 
10 
28 
ND 
31 
45 
30 
ND 
30 
22 
32 
35 
21 
42 
34 
ND 
36 
57 
35 
34,29 
25 
20 
54.5 
14.3 
35.71 
ND 
2.2 
ND 
6.7 
13.64 
46.88 
80 
28.57 
23.8 
28.5 
ND 
33 
5.71 
5.75+4.06 
0.25+0.5 
432.2 
18+2.6 
0.1+0.4 
2.8 + 1.96 
ND 
1 
1 
3.5+0.71 
ND 
ND 
1.67 + 0.69 
ND 
4.68 +5.6 
ND 
5.67 + 5.76 
1 
1.5+0.71 
Martínez-Aquino et al., 2013 
Mejía-Madrid et al., 2005 
Martínez-Aquino et al., 2013 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Martínez-Aquino et al., 2013 
Pérez-Ponce de León, 2001 
Salgado-Maldonado, 2006 
Martínez-Aquino ef al., 2011 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Romero-Tejada ef al., 2008 
Martínez-Aquino ef al., 2013 
Martínez-Aquino et al., 2012 
Martínez-Aquino et al., 2009a 
Aguilar-A guilar et al., 2010 
Pérez-Ponce de León et al., 2001 
Pérez-Ponce de León et al., 2001 
Salgado-Maldonado et al., 2006 
Martínez-Aquino, 2005 (datos de tesis) 
Pérez-Ponce de León (com. pers.) 
Pérez-Ponce de León (com. pers.) 
Salgado-Maldonado et al., 2004b 
Martínez-Aquino el al., 2009b
 68 
 
 
Phyllodistomum pe Allodontichthys zonistius / 1 Tama 32 9.38 1.33 + 0,42 Presente trabajo 
Nota 3 Allotoca zacapuensis / 1, Vu Zaca 32 9.38 ND Martínez-Aquino et al., 2012 
Hubbsina turneri | Vu Zaca 20 10 ND Martínez-Aquino et al., 2012 
Ilyodon furcidens / 1 Tama 56 7.14 1.25 +0.35 Presente trabajo 
Zoogoneticus purhepechus / Vu Luz 45 2.2 0.02 +0.15 Martínez-Aquino et al., 2011 
Zoogoneticus quitzeoensis / Vu  Zaca 32 15.63 ND Martínez-Aquino et al., 2012 
Fam. Haploporidae Nicoll, 1914 
Saccocoeliodes cf. 
Gn . 
sogandaresi Allodontichthys zonistius / 1 Siem 16 56 69 + 68 Salgado-Maldonado et al., 2004b 
Lumsden, 1961 Goodea atripinnis / 1 Zaca 20 75 ND Martínez-Aquino et al., 2012 
Ilyodon furcidens / 1 Siem 51 10 10+1 Salgado-Maldonado et al., 2004b 
Ilyodon whitei / 1 Chis 22 5 ND Salgado-Maldonado ef al., 2001a 
. Au/Es? , . : 
Saccocoeliodes sp. Ameca splendens / 1 Teuc 35 28 3.2+3 Martínez-Aquino, 2005 (datos de tesis) 
Nota 4 33 54.55 3.61 + 2.32 Presente trabajo 
Fam. Macroderoididae 
McMullem, 1937 
ass Au/Gn 
Magnivitellinum simplex Ilyodon furcidens / 1 Siem 51 2 1 Salgado-Maldonado et al., 2004b 
Kloss, 1966 
Metacercarias 
Fam. Clinostomidae Liihe, 1901 
Clinostomun cf. 
A . 
complanatum vGn Allodontichthys zonistius / Cc Siem 5 20 1 Salgado-Maldonado et al., 2004b 
(Ruddolphi, 1814) Tama 32 9.38 1.67 + 0.57 Presente trabajo 
Alloophorus robustus / N. R. Cuit 30 90 ND Guzmán-Cornejo y García-Prieto, 1999 
/H,M Pátz 41 ND ND Peresbarbosa-Rojas ef al., 1994
 69 
 
 
/ Cc 
Allotoca diazi / H, M 
Chapalichthys encaustus | Cc 
Characodon audax / H 
/ Cc, H, M 
/H 
Goodea atripinnis / N. R. 
/H 
/H 
/M 
/N.R. 
/N.R. 
Ilyodon furcidens / Cc 
Skiffia lermae | Ce 
Xenotoca variata | N. R. 
/ N.R. 
/M 
/N.R. 
/ Cc 
N.R. 
N.R. 
N.R. 
/ Cc 
Xenotaenia resolanae | Cc 
Zoogoneticus purhepechus 
Pátz 
Mint 
Zaca 
Pátz 
Luz 
Tobo 
Pinl 
Pin2 
27No 
Berr 
Cuit 
Igna 
Pátz 
Mint 
Atot 
Reme 
Potg 
Siem 
Siem 
Tama 
Mint 
Cuit 
Laja 
Mint 
Reme 
Ign 
Atot 
Zaca 
Cuza 
Luz 
67 
17 
40 
30 
34 
21 
30 
22 
178 
27 
ND 
ND 
10 
10 
51 
51 
S6 
61 
ND 
30 
41 
ND 
31 
ND 
ND 
ND 
ND 
21 
35 
45 
27 
43 
11.76 
ND 
10 
12.5 
6.7 
28.3 
28.3 
22.2 
21.7 
13 
0.6 
30 
ND 
ND 
20 
10 
3.57 
ND 
3.33 
26.8 
ND 
ND 
14.29 
ND 
ND 
ND 
4.76 
2.86 
11.1 
ND 
4.7+4.7 
ND 
ND 
ND 
4.7:7.07 
1 
ND 
9+ND 
4 ND 
2+1.41 
ND 
ND 
1 
10.32 
1 
1 
10,19 
2 
ND 
ND 
ND 
ND 
1 
ND 
ND 
ND 
ND 
ND 
ND 
1 
0.13 +0,4 
Pérez-Ponce de León et al., 2000 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino et al., 2012 
Peresbarbosa-Rojas et al., 1994 
Pérez-Ponce de León et al., 2000 
Presente trabajo 
Martínez-Aquino et al., 2007b 
Pérez-Ponce de León et al., 2009 
Pérez-Ponce de León et al., 2009 
Pérez-Ponce de León et al., 2009 
Pérez-Ponce de León et al., 2009 
Guzmán-Cornejo y García-Prieto, 1999 
Salgado-Maldonado et al., 2001b 
Salgado-Maldonado y Osorio-Sarabia, 
1987 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Martínez-Aquino, 2005 (datos de tesis) 
Presente trabajo 
Salgado-Maldonado et al., 2004b 
Salgado-Maldonado et al., 2004b 
Presente trabajo 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Romero-Tejada ef al., 2008 
Guzmán-Cornejo y Garcia-Prieto, 1999 
Salgado-Maldonado, 2006 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Romero-Tejada ef al., 2008 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Martínez-Aquino et al., 2012 
Martínez-Aquino et al., 2009a 
Martínez-Aquino et al., 2011
 70 
 
 
Fam. Diplostomidae Poirier, 1886 
. Al/Gn 
Apharyngostrigea sp. 
Tylodelphys sp. 
1/Gn 
/ Cc, M 
Zoogoneticus quitzeoensis / Cc 
/N.RR 
/ Ce 
Goodea atripinnis /N. R. 
Allodontichthys zonistius / Cc 
Állotoca zacapuensis / Cc 
Girardinichthys multiradiatus 
/Cc,M, O 
Goodea atripinnis / Cc 
/N.R. 
/N.R. 
Hubbsina turneri / Cb 
Mint 
Laja 
Tama 
Zaca 
Almo 
Sant 
Atla 
Chic 
Huap 
Ignr 
Juan 
Lagu 
Mina 
Sala 
Sant 
Trin 
Vent 
Vict 
Zemp 
Bizn 
Igna 
Trin 
Mint 
Laja 
Cuit 
Zaca 
Zaca 
30 
ND 
30 
ND 
32 
32 
20 
49 
15 
94 
92 
75 
53 
58 
50 
21 
12 
11 
31 
40 
20 
18 
20 
29 
27 
ND 
30 
20 
20 
ND 
6.6 
ND 
3.13 
6.25 
70 
71.4 
45 
45.7 
100 
15 
70 
3.4 
20 
19 
67 
73 
7.5 
20 
40 
61 
30 
15 
ND 
6.6 
10 
15 
ND 
ND 
1 +0.13 
ND 
5.1 +4.5 
8.9 +16 
6.4 + ND 
6.2 +9.,2 
312.4 
45+5.2 
4+4.2 
2.6 +31 
2.6+31 
42+3.6 
6+3.9 
44+2.4 
2.4 +ND 
97+ND 
7+6.98 
ND 
ND 
ND 
ND 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Romero-Tejada et al., 2008 
Salgado-Maldonado, 2006 
Presente trabajo 
Martínez-Aquino ef al, 2012 
Sánchez-Nava ef al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Salgado-Maldonado ef al., 2001b 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava ef al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Salgado-Maldonado et al., 2001b 
Salgado-Maldonado et al., 2001b 
Salgado-Maldonado et al., 2001b 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Guzmán-Cornejo y García-Prieto, 1999 
Martínez-Aquino ef al., 2012 
Martínez-Aquino et al., 2012
 71 
 
 
Posthodiplostomum 
minimum 
(MacCallum, 1921) Dubois, 1936 
Skiffia lermae / Cb, Cc, H, M 
/N.R. 
/Cc 
Xenotoca variata / Cb, Cc 
/N.R. 
/0 
/ Cc 
Zoogoneticus quitzeoensis / Cc 
/N.R, 
1 Cc 
Allodontichthys zonistius / M 
/ Cc 
ÁAlloophorus robustus | H, M, 
Mu, O 
/ H, M, Mu, 
/N.R. 
/N.R, 
/1G 
/ Cc 
Állotoca diazi / H, M, Mu, O 
Állotoca goslinei / Cc 
Allotoca zacapuensis / Cc, H, M 
Chapalichthys encaustus 
/ HA, M, O, Cc 
Characodon audax 
/ Cb, Cc, H, M 
Mint 
Zaca 
Mint 
Zaca 
Mint 
Zaca 
Siem 
Tama 
Pátz 
Cuit 
Mint 
Pasj 
Ucas 
Pátz 
Mcha 
Potg 
Zaca 
Lcha 
Tobo 
27No 
Guad 
Tobo 
61 
ND 
19 
ND 
21 
30 
ND 
32 
16 
32 
41 
67 
30 
30 
11 
31 
40 
32 
50 
14 
42 
24 
ND 
68.42 
13 
ND 
14.29 
4.76 
13 
ND 
6.25 
13 
3.13 
ND 
81 
93.3 
93 
28 
60 
54.55 
N.D 
70 
88.89 
100 
28.13 
88 
100 
22.2 
42.8 
80.9 
2.6 +3.8 
ND 
ND 
1.5+0.58 
ND 
ND 
ND 
1 
ND 
ND 
40.71 
ND 
ND 
ND 
57.1 + ND 
1.5+0.71 
5 + 4.64 
44.83 + 77.47 
N.D 
N.D 
57.1+ 56.90 
1 
ND 
77.18 + 130.3 
53.63 + 41.2 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Martínez-Aquino et al., 2012 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Romero-Tejada et al., 2008 
Martínez-Aquino et al., 2012 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Martínez-Aquino et al., 2012 
Salgado-Maldonado et al., 2004b 
Presente trabajo 
Peresbarbosa-Rojas et al., 1994 
Pérez-Ponce de León et al., 2000 
Guzmán-Cornejo y García-Prieto, 1999 
Salgado-Maldonado et al., 2001b 
Martínez-Aquino, 2005 (datos de tesis) 
Presente trabajo 
Presente trabajo 
Peresbarbosa-Rojas et al., 1994 
Pérez-Ponce de León et al., 2000 
Presente trabajo 
Presente trabajo 
Martínez-Aquino ef al., 2012 
Martínez-Aquino et al., 2004 
Martínez-Aquino el al., 2007b 
Pérez-Ponce de León et al., 2009 
Pérez-Ponce de León et al., 2009 
Pérez-Ponce de León et al., 2009
 72 
 
 
Girardinichthys multiradiatus 
/H, M 
Girardinichthys viviparus / H, 
M 
Goodea atripinnis / M 
/ A, Mu 
/H, M, Mu, O 
/ A, M, Mu 
/H, M 
/M 
/ Cc, H, M, Mu, O 
/N.R. 
/H 
/ Cc, H, M 
/H, M 
/N.R. 
/H, M
/N.R. 
Chic 
Ignr 
Juan 
Porv 
Sala 
Sant 
Sier 
Vent 
Tica 
Ties 
Tipr 
Chap 
Bizn 
Pátz 
Igna 
Trin 
Juam 
Cuit 
Chap 
Lcha 
Mint 
Laja 
Coin 
118 
52 
13 
14 
53 
58 
50 
36 
32 
11 
11 
30 
40 
12 
31 
25 
178 
35 
59 
30 
22 
30 
20 
27 
ND 
ND 
22 1 
1.9 8 
S0 1.27 +0.89 
8 3 
28.57 9 + 4,83 
ND ND 
5.7 1.3+0.6 
5.2 1 
2 1 
2.8 3 
93.75 29.67 + 44.38 
9.1 1 
9 1 
6.7 1 
2.5 1 
91.67 10.29 
33.33 64 
50 10=+7.07 
13 1.75 +0.96 
60 10.8 + ND 
62 13.3 +ND 
ND ND 
83 ND 
76.67 36.87 + 36.19 
55 5.7 + ND 
25 7+ND 
100 ND 
86.6 ND 
15 1 
62 61.4+76.5 
22 1.67 + 1.03 
ND ND 
75 36.67 + 30.93 
ND ND 
Salgado-Maldonado ef al., 2001b 
Sanchéz-Nava et al., 2004 
Presente trabajo 
Salgado-Maldonado et al., 2001b 
Presente trabajo 
León-Régagnon, 1992 
Sánchez-Nava ef al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Presente trabajo 
Sánchez-Nava et al., 2004 
Sánchez-Nava ef al., 2004 
Sánchez-Nava ef al., 2004 
Sánchez-Nava elf al., 2004 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado ef al., 2001b 
Salgado-Maldonado y Osorio-Sarabia, 
1987 
Peresbarbosa-Rojas et al., 1994 
Pérez-Ponce de León et al., 2000 
Presente trabajo 
Salgado-Maldonado et al., 2001b 
Salgado-Maldonado et al., 2001b 
Salgado-Maldonado et al., 2001a 
Guzmán-Cornejo y García-Prieto, 1999 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado 2006 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006
 73 
 
 
/N.R. 
/N.R. 
/N.R. 
/N.R. 
/N.R. 
/N.R. 
/N.R. 
/ Cc, H, M 
/ Ce 
/ Ce 
Ilyodon furcidens / M 
/H, M 
/G 
/ Ce 
Skiffia lermae / C, Cc, M 
/N.R. 
/C, Ce 
/C, Cc, M 
/ Cc 
Xenotaenia resolanae / M 
Ilyodon whitei / Cc 
Xenotoca variata | N. R. 
/N.R. 
/H, M 
/H, M 
/ N.R. 
/ C, Co, M 
/ N.R. 
Z
L
L
Z
Z
 
D
A
 
Rinc 
Marí 
Cien 
Sori 
Laad 
Atot 
Ferr 
Zaca 
Teuc 
Chic 
Siem 
Potg 
Puen 
Tama 
Mint 
Zaca 
Chap 
Cuza 
Tlap 
Cuit 
Igna 
Mint 
Laja 
Cien 
Rinc 
Atot 
Marí 
Igna 
ND 
ND 
ND 
ND 
ND 
ND 
ND 
20 
38 
29 
51 
10 
10 
S6 
D
V
U
U
U
U
U
 
ND 
ND 
ND 
ND 
ND 
ND 
ND 
25 
100 
33 
70 
30 
1.79 
39 
ND 
30 
21 
100 
2.86 
97.14 
80.4 
80 
57 
6,45 
14.29 
N.D 
2
2
2
2
2
 
V
U
U
U
U
 
ND 
ND 
ND 
ND 
ND 
ND 
ND 
ND 
140 + 134 
2+2 
8.29 + 10.23 
12.33 + 6.07 
2 
10.13 
421:+3.,5 
ND 
N.D 
N.D 
50.13 + 34.05 
1.67+1 
1 
5.74+9.25 
ND 
80 + 26.1 
13.8+ ND 
3.5+2.12 
N. 
V
U
U
U
U
U
U
O
U
 
N 
N 
N. 
N. 
N 
N 
N 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Martínez-Aquino et al., 2012 
Presente trabajo 
Presente trabajo 
Salgado-Maldonado et al., 2004b 
Martínez-Aquino, 2005 (datos de tesis) 
Presente trabajo 
Martínez-Aquino, 2005 (datos de tesis) 
Presente trabajo 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Romero-Tejada et al., 2008 
Martínez-Aquino et al., 2012 
Presente trabajo 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino et al., 2009a 
Presente trabajo 
Guzmán-Cornejo y García-Prieto, 1999 
Salgado-Maldonado et al., 2001b 
Salgado-Maldonado ef al., 2001b 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Romero-Tejada ef al., 2008 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006
 74 
 
 
Uvulifer sp. Avena 
Fam. Heterophyidae Odhner, 1914 
Ascocotyle (Ascocotyle) 
tenuicollis 
Price, 1935 
AVGn 
Centrocestus formosanus 
(Nishigori, 1924) 
Fam. Plagiorchiidae Lúhe, 1901 
Ochetosoma brevicaecum 
(Caballero y Caballero, 1941) 
Monogenea 
Zoogoneticus quitzeoensis 
/ Cc, H, M 
/ N.R. 
Goodea atripinnis / N. R. 
Xenotoca variata / N.R. 
Allodontichthys zonistius / Co 
Ameca splendens | Ab 
Goodea atripinnis / Ab 
/N.R. 
/N.R. 
/N.R. 
Ilyodon whitei / Ab 
Ilyodon furcidens / Ab 
Girardinichthys multiradiatus 
/M 
Allotoca diazi / 1 
Goodea atripinnis / 1 
Mint 
Laja 
Cien 
Siem 
Teuc 
Igna 
Cien 
Atot 
Laja 
Amac 
Chis 
Siem 
Puen 
Chic 
Pedr 
Juan 
Porv 
Sant 
Pátz 
Pátz 
30 
N.D 
ND 
ND 
16 
35 
11 
ND 
ND 
ND 
520 
22 
51 
52 
25 
58 
36 
49 
31 
59 
17 
N.D 
ND 
ND 
27 
ND 
ND 
ND 
50 
49 
81.81 
14 
100 
17 
1.7 
2.8 
ND 
ND 
2.4+2 
N.D 
ND 
ND 
2.3+2.3 
5+ND 
ND 
ND 
ND 
ND 
5+ND 
ND 
157 
26 + 15.62 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado et al., 2004b 
Martínez-Aquino, 2005 (datos de tesis) 
Scholz y Salgado-Maldonado, 2000 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado ef al., 2001a 
Scholz y Salgado-Maldonado, 2000 
Salgado-Maldonado el al., 2001a 
Salgado-Maldonado et al., 2004b 
Martínez-Aquino, 2005 (datos de tesis) 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava ef al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Peresbarbosa-Rojas et al., 1994 
Pérez-Ponce de León et al., 2000
 75 
 
 
Fam. Girodactylidae Van Beneden y 
Hesse, 1863 
Gyrodactylus lamothei es 
Mendoza-Palmero, 
Sereno-Uribe 
y Salgado-Maldonado, 2009 
Nota 5 
Gyrodactylus mexican e 
Mendoza-Palmero, 
Sereno-Uribe 
y Salgado-Maldonado, 2009 
Nota 6 
Gyrodactylus sp. 1 Au/Es? 
Nota 7 
Allotoca diazi / Ab 
Állotoca dugesii / Ab 
Goodea atripinnis / A 
Girardinichthys multiradiatus 
/ A, Ab, P 
/A 
Állotoca dugesii / Ab 
Girardinichthys multiradiatus 
/ A, Ab, P 
Goodea atripinnis / A 
Shaffia lermae / Ab 
Xenotoca variata / Ab 
Állotoca diazi / A, Ab 
Allotoca dugesii / A, Ab 
Characodon audax | A 
Characodon lateralis / A 
Girardinichthys multiradiatus / 
A 
Goodea atripinnis / A 
Mcha 
Mcha 
Zúñi 
Chic 
Cano 
Mcha 
Chic 
Rinc 
Laja 
Atot 
Chap 
Chap 
Igna 
Mcha 
Mcha 
Tobo 
Berr 
Chic 
Trin 
21 
22 
258 
22 
258 
ND 
32 
ND 
24 
10 
13 
32 
30 
21 
22 
42 
23 
44 
29 
10 
14 
14 
24 
20 
10 
14 
ND 
12 
ND 
13 
10 
S0 
5.26 
20 
19 
2.66 
7+ND 
3+ND 
1.6+ND 
db 
>
.
 
o
.
 
po
 
2+1.41 
15+ND 
0.7 + ND 
1:ND 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Mendoza-Palmero et al., 2009 
Mendoza-Palmero et al., 2007 
Presente trabajo 
Mendoza-Palmero et al., 2009 
Salgado-Maldonado, 2006 
Presente trabajo 
Salgado-Maldonado, 2006 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo
 76 
 
 
Gyrodactylus sp. 2 Au/Es? 
Nota 8 
Gyrodactylus sp. Al 
Nota 9 
Fam. Dactylogyridae Bychowsky, 
1933 
. . Au/Es? 
Salsuginus angularis 
(Mueller, 1934) 
Beverly-Burton, 1984 
Nota 10 
/ Ab 
Skiffia lermae / A, Ab 
Xenotoca melanosoma / Ab 
Zoogoneticus quitzeoensis | A 
Állotoca duguesii / Ab 
Skiffia lermae / Ab 
Goodea atripinnis / A 
Állotoca diazi / Ab 
Allotoca dugesii / Ab 
Ámeca splendens / Ab 
Chapalichthys encaustus / Ab 
Characodon audax / Ab 
Goodea atripinnis / Ab 
Ilyodon furcidens / Ab 
Ilyodon whitei / Ab 
Skiffia lermae / Ab 
Skiffia multipunctata 
/ Ab 
Xenotaenia resolanae / Ab 
Xenotoca melanosoma / Ab 
Xenotoca variata | Ab 
Mcha 
Mcha 
Nori 
Mint 
Mcha 
Mcha 
Sori 
Mcha 
Mcha 
Teuc 
Lcha 
Tobo 
Mint 
Rinc 
Sori 
Puen 
Ahue 
Mint 
Duer 
Cuza 
Cuis 
Nori 
Mint 
13 
32 
38 
22 
22 
19 
ND 
35 
20 
31 
ND 
40 
50 
47 
11 
13 
10 
26 
ND 
41 
41 
5.71 
16 
43.3 
ND 
4.54 
ND 
ND 
33.33 
ND 
33.33 
12 
69.44 
20 
S0 
19 
ND 
7.69 
1+ND 
1.66 + ND 
2 
1.6+ND 
1+ND 
1,2 + ND 
ND 
2.4+ 0.82 
2.4+ 1.77 
10 
3.13 +1.55 
1.85 + 0.99 
2 
ND 
6 
ND 
ND 
4 
ND 
2.5: 0.75 
1 
1.46 + 1.3 
0.2 
1.78 + 0.62 
1.33 + 0.82 
ND 
1 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Salgado-Maldonado, 2006 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Martínez-Aquino et al., 2004 
Martínez-Aquino et al., 2007b 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Presente trabajo 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Presente trabajo
 77 
 
 
Rinc ND ND ND Salgado-Maldonado, 2006 
Cien ND ND ND Salgado-Maldonado, 2006 
27 5 1 Presente trabajo 
Zoogoneticus quitzeoensis / Ab Mint 30 13 3.25+2.6 Martínez-Aquino, 2005 (datos de tesis) 
ND ND ND Salgado-Maldonado, 2006 
22 100 2.8 Presente trabajo 
Cestoda 
Fam. Bothriocephalidae 
Blanchard, 1849 
Bothriocephalus 
acheilognathi? o” Álloophorus robustus / 1 Pátz 41 ND ND Peresbarbosa-Rojas et al., 1994 
Y amaguti, 1934 67 1.5 ND Pérez-Ponce de León et al., 2000 
Mint 27 7.4 ND Romero-Tejada ef al., 2008 
Állotoca diazi / 1 Pátz 31 ND ND Peresbarbosa-Rojas ef al., 1994 
40 8 ND Pérez-Ponce de León et al., 2000 
Allotoca zacapuensis / 1 Zaca 17 11.8 0.3+0.1 Mejía-Madrid et al., 2005 
32 3.13 ND Martínez-Aquino et al., 2012 
Characodon audax / 1 Berr 13 1.71 0.3+1.1 Mejía-Madrid et al., 2005 
Pinl 34 8.8 Pérez-Ponce de León et al., 2009 
Pin2 21 14.2 Pérez-Ponce de León et al., 2009 
27No 9 22.2 Pérez-Ponce de León et al., 2009 
Guad 14 22.2 Pérez-Ponce de León et al., 2009 
Characodon lateralis / 1 Juas 11 7.1 Pérez-Ponce de León et al., 2009 
Girardinichthys multiradiatus / 
1 Cler ND ND ND García-Prieto y Osorio-Sarabia, 1991 
Lerm 9 ND ND León-Régagnon, 1992 
Chic 63 3 1 Salgado-Maldonado et al., 2001b 
92 2.2 1 Sánchez-Nava et al., 2004 
52 1.9 1 Sánchez-Nava et al., 2004 
Lagu 50 26 2.5+1.8 Sánchez-Nava et al., 2004 
Atla 15 13,3 1 Sánchez-Nava et al., 2004 
Cimm 7 42.9 1.7+0.6 Sánchez-Nava et al., 2004
 78 
 
 
Goodea atripinnis / 1 
Ilyodon cortesae / 1 
Ilyodon whitei / 1 
Neotoca lermae / 1 
Xenotoca variata / 1 
Skiffia bilineata / 1 
Zoogoneticus purhepechus / 1 
Zoogoneticus quitzeoensis / 1 
Ignr 
Juan 
Pedr 
Sala 
Sier 
Vent 
Trin 
Mara 
Cano 
Tica 
Lcha 
Bata 
Lcha 
Galv 
Xote 
Laad 
Cutz 
Ahue 
Mint 
Cons 
Igna 
Galv 
Xote 
Mint 
Cien 
Laad 
Atot 
Rinc 
Quer 
Negr 
Mint 
75 
53 
58 
S0 
25 
12 
30 
40 
ND 
14 
12 
ND 
41 
ND 
ND 
ND 
ND 
30 
51 
61 
ND 
36 
10 
ND 
ND 
31 
ND 
ND 
ND 
ND 
ND 
15 
27 
30 
2.7 
24.5 
6.9 
8.3 
10 
12.5 
ND 
50 
60 
91.67 
ND 
12 
ND 
ND 
ND 
ND 
6.7 
1.96 
ND 
ND 
ND 
19 
ND 
ND 
ND 
ND 
ND 
6.6 
7.4 
3 
2ND 
1=+0.29 
ND 
4ND 
ND 
ND 
ND 
ND 
0.2+0.9 
10.14 
1 =2.83 
ND 
3.2 + ND 
ND 
ND 
2+2,45 
ND 
ND 
ND 
ND 
N.D 
0.1+0.,3 
0.07 + 0.27 
1 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava ef al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava ef al., 2004 
Salgado-Maldonado y Pienda-López, 2C 
Mejía-Madrid et al., 2005 
Astudillo-Ramos y Soto-Galera, 1997 
Mendoza-Palmero et al., 2007 
Presente trabajo 
García-Prieto y Osorio-Sarabia, 1991 
Pineda-López y González-Enríquez, 19 
Garcia-Prieto y Osorio-Sarabia, 1991 
Salgado-Maldonado y Pineda-López, 2€ 
Salgado-Maldonado y Pineda-López, 2( 
Pineda-López y González-Enríquez, 19 
Salgado-Madonado, 2006 
Mejía-Madrid et al., 2005 
Presente trabajo 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Madonado, 2006 
Pineda-López y González-Enríquez 199 
Salgado-Maldonado et al., 2001b 
Salgado-Maldonado y Pineda-López, 2C 
Salgado-Maldonado y Pineda-López, 2( 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Madonado, 2006 
Salgado-Madonado, 2006 
Salgado-Madonado, 2006 
Salgado-Madonado, 2006 
Salgado-Madonado, 2006 
Mejía-Madrid et al., 2005 
Martínez-Aquino et al., 2011 
Martínez-Aquino, 2005 (datos de tesis)
 79 
 
 
Proteocephalus 
longicollis 
(Zeder, 1800) Nota 11 
Fam. Caryophyllacidae Leuckart, 
1878 
Caryophyllidea gen. sp. Av 6n? 
Metacéstodos 
Fam. Dilepididae Railliet 
y Henry, 1909 
Dilepididae gen. gp On 
Cyclustera cf. raven 
(Underwood y Dronnen, 1986) 
Bona, 1994 
Alloophorus robustus / 1 
Goodea atripinnis / 1 
Skiffia lermae / 1 
Állotoca zacapuensis / M 
Characodon audax | M 
Allodontichthys zonistius / M 
Ilyodon furcidens / M 
Alloophorus robustus / M 
Álloophorus robustus / M 
Girardinichthys multiradiatus 
/M 
Mint 
Pátz 
Pátz 
Mint 
Zaca 
Tobo 
Siem 
Siem 
Mint 
Pátz 
Chic 
Juan 
Mina 
Porv 
Sier 
Vent 
Ties 
ND 
27 
ND 
178 
25 
32 
30 
16 
51 
25 
211 
92 
52 
44 
50 
21 
36 
30 
40 
ND 
16.67 
ND 
34 
24 
3.13 
20 
10 
5.4 
5.8 
2.27 
28 
4.8 
36.1 
3.3 
16.67 
ND 
ND 
ND 
1.5 
0.4=1 
ND 
1.7+0.8 
Salgado-Madonado, 2006 
Romero-Tejada et al., 2008 
Mejía-Madrid et al., 2005 
Salgado-Maldonado y Osorio-Sarabia, 
1987 
Mejía-Madrid et al., 2005 
Martínez-Aquino ef al., 2012 
Martínez-Aquino et al., 2007b 
Salgado-Maldonado et al., 2004b 
Salgado-Maldonado et al., 2004b 
Martínez-Aquino, 2005 (datos de tesis) 
Scholz y Salgado-Maldonado, 2001 
Scholz y Salgado-Maldonado, 2001 
Sánchez-Nava et al., 2004 
Sánchez-Nava ef al., 2004 
Presente trabajo 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava el al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Presente trabajo
 80 
 
 
Ignr 14 14.29 10.36 Presente trabajo 
Chapalichthys encaustus / M Lcha 50 2 1 Martínez-Aquino el al., 2004 
Xenotoca variata / M Igna 24 8 1 Scholz y Salgado-Maldonado, 2001 
.. AVGn o , . . 
Glossocercus auritus Goodea atripinnis / H Lcha 8 12 1 Martínez-Aquino, 2005 (datos de tesis) 
(Rudolphi, 1819) 
Valipora 
. AlVGn . o. . . 
campylancristrota Girardinichthys multiradiatus 
(Wedl, 1855) / Vb Lagu 50 1 1 Scholz y Salgado-Maldonado, 2001 
Baer y Bona, 1960 Chic 92 3.1 1.7+0.6 Sánchez-Nava et al., 2004 
52 1.9 1 Sánchez-Nava et al., 2004 
Almo 20 5 1 Sánchez-Nava et al., 2004 
Ignr 75 9.3 19+1 Sánchez-Nava ef al., 2004 
Juan 53 20.8 18+1 Sánchez-Nava et al., 2004 
58 12.1 1.1+0,4 Sánchez-Nava et al., 2004 
50 6 1.7+0.6 Sánchez-Nava et al., 2004 
Sier 30 3 2 Sánchez-Nava et al., 2004 
Sant 49 6.1 1 Sánchez-Nava et al., 2004 
11 9.1 1 Sánchez-Nava et al., 2004 
Mina 21 9.5 1.5%0.7 Sánchez-Nava et al., 2004 
Vent 40 12.5 1 Sánchez-Nava et al., 2004 
Tica 12 91.67 1=+0.29 Presente trabajo 
Girardinichthys viviparus / Vb  Chap 31 19 1.33 + 0.96 Martínez-Aquino, 2005 (datos de tesis) 
Xenotoca variata | Vb Atot ND ND ND Salgado-Maldonado, 2006 
.,. AVGn 
Valipora mutabilis Xenotoca variata | Vb Igna ND ND ND Salgado-Maldonado, 2006 
Linton , 1927 
Fam. Proteocephalidea La Rue, 1911 
Cyclophyllidae gen. sp. VOR Állotoca diazi | Vb Pátz 40 2 ND Pérez-Ponce de León ef al., 2000 
Zoogoneticus purhepechus / Vb Negr 27 31 0.04 +0.10 Martínez-Aquino et al., 2011 
Gn . Au/ . 
Proteocephalidae gen. sp. Alloophorus robustus / H,L M  Pátz 41 ND ND Peresbarbosa-Rojas et al., 1994
 81 
 
 
Proteocephalus 
ambloplitis e? 
(Leidy, 1758) 
Fam. Diphyllobothriidae Líhe, 1910 
. . .. y. Au/Gn 
Ligula intestinalis 
(Linneo, 1758) Bloch, 1782 
Nematoda 
Fam. Capillariidae 
Neveau-Lemaire, 1936 
/T 
Állotoca diazi / H, L, M 
/T 
Goodea atripinnis / Cb 
/1 
Alloophorus robustus / M 
Skiffia lermae / 1 
Xenotoca variata | Cb 
Goodea atripinnis / N. R. 
Xenotoca variata /N. R 
Goodea atripinnis / Cc 
Girardinichthys multiradiatus 
/ Cc 
Pátz 
Pátz 
Mint 
Mint 
Mint 
Laja 
Atot 
Cien 
Pátz 
Lagu 
Trin 
Tgnr 
Juan 
Lagu 
Zemp 
Sala 
67 
31 
40 
35 
59 
61 
31 
ND 
ND 
ND 
ND 
59 
S0 
50 
223 
563 
75 
53 
S0 
20 
32 
58 
ND 
ND 
30 
14 
ND 
ND 
ND 
ND 
9.2 
16 
80 
1.3 
1.9 
55 
25 
ND 
ND 
ND 
ND 
ND 
15+1 
ND 
ND 
ND 
ND 
ND 
3+ND 
1.5+0.7 
ND 
1.6+ND 
1.7 
1 
1 
1.5+0.7 
2.7+1.7 
1.38 +0.79 
Pérez-Ponce de León et al., 2000 
Peresbarbosa-Rojas et al., 1994 
Pérez-Ponce de León et al., 2000 
Peresbarbosa-Rojas et al., 1994 
Pérez-Ponce de León et al., 2000 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
García-Prieto ef al., 1998 
Pérez-Ponce de León et al., 2000 
Salgado-Maldonado et al., 2001b 
Sánchez-Nava ef al., 2004 
Lamothe-Argumedo y Cruz-Reyes, 197: 
Astudillo-Ramos y Soto-Galera, 1997 
Salgado-Maldonado et al., 2001b 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Sánchez-Nava et al., 2004 
Presente trabajo
 82 
 
 
Capillaria eyprinodonticola o 
Huffiman y Bullock, 1973 
Capillaridae gen. sp. On 
. . AvG 
Pseudocapillaria tomentosa » 
(Dujardin, 1843) 
Fam. Rhabdochonidae Travassos, 
Artigas y Pereira, 1928 
Rhabdochona 
ahuehuellensis Es 
Mejía-Madrid y 
Pérez-Ponce de León, 2003 
Ilyodon furcidens / 1 
Goodea atripinnis / 1 
Alloophorus robustus / 1 
Goodea atripinnis / 1 
Goodea gracilis / 1 
Skiffia lermae / 1 
Xenotoca variata / 1 
Allodontichthys hubbsi / 1 
Allodontichthys tamazulae / 1 
Allodontichthys zonistius / 1 
Ataeniobius toweri / 1 
Ilyodon furcidens / 1 
Ilyodon whitei / 1 
Siem 
Ignr 
Bizn 
Pátz 
Igna 
Pátz 
Bizn 
Mara 
Igna 
Jesú 
Mcha 
Laja 
Pihu 
Tama 
Ahue 
Luna 
Guac 
Pihu 
Tama 
Ahue 
21 
20 
25 
20 
ND 
178 
18 
25 
20 
14 
51 
ND 
32 
19 
12 
11 
56 
40 
180 
51 
un
 
ND 
10 
11.1 
20 
7.1 
5.8 
ND 
60 
42.9 
9.38 
84.2 
8.3 
62.5 
36.4 
10.71 
58.3 
63.9 
68.63 
3 + ND 
ND 
2.7 + ND 
0.11 +0,3 
1+ND 
0.2+0.4 
2+ND 
0.1+0.3 
0.2+0,8 
ND 
11.1 
0.6 + 0.8 
1.67 + 0.57 
4.8+3.6 
0.08 + 0.3 
0.08 + 0.3 
0.5+0.7 
1.67 + 0.64 
ND 
1.14+2.4 
3.23 +2,54 
Salgado-Maldonado et al., 2004b 
Salgado-Maldonado et al., 2001b 
Salgado-Maldonado et al., 2001b 
Moravec et al., 2001 
Salgado-Maldonado, 2006 
Salgado-Maldonado y Osorio-Sarabia, 
1987 
Mejía-Madrid et al., 2005 
Salgado-Maldonado ef al., 2001b 
Mejía-Madrid et al., 2005 
Salgado-Maldonado et al., 2001b 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Salgado-Maldonado, 2006 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Presente trabajo 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Presente trabajo 
Mejía-Madrid y Pérez-Ponce de León, 
2003 
Mejía-Madrid et al., 2005 
Presente trabajo
 83 
 
 
Xenotaenia resolanae / 1 
Rhabdochona kidderi en Ilyodon whitei / 1 
Pearse, 1936 
Rhabdochona lichtenfelsi2 ES Álloophorus robustus / 1 
Sánchez-Álvarez, 
Garcia-Prieto y 
Pérez-Ponce de León, 1998 
Állotoca diazi / 1 
Allotoca dugesii / 1 
Állotoca zacapuensis / 1 
Ámeca splendens / 1 
Chapalichthys encaustus / 1 
Teco 
Cuza 
Cuit 
Pátz 
Luz 
Mint 
Oran 
Lcha 
Zaca 
Came 
Pasj 
Ucas 
Pátz 
Mcha 
Mcha 
Zaca 
Teuc 
Lcha 
Luz 
14 
35 
36 
ND 
360 
41 
67 
19 
10 
27 
14 
13 
ND 
17 
11 
31 
40 
10 
22 
17 
32 
35 
17 
33 
50 
17 
28.6 
20 
14 
ND 
40 
ND 
15 
63.2 
80 
50 
14 
3.7 
7.14 
1.1 
S0 
ND 
35.29 
100 
40 
45.45 
ND 
40 
44,44 
ND 
76.5 
65.63 
80 
23.5 
27.27 
28 
58.8 
0.4+0.6 
2.29 + 1.49 
1.2+0.4 
ND 
18 + ND 
ND 
ND 
54+8 
193+1.2 
15+2.4 
ND 
10.27 
0.1 =+0.3 
6 
ND 
ND 
4.5+3.54 
5.5+3.9 
4.80 + 3.82 
ND 
ND 
6.1 +12.2 
8.5 +5.67 
ND 
913.8 
ND 
4.835 
0.2+0.4 
2.11+1.17 
3.93 + 2.92 
1+1.2 
Mejía-Madrid et al., 2005 
Martínez-Aquino et al., 2009a 
Martínez-Aquino, 2005 (datos de tesis) 
Mejía-Madrid y Pérez-Ponce de León, 
2003 
Sánchez-Álvarez et al., 1998 
Peresbarbosa-Rojas et al., 1994 
Pérez-Ponce de León et al., 2000 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Salgado-Maldonado 2006 
Romero-Tejada ef al., 2008 
Presente trabajo 
Mejía-Madrid et al., 2005 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Martínez-Aquino et al., 2012 
Presente trabajo 
Presente trabajo 
Presente trabajo 
Peresbarbosa-Rojas et al., 1994 
Pérez-Ponce de León et al., 2000 
Mejía-Madrid et al., 2005 
Presente trabajo 
Presente trabajo 
Mejía-Madrid et al., 2005 
Martínez-Aquino et al., 2012 
Martínez-Aquino, 2005 (datos de tesis) 
Mejía-Madrid et al., 2005 
Presente trabajo 
Martínez-Aquino et al., 2004 
Mejía-Madrid et al., 2005
 84 
 
 
Chapalichthys pardalis / 1 
Characodon audax / 1 
Goodea atripinnis / 1 
Tocu 
Berr 
Cuit 
Pátz 
Juam 
Esto 
Luz 
Mint 
Oran 
Tapi 
Merc 
Quer 
Cris 
Tocu 
Coro 
Verd 
Teuc 
Chig 
Lcha 
Rinc 
Igna 
Laja 
Cien 
Sori 
Laad 
Atot 
Zaca 
Idel 
11 
38 
13 
178 
35 
59 
30 
18 
19 
27 
17 
15 
15 
15 
15 
15 
25 
u
a
 
ND 
ND 
ND 
ND 
ND 
ND 
ND 
ND 
20 
36.4 
2.63 
38.5 
ND 
33 
43.33 
94.4 
83.33 
78.9 
80 
19 
11.8 
93.3 
53.3 
6.7 
93.3 
66.7 
80 
60 
100 
50 
100 
S0 
ND 
ND 
ND 
ND 
ND 
ND 
ND 
ND 
25 
100 
0.9+2.1 
1+0.16 
0.7+1.4 
18 +ND 
7.8 +ND 
ND 
ND 
19 + 13.62 
9:77 
ND 
4 
12 + 15.17 
13 +12 
15.85 + 13.76 
0.8+2.7 
24.3 +21.7 
2,4+3.5 
0.1+0.2 
5.7+3.1 
7.218.4 
2.3+2.1 
3816 
9.63 6.2 
2.5+0.71 
62 
8.75 + 11.03 
ND 
ND 
ND 
ND 
ND 
ND 
ND 
ND 
ND 
ND 
Mejía-Madrid et al., 2005 
Presente trabajo 
Mejía-Madrid et al., 2005 
Sánchez-Álvarez et al., 1998 
Salgado-Maldonado y Osorio-Sarabia, 
1987 
Peresbarbosa-Rojas et al., 1994 
Pérez-Ponce de León et al., 2000 
Presente trabajo 
Mejía-Madrid et al., 2005 
Salgado-Maldonado ef al., 2001a 
Salgado-Maldonado et al., 2004a 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Salgado-Maldonado, 2006 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Martínez-Aquino et al., 2012 
Presente trabajo
 85 
 
 
Goodea gracilis / 1 
Hubbsina turneri / 1 
Ilyodon furcidens / 1 
Ilyodon whitei / 1 
Neoophorus regalis / 1 
Skaffía bilineata / 1 
Skiffia lermae / 1 
Skiffia multipunctata / 1 
Xenotoca variata / 1 
Zoogoneticus purhepechus / 1 
Zoogoneticus quitzeoensis / 1 
Opop 
Quem 
Zaca 
Siem 
Tocu 
Rico 
Quer 
Mint 
Zaca 
Duer 
Luz 
Cupa 
Mint 
Igna 
Oran 
Tapi 
Cris 
Cien 
Rinc 
Zaca 
Luz 
Mint 
Zaca 
Came 
Cupa 
Eh 
24 
14 
20 
52 
37 
28 
15 
25 
61 
30 
19 
22 
13 
31 
ND 
29 
ND 
26 
12 
21 
ND 
ND 
21 
45 
30 
ND 
30 
15 
32 
11 
16 
44.44 
25 
92 
92.9 
15.7 
13.51 
46.43 
6.7 
88 
85 
96.67 
100 
12 
86.4 
100 
13 
ND 
21 
ND 
34.6 
66.75 
42.9 
ND 
ND 
71.43 
15.6 
87 
ND 
6.67 
46.7 
15.63 
9.09 
31.25 
7.5+ 6.65 
10.5 
43.4 
13.9+12.4 
ND 
1 
2.40 + 0.97 
6.62 + 6.23 
0.1+0.3 
9.6+8.4 
5.123+6.76 
ND 
ND 
1 
5.3 +6.1 
2 +3.06 
3.25+2.22 
ND 
1.33 + 0.52 
ND 
12+2.1 
3 +3.4 
15+2.6 
ND 
ND 
ND 
2.14 + 1.57 
8.54 + 4.9 
ND 
ND 
1.5+3.1 
ND 
10.30 
2.40 + 1.77 
Presente trabajo 
Presente trabajo 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Martínez-Aquino et al., 2012 
Salgado-Maldonado et al., 2004b 
Presente trabajo 
Presente trabajo 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Salgado-Maldonado 2006 
Romero-Tejada ef al., 2008 
Martínez-Aquino el al., 2012 
Martínez-Aquino, 2005 (datos de tesis) 
Mejía-Madrid et al., 2005 
Presente trabajo 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Mejía-Madrid et al., 2005 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Martínez-Aquino et al., 2012 
Martínez-Aquino et al., 2011 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Romero-Tejada et al., 2008 
Mejía-Madrid et al., 2005 
Martínez-Aquino ef al., 2012 
Presente trabajo 
Presente trabajo
 86 
 
 
Rhabdochona xiphophori“**  Allotoca catarinae / 1 Calt 16 188  28+64 Mejía-Madrid et al., 2005 
Caspeta-Mandujano, Moravec Xenotoca eiseni / 1 Ener 14 35.7 0.6 +1.2 Mejía-Madrid et al., 2005 
y Salgado-Maldonado, 2001 
Au/? . . 
Rhabdochona sp. Ilyodon furcidens / 1 Oro 15 13.33 10.35 Presente trabajo 
Skiffia multipunctata / 1 Adju 2 100 1 Presente trabajo 
Chil 10 100 3.8 + 2,49 Presente trabajo 
Zoogoneticus purhepechus / 1 Negr 27 3.7 2 Martínez-Aquino et al., 2011 
Larvas de Nematoda 
Fam. Acuariodidea Railliet, 
Henry y Sisoff, 1912 
Streptocara sp. AVn Characodon lateralis / 1 Juas 11 9.1 ND Pérez-Ponce de León et al., 2009 
Fam. Anisakidae Railliet 
y Henry, 1912 
Contracaecum sp. On Alloophorus robustus / M Pátz 67 1 ND Pérez-Ponce de León et al., 2000 
Chapalichthys encaustus 
/ Mu, M, G, CC Lcha 50 40 4.05+4.9 Martínez-Aquino et al., 2004 
Characodon audax / CC, M Pin1 34 2.9 ND Pérez-Ponce de León et al., 2009 
Guad 14 7.1 ND Pérez-Ponce de León et al., 2009 
27No 9 33.3 ND Pérez-Ponce de León et al., 2009 
Tobo 42 2.3 ND Pérez-Ponce de León et al., 2009 
Girardinichthys multiradiatus 
/M Almo 20 5 1 Sánchez-Nava et al., 2004 
Atla 25 1 Sánchez-Nava et al., 2004 
Chic 52 1.9 1 Sánchez-Nava ef al., 2004 
Ignr 75 1.3 1 Sánchez-Nava et al., 2004 
Juan 58 2 2 Sánchez-Nava et al., 2004 
50 4 1 Sánchez-Nava et al., 2004 
Pedr 25 8 1 Sánchez-Nava et al., 2004 
Sier 30 10 1 Sánchez-Nava et al., 2004 
Vent 40 5 2.5+2.1 Sánchez-Nava et al., 2004
 87 
 
 
Fam. Camallanidae Raillet y 
Henry, 191 5 
Serpinema trispinosum 
(Leidy, 1852) 
Fam. Dioctophymatidae 
Railliet, 1915 
Eustrongylides sp 
Gn 
Goodea atripinnis / Cc, 1 
Xenotoca variata | M 
Zoogoneticus purhepechus / H 
Alloophorus robustus / M 
Characodon audax / Cc, M 
Goodea atripinnis / M 
Ilyodon furcidens / Cc 
Alloophorus robustus / 1 
Characodon audax / 1 
Álloophorus robustus / Cc, M 
/M 
Állotoca diazi / M 
Characodon audax 1 Cc, M 
Goodea atripinnis / Mu 
Vict 
Igna 
Laja 
Marí 
Cien 
Rinc 
Igna 
Laja 
Rinc 
Marí 
Negr 
Mint 
Tobo 
Lcha 
Puen 
Mint 
Tobo 
Pátz 
Igna 
Zaca 
Ucas 
Pátz 
Tobo 
Pátz 
Bizn 
Atot 
22 
ND 
ND 
ND 
ND 
35 
ND 
ND 
ND 
27 
30 
27 
30 
41 
67 
ND 
ND 
17 
11 
40 
42 
178 
30 
10 
ND 
20 
ND 
ND 
ND 
ND 
31 
ND 
ND 
ND 
3.7 
14 
6.7 
12 
33 
3.3 
3.3 
ND 
15 
ND 
ND 
5.88 
9.09 
11.9 
6.67 
10 
ND 
ND 
ND 
ND 
ND 
1.4+ND 
ND 
ND 
ND 
ND 
ND 
ND 
1=0.3 
ND 
1.3+ND 
10.25 
ND 
Sánchez-Nava et al., 2004 
Salgado-Maldonado ef al., 2001b 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado et al., 2001b 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Martínez-Aquino ef al., 2011 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino et al., 2007b 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino, 2005 (datos de tesis) 
Romero-Tejada et al., 2008 
Martínez-Aquino el al., 2007b 
Peresbarbosa-Rojas ef al., 1994 
Pérez-Ponce de León et al., 2000 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Martínez-Aquino et al., 2012 
Presente trabajo 
Pérez-Ponce de León et al., 2000 
Pérez-Ponce de León et al., 2009 
Salgado-Maldonado y Osorio-Sarabia, 
1987 
Presente trabajo 
Salgado-Maldonado et al., 2001b 
Salgado-Maldonado, 2006
 88 
 
 
Fam. Gnathostomatidae 
Railliet, 1895 
u/Gn A 
Gnathostoma sp. 
. Au/Gn 
Spiroxys sp. 
Girardinichthys multiradiatus 
/Ce 
Girardinichthys viviparus / Cc 
Goodea atripinnis / Mu 
Shaffia lermae / Cc 
Zoogoneticus purhep echus / H 
Alloophorus robustus / H 
Allodontichthys zonistius / Cc 
Alloophorus robustus / M, 1 
Állotoca diazi / M, 1 
Characodon audax ! 
/ 
/M 
/ Cc, M, I 
M 
M, Pi 
Characodon lateralis / H, M 
Goodea atripinnis / 1 
/ M, Pi 
/M,I 
/1 
Almo 
Chap 
Chap 
Mint 
Negr 
Pátz 
Ahua 
Pátz 
Mint 
Mint 
Pátz 
Tobo 
Pinl 
Abra 
27No 
Pin2 
Abra 
Juas 
27No 
Bizn 
Pátz 
ND 
31 
20 
61 
ND 
27 
20 
11 
41 
67 
27 
31 
40 
30 
34 
12 
21 
27 
11 
18 
35 
178 
59 
ND 
35 
ND 
ND 
3.7 
9.09 
ND 
26 
86 
3.7 
ND 
50 
2.9 
16.6 
33.3 
9.5 
29.6 
11.1 
3.5 
ND 
27 
ND 
2.36 + 1.27 
ND 
1 
ND 
1 
1=0.3 
ND 
ND 
2.33 + 1.03 
ND 
ND 
1.87+1.51 
1.38 + 1.06 
ND 
ND 
Sánchez-Nava et al., 2004 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Martínez-Aquino et al., 2011 
Salgado-Maldonado et al., 2001b 
Presente trabajo 
Peresbarbosa-Rojas ef al., 1994 
Pérez-Ponce de León et al., 2000 
Martínez-Aquino, 2005 (datos de tesis) 
Romero-Tejada ef al., 2008 
Peresbarbosa-Rojas et al., 1994 
Pérez-Ponce de León et al., 2000 
Martínez-Aquino et al., 2007b 
Pérez-Ponce de León et al., 2009 
Pérez-Ponce de León et al., 2009 
Pérez-Ponce de León et al., 2009 
Pérez-Ponce de León et al., 2009 
Martínez-Aquino et al., 2007b 
Pérez-Ponce de León et al., 2009 
Pérez-Ponce de León et al., 2009 
Salgado-Maldonado et al., 2001b 
Peresbarbosa-Rojas et al., 1994 
Salgado-Maldonado y Osorio-Sarabia, 
1987 
Pérez-Ponce de León et al., 2000
 89 
 
 
Fam. Kathlaniidae Lane, 1914 
Au/G 
Falcaustra sp. . 
Acanthocephala 
Fam. Pomphorhynchidae 
Y amaguti, 1939 
Pomphorhynchus cf. 
bulbocol 1257 
/ 
/ 
/ Z
Z
Z
 
A
A
A
 
/ N.R. 
Girardinichthys multiradiatus 
/1 
/M 
Ilyodon furcidens / M 
Xenoophorus captivus | Cc, M 
Xenotaenia resolanae / M 
Xenotoca variata / 1 
/M 
Zoogoneticus purhepechus / M 
Zoogoneticus quitzeoensis / M 
Girardinichthys multiradiatus 
/1, M 
ÁAlloophorus robustus / 1 
Zoogoneticus purhepechus / 1 
Trin 
Mint 
Mint 
Laja 
Igna 
Atot 
Ignr 
Porv 
Potg 
Moct 
Cuza 
Igna 
Mint 
Rinc 
Luz 
Cupa 
Mint 
Came 
Lagu 
Tepe 
Luz 
Luz 
Adju 
29 
27 
ND 
ND 
ND 
ND 
13 
36 
10 
30 
2.86 
21 
31 
ND 
ND 
45 
27 
16 
30 
30 
11 
34 
45 
ND 
ND 
ND 
ND 
15 
2.8 
20 
10 
0.06 
ND 
ND 
8.9 
3.7 
18.75 
3.3 
9.09 
12 
100 
5.88 
13.3 
100 
1:ND 
ND 
1.5+1 
3 
1.33 + 0.58 
1 
ND 
3=0.9 
10 + 13.8 
4 
7+1.67 
Salgado-Maldonado et al., 2001b 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Salgado-Maldonado et al., 2001b 
Sánchez-Nava et al., 2004 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino et al., 2009b 
Salgado-Maldonado et al., 2001b 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Salgado-Maldonado, 2006 
Martínez-Aquino et al., 2011 
Martínez-Aquino ef al., 2011 
Presente trabajo 
Martínez-Aquino, 2005 (datos de tesis) 
Romero-Tejada ef al., 2008 
Presente trabajo 
Sánchez-Nava et al., 2004 
Sánchez-Nava ef al., 2004 
Presente trabajo 
Martínez-Aquino et al., 2011 
Presente trabajo
 90 
 
 
Cistacantos 
Fam. Polymorphidae Meyer, 1931 
Polymorphus brevis* 
Van Clave, 1916 
Alloophorus robustus / M, Mu 
/M 
/ Cc, M 
/M 
/ Cc, M 
Allotoca catarinae / Cc. M 
Allotoca diazi / M, Mu 
/M 
Állotoca zacapuensis / Cc, M 
Ámeca splendenss | Cc 
Chapalichthys encaustus / M 
/ Cc, 
M 
Characodon lateralis / M 
Girardinichthys multiradiatus 
/M 
Goodea atripinnis / HA, M 
/H, M 
/Cc, M 
/M 
/Cc 
Hubbsina turneri / Cc, M 
Pátz 
Mint 
Zaca 
Ucas 
Calt 
Pátz 
Zaca 
Teuc 
Lcha 
Luz 
Juas 
Sala 
Sant 
Ignr 
Pátz 
Lcha 
Ucas 
Zaca 
41 
67 
11 
17 
11 
31 
40 
32 
35 
S0 
00
 
12 
32 
11 
ND 
178 
59 
30 
20 
ND 
16 
ND 
100 
14 
5.88 
54.44 
ND 
12.5 
27.2 
8.3 
ND 
3.13 
18.2 
ND 
ND 
27 
ND 
10 
12 
100 
15 
ND 
ND 
ND 
7>+1.41 
3 
ND 
4.33 + 3.35 
ND 
ND 
ND 
ND 
1 
1 
ND 
10.71 
ND 
1 
ND 
1+0.18 
ND 
ND 
ND 
ND 
3 =+1.02 
ND 
Peresbarbosa-Rojas et al., 1994 
Pérez-Ponce de León et al., 2000 
Alcántar-Escalera et al., 2013 
Presente trabajo 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino el al., 2012 
Presente trabajo 
Alcántar-Escalera ef al., 2013 
Peresbarbosa-Rojas ef al., 1994 
Pérez-Ponce de León et al., 2000 
Martínez-Aquino et al., 2012 
Martínez-Aquino, 2005 (datos de tesis) 
Martínez-Aquino ef al., 2004 
Alcántar-Escalera et al., 2013 
Presente trabajo 
Pérez-Ponce de León et al., 2009 
Sánchez-Nava et al., 2004 
Alcántar-Escalera et al., 2013 
Presente trabajo 
Sánchez-Nava et al., 2004 
Alcántar-Escalera ef al., 2013 
Salgado-Maldonado, 2006 
Salgado-Maldonado y Osorio-Sarabia, 
1987 
Pérez-Ponce de León et al., 2000 
Alcántar-Escalera et al., 2013 
Presente trabajo 
Martínez-Aquino, 2005 (datos de tesis) 
Presente trabajo 
Martínez-Aquino et al., 2012
 91 
 
 
Skiffia lermae | Cc, M 
Skiffia multipunctata | Cc, M 
Xenotoca variata | H 
/M 
/H 
/H 
Zoogoneticus purhepechus / M 
/ Cc, M 
Zoogoneticus quitzeoensis 
/ Cc, M 
Zaca 
Cupa 
Igna 
Mint 
Zaca 
Negr 
Adju 
Came 
Cupa 
Magd 
Zaca 
19 
13 
35 
31 
ND 
21 
27 
11 
13 
16 
32 
5.26 
ND 
15.38 
ND 
19.05 
3.7 
ND 
100 
ND 
27.27 
ND 
43.75 
14.29 
6.25 
ND 
ND 
10.38 
1 
1 
ND 
ND 
1 
ND 
1 
ND 
3.67 + 2.68 
ND 
2.86 + 2.52 
3 +1.13 
ND 
Martínez-Aquino et al., 2012 
Alcántar-Escalera et al., 2013 
Presente trabajo 
Salgado-Maldonado et al., 2001b 
Martínez-Aquino, 2005 (datos de tesis) 
Salgado-Maldonado, 2006 
Martínez-Aquino et al., 2012 
Martínez-Aquino et al., 2011 
Alcántar-Escalera et al., 2013 
Presente trabajo 
Alcántar-Escalera et al., 2013 
Presente trabajo 
Alcántar-Escalera ef al., 2013 
Presente trabajo 
Presente trabajo 
Martínez-Aquino et al., 2012 
 92 
 
 
 93 
 
Nota 1.  Este taxón corresponde a una nueva especie, la cual será descrita posteriormente (Choudhury A., com. pers.). 
Nota 2. De acuerdo con Martínez-Aquino et al., 2013, M. guillerminae es sinónimo de M. bravoae, por lo cual los registros aqui presentados 
consideran la distribución de la especie actualmente válida únicamente. 
Nota 3.  Este taxón corresponde a una nueva especie, la cual será descrita posteriormente (Pérez-Ponce de León, com. pers.). 
Nota 4.  Este taxón corresponde a una nueva especie, la cual será descrita posteriormente (Pérez-Ponce de León, com. pers.). 
Nota 5.  Mendoza-Palmero et al. (2007) registaron Gyrordactylus sp. en la Cantera Oriente (Cano), Ciudad Universitaria, UNAM, Ciudad de 
México, D.F; sin embargo, con base en un datos morfológicas más detallados, Mendoza-Palmero (en este trabajo) detectó que la clasificación 
taxonómica correcta es G. lamothei. 
Nota 6.  Salgado-Maldonado (2006) registro Gyrodactylus sp. de las localidades de Rinc y Laja (ver cuadro TAL para más información); sin 
embargo, Martínez-Aquino et al. (en este trabajo), detectaron con base en distintas medidas morfológicas que la clasificación taxonómica correcta 
de este taxón es Gyrodactylus mexicanus. 
Nota 7.  Este taxón corresponde a una nueva especie, la cual será descrita posteriormente (Mendoza-Palmero, com. pers.). 
Nota 8.  Este taxón corresponde a una nueva especie, la cual será descrita posteriormente (Mendoza-Palmero, com. pers.). 
Nota 9.  Salgado-Maldonado et al., (2001) y Sánchez-Nava et al., (2004) registraron Gyrodactylus elegans en Atla, Cimm, Chic, Juan, Pedr, Sala, 
Sant y Sier (ver Cuadro 3 para más información referente a las localidades). Mendoza-Palmero et al., (2009) mencionan que estos autores no 
depositaron ejemplares de referencia en ninguna colección científica que valide dichos registros. Harris et al., (2004) han sugerido que G. elegans 
es específico de Abramis brahama (Linnaeus, 1758) (Cyprinidae). Mendoza-Palmero et al., (2009) sugirieron que la determinación realizada por 
Salgado-Maldonado et al., (2001) y Sánchez-Nava et al., (2004) es dudosa. Por tanto, debido a la no existencia de vouchers depositados en ninguna 
colección científica, en este trabajo nosotros tomamos la postura conservadora de (según el Código Internacional de Nomenclatura Zoológica; 
Ride, 1985) y no consideramos validos los registros de Salgado-Maldonado et al. (2001) y Sánchez-Nava et al. (2004) ya que carecen de rigor 
científico. 
Nota 10.  Martínez-Aquino et al (2004; 2007b) registraron este taxón como posible nueva especie; sin embargo, Mendoza-Palmero (en este 
trabajo), detectó, con base distintas observaciones morfológicas más detalladas, que la determinación y clasificación taxonómica corresponde con 
Salsuginus angularis. 
 94 
 
Nota 11.  Proteocephalus longicollis es considerada un sinónimo de P. pusillus (sin. P. exiguus) La Rue, 1911 (Scholz y Hanzelová, 1998) que 
parasita exclusivamente peces de la familia Salmonidae de distribución holártica por lo que la presencia de esta especie en peces de la familia 
Goodeidae de México requiere una revisión más detallada. 
Cuadro 2. Listado huésped-helminto parásito de Goodeinae (con base en el Cuadro  1). DA = 
Digéneo Adulto; LD = Larva de Digéneo; M = Monogéneo; CA = Céstodo Adulto; LC = Larva 
de Céstodo; NA = Nemátodo Adulto; LN = Larva de Nemátodo; AA = Acantocéfalo; LA = 
Larva de Acantocéfalo. 
Especie de huésped  Helmintos 
    
Allodontichthys hubbsi Miller y Uyeno, 1980 Margotrema bravoae
DA
 
  Rhabdochona ahuehuellensis
NA                           
    
Allodontichthys tamazulae Turner, 1946 Margotrema bravoae
DA
 
  Rhabdochona ahuehuellensis
NA                           
    
    
Allodontichthys zonistius Hubbs, 1932  Ascocotyle (Ascocotyle) tenuicollis
LD 
  Clinostomun complanatum
LD
 
  Dilepididae gen. sp.LC 
  Margotrema bravoae
DA
 
  Phyllodistomum sp.DA 
  Posthodiplostomum minimum
LD
 
  Rhabdochona ahuehuellensis
NA                           
  Saccocoeliodes cf. sogandaresi
DA 
  Spiroxys sp.LN
 
  Tylodelphys sp.LD
 
    
Alloophorus robustus Bean, 1892 Bothriocephalus acheilognathi
CA     
  Clinostomun complanatum
LD
 
  Contracaecum sp.LN 
  Cyclustera cf. ralli
LC 
  Dilepididae gen. sp.LC 
  Eustrongylides sp.LN
 
  Gnathostoma sp.LN
 
  Margotrema bravoae
DA
 
  Polymorphus brevis
LA 
  Pomphorhynhcus cf. bulbocolli
AA 
  Posthodiplostomum minimum
LD
 
  Proteocephalidae gen. sp.LC 
  Proteocephalus longicollis
CA     
  Pseudocapillaria tomentosa
NA                             
  Rhabdochona lichtenfelsi
NA                                  
  Serpinema trispinosum
LN
 
 96 
 
  Spiroxys sp.LN
 
    
Allotoca catarinae de Buen, 1942 Polymorphus brevis
LA 
  Rhabdochona xiphophori
NA                               
    
Allotoca diazi Meek, 1902 Bothriocephalus acheilognathi
CA     
  Clinostomun complanatum
LD
 
  Cyclophyllidae gen. sp.LC   
  Eustrongylides sp.LN
 
  Margotrema bravoae
DA
 
  Ochetosoma brevicaecum
LD
 
  Polymorphus brevis
LA 
  Posthodiplostomum minimum
LD
 
  Proteocephalidae gen. sp.LC 
  Rhabdochona lichtenfelsi
NA                                  
  Spiroxys sp.LN
 
    
Allotoca dugesii Bean,1887  Gyrodactylus lamothei
M
 
  Gyrodactylus mexicanus
M
 
  Gyrodactylus sp. 1 
M
 
  Margotrema bravoae
DA
 
  Rhabdochona lichtenfelsi
NA                                  
  Salsuginus angularis
M 
    
Allotoca goslinei Smith y Miller, 1987 Posthodiplostomum minimum
LD
 
    
Allotoca maculata Smith y Miller, 1980 Margotrema bravoae
DA
 
    
Allotoca meeki Álvarez del Villar, 1959 Margotrema bravoae
DA
 
    
Allotoca zacapuensis Meyer, Radda y Domínguez, 2001 Allocreadium lobatum
DA
 
  Bothriocephalus acheilognathi
CA    
  Caryophyllidea gen. sp.LC 
  Margotrema bravoae
DA
 
  Phyllodistomum sp.DA 
  Polymorphus brevis
LA 
  Posthodiplostomum minimum
LD
 
  Rhabdochona lichtenfelsi
NA                               
  Tylodelphys sp.LD
 
    
Ameca splendens Miller y Fitzsimons, 1971 Ascocotyle (Ascocotyle) tenuicollis
LD 
  Polymorphus brevis
LA 
  Rhabdochona lichtenfelsi
NA                                  
 97 
 
  Saccocoeliodes spDA 
  Salsuginus angularis
M 
    
Ataeniobius toweri Meek, 1904 Rhabdochona ahuehuellensis
NA                           
    
Chapalichthys encaustus Jordan y Snyder, 1899 Clinostomun complanatum
LD
 
  Contracaecum sp.LN 
  Cyclustera cf. ralli
LC 
  Polymorphus brevis
LA 
  Posthodiplostomum minimum
LD
 
  Rhabdochona lichtenfelsi
NA                                  
  Salsuginus angularis
M 
    
Chapalichthys pardalis Álvarez del Villar, 1963 Margotrema bravoae
DA
 
  Rhabdochona lichtenfelsi
NA                                  
    
Characodon audax Smith y Miller, 1986 Allocreadium mexicanum
DA
 
  Allocreadium sp.DA
 
  Bothriocephalus acheilognathi
CA     
  Caryophyllidea gen. sp.
LC
 
  Clinostomun complanatum
LD
 
  Contracaecum sp.LN 
  Gyrodactylus sp. 1M
 
  Eustrongylides sp.LN
 
  Margotrema bravoae
DA
 
  Margotrema sp.DA 
  Posthodiplostomum minimum
LD
 
  Rhabdochona lichtenfelsi
NA                                 
  Salsuginus angularis
M 
  Serpinema trispinosum
LN
 
  Spiroxys sp.LN
 
    
Characodon lateralis Gunther, 1866 Allocreadium mexicanum
DA
 
  Allocreadium sp.DA
 
  Bothriocephalus acheilognathi
CA  
  Gyrodactylus sp. 1 
M
 
  Polymorphus brevis
LA 
  Spiroxys sp.LN
 
  Streptocara sp.LN 
    
Girardinichthys multiradiatus Meek, 1904 Bothriocephalus acheilognathi
CA
 
  Contracaecum sp.LN 
  Cyclustera cf. ralli
LC 
 98 
 
  Eustrongylides sp.LN
 
  Falcaustra sp.LN
 
  Gyrodactylus cf. elegans 
M
 
  Gyrodactylus lamothei
M
 
  Gyrodactylus mexicanus
M
 
  Gyrodactylus sp. 1M
 
  Ligula intestinalis
LC
 
  Margotrema bravoae
DA
 
  Ochetosoma brevicaecum
LD
 
  Polymorphus brevis
LA 
  Posthodiplostomum minimum
LD
 
  Spiroxys sp.LN
 
  Tylodelphys sp.LD
 
  Valipora campylancristrota
LC   
    
Girardinichthys viviparus Bustamante, 1837 Eustrongylides sp.LN
 
  Posthodiplostomum minimum
LD
 
  Valipora campylancristrota
LC   
    
Goodea atripinnis Jordan, 1880 Apharyngostrigea sp.LD
 
  Bothriocephalus acheilognathi
CA     
  Capillaria gen. sp.NA                                            
  Centrocestus formosanus
LD
 
  Clinostomun complanatum
LD
 
  Contracaecum sp.LC 
  Eustrongylides sp.LN
 
  Glossocercus auritus
LC
 
  Gyrodactylus lamothei
M
 
  Gyrodactylus mexicanus
M
 
  Gyrodactylus sp.M 
  Gyrodactylus sp. 1 
M
 
  Ligula intestinalis
LC
 
  Margotrema bravoae
DA
 
  Margotrema sp.DA 
  Ochetosoma brevicaecum
LD
 
  Polymorphus brevis
LA 
  Posthodiplostomum minimum
LD
 
  Proteocephalidae gen. sp.LC 
  Proteocephalus ambloplitis
LC
 
  Proteocephalus longicollis
CA     
  Pseudocapillaria tomentosa
NA                             
  Rhabdochona lichtenfelsi
NA                                  
  Saccocoeliodes cf. sogandaresi sp.DA 
 99 
 
  Salsuginus angularis
M 
  Spiroxys sp.LN
 
  Tylodelphys sp.LD
 
  Uvulifer sp.LD 
    
Goodea gracilis Hubbs y Turner, 1939  Pseudocapillaria tomentosa
NA                             
  Rhabdochona lichtenfelsi
NA                                  
    
Hubbsina turneri de Buen, 1941  Phyllodistomum sp.DA 
  Polymorphus brevis
LA 
  Rhabdochona lichtenfelsi
NA                                  
  Tylodelphys sp.LD
 
    
Ilyodon cortesae Paulo-Maya y Trujillo-Jiménez, 2000 Bothriocephalus acheilognathi
CA     
  Margotrema bravoae
DA
 
    
Ilyodon furcidens Jordan y Gilbert, 1882 Centrocestus formosanus
LD
 
  Capillaria cyprinodonticola
NA                             
  Clinostomun complanatum
LD
 
  Contracaecum sp.LN 
  Dendrorchis sp.DA 
  Dilepididae gen. sp.LC 
  Magnivitellinum simplex
DA 
  Margotrema bravoae
DA
 
  Phyllodistomum sp.DA 
  Posthodiplostomum minimum
LD
 
  Rhabdochona ahuehuellensis
NA                           
  Rhabdochona lichtenfelsi
NA                                  
  Rhabdochona sp.NA                                             
  Saccocoeliodes cf. sogandaresi sp.LD 
  Salsuginus angularis
M 
  Spiroxys sp.LN
 
    
Ilyodon whitei Meek, 1904 Bothriocephalus acheilognathi
CA     
  Centrocestus formosanus
LD
 
  Eustrongylides sp.LN
 
  Margotrema bravoae
DA
 
  Posthodiplostomum minimum
LD
 
  Rhabdochona ahuehuellensis
NA                           
  Rhabdochona kidderi
NA                                        
  Saccocoeliodes cf. sogandaresi
DA 
  Salsuginus angularis
M 
Neoophorus regalis Álvarez del Villar, 1959  
 100 
 
Gyrodactylus sp. 1
M
 
  
Margotrema bravoae
DA
 
Rhabdochona lichtenfelsi
NA           
Salsuginus angularis
M                                       
  
Neotoca bilineata Bean, 1887 Bothriocephalus acheilognathi
CA     
  Rhabdochona lichtenfelsi
NA                                  
    
Skiffia lermae Meek, 1902 Bothriocephalus acheilognathi
CA    
  Clinostomun complanatum
LD
 
  Eustrongylides sp.LD
 
  Gyrodactylus mexicanus
M
 
  Gyrodactylus sp. 1M
 
  Gyrodactylus sp. 2M
 
  Polymorphus brevis
LA 
  Posthodiplostomum minimum
LD
 
  Proteocephalidae gen. sp.LC 
  Proteocephalus longicollis
CA    
  Pseudocapillaria tomentosa
NA                             
  Rhabdochona lichtenfelsi
NA                                  
  Salsuginus angularis
M 
  Tylodelphys sp.LD
 
    
Skiffia multipunctata Pellegrin, 1901 Polymorphus brevis
LA 
  Rhabdochona lichtenfelsi
NA                                  
  Rhabdochona sp.NA                                               
  Salsuginus angularis
M 
    
Xenoophorus captivus Hubbs, 1924 Spiroxys sp.LN
 
    
Xenotaenia resolanae Turner, 1946 Clinostomun complanatum
LN
 
  Dendrorchis sp.DA 
  Margotrema resolanae
DA
 
  Margotrema sp.DA 
  Posthodiplostomum minimum
LD
 
  Rhabdochona ahuehuellensis
NA                           
  Salsuginus angularis
M 
  Spiroxys sp.LN
 
    
Xenotoca eiseni Rutter, 1896 Rhabdochona xiphophori
NA                               
    
Xenotoca melanosoma Fitzsimons, 1972 Gyrodactylus sp. 1M
 
  Margotrema bravoae
DA
 
 101 
 
  Salsuginus angularis
M 
    
Xenotoca variata Bean, 1887 Bothriocephalus acheilognathi
CA     
  Clinostomun complanatum
LD
 
  Contracaecum sp.LN 
  Cyclustera cf. ralli
LC 
  Gyrodactylus mexicanus
M
 
  Margotrema bravoae
DA
 
  Polymorphus brevis
LA 
  Posthodiplostomum minimum
LD
 
  Proteocephalidae gen. sp.LC 
  Proteocephalus ambloplitis
LC
 
  Pseudocapillaria tomentosa
NA                             
  Rhabdochona lichtenfelsi
NA                                  
  Salsuginus angularis
M 
  Spiroxys sp.LN
 
  Tylodelphys sp.LD
 
  Uvulifer sp.LD 
  Valipora campylancristrota
LC   
  Valipora mutabilis
LC   
    
Zoogoneticus purhepechus  Bothriocephalus acheilognathi
CA     
Domínguez-Domínguez, Clinostomun complanatum
LD
 
Pérez-Rodríguez y Contracaecum sp.LN 
Doadrio, 2008 Cyclophyllidae gen. sp.LC   
  Eustrongylides sp.LN
 
  Margotrema bravoae
DA
 
  Phyllodistomum sp.DA 
  Polymorphus brevis
LA 
  Pomphorhynhcus cf. bulbocolli
AA 
  Rhabdochona lichtenfelsi
NA                                 
  Rhabdochona sp.NA                                             
  Spiroxys sp.LN
 
    
Zoogoneticus quitzeoensis Bean, 1898 Allocreadium lobatum
DA
 
  Bothriocephalus acheilognathi
CA     
  Clinostomun complanatum
LD
 
  Gyrodactylus lamothei
M
 
  Gyrodactylus sp. 1 
M
 
  Gyrodactylus sp. 2 
M
 
  Margotrema bravoae
DA
 
  Phyllodistomum sp.DA 
  Polymorphus brevis
LA 
 102 
 
  Posthodiplostomum minimum
LD
 
  Rhabdochona lichtenfelsi
NA                                  
  Salsuginus angularis
M 
  Spiroxys sp.LN
 
  Tylodelphys sp.LD
 
    
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 103 
 
Cuadro 3. Localidades de registros de helmintos parásitos de Goodeinae. Los asteriscos (*) hacen 
referencia las localidades nuevas aportadas por nuestros propios muestreos y aportadas al 
presente estudio. 
Acrónimo Nombre de la localidad y estado 
Tipo de 
hábitat Georreferencias 
    
Abra Abraham González, Durango Canal 24° 12' 50.7'' N; 104° 36' 25.5'' W 
Adju Las Adjuntas, Michoacán Río 19° 54′ 39.3″ N, 102° 12′ 20.0″ W 
Ahua Ahuacapán, Jalisco Arroyo 19º 39' 44.7'' N; 104º 19' 13.7'' W 
Ahue Ahuehuello, Puebla Río 18° 45' 19.0'' N; 98° 34' 20.4'' W 
Almo 
Almoloya, Almoloya del Río, Estado de 
México  Canal 19° 11' 20'' N; 99° 29' 30'' W 
Amac Amacuzac, Morelos Río 18° 38' 47'' N; 99° 27' 02'' W 
Amad Amado Nervo, Durango Manantial 23º 50' 32.0'' N; 104º 11' 13.7'' W 
Atla Atlacomulco, Estado de México Bordo/Lago 19° 47' N; 99° 51' W 
Atot Río La Laja en Atotonilco, Guanajuato Río 21º 00' 07'' N; 100º 47' 42'' W 
Bata El Batán, Querétaro Presa 20° 13' 13'' N; 100° 24' 39'' W 
Berr Los Berros, Durango Manantial 23º 56'' 18.2'' N, 104º 16' 26.4'' W 
Bizn Biznaga, Guanajuato Presa 21° 25' 30'' N; 100° 52' 52.7'' W 
Buen Buenaventura, Chihuahua ? 
29° 50' 16.94'' N; 107° 28' 24.86'' 
W 
Calt Presa Caltzonzin, Michoacán Presa 19º 25' 14.8'' N; 102º 07' 05.8'' W 
Came Lago de Camécuaro, Michoacán Lago 19° 54′ 2.3″ N, 102° 12′ 24.4″ W 
Cano 
Cantera Oriente, Ciudad Universitaria, 
UNAM, Ciudad de México, D.F. Cantera 19º 19' 3'' N; 99º 10' 22.2'' W 
Chap 
Parque Chapultepec, Ciudad de México, 
D.F.,     
Lago 
artificial 19° 25' 21.1'' N; 99° 11' 02.7'' W  
Chic 
Lago de Chicnahuapan, ("Almoloya del 
Río"), Estado de México Lago 19° 11' 20''N; 99° 29' 30'' W  
Chil Chilchota, Michoacán* ?  
Chiq Chiquimitio, Michoacán Arroyo 19° 47' 56.4'' N; 101° 14' 45.9'' W 
Chis El Chisco, Morelos  Río 18° 33' 00'' N; 99° 13' 00'' W  
Cien 
Río La Laja en La Cieneguita, 
Guanajuato Río 20° 57' 08'' N; 100° 47' 42'' W  
Cimm 
"El CIMMYT" Metepec, Estado de 
México Bordo 19° 13' 55'' N; 99° 33' 05 '' W 
Cler Cienega del Lerma Cienega  N. R. 
Coin Cointzio, Michoacán Presa 19° 37' 7''N; 101° 16' 31'' W 
Cons Constitución de 1917, Querétaro Presa 20° 25' 00'' N; 100° 05' 00'' W 
Coro La Coronilla, Jalisco Manantial 20º 28' 9.4'' N; 104º 04' 10.6'' W 
Cris San Cristóbal, Michoacán Manantial 19º 57' 41.6'' N; 101º 18' 57.3''W 
 104 
 
Cuis 
Pueblo de Cuisillos, Rancho de Don 
Ramón Simón, Jalisco* Manantial  20º 35'' 44' N; 103º 46' 33'' W 
Cuit Cuitzeo, Guanajuato-Michoacán Lago 
20° 04' 34''-19° 53' 25'' N; 101° 
19' 34''-100° 50' 20'' W 
Cupa Cupatziro, Michoacán Manantial 19° 52′ 51.3″ N, 102° 12′ 34.7″ W 
Cutz Cutzaróndiro, Durango Manantial 19º 10'' 59.0' N; 101º 30' 13.0'' W 
Cuza Arroyo El Durazno, Jalisco  Arroyo 19° 30.550' N; 104° 17.665' W 
Duer Río Duero, Michoacán Río 19° 53' 03.6'' N; 102° 08' 53.1'' W 
Ener Colonia 6 de enero, Nayarit Lago 21º 31' 31.7'' N; 104º 48' 14.8'' W 
Estó Río Estórax, Querétaro Río 21° 02' 11'' N; 99° 50' 45'' W 
Ferr 
Río La Laja en Ferrocarrileros, 
Guanajuato Río 21º 48' 45'' N; 100º 49' 07'' W 
Galv Los Galvanes, Guanajuato Río 21° 03' N; 100° 48' W 
Guac Guachinango, Michoacán N.D.  20º 32' 0.5'' N; 104º 24' 8.7'' W 
Guad 
Manantial en la UMA de caza, poblado 
de Guadalupe Aguilera, Durango Manantial 24º 25' 59.5'' N; 104º 38' 29'' W 
Idel 
Tributario de Río San Idelfonso, 
Querétaro* Tributario  
Igna Ignacio Allende, Guanajuato Presa 20° 55' N; 100° 50' W  
Ignr Ignacio Ramírez, Estado de México Presa 19° 26' 54'' N; 99° 54' 39'' W  
Jesú Jesús María, San Luis Potosí ? 21º 55' 31.0''N; 100º 54' 38.3'' W  
Juam San Juanico, Michoacán Presa 19° 50' 36'' N; 102° 40' 41'' W  
Juan San Juanico, Estado de México Presa 19° 55' N; 99° 46' W 
Juas Ojo de agua de San Juan, Durango Manantial 23° 57' 11.6'' N;  104° 16' 15'' W 
Laad Río La Laja en Las Adjuntas, Guanajuato Río 21° 07' 29'' N; 100° 52' 12'' W 
Lagu La Lagunilla , Estado de México Bordo 19° 08' 30'' N;  99° 30' 12'' W 
Laja Río La Laja, Guanajuato Río 21° 20' 26'' N;  100° 55' 20'' W 
Lcha Chapala, Jalisco Lago 20° 14' N; 103° 10' W 
Lerm Ciénega del Lerma, Estado de México Humedal 19° 22' 41'' N; 99° 59' 39'' W 
Luna Lago de la Media Luna, San Luis Potosí Lago 21º 51' 18.6''  N; 100º 01' 22.3''  W 
Luz La Luz, Michoacán Manantial  19º 56' 08.1'' N; 102º 18' 0.2'' W 
Magd Canal La Magdalena, Jalisco* Canal  
Mara Maravatío, Michoacán Lago? 19º 52' 56.1'' N; 100º 26' 51.9'' W 
Marc Río San Marcos, Jalisco Río 20º 46' 35.7'' N; 104º 09' 52.6'' W 
Marí 
Río La Laja en Presa Jesús María, 
Guanajuato Presa 21º 21' 16'' N; 101º 12' 49'' W 
Mcha 
Pueblo de Chapultepec, Manantial de 
Chapultepec, Michoacán  Manatial 19º 34' 20'' N; 101º 31' 18.7'' W 
Merc Presa Aristeo Mercado, Michoacán Presa 19º 55' 34.6'' N; 101º 39' 38'' W 
Mina Mina, Toluca, Estado de México Bordo N. D. 
Mint La Mintzita, Michoacán Manantial 
19° 38' 40.3''-19° 38' 52.3'' N;  
101° 16' 28.20''-101° 16' 13.0'' W 
Moct Moctezuma, San Luis Potosí Arroyo 22° 44.673' N; 101° 05.802' W  
 105 
 
Negr Los Negritos, Michoacán Manantial 20º 03' 23.1'' N; 102º 36'38.3'' W 
Nori La Noria, Jalisco* Manantial 20º 35' 45'' N; 103º 46' 54'' W 
Opop Opopeo, Michoacán Lago 19º 24' 16.7'' N; 101º 36' 09.1'' W 
Oran Orandino, Michoacán Lago 19º 57' 21.8'' N; 102º 19' 29.7'' W 
Pásj 
San Jerónimo en Lago de Pátzcuaro,  
Michoacán* 
Pátz Lago de Pátzcuaro, Michocacán Lago 
19° 41' - 19° 32' N; 101° 27' - 
101° 53' W 
Pedr 
San Pedro del Rosal, Atlacomulco, 
Estado de México Bordo N. D. 
Piax 
Río Piaxtla, Municipio de San Dimas, 
Durango Río 24º 21' 59'' N; 105º 31' 7.8'' W 
Pihu Pihuamo, Jalisco Río 19º 15' 23.5'' N; 103º 22' 37.3'' W 
Pin1 
Puente en el poblado de Pino Suárez, 
carretera Durango-Mezquital, Durango ? 23º 52' 43.5'' N; 104º 31' 54.7'' W 
Pin2 Arroyo Pino Suárez 2, Durango ? 23º 52' 12.4'' N; 104º 29' 39.3'' W 
Porv Canal el Porvenir, Michoacán Canal 19° 40' 29'' N; 100° 38' 25'' W  
Potg Potrero Grande, Jalisco Río 20° 31' 17.2'' N; 104° 07' 29.2'' W  
Puen Puente la Rosa, Jalisco Río 19° 27.766' N; 104° 19.134' W 
Quem Tierra Quemada, San Luis Potosí Manantial 21º 42' 39.1'' N; 100º 41' 32.6'' W 
Quer Puente Río Queréndaro, Michoacán Río 19º 53' 09.6'' N; 100º 57' 06.9'' W 
Reye Los Reyes, Michoacán Lago 19º 33' 43.5'' N; 102º 27' 39'' W 
Rico Manantial Rico, Michoacán Manantial 19°49'51.85''N; 102°30‟7.98‟‟W 
Rinc 
Río La Laja en el Rincón de los 
Remedios, Guanajuato Río 20º 47' 20'' N; 100º 48' 25'' W 
Sala Salazar, Estado de México Lago 19° 18' 34'' N; 99° 23' 45'' W  
Sand Rio Santa Isabel en Sandoval, Chihuahua Río 
28° 33' 28.36'' 
N; 106°  31'  38.4''  W 
Sant 
Santiago Tiacaque, Ixtlahuaca, Estado de 
México Presa 19° 40' 22'' N; 99° 42' 28'' W  
Siem Sierra de Manantlán, Jalisco Río 19° 39' N; 104° 14' 24'' W 
Sier 
Parque Sierra Morelos, Estado de 
México Bordo 19° 18' 31'' N; 99° 41' 18'' W 
Sofi 
Río Guatimape en el poblado de Sofía, 
Durango Río 24° 54' 41.1'' N; 104° 32' 7.4'' W 
Sori 
Río La Laja en Soria La Huerta, 
Guanajuato Río 20° 48' 45'' N; 100° 49' 07'' W 
Tama Río Tamazula, Jalisco Río 19º 43' 22.7'' N; 103º 12' 08.5'' W  
Tamo Rio Tamochi, Chihuahua Río 28° 21' 6.8'' N; 107° 51' 10.44'' W 
Tapia Naranja de Tapia, Michoacán Lago 19º 16' 58.2'' N; 101º 45' 50.3'' W 
Teco Río Tecolote, Jalisco Río 19º 27' 40.1'' N; 104º 19' 12.3'' W 
Tepe Tepetitlan, Estado de México Presa 19° 37' 50'' N; 99° 58' 27'' W 
Teuc 
Balneario "El Rincón", Teuchintlán, 
Jalisco Manantial 20°  41.537' N; 103º  50.685' W 
 106 
 
 
 
 
 
 
 
 
 
 
 
Tica 
Canal Santiago Tiacaque, Estado de 
México Canal  
Ties 
Estanque de río en Canal Santiago 
Tiacaque, Estado de México*   Estanque  
Tipr 
Presa en Canal Santiago Tiacaque, 
Estado de México Presa  
Tlap Pueblo Tlapetlahuaya, Puebla “Manantial” 18° 45' 20.4'' N; 98° 34‟ 28.8‟‟ W 
Tobo El Toboso, Durango Manantial 24° 16' 30.7'' N; 104° 34' 52.8'' W  
Tocu Tocumbo, Michoacán Manantial 19º 42' 70'' N; 102º 30' 58.4'' W 
Trin Trinidad Fabela, Estado de México Presa 19° 49' 27'' N; 99° 47' 12'' W  
Tule El Tule, Jalisco Lago 19º 19'' 34.2'' ; 103º 22' 15.0'' W  
Ucas Ucasanastacua, Michoacán* ¿? ¿? 
Vent 
Rancho la Venta, Acambay, Estado de 
México Bordo N. D. 
Verd Río Verde, Jalisco Río 21º 49'' 12.0'' N; 101º 46' 21.3'' W 
Vict Villa Victoria, Estado de México Presa 19° 27' 30'' N; 99° 59' 39'' W 
Xote Río Xote, Querétaro Río N. D. 
Zaca Zacapu, Michoacán Lago 19° 49' N; 101° 47' W 
Zemp Zempoala, Estado de México-Morelos Lago 19° 03' 00'' N; 99° 18' 42'' W 
Zúñi Río Las Zúñigas, Querétaro* Río 20°16‟N, 100°48‟45‟‟W 
27No 
Manantial en el pubelo 27 de Noviembre, 
Durango Manantial 24° 12' 16.5'' N; 104° 29' 38'' W 
        
 107 
 
Apéndice 1. Cuadro de localidades de nuestros muestreos para helmintos parásitos de Goodeinae 
en México. Las georreferencias de cada localidad se detallan en el cuadro 3. N = tamaño de 
muestra de cada especie de huésped por localidad.   
Localidad Especie de huésped N 
1.  Manantial en Ahuacapán, Jalisco Allodontichthys zonistius 11 
 
Ilyodon furcidens 11 
2.  Manantial en Canal La Magdalena, Michoacán Chapalichthys pardalis 3 
3.  Canal la Magdalena, Michoacán Ilyodon furcidens 2 
 
Zoogoneticus purhepechus 7 
4.  Canal de Santiago Tiacaque, Estado de México Girardinichthys multiradiatus 12 
5.  Manantial Chapultepec, Michoacán Allotoca diazi 21 
 Allotoca diazi 9 
 
Allotoca dugesii   22 
Goodea atripinnis 13 
 
 
Skiffia lermae 32 
6.  Manantial Chilchota, Michoacán Skiffia multipunctata 10 
7.  Manantial Cupatziro, Michoacán Skiffia multipunctata 13 
 
Zoogoneticus purhepechus 16 
8.  Arroyo El Durazno en el Río Cuzalapa, Jalisco Xenotaenia resolanae  35 
9.  El Tule (Río), Jalisco Allodontichthys tamazulae 19 
10. Estanque en el Río del Canal Santiago Tiacaque, 
Estado de México 
Girardinichthys multiradiatus 6 
11.  La Angostura, lago Zacapu (balneario), 
Michoacán 
Skiffia lermae 11 
 
Allotoca zacapuensis 32 
 
Goodea atripinnis 20 
 
Hubbsina turneri 16 
 
Skiffia lermae 19 
 
Zoogoneticus quitzeoensis 30 
12.  Manantial La Luz, en Jacona de Plancarte, 
Michoacán 
Zoogoneticus purhepechus  32 
 
Zoogoneticus purhepechus  12 
 
Chapalichthys encaustus 8 
 
Skiffia multipunctata 4 
 
Alloophorus robustus 35 
13.  Manantial La Mintzita, Michoacán, Michoacán Zoogoneticus quitzeoensis 22 
 
Alloophorus robustus 14 
Goodea atripinnis 5 
 108 
 
 Skiffia lermae 6 
 Xenotoca variata 40 
 
14.  Lago de Camecuaro, Michoacán  
Alloophorus robustus 2 
 
Zoogoneticus purhepechus  11 
15. Lago de Opopeo, Michoacán Goodea atripinnis 4 
 
Allotoca meeki 4 
16.  Las Adjuntas (Río), Michoacán  Skiffia multipunctata 2 
 
Zoogoneticus purhepechus  5 
17.  Manantial Los Negritos, Michoacán Chapalichthys encaustus 2 
 
Zoogoneticus purhepechus  19 
 
Zoogoneticus purhepechus  9 
 
Zoogoneticus purhepechus  8 
18.  Manantial Cutzaróndiro, Michoacán Ilyodon cortesae 31 
19.  Manantial La Estancia, Michoacán Zoogoneticus purhepechus  21 
20.  Parque Ecológico Chicnahuapan (Lago), Estado 
de México 
Girardinichthys multiradiatus 44 
 
Girardinichthys multiradiatus 29 
21.  Lago de Pátzcuaro, Michoacán Goodea atripinnis 31 
 
Alloophorus robustus 2 
22.  Predio Porfirio, La Angustura, Lago de Zacapu, 
Michoacán 
Allotoca zacapuensis 3 
 
Xenotoca variata 1 
 
Alloophorus robustus 2 
23. Bordo en el Canal de Santiago, Tiacaque, Estado 
de México 
Girardinichthys multiradiatus 2 
24.  Bordo en Ignacio Ramírez, Estado de México Girardinichthys multiradiatus 14 
25.  Bordo en Salazar, Estado de México Girardinichthys multiradiatus 35 
26.  Manantial Rico, Michoacán Neophorus regalis 39 
26.  Río Ahuehuello en Santo Domingo, Puebla Ilyodon whitei 51 
28.  Río Ángulo cerca del lago de Zacapu, 
Michoacán 
Alloophorus robustus 9 
 
Xenotoca variata 20 
 
Zoogoneticus quitzeoensis 11 
 
Allotoca sp. 2 
29.  Río Tamazula, Jalisco Allodontichthys zonistius 32 
 
Ilydon furcidens 56 
30.  Tributario del Río San Idelfonso, Querétaro Goodea atripinnis 10 
31.  San Jerónimo, Lago Pátzcuaro, Michoacán Alloophorus robustus 5 
32.  Santa María del Oro (Río), Jalisco Ilydon furcidens 15 
 109 
 
33.  Bordo en Tlapetlahuaya, Puebla Ilyodon whitei 34 
34.  Manantial en el parque de Tocumbo, Michoacán Chapalichthys pardalis 38 
 
Goodea atripinnis 16 
 
Ilydon whitei 18 
35.  Ucasanastacua, Pátzcuaro, Michoacán Alloophorus robustus 11 
 
Goodea atripinnis 
 
36.  Puente en el poblado de Pino Suárez, carretera 
Durango-Mezquital, Durango  
Characodon audax 21 
37.  Manantial en Abraham González, Durango  Characodon audax 12 
38.  Manantial en la Unidad de Manejo Ambiental de 
caza, Guadalupe Aguilera, Durango 
Characodon audax 14 
39.  Manantial el Toboso, Durango Characodon audax 42 
40.  Manantial en el poblado Amado Nervo, 
Durango  
Characodon lateralis 9 
41.  Ojo de Agua de San Juan, Durango  Characodon lateralis 11 
42.  Ojo de Agua del poblado de los Berros,  
Durango  
Characodon lateralis 23 
43.  Río Potrero Grande, Jalisco Ilydon furcidens 10 
 
Allotoca goslinei 2 
44.  Río Piaxtla, Municipio San Dimas, Durango Codoma ornata 21 
   
45.  Manantial en Teuchitlán (balneario), Jalisco Ameca splendens  33 
46.  Manantial Veneros, Jalisco Ameca splendens  6 
47.  Río Zúñigas, Queretaro Goodea atripinnis 7 
48.  Río La Laja en el Rincón de los Remedios, 
Guanajuato 
Goodea atripinnis 32 
49.  Río La Laja, Guanajuato Goodea atripinnis 24 
50.  Río La Laja en Atotonilco, Guanajuato Goodea atripinnis 10 
51.  Ignacio Allende, Guanajuato Xenotoca variata 30 
52.  Trinidad Fabela, Estado de México Goodea atripinnis 29 
53.  Puente La Rosa, Jalisco Ilydon furcidens 3 
54.  Río Duero, Michoacán Skiffia multipunctata 8 
55.  Pueblo de Cuisillos, Rancho de  
Don Ramón Simón, Jalisco 
Xenotoca melanosoma 20 
56.  La Noria, Jalisco Xenotoca melanosoma 38 
57.  Río La Laja en La Cieneguita, 
 Guanajuato 
Xenotoca variata 31 
      
    
 110 
 
 
 
 
 
 
 
 
 
 
 
CAPÍTULO II 
MOLECULAR PHYLOGENY OF THE GENUS MARGOTREMA (DIGENEA: ALLOCREADIIDAE), 
PARASITIC FLATWORMS OF GOODEID FRESHWATER FISHES ACROSS CENTRAL MEXICO: 
SPECIES BOUNDARIES, HOST-SPECIFICITY, AND GEOGRAPHICAL CONGRUENCE 
 
 
 
 
 
 
 
 
 
 
 
 
 
 111 
 
En este proyecto se planteo como segundo objetivo particular reconstruir las relaciones 
filogenéticas intraespecíficas del género Margotrema para esclarecer la validez taxonómica de 
sus dos especies putativas (M. bravoae y M. guillerminae), con base en marcadores moleculares. 
Para ello, se reconstruyeron las relaciones genealógicas de 125 ejemplares de Margotrema, 
asociados a 14 especies de goodeinos (incluídas en las cuatro tribus de la subfamilia), además de 
una especie huésped de la familia Cyprinidae (Codoma ornata). Estos ejemplares estaban 
distribuidos en 15 localidades de siete sistemas hidrológicos del centro de México (Martínez-
Aquino et al., 2013). La reconstrucción filogenética se realizó usando una base de datos de 
secuencias de ADN, obtenidos de dos marcadores moleculares: COX-1, mitocondrial e ITS1, 
nuclear. Las bases de datos fueron analizadas, tanto de manera independiente como combinada, a 
través de análisis probabilísticos para la reconstrucción filogenética de secuencias de ADN, es 
decir, de probabilidad posterior (Huelsenbeck & Ronquist, 2001), teoría de la coalescencia 
(GMYC, por sus siglas en ingles General Mixed Yule Coalescent (Pons et al., 2006; Fontaneto et 
al., 2007) y árboles de genes y árboles de especies (Species Tree multispecies coalescent; 
Maddison, 1997; Edwards, 2009). Con base en las relaciones filogenéticas de Margotrema, se 
propusieron las primeras hipótesis biogeográficas y cofilogenéticas observadas para la asociación 
Goodeinae-Margotrema. 
  A continuación se presenta una versión del documento publicado referente a las relaciones 
filogenéticas intraespecificas de Margotrema spp., intitulado:  
Molecular phylogeny of the genus Margotrema (Digenea: Allocreadiidae), parasitic 
flatworms of goodeid freshwater fishes across central Mexico: species boundaries, 
host-specificity and geographical congruence (Martínez-Aquino et al., 2013). 
 
 
 
 
 
 
 
  
Citas $54 ZOOLOGICAL Ve 
Journal ft suis     
Zoological Journal of the Linnean Society, 2013, 168, 1-16. With 5 figures 
Molecular phylogeny of the genus Margotrema 
(Digenea: Allocreadiidae), parasitic flatworms 
of goodeid freshwater fishes across central 
Mexico: species boundaries, host-specificity, 
and geographical congruence 
ANDRÉS MARTÍNEZ-AQUINO*”*, FADIA SARA CECCARELLI* and 
GERARDO PÉREZ-PONCE DE LEÓN! 
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, 
Apartado Postal 70-153, Ciudad Universitaria, México, D.F., México 
?Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Av. Ciudad 
Universitaria 3000, C.P. 04360, Coyoacán, Distrito Federal, México 
“Colección Nacional de Insectos, Instituto de Biología, Universidad Nacional Autónoma de México, 
Apartado Postal 70-153, Ciudad Universitaria, México, D.F., México 
Received 8 November 2012; revised 30 January 2013; accepted for publication 1 February 2013 
We explored the genetic variation at the intraspecific level of two putative species of Margotrema, M. bravoae 
and M. guillerminae, to establish the species boundaries. Sequences of a mitochondrial (COD and nuclear (1TS 1) 
gene were obtained for 125 specimens distributed in 15 localities from seven hydrological systems. An alignment 
of 750 and 831 bp including gaps of COI and ITS1, respectively, was assembled. We analysed the gene fragments 
separately as well as together by using Bayesian inference for phylogenetic reconstruction. Based on the 
phylogenetic analyses, an ultrametric tree was built for each gene, and a general mixed Yule-coalescent model for 
species delimitation was carried out. A multispecies coalescent analysis was performed in *BEAST using both 
molecular markers. The results show four independent evolutionary lineages that we interpret as two valid species 
of Margotrema; the first is represented by an independent lineage, and the second is composed of three lineages. 
Because the species M. bravoae and M. guillerminae nested together within these three lineages, the validity of 
M. guillerminae as an independent species is questioned, and it is proposed to represent a junior synonym of 
M. bravoae. Each lineage shows a congruent geographical pattern with respect to the hydrological system where 
they occur. Additionally, each lineage shows congruence with respect to the hosts they parasitize, either at the 
species or at higher taxonomical levels (tribe). The parasite evolutionary history is congruent with the evolutionary 
and biogeographical history of their hosts. 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16. 
doi: 10.1111/z03.12027 
ADDITIONAL KEYWORDS: COI -— GMYC -— goodeinae — ITS1 — species tree. 
INTRODUCTION they establish with their hosts, has greatly improved 
with the use of molecular tools and a range of ana- 
lytical methods that are available for analysing 
these data sets. Advancements in methodological 
tools has resulted in establishing more robust species 
*Corresponding author. E-mail: delimitation criteria for parasitic organisms and 
maandresCibiologia.unam.mx understanding the influence of host specificity and 
Our understanding of the evolution of parasitic organ- 
isms, as well as the complex and intricate association 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16 1
 112 
 
 
 
2 A. MARTÍNEZ-AQUINO ET AL.  
geography on speciation mechanisms in parasites 
(see Poulin, Krasnov 8; Mouillot 2011a; Poulin et al., 
2011b). Species limits based on molecular results are 
sometimes not congruent with limits established by 
using traditional characters such as morphology. This 
discrepancy is because each gene has a phylogenetic 
history that is intimately connected with, but not 
necessarily identical to, the history of the organism 
in which the genes exist (¡.e. Maddison, 1997; Page € 
Charleston, 1997). Molecular phenomena such as 
gene duplication, incomplete lineage sorting, and 
horizontal gene transfer can produce complex gene 
trees that differ from species trees (i.e. Funk € 
Omland, 2003; Maddison € Knowles, 2006). The 
apparent incongruence between gene trees and our 
conception of what a parasite species is (based only 
on morphological criteria) is still poorly understood. 
Likewise, host-parasite associations might be the 
result of a long evolutionary history that may be 
reflected in similarities in their evolutionary trees 
(Page, 2003, and references therein). Few studies 
have been conducted to address the evolutionary 
history of freshwater fish helminth parasites. For 
example, Choudhury € Dick (2001) analysed the 
historical biogeography of a geologically old group 
of fishes, sturgeons, and their parasite assemblage. 
Apparently, this host—parasite association was his- 
torically structured by colonization and subsequent 
coevolution, and these authors concluded that vicari- 
ance and the dispersal of acipenserids resulted in 
small but widespread and highly distinct mono- 
phyletic parasite lineages. 
In this paper, we have made use of relatively 
novel methodological approaches, and we have 
chosen a host—parasite system that involves a genus 
of digeneans that are allegedly host-specific to 
goodein freshwater fishes, i.e. that form part of the 
biogeographical helminth parasite core fauna (sensu 
Pérez-Ponce de León € Choudhury, 2005). Goodeines 
are an endemic monophyletic group of freshwater 
cyprinodontiforms that are restricted to central 
Mexico (Domínguez-Domínguez etal., 2010). The 
subfamily Goodeinae is represented by 42 species 
included in four monophyletic groups: Girardinich- 
thyini, Chapalichthyini, Ilyodontini, and Characodon- 
tini (each recognized taxonomically as a tribe); the 
phylogenetic relationships and historical biogeogra- 
phy of this group has been studied to a certain extent 
(see Domínguez-Domínguez etal., 2010, and refer- 
ences therein). The diversification of this fish group is 
the result of complex geological events that have been 
taking place since the Miocene in central Mexico, as a 
result of hydro-geomorphological changes that influ- 
enced the orography of this area. Goodeinae repre- 
sents one of the freshwater fish groups that have been 
studied intensively from the parasitological point of 
view (Peresbarbosa-Rojas, Pérez-Ponce de Léon éz 
García-Prieto, 1994; Pérez-Ponce de León et al., 2000; 
Martínez-Aquino etal., 2004, 2007, 2009a, 2011, 
2012; Sánchez-Nava etal., 2004; Mejía-Madrid, 
Domínguez-Domínguez € Pérez-Ponce de León, 
2005). Their helminth parasite faunas consist of 40 
species (Pérez-Ponce de León é€ Choudhury, 2010; 
Martínez-Aquino etal., 2011, 2012). Among the 
helminth species that infect goodeines in central 
Mexico, two putative species of Margotrema, M. bra- 
voae Lamothe-Argumedo, 1972 and M. guillerminae 
Pérez-Ponce de León, 2001, are apparently specific to 
goodein hosts. Subtle morphological differences, i.e. 
extension of the intestinal ceca, being shorter and 
extending posteriad to reach the region of the anterior 
testis in M. guillerminae, vitelline follicles primarily 
lateral to the ceca, and the seminal receptacle located 
immediately posterior to the ovary, are used to dis- 
tinguish Margotrema species, and some authors have 
discussed the need for a study of the intraspecific 
morphological variability (Pineda-López et al., 2005). 
Species of Margotrema have been recorded along 13 
independent hydrological systems in central Mexico, 
parasitizing 22 species of goodeines included in the 
four recognized tribes, although scattered records are 
available for two species of cyprinids, Codoma ornata 
and Notropis calientis, and one species of cyprinodon- 
tid, Cyprinodon nazas. 
In this paper, we study this host—parasite system in 
order to: (1) describe the molecular phylogenetic 
history of populations of the two species of parasites; 
(2) delimit species boundaries based on phylogene- 
tic reconstructions and novel algorithms that use 
maximum likelihood as a means of providing more 
objective outcomes; and (3) test the hypothesis that 
each subgroup of goodeines (tribes) possesses their 
own species of Margotrema as a result of a similar 
history of vicariance and dispersal. This paper is 
based on three main premises: (1) full characteriza- 
tion of parasite biodiversity requires finding all 
species, including those that have formed relatively 
recently and may therefore have minimal levels of 
genetic and morphological divergence; (2) two differ- 
ent species may show no morphological divergence 
because the speciation event is very recent (and struc- 
tural changes have not yet evolved) or, conversely, due 
to morphological stasis over long periods of evolution- 
ary time (Nadler € Pérez-Ponce de León, 2011); and 
(3) the evolutionary history of the parasite reflects 
that of their hosts due to establishing a host-specific 
association and congruent geographical and host 
distribution patterns, at the species or population 
levels. While addressing species delimitation and 
the discovery of independent evolutionary lineages 
at the intraspecific level as the main question, this 
study further intends to decipher the relative role of 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 113 
 
 
 
MOLECULAR PHYLOGENY OF MARGOTREMA 3  
geographical distribution and host-specificity in 
current patterns of parasite genetic variability. 
MATERIAL AND METHODS 
COLLECTION OF HOSTS AND PARASITES 
Between August 2008 and July 2010, a total of 1213 
individual hosts representing 24 goodein species 
(included in the four tribes of Goodeinae) were col- 
lected. Samples were collected from 44 localities dis- 
tributed along seven hydrological systems in central 
Mexico: the San Pedro Mezquital River, Ameca River, 
Ayuquila River, Coahuayana River, Lerma River, 
Cuzalapa River, and Balsas River. Specimens of Mar- 
gotrema spp. were found in 15 of the 44 localities and 
in 15 of the 24 goodein species (see Supporting Infor- 
mation Appendix S1; Fig. 1). We also sampled a few 
specimens of Margotrema spp. in the upper Piaxtla 
River in north-western Mexico (Aguilar-Aguilar et al., 
2010) (Appendix S1). Additionally, in January 2010, 
we collected specimens of two species of digeneans 
in tributaries of the Chagres River in Panama: Wal- 
linia chavarriae Choudhury, Hartvigsen-Daverin «€: 
Brooks, 2002 (Digenea: Allocreadiidae) as a parasite 
of Gephyrocharax sp. (Characidae) at the locality 
of the Frijolito River (09*”08'58.1”N, 79"43'53.8”W), 
and specimens of Prosthenhystera sp. (Digenea: Cal- 
lodistomidae) as a parasite of another species of 
characid at the locality of Quebrada Juan Grande 
(09*08'50.5"N, 79*43'21.1"W); these worms were used 
as outgroups for the phylogenetic analysis in this 
study. Fishes were sampled using minnow traps, 
seine nets, and electrofishing, taken alive to the labo- 
ratory, killed, and individually examined for para- 
sites. Internal organs were removed, placed in a Petri 
dish with 0.65% saline, and examined for helminths 
under a stereomicroscope. Digeneans were removed 
from the intestine of their hosts and placed in 0.65% 
saline. For molecular analysis, some specimens 
of Margotrema spp. (from 14 localities) were cleaned 
with saline and preserved in 100% ethanol. Of all the 
specimens preserved in ethanol and used for molecu- 
lar analysis, digital vouchers (i.e. microphotography 
and videotape) were obtained for 23.3%, Another set 
of specimens were collected and fixed in hot (steam- 
ing) 4% formalin for morphological identification. 
Unflattened specimens were stained with Mayer's 
paracarmine and mounted as permanent slides using 
T 
Conchos River Basin 
eZ 
t-- 
Ayuquila 
  
    
Cuzalapa 
River 
100 0 100 Kilometers   
-25 
-20 
San Pedro Mezquital River Basin 
Lerma River Basin 
  
  
-20        -15  
  
  
 
7 
Balsas River Basin   
Figure 1. Hydrological systems and collection sites for Margotrema spp. in Mexico. Numbers correspond to each locality 
where specimens of Margotrema spp. were collected (for more information see Supporting Information Appendix $2). 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 114 
 
 
 
4 A. MARTÍNEZ-AQUINO ET AL.  
Canada balsam. Digeneans were identified by conven- 
tional morphological criteria following Caira €: Bogéa 
(2005) and Cribb (2005) and the original species 
descriptions (Lamothe-Argumedo, 1972; Pérez-Ponce 
de León, 2001). All specimens collected for morpho- 
logical analysis were deposited as voucher specimens 
of Margotrema spp. in the Colección Nacional de 
Helmintos (CNHE), Instituto de Biología, Universi- 
dad Nacional Autónoma de México (UNAM) [National 
Helminth Collection, Biology Institute, National 
Autonomous University of Mexico], Mexico City 
(Appendix S2). 
DNA EXTRACTION, PCR AMPLIFICATION, 
AND SEQUENCING 
Sequences from two markers were obtained: 750 bp of 
the COI gene and a range of 666-810 bp from the 
ITS1 gene. These markers have proven to be useful 
for establishing species delimitation among digeneans 
(Blair, 2006; Miura etal., 2006; Razo-Mendivil, 
Rosas-Valdez €; Pérez-Ponce de León, 2008). To obtain 
a range of the Margotrema species” genetic variability 
(while avoiding sequencing individuals from the same 
host), DNA was extracted from one individual of Mar- 
gotrema spp. for each host, per locality. In addition, 
specimens of W. chavarriae, Prosthenhystera sp., and 
Allocreadium lobatum Wallin, 1909 (from Semotilus 
atromaculatus from Tobacco Creek, Manitoba, 
Canada) were used for DNA extraction. DNA was 
obtained by using the DNAeasy blood and tissue 
extraction kit (Q)iagen, Valencia, CA, USA) following 
the manufacturer's instructions. Amplifications of 
the selected DNA fragments were carried out in 
a total volume of 25 uL, with 2.5 uL of 10 x PCR 
buffer, 1.25 uL of MgCl,, 1uL of dNTPs (0.25 mm), 
1uL of each primer, 0.4u4L of Tag polymerase 
(OMEGA; 0.625 U), 1-5uL of DNA template and 
13.85 or 17.85 uL of ddHz20. PCRs were carried out 
using primers JB3 fwd (5-TITTTIGGGCATC 
CTGAGGTTTAT-35) (Morgan € Blair, 1998) and 
CO1-R trema rev (5'-CAACAAATCATGATGCAAA 
AGG-3) (Miura et al., 2005) for the COI fragment, 
and Glyp1 fwd (5-GCTGAGAAGACGACCAAACTT 
GAT-35 (Razo-Mendivil etal., 2010) and BD2 rev 
(5'-TATGCTTAAATTCAGCGGGT-3) (Luton, Walker 
$ Blair, 1992) for 1781. To obtain DNA sequences 
of ITS1, we used the following internal primers: 
5.88 rev (5”-AATGTGCGTTCAAGATGTCGAT-3” and 
Relnt BD1 (5'-ATGTTCATAAGACAACCCAGCTC-353, 
specifically designed for this study. PCR cycling con- 
ditions were as follows: for COI, an initial denaturing 
step of 5 min at 94 *C, followed by 35 cycles of 92 *C 
for 30 s, 47 *C for 45/50 s, and 72*C for 90 s, and a 
final extension step at 72 *C for 10 min; for 1TS1, an 
initial denaturing step of 2 min at 94 *C, followed by 
30 cycles of 94 *C for 1 min, 50 *C for 15 s, and 60 *C 
for 4 min, and a final extension step at 60 ”C for 
5 min. PCR products were either purified using 
Millipore columns (Millipore, Bedford, MA, USA) 
and then sequenced on an ABI Prism 3100 Genetic 
Analyser, or sent directly to the High-Throughput 
Genomics Unit at the University of Washington 
(http://www.htseq.org/index.html). 
MOLECULAR DATA SETS 
All sequences were edited using the platform 
Geneiuos Pro v5.1.7 (Drummond et al., 2010). COI 
and /TS1 alignments were assembled using an inter- 
face available with MAFFT v6.717b (Katoh € Toh, 
2008) within Geneiuos Pro, with a final edition by eye 
in the same platform. For the COI sequences, we 
checked the nucleotide alignment and for the pres- 
ence of pseudogenes in Geneiuos Pro, using the trans- 
lated amino acid sequences based on the flatworm 
mitochondrial genetic code. In the I/TS1 marker 
sequences, we detected two 5'-3” regions with differ- 
ent short tandem repeats (STRs). The first region was 
detected after 88 bp in all sequences of Margotrema 
spp., and the second region of 345 bp was only found 
in sequences of individuals from Cuzalapa River, 
Jalisco. As the first region of STRs possesses a total of 
97 variants and second region posseses two variants, 
where homology cannot be established based on 
model substitution (Li ef al., 2002; Ellegren, 2004; 
Guy-Franck, Kerrest € Dujon, 2008), we did no 
use this molecular information in the phylogenetic 
analysis. 
PHYLOGENETIC RECONSTRUCTION AND SPECIES 
DELIMITATION ANALYSES 
The most appropriate DNA sequence evolution model 
was selected by using j¡ModelTest 0.1.1. (Posada, 
2008) and applying the Bayesian Information Crite- 
rion (BIC) (Schwarz, 1978) for each data set sepa- 
rately (COI and ITSI). The COI data set was 
partitioned into first-, second- and third-codon posi- 
tions with the appropriate nucleotide substitution 
model implemented for each codon position [HKY+G 
for the first (Hasegawa, Kishino € Yano, 1985); 
TPM2uf+G for the second (Kimura, 1981); and 
HKY+I-G for the third codon position (Hasegawa 
et al., 1985)]. The nucleotide substitution model that 
fit the ITS1 best was HKY+G. Sequences from two 
additional species, A. lobatum and W. chavarriae, 
were used to root the trees because they belong to 
the same family as Margotrema (Allocreadiidae). An 
additional taxon, Prosthenhystera sp. (Callodistomi- 
dae), was used as an outgroup because it is a sister 
group of the family Allocreadiidae (Curran, Tkach, € 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 115 
 
 
 
MOLECULAR PHYLOGENY OF MARGOTREMA 5  
Ovestreet, 2006, 2011). We inferred the phylogenetic 
relationships using Bayesian inference (BD through 
MrBayes v. 3.1.2. (Huelsenbeck € Ronquist, 2001). 
The phylogenetic trees were reconstructed for 
both genes separately using two parallel analyses 
of Metropolis-coupled Markov chain Monte Carlo 
(MCMO) for 20 x 10% generations each to estimate 
the posterior probability (PP) distribution. Topologies 
were sampled every 1000 generations. Once the 
average standard deviation of split frequencies was 
less than 0.01, as suggested by MrBayes 3.1.2., the 
convergence between runs was checked. The robust- 
ness of the clades was assessed using Bayesian PP for 
the BI analysis, where PP>0.95 was considered 
strongly supported. A majority consensus tree with 
branch lengths was reconstructed for each run after 
discarding the first 15 000 sampled trees. All phylo- 
genetic analyses in this study were carried out using 
the supercomputer HERCULES (http://www.ub.edu/ 
molevol/) at the Universitat de Barcelona, Spain. 
We used general mixed Yule-coalescent (GMYC) 
modelling for estimating species boundaries directly 
based on the phylogenetic tree topology (Pons et al., 
2006; Fontaneto et al., 2007). The GMYC algorithm 
detects differences in the rate of lineage branching at 
the species and population levels, recognizable as a 
sudden increase in the apparent diversification rate 
when the ultrametric node height (distances to tips) is 
plotted against the log number of nodes in a lineage- 
through-time plot (Nee, Mooers € Harvey, 1992). 
Analyses were conducted with each data set sepa- 
rately (COI and ITS1). The consensus trees from the 
BI analyses were passed through the program Tree 
Edit v1.0a10 (Rambaut €: Charleston, 2002) to obtain 
an ultrametric tree with branch lengths using non- 
parametric rate smoothing (NPSR), with the model 
welght rate differences across the root (Sanderson, 
1997). A single threshold value for the input tree 
was used (Monaghan et al., 2009), a method that has 
already been applied successfully to certain groups of 
organisms (i.e. Ahrens, Monaghan € Vogler, 2007; 
Monaghan et al., 2009). The ultrametric phylogenies 
recovered with the MrBayes/Tree Edit were subjected 
to the GMYC analyses script (freely available as part 
of the splits package from http//r-forge.r-project.org/ 
projects/splits/) with the platform R 2.12.0 (R Devel- 
opment Core Team, 2009). A list of delimited GMYC 
species (described in the file's output as maximum- 
likelihood entities) was compiled from the graphical 
output of the GMYC analysis in R. 
We performed a Species Tree (multispecies coales- 
cent) analysis using a multiple marker approach 
applied to the combined data set of COHITS1 to infer 
a species tree from separate genes trees (ie. 
Maddison, 1997; Edwards, 2009). We used the Baye- 
sian MCMC method implemented in *BEAST (star 
BEAST) software (version 1.7.2, Drummond € 
Rambaut, 2007; Heled € Drummond, 2010) to infer 
the genealogical relationship between the lineages of 
Margotrema spp. We performed that analysis on a 
data set that combined both COI and IT'S] data sets, 
implementing the gene-specific substitution models 
of GTR available in the BEAST package (BEAUti 
v.1.7.0; Drummond € Rambaut, 2007). Specifically, we 
used *BEAST to infer the Species Tree of combined 
data sets assuming a Yule speciation process tree prior 
and ran two independent tree searches of 20 x 10% 
generations each, retaining one in every 1000 samples 
from the posterior distribution of the model parameter 
log files and tree files. Branch support for the different 
tree topologies was evaluated by the PP of the inferred 
relationships, where PP>0.95 was considered to 
provide strong nodal support. The trees with the 
highest lineage PP were chosen from the *BEAST 
output files using the program TreeAnnotator v. 1.7.2 
(Drummond € Rambaut, 2007). The Species Tree 
analysis was run in the aforementioned programs 
in the Bioportal of the University of Oslo (http:// 
www.bioportal.uio.no/). Furthermore, the proportion 
(p) of absolute nucleotide sites (p-distance) (Nei éz 
Kumar, 2000) was obtained to compare the genetic 
distance among and between lineages, with and 
without outgroups. We generated two data sets for 
COT and ITS1 as follows: (1) a data set including all 
Margotrema individuals together with sequences of 
species of the same family Allocreadiidae, and (2) a 
data set that included only all individuals of Margot- 
rema. The p-value matrices were obtained for each 
data set gene using MEGA version 5 (Tamura el al., 
2011), with variance estimation with the bootstrap 
method (100 replicates) and with a nucleotide substi- 
tution (transitions + transversions) uniform rate. 
RESULTS 
We obtained DNA sequences from a total of 134 
individuals assigned to Margotrema spp. (127 speci- 
mens, ingroup), Allocreadium lobatum (one specimen, 
outgroup), Prosthenhystera sp. (three specimens, out- 
group), and Walliniae chavarriae (three specimens, 
outgroup). In total, for the ingroup, we obtained 
sequences of COT and 1TS1 from 14 localities that 
were associated with 15 goodein and one cyprinid 
species, respectively (Appendix 2; Fig. 1). In the next 
section, we show the results obtained for each molecu- 
lar marker. 
Col 
We sequenced 125 specimens corresponding to 118 
individuals of Margotrema, one of A. lobatum, three 
of Prostenhystera sp., and three of W. chavarriae. This 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 116 
 
 
 
6 A. MARTÍNEZ-AQUINO ET AL.  
data set consisted of 750 bp, except for two individu- 
als that had 698 bp (one from Chapalichthys pardalis 
and one from llyodon furcidens in Tocumbo), and one 
individual with 621 bp (from Alloophorus robustus). 
For the outgroups, COT sequences of W. chavarriae 
also had 750 bp, Prostenhystera sp. had 445 bp, and 
those of A. lobatum had 687 bp. The level of variation 
in the single nucleotide polymorphisms (SNPs) for 
each partition (first, second, and third codon posi- 
tions) was 97/116/49 conserved, 153/134/201 variable, 
140/131/171 parsimony-informative, and 13/3/30 
singleton sites, respectively. In the partition of the 
protein-coding gene, the third codon position was 
the most variable, followed by the first and then the 
second position. 
We inferred the Bayesian phylogenetic relation- 
ships for 118 individuals of Margotrema to assess 
species limits using GMYC analyses. The results of 
these analyses are presented in Table 1. The number 
of species — independent evolutionary lineages — 
detected by the GMYC analyses with the COI data set 
was 4 (Fig. 2). The genetic distance values among 
the four lineages of Margotrema with COI ranged 
from 2.87 to 9.39% (Table 2), and when the ingroup 
was compared with the outgroups, from 13.65 to 
14.57% with W. chavarriae, from 20.09 to 21.25% 
with A. lobatum, and from 72.47 to 73.07% with 
Prosthenhystera sp. 
Table 1. Number of GMYC species recovered and outputs 
obtained from the single-threshold GMYC analyses per- 
formed for the two data sets examined 
Dataset T NC NS CI LO LGMYC LR 
COI 0.32 5 9 415 590.8 596.8 12.0* 
ITS1 -1.40 4 5 4-14 310.1 320.9 8.3* 
Ultrametric tree reconstruction with the following param- 
eters: T, threshold genetic distance from the branch tips 
where the coalescent-speciation transition occurred; NC, 
number of clusters (GMYC species with more than one 
individual); NS, number of GMYC species discriminated; 
CI, confidence intervals of GMYC species; LO, likelihood of 
null model; LGMYC, likelihood of GMYC model; LR, like- 
lihood ratio with significance indicated by an asterisk 
(FP < 0.01), 
ITS1I 
We successfully obtained a range of 799-810 bp for 98 
individuals of Margotrema, except for one individual 
from Alloophorus robustus from La Mintzita spring 
and one from Characodon audax from the Abraham 
González spring, for which 365 and 722 bp, respec- 
tively, were obtained. The variation in SNPs of the 
ingroup was from 365 to 810 bp, with 715 conserved 
sites, 99 variable sites, 45 parsimony-informative 
sites, and 54 singleton sites. Meanwhile, for out- 
groups, the size of ITS1 was shorter, with 487, 630, 
and 606 bp for one specimen of A. lobatum, two speci- 
mens of Prosthenhystera sp., and two specimens of 
W. chavarriae, respectively. 
The number of species — independent evolutionary 
lineages — detected by GMYC using the topology of 
the Bayesian inference of 98 individuals of Margot- 
rema of I1TS1 was 2 (Fig. 3). The results of the GMYC 
analysis are presented in Table 1. The genetic dis- 
tance value between the two lineages of Margotrema 
with I1TS1 was 3.48%. Lineage I and Lineage ll varied 
by 46.11 and 47.02% with respect to W. chavarriae, 
43.93 and 44.86% with A. lobatum, and 52.3 and 
54.44% with Prosthenhystera  sp., respectively. 
Lineage l, delimited using GMYC based on the 
ITS1 ultrametric tree, corresponds to Lineage 1 from 
the COI-based GMYC analysis as far as individuals, 
hosts, and geographical locations are concerned. On 
the other hand, 17S1-based Lineage II contains indi- 
viduals that were grouped into Lineages II, III and IV 
based on the ultrametric tree obtained with COI. 
COMBINED DATA SET (COL+HITSTD) 
The complete alignment using both COÍ and ITS1 
gene fragments consisted of 93 sequences, of which 
88 corresponded to individuals of Margotrema, two of 
Prosthenhystera sp., one of A. lobatum, and two of 
W. chavarriae, with 1711 bp including gaps. The com- 
bined data set was used to perform a multispecies 
coalescent analysis as implemented in *BEAST, 
resulting in a Species Tree (ST) (Fig. 4). 
The ST analysis represents the most clear-cut 
summary of the data. A brief description of the host— 
parasite association and geographical distribution of 
each of the four lineages recovered by analysis of the 
combined data set of COÍ and ITS]1 gene trees is 
presented next: Lineage 1 is composed of one single 
» 
Figure 2. Bayesian ultrametric tree inferred from the COI data set and subjected to GMYC analysis. Names of terminal 
taxa include a code referring to the locality (four upper-case letters), the host species (three letters), and numbers 
indicating the isolate (for more information see Supporting information Appendix S2). The scale bar represents 
the number of nucleotide substitutions per site. Filled circles above/below branches represent Bayesian posterior 
probability = 0.95. 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 117 
 
 
 
MOLECULAR PHYLOGENY OF MARGOTREMA 17  
mi sp. 
   Wall hi 
Wailinia hi   
 
   
Allocreadium lobatum 
  
   
       
  ZA X 
ZN Es 
TLAP Iwh11 
TLAP [wh10 
LA! 6 
+ 
o 
AHUA Ifu6 
AHUA Ifu5 
AHUA Azo10 
AHUA Azo8 
AHUA Az  
   
   
  
AHUA Azo11 
AHUA Azo9 
AHUA Ifu3 
AHUA Azo4    
  
OPOP Amet 
MINT Zquá 
MINT Zqu3 
MINT Zquí7 
MINT Zqu6 
MINT Zque 
MINT Zquí 
MINT Aro 
o 
o 
La 
hs 
o 
e 
. OPOP Ame3 
MINT Zqu5 
MINT Zquá 
CHAP Adi8 
CHAP Aduá4 
CHAP Adi6 
CHAP Adig 
CHAP Adi 
OPOP Am4 
OPOP Am2 
CHAP Adu6 
CHAP Adu5 
CHAP Adu8 
SHAB Adi 
HAP Adu 
  
CHAP Adi10 
ZACA Aza 
CHAP Adi2 
CHAP Adi13 
CHAP Adi12 
  
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16 
LINEAGE |
LINEAGE ll 
LINEAGE lll 
LINEAGE IV
 118 
 
 
 
8 A. MARTÍNEZ-AQUINO ET AL.  
Table 2. Distance matrix of uncorrected p-distances of 
among and within lineages derived from COI analysis by 
general mixed Yule-coalescence model 
I TI TIT Intralineage 
Lineage 1 0 
Lineage II 8.78 1.15 
Lineage TI 9.39 6.62 1.13 
Lineage IV 9.08 6.04 2.87 0.08 
population distributed in Arroyo Durazno in the 
Cuzalapa River, Jalisco State. This lineage is also 
restricted to a single species of goodein, Xenotaenia 
resolanae, a member of the Tribe Ilyodontini (Figs 1, 
2). The intralineage genetic distance (for COD is null. 
Lineage Il was found in four localities, two of them 
corresponding to the Balsas River Basin (Tlapetla- 
huaya spring, Puebla State, and Tocumbo spring, 
Michoacan State) parasitizing Allodontichthys zonis- 
tius, Ilyodon whitei, I. furcidens (Tribe: Ilyodontini), 
and Chapalichthys pardalis (Tribe: Chapalichthyini), 
one in the Armeria River (stream in Ahuacapán, 
Jalisco State), and the last locality was further 
north in a tributary of the Conchos River Basin 
(Bocoyna, Chihuahua State) parasitizing Codoma 
ornata (Cyprinidae) (Figs 1, 2). Interestingly, no 
species of goodeines are currently distributed in that 
river basin. The intralineage genetic distance in 
Lineage II (for COD is 1.15%. Lineage III is the most 
widespread within Margotrema and contains six 
localities along four hydrological systems included in 
the Lerma River Basin: Opopeo Lake, La Mintzita 
spring, Chapultepec spring, La Luz spring, La Angos- 
tura at Zacapu Lake, and Rico spring, all in Micho- 
acán State (Figs 1, 2). The hosts where Lineage 
III was found correspond to members of the Tribe 
Chapalichthyini (i.e. A. robustus, Zoogoneticus pur- 
hepechus, and Z. quitzeoensis), as well as members 
of the Tribe Girardinichthyini (i.e. Allotoca diazi, 
A. duguest, A. meekti, A. zacapuensis, and Neoophorus 
regalis). The intralineage genetic distance in Lineage 
TIT (for COD is also very low, 1.13%. Finally, Lineage 
IV is found in four localities whose distribution is 
restricted to the Mezquital River Basin (Figs 1, 2), 
and the specimens are found parasitizing Characodon 
audax, a member of the basal tribe of Characodontini 
goodeines. The intralineage genetic distance in 
Lineage IV (for COD is also very low, 0.08%. 
The distinction of the two putative species of 
Margotrema (M. bravoae and M. guillerminae) is not 
supported by the molecular data. As previously men- 
tioned, these two species are separated by having 
intestinal ceca that extend to different levels of the 
body's length. Our molecular analysis clearly shows 
that the two morphs representing such conditions, i.e. 
the long and short ceca, are nested together in what 
is recognized as Lineages II, III and IV (see Figs 2, 3). 
DISCUSSION 
GENERAL PATTERNS OF SPECIES DIVERSIFICATION 
The results of the methodological approach we con- 
ducted in this paper to test species boundaries and as 
a subsequent result to uncover the number of genetic 
lineages of Margotrema based on separate or com- 
bined data sets (¡.e. GMYC analyses) show that only 
Lineage l is consistently recovered by all three analy- 
ses (Figs 2, 3). An important difference between the 
COI and ITS1 species delimitation analyses using 
the GMYC model is the number of lineages recov- 
ered, as COI recovers four lineages (Fig. 2), while 
ITS1 actually recovers only two (Fig. 3). Apparently, 
ITS1 possesses a weaker phylogenetic signal, result- 
ing in two species based on coalescent resolution. 
This finding might be explained by the relatively 
slower rate of evolution (i.e. nucleotide substitution) 
of this gene. In contrast, COI exhibits a higher reso- 
lution because, as a mitochondrial gene, it is consid- 
ered to be a rapidly evolving gene (Avise, 2008; 
Hickerson et al., 2010). Reciprocal monophyly was 
found only in Lineage 1 when the data sets were 
analysed separately. This result strongly supports 
the idea that Lineage 1 represents an undescribed 
species of Margotrema. 
The GMYC model represents an approach designed 
for the identification of independently evolved line- 
ages (species) as the most likely point of transition 
from coalescence to speciation branching patterns on 
an ultrametric phylogenetic tree with branch lengths 
scaled to time (Pons et al., 2006; Fontaneto et al., 
2007). This approach recovers highly diverse biologi- 
cal groups whose boundaries are determined by using 
molecular markers; it has been used in taxonomically 
neglected taxa such as weevils and wasps (see Astrin 
et al., 2012; Ceccarelli, Sharkey € Zaldívar-Riverón, 
2012). Likewise, recent studies have used this 
approach to determine species boundaries at the 
intraspecific level, i.e. using subpopulations that seem 
to represent only one morphologically valid species 
(Marshall et al., 2011). In this study, we used GMYC 
for establishing species boundaries in populations of 
two putative species of Margotrema and for providing 
data to support the idea that species can be delimited 
by using shifts in the phylogenetic branching rate 
that are found by a single-threshold mixed Yule- 
coalescent model (Marshall ef a/., 2011; Powell, 2012). 
In our study, we found contrasting results between 
the two molecular markers in the number of lineages 
delimited because the rates of molecular evolution 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 119 
 
 
 
MOLECULAR PHYLOGENY OF MARGOTREMA 9 
fobatum 
sp. 
  
  
  
  “LINEAGE |
  
  [o
 
P
P
D
 
T
I
T
I
O
 
E
E
C
C
O
!
 
S
P
P
 
E5z
09 
o
 
—_
 
   
TOGU Ifu2 
TOCU Ifu1 
BOGO Cor 
AHUA Azo10 
TLAP Iwh2 
AHUA Azo13 
AHUA Ifu8 
e AHUA Ifu6 
  
 
  
 
  0.4 subst./site 
LINEAGE ll 
  
  
O el
 
Or
 0 S 
O 0
3
 
D N'   
'
O
Z
O
Z
3
I
O
1
 
0
1
0
 
S
O
S
O
R
O
%
 
0
2
0
%
»
 
3
D
 
E 
Ea
 
DA
TA
 
DA
DA
 
DA
D 
2
7
3
4
3
2
4
3
 
O
D
O
D
Z
Z
A
D
Z
N
 
D
U
I
D
S
D
S
 
z
 
z
 
10
00
90
 
0
0
2
0
2
 NL" 
2
2
7
 
Ru 
V
E
 
58
 
a
 
O
S
 D a 
¡as 
GUAG Cha2 
GUAG Cha1 
 
——— Wallinia chavarriao 
——— Wallinia chavarriao 
Figure 3. Bayesian ultrametric tree inferred from the 71781 data set and subjected to GMYC analysis. Names of terminal 
taxa include a code referring to the locality (four upper-case letters), the host species (three letters), and numbers 
indicating the isolate (for more information see Supporting information Appendix $2). The scale bar represents the 
number of nucleotide substitutions per site. Filled circles above/below branches represent Bayesian posterior probabil- 
ity > 0.95. 
differ between the two markers. We chose to follow a 
conservative approach by considering Lineages II, III, 
and IV as a single species with three independently 
evolving lineages with a strong phylogenetic struc- 
ture, suggesting a case of incipient speciation that 
results from the potential lack of gene flow among 
lineages due to geographical separation. The branch- 
ing pattern of the I1TS1 phylogenetic tree, i.e. short 
branches for all terminals, is a strong indicator of 
insufficient time to accumulate polymorphisms and to 
complete the speciation process, even with geographi- 
cal separation of their populations (Figs S1 and S2). 
For instance, Bueno-Silva, Boeger € Pie (2011) found 
similar results while studying a monogenean parasite 
species with freshwater and brackish fish hosts using 
the same molecular markers. 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 120 
 
 
 
10 A. MARTÍNEZ-AQUINO ET AL. 
 
 
 
   
  
[ Prosthenhystera sp. 
[ turn lobatum 
Wallinía ch 
l 1 n= LINEAGE | 
1 
LINEAGE ll 
0.99 
LINEAGE lll 
0.9 
0.003 subst./site LINEAGE IV 
Figure 4. Coalescent-based phylogenetic tree obtained 
from the Species Tree analysis of the combined data set 
(COH+ITS1). The scale bar represents the number of nucle- 
otide substitutions per site. Bayesian posterior probabili- 
ties > 0.95 are shown above the node. 
We took a second step in our analysis and tested 
the genealogical relationships for the combined data 
set of COT and I1T'S1 by using an ST approach with a 
consensus method that allowed us to eliminate the 
effect of the weight of a particular gene (Edwards, Liu 
$: Pear, 2007; Liu et al., 2008). This analysis has the 
ability to jointly infer a summary tree from different 
gene trees (i.e. genealogies) sampled from multiple 
individuals. In this context, a *BEAST analysis works 
by embedding separate genealogies inside a summary 
tree through coalescence backwards in time, starting 
from the tips of the tree (Rannala € Yang, 2003). The 
model assumes that there is no gene flow among the 
focal groups (in our case, the terminal ingroup taxa 
representing independent evolutionary lineages), 
regardless of whether the lineages are taxonomically 
or geographically related, and therefore any incongru- 
ence between the genealogies and the summary tree 
can be explained by the retention of ancestral poly- 
morphisms. This assumption is particularly appropri- 
ate for autogenic digenean parasites with some level 
of host specificity that are distributed in a restricted 
geographical area (i.e. water bodies) that do not natu- 
rally disperse over water and that therefore have no 
gene exchange among host species or hydrological 
systems. For this reason, the *BEAST approach has 
been used recently to analyse all information in the 
mtDNA and nuclear DNA data sets in a single analy- 
sis, given the ability of *FBEAST to account for differ- 
ences in the time to coalesce between haploid 
(mitochondrial) and diploid (nuclear) markers (Heled 
$ Drummond, 2010). This approach can improve the 
accuracy of tree reconstruction compared with the 
more traditional approaches that do not account for 
the coalescent process, assuming that the condition 
of no gene flow among lineages is met (Heled é 
Drummond, 2010). The *BEAST approach is espe- 
cially useful in cases involving recent divergence 
events, where retention of ancestral polymorphisms 
among lineages is more likely to mislead phylogenetic 
reconstruction. This observation may explain the 
results of our analysis as a case of either incipient 
speciation for Lineages II, TI, and IV or the lack of 
gene flow among them. For this reason, we followed 
a conservative position and consider them as a single 
species. The phylogenetic relationships detected 
with the ST approach and the high values of PP 
support these relationships (PP > 98) (Fig. 4), provid- 
ing unambiguous genetic evidence of the discovery of 
four independent evolutionary lineages among Mar- 
gotrema that represent two monophyletic species, 
irrespective of the outgroups analysed. Additionally, 
our results reinforce the idea that species limits can 
be established by using not just the results of a 
phylogenetic inference but also the shifts in the phy- 
logenetic branching rate revealed by the single- 
threshold mixed Yule-coalescent model; furthermore, 
the ST approach was used for combining information 
of two molecular markers as suggested by Marshall 
et al. (2011) and Satler et al. (2011), obtaining a more 
reliable phylogenetic tree of species” relationships. 
TAXONOMIC IMPLICATIONS 
Two species of Margotrema have been described 
thus far, M. bravoae as a parasite of Girardynych- 
thys multiradiatus from the Ciénega de Lerma 
(Lamothe-Argumedo, 1972), and M. guillerminae as a 
parasite of Notropis (=Hybopsis) calientis and 
Alloophorus robustus from Zacapu Lake (Pérez-Ponce 
de León, 2001), both in the Lerma River Basin in 
central Mexico. These species were distinguished 
solely on morphological grounds, and the major dif- 
ference was the extension of the intestinal ceca along 
the body, with M. guillerminae representing a mor- 
photype with short ceca, while M. bravoae exhibited 
long ceca extending posteriorly to half the distance 
between the testes and the posterior end of the body 
(Pérez-Ponce de León, 2001: 1113). Additional records 
of these two species were established in several pub- 
lished accounts after they were originally described, 
even though observation of the distinguishing char- 
acter was particularly difficult in gravid specimens 
because the uterus is normally full with large-sized 
embryonated eggs. Margotrema bravoae had been 
recorded in at least 14 species of goodeines in 14 
localities, while M. guillerminae had been found in 13 
goodeines in 15 localities. Actually, in some localities, 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 121 
 
 
 
MOLECULAR PHYLOGENY OF MARGOTREMA 11  
both species had been recorded in independent 
publications. For instance, in Zacapu Lake, the type 
locality for M. guillerminae, other authors have 
reported the presence of M. bravoae. Mejía-Madrid 
et al. (2005) studied 35 species of goodeines. Of the 
species examined, 18 were infected with Margotrema 
spp., ten were infected with M. bravoae, and eight 
were infected with M. guillerminae; only M. bravoae 
was found in Zacapu Lake. More recently, 
Martínez-Aquino et al. (2012) conducted a study of 
the helminth parasite fauna of goodeines from Zacapu 
Lake, and they only reported the presence of M. cf. 
bravoae. In all of those cases, identification was based 
solely on morphology. Some authors have argued 
about the validity of M. guillerminae; however, they 
provided no empirical evidence and no reliable argu- 
ments to demonstrate that this species was not valid 
(Pineda-López et al., 2005). The results we provide 
in this study are based on molecular evidence and 
demonstrate that, irrespective of the tree topologies 
obtained from either mitochondrial or nuclear genes, 
M. guillerminae should be synonymized with M. bra- 
voae. In all analyses, it can be seen that M. guiller- 
minae, i.e. morphotypes with short ceca, do not 
comprise a monophyletic assemblage. This finding 
means that in Lineages II, III, and IV, representative 
specimens with long ceca are nested together with 
those exhibiting short ceca. Therefore, M. guillermi- 
nae is synonymized with M. bravoae, and it is con- 
cluded that the ceca extension in this group of 
digeneans should not be used as a taxonomic charac- 
ter to establish species distinction. We are currently 
preparing a strictly taxonomic paper in which the 
synonymy will be formally presented by emending the 
diagnosis of M. bravoae and by describing, in a formal 
way, the new species uncovered by the molecular 
data. Furthermore, this synonymy can explain the 
fact that both species have been recorded as occurring 
in sympatry, i.e. in the same localities and host 
species. For instance, both species were recorded as 
parasites of Characodon audax in the Toboso spring, 
Durango (Mejía-Madrid et al., 2005; Martínez-Aquino 
et al., 2007). 
As previously stated, our results provide unambigu- 
ous evidence that Margotrema currently consists of 
two putative species, M. bravoae (represented by 
three well-defined lineages) and an undescribed 
species found exclusively in X. resolanae in the Cuza- 
lapa River, represented in all of our analyses consist- 
ently as Lineage I. Martínez-Aquino et al. (2009a) 
previously recorded M. guillerminae as a parasite of 
X. resolanae; however, this identification was based 
solely on morphological grounds. In the present study, 
we demonstrate that these specimens are an inde- 
pendent evolutionary entity, which was described as 
Lineage l in all analyses, either through GMYC (for 
both molecular markers analysed separately) or 
through ST with the combined data set. This species 
represents an undescribed species, which requires 
further taxonomic work to establish the proper 
species description. Because traditional morphologi- 
cal traits would not be useful, other sources of infor- 
mation need to be explored. 
HOST ASSOCIATION AND BIOGEOGRAPHY 
In the literature, phylogenetic analyses of several 
parasite taxa have been used to uncover patterns of 
close association between both the host species/ 
parasitic taxa and the geographical distribution of 
both associates, resulting, in some cases, in incongru- 
ent patterns due to instances of speciation via host- 
switching or ecological host extensions (Nieberding 
etal., 2008, and references therein). In the case of 
Margotrema spp. and their goodein hosts, it seems 
plausible to postulate, based on the phylogenetic 
information obtained herein, that each lineage shows 
some level of congruence with the hosts they infect 
and the river basin these hosts inhabit. Lineage 1 
shows a restricted distributional range in the Cuza- 
lapa River, in Jalisco State, on the Pacific slope of 
Mexico, and it is only found, as previously mentioned, 
in X. resolanae. Likewise, even though M. bravoae 
sensu lato contains three well-supported genetic lin- 
eages, lt appears that each one of these lineages also 
shows some level of congruence with the hosts and 
geographical region (hydrological system) in which 
they live, as shown in Fig. 5A, which represents a 
summary of the results obtained in this study. The 
geographical range of Lineage Il is wide and consists 
of three independent hydrological systems, and it is 
primarily found in members of the tribe Ilyodontini, 
even though some isolates were found in a member of 
the tribe Chapalichthyini, and one was even found 
infecting a member of the family Cyprinidae. Lineage 
III is apparently restricted to water bodies of the 
Lerma River Basin and is only associated with 
members of the tribes Girardinichthyini and Chapali- 
chthyini. Finally, Lineage IV also shows a restricted 
geographical distribution, in four localities along the 
San Pedro Mezquital River Basin in north-western 
Mexico. This lineage is only associated with Chara- 
codon audax, a member of the tribe Characodontini, 
allegedly representing the basal members in the phy- 
logenetic history of goodeines (Domínguez-Domínguez 
et al., 2010) (Fig. 5B, C). In this context, and based on 
the diversification and biogeographical patterns of 
Goodeinae in central Mexico, we argue that the evo- 
lutionary history and the historical biogeography of 
the four genetic lineages of Margotrema are closely 
linked to that of their hosts, reflecting the three types 
of historical associations as described by Page € 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 122 
 
 
 
12 A. MARTÍNEZ-AQUINO ET AL. 
  
        
(A) 
SPECIES A SPECIES B 
Lineage | Lineage Il Lineage lll Lineage IV 
(B) Cuzalapa Ayuquila, Balsas and Lerma Mezquital 
Conchos 
(C) Ilyodontini Ilyodontini 7 Chapalichthyini 
Xenotaenia resolanae Allodontichthiys zonistius 
llyodon whitei 
[. furcidens 
Chapalichthys pardalis 
Codoma omata* 
Girardinichthyini / Chapalichthyini Characodontini 
Allotoca diazi Characodon audax 
A. duguesii 
A. meeki 
A. zacapuensis 
Neoophorus reagalís 
Alloophorus robustus 
Zoogoneticus purhepechus 
Z. quitzecensis 
Figure 5. Schematic representation depicting the types of historical associations among genes, areas, and hosts of 
Margotrema. A, phylogenetic inferences (organisms and gene) (diffuse grey, I1TS1; black lines, COD. Each colour 
represents independent evolutionary lineages. B, hydrological systems representing the distribution area of each lineage 
(area and organism). C, host association for each lineage of Margotrema at tribe or species level (host and parasite). 
Colours in the scientific names are used to correlate the name of the tribe with the species contained in each tribe. An 
asterisk (*) indicates a species of host belonging to the family Cyprinidae (for more information see Supporting 
Information Appendix S2). 
Charleston (1998: 356): (1) organism and gene, (2) 
area and organisms, and (3) host and parasites 
(Fig. 5A-C). Interestingly, each of the Margotrema 
lineages show some host-specificity with a particular 
tribe of goodein, and in the particular case of Line- 
ages 1 and IV, this host-specificity is even narrower 
because these lineages are found at the fish species 
level (Fig. 5C). This host-specificity pattern might 
be explained as a result of a parasite speciation via 
host-switching of the most recent common ancestor or 
host—parasite co-divergence events of each Margot- 
rema lineage. It has been argued that several factors 
have shaped the evolutionary and biogeographical 
history of goodeines in central Mexico (Parenti, 
1981; Miller € Smith, 1986; Domínguez-Domínguez 
et al., 2010). If tecto-volcanic activity as well as river 
capture promoted the diversification of goodeinae 
in central Mexico, then we hypothesize that the 
distribution patterns as well as host associations of 
each lineage of Margotrema will be concordant with 
the hydro-geomorphological events that occurred in 
central Mexico and that the vicariant and dispersal 
events that caused the goodein diversification pro- 
moted at the same time the diversification of each 
Margotrema lineage. 
Other molecular phylogenetic studies of parasite 
taxa of freshwater fish, including extensive sampling 
of populations along their distributional range, have 
shown similar patterns of diversification, in that inde- 
pendent evolutionary lineages are detected even in 
the absence of morphological data supporting those 
patterns. For instance, Martínez-Aquino et al. (2009b) 
and Rosas-Valdez, Choudhury €: Pérez-Ponce de Léon 
(2011) uncovered a diversification process in species 
belonging to the acanthocephalan genus Neoechinor- 
hynchus and the digenean genus Phyllodistomum, 
respectively, where the evolutionary history of 
the parasite lineages is also closely tied to that of 
their hosts, showing clear instances of speciation via 
host-switching. 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 123 
 
 
 
MOLECULAR PHYLOGENY OF MARGOTREMA — 13  
ACKNOWLEDGEMENTS 
We thank R. Aguilar, R. Pérez, D. I. Hernández, and 
F. J. Alcántar for their help during fieldwork in 
Mexico; A. Choudhury and Ch. Brosseau for their help 
during fieldwork in Panama; A. Choudhury for finan- 
cial support; and staff of the Smithsonian Tropical 
Research Institute (STRD, Tupper Center, for facili- 
ties to conduct fieldwork in Panama. Donation of 
specimens for sequencing by A. Choudhury and R. 
Rosas is appreciated. We are grateful to L. Cervantes 
for her technical assistance in the molecular lab, U. 
Razo for his help designing primers, L. Marquez for 
sequencing specimens, B. Mendoza for processing 
some of the specimens, and L. García for providing 
specimens from the CNHE. We also thank P. Librado 
for his help in performing a script for using 
HERCULES, and A. Sánchez and J. Rozas for 
earlier discussions of this manuscript. We thank the 
American Journal Experts for editing the English 
text. A.M.A. was supported by a scholarship from 
the Consejo Nacional de Ciencia y Tecnología 
(CONACyT). This paper fulfils the requirements of 
A.M.A. to obtain his PhD degree within Posgrado en 
Ciencias Biológicas, Universidad Nacional Autónoma 
de México. This study was supported by grants 
from the Consejo Nacional de Ciencia y Tecnología 
(CONACyT 83043), and Programa de Apoyo a Proyec- 
tos de Investigación e Inmovación Tecnologíca 
(PAPIT-UNAM IN 202111) to G.P.P.L. 
REFERENCES 
Aguilar-Aguilar R, Rosas-Valdez R, Martínez-Aquino A, 
Pérez-Rodríguez R, Domínguez-Domínguez O, Pérez- 
Ponce de León G. 2010. Helminth fauna of two cyprinid 
fish (Campostoma ornatum and Codoma ornata) from the 
upper Piaxtla River, Northwestern Mexico. Helminthologia 
47: 251-256. 
Ahrens D, Monaghan MT, Vogler AP. 2007. DNA-based 
taxonomy for associating adults and larvae in multi-species 
assemblages of chafers (Coleptera: Scarabaeidae). Molecular 
Phylogenetic and Evolution 44: 436-449. 
Astrin JJ, Stiben PE, Misof B, Wágele JW, Gimnich F, 
Raupach MJ, Ahrens D. 2012. Exploring diversity in 
cryptorhynchine weevils (Coleoptera) using distance-, char- 
acter and tree based species delineation. Molecular Phylo- 
genetics and Evolution 63: 1-14. 
Avise JC. 2008. Phylogeography: retrospect and prospect. 
Journal of Biogeography 36: 3-15. 
Blair D. 2006. Ribosomal DNA variation in parasitic flat- 
worms. In: Maule AG, Marks NJ, eds. Parasitic flatworms: 
molecular biology, biochemistry, immunology and control. 
Wallingford, UK: CABI, 96-123. 
Bueno-Silva M, Boeger WA, Pie MR, 2011. Choice matters: 
incipient speciation in Gyrodactylus corydori (Monogenoidea: 
Gyrodactylidae). International Journal of Parasitology 41: 
657667. 
Caira JN, Bogéa T. 2005. Family Allocreadiidae Looss, 1902. 
In: Jones A, Bray RA, Gibson DI, eds. Keys to the Trema- 
toda. Vol. 11. London: CAB International and The Natural 
History Museum, 417436. 
Ceccarelli FS, Sharkey MJ, Zaldívar-Riverón A. 2012. 
Species identification in the taxonomically neglected, highly 
diverse, neotropical parasitoid wasp genus Notiospathius 
(Braconidae: Doryctinae) based on an integrative molecular 
and morphological approach. Molecular Phylogenetics and 
Evolution 62: 485495. 
Choudhury A, Dick TA. 2001. Sturgeons (Chondrostei: Aci- 
penseridae) and their metazoan parasites: patterns and 
process in historical biogeography. Journal of Biogeography 
28: 1411-1439. 
Cribb TH. 2005. Superfamily Allocreadioidea Looss, 1902. In: 
Jones A, Bray RA, Gibson DI, eds. Keys to the Trematoda. 
Vol. II. London: CAB International and The Natural History 
Museum, 413416. 
Curran SS, Tkach VV, Overstreet RM. 2006. A review 
of Polylekithum Arnold, 1934 and its familial affinities 
using morphological and molecular data, with description of 
Polylekithum catahoulensis sp. nov. Acta Parasitologica 51: 
238-248. 
Curran SS, Tkach VV, Overstreet RM. 2011. Phylogene- 
tic affinities of Auriculostoma (Digenea: Allocreadiidae), 
with descriptions of two new species from Peru. Journal of 
Parasitology 97: 661-670. 
Domínguez-Domínguez O, Pedraza-Lara C, Gurrola- 
Sánchez N, Perea S, Pérez-Rodríguez R, Israde- 
Alcántara 1, Garduño-Monroy VH, Doadrio 1, 
Pérez-Ponce de León G, Brooks DR. 2010. Historical 
biogeography of the Goodeinae (Cyprinodontiforms). In: 
Uribe-Aranzabal MC, Grier H, eds. Viviparous fishes II. 
Homestead, FL: New Life Publications, 33-74. 
Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper 
A, Duran C, Field M, Heled J, Kearse M, Markowitz S, 
Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson 
A, 2010. Geneious v5.0.4 Available at: http://www. 
geneious.com/ 
Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evo- 
lutionary analysis by sampling trees. BMC Evolutionary 
Biology 7: 214. 
Edwards SV. 2009. Is a new and general theory of molecular 
systematics emerging? Evolution 63: 1-19. 
Edwards SV, Liu L, Pear DK. 2007. High-resolution species 
trees without concatenation. Proceedings of the National 
Academy of Sciences of the United States of America 104: 
5936-5941. 
Ellegren H. 2004. Microsatellites: simple sequences with 
complex evolution. Nature Reviews Genetics 5: 435445. 
Fontaneto D, Herniou EA, Boschetti C, Caprioli M, 
Melone G, Ricci C, Barraclough TG. 2007. Independ- 
ently evolving species in asexual bdelloid rotifers. Public 
Library of Science Biology Biology 5: e87. 
Funk DJ, Omland KE. 2003. Species-level paraphyly 
and polyphyly: frequency, causes, and consequences, with 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 124 
 
 
 
14 A. MARTÍNEZ-AQUINO ET AL. 
insights from animal mitochondrial DNA. Annual Review of 
Ecology, Evolution, and Systematics 34: 397-423. 
Guy-Franck R, Kerrest A, Dujon B. 2008. Comparative 
genomics and molecular dynamics of DNA repeats in 
eukaryotes. Microbiology and Molecular Biology Reviews "12: 
686-727. 
Hasegawa M, Kishino H, Yano TA. 1985. Dating of the 
human-ape splitting by a molecular clock of mitochondrial 
DNA. Journal of Molecular Evolution 22: 160-174. 
Heled J, Drummond AJ. 2010. Bayesian inference of 
species trees from multilocus data. Molecular Biology and 
Evolution 27: 570-580. 
Hickerson MJ, Carstens BC, Cavender-Bares J, Cran- 
dall KA, Graham CH, Johnson JB, Rissler L, Victori- 
ano PF, Yoder AD. 2010. Phylogeography's past, present, 
and future: 10 years after Avise, 2000. Molecular Phyloge- 
netics and Evolution 54: 291-301. 
Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian 
inference of phylogenetic trees. Bioinformatics 17: 754-755. 
Katoh K, Toh H. 2008. Recent developments in the MAFFT 
multiple sequence alignment program. Briefings in Bioin- 
formatics 9: 286-298. 
Kimura M. 1981. Estimation of evolutionary distances 
between homologous nucleotide sequences. Proceedings of 
the National Academy of Sciences of the United States of 
America 78: 454-458. 
Lamothe-Argumedo R. 1972. Tremátodos de peces VI. Mar- 
gotrema bravoae gen. nov. sp. nov. (Trematoda: Allocreadi- 
idae) parásito de Lermichthys multiradiatus Meek. Anales 
del Instituto de Biología, UNAM, Serie Zoología 41: 87-92. 
Li YC, Korol AB, Fahima T, Beiles A, Nevo E. 2002. 
Microsatellites: genomic distribution, putative functions 
and mutational mechanisms: a review. Molecular Ecology 
11: 2453-2465. 
Liu L, Pearl DK, Brumfield RT, Edwards SV. 2008. Esti- 
mating species trees using multiple-allele DNA sequence 
data. Evolution 62: 2080-2091. 
Luton K, Walker D, Blair D. 1992. Comparisons of ribos- 
omal internal transcribed spacers from two congeneric 
species of flukes (Platyhelminthes: Trematoda: Digenea). 
Molecular and Biochemical Parasitology 56: 323-328. 
Maddison WP. 1997. Gene trees in species trees. Systematic 
Biology 46: 523-536. 
Maddison WP, Knowles LL. 2006. Inferring phylogeny 
despite incomplete lineage sorting. Systematic Biology 55: 
21-30. 
Marshall DC, Hill KBR, Cooley JR, Simon C. 2011. 
Hybridization, mitochondrial DNA phylogeography, and pre- 
diction of the early stages of reproduction isolation: lesson 
from New Zealand cicadas (genus Kikihia). Systematic 
Biology 60: 482-502. 
Martínez-Aquino A, Aguilar-Aguilar R, Pérez-Rodríguez 
R, Pérez-Ponce de León G. 2009a. Helminth parasites of 
Xenotaenia resolanae (Osteichthyes: Cyprinodontiformes: 
Goodeidae) from the Cuzalapa hydrological system, Jalisco, 
Mexico. Journal of Parasitology 95: 1221-1223. 
Martínez-Aquino A, Hernández-Mena DI, Pérez- 
Rodríguez R, Aguilar-Aguilar R, Pérez-Ponce de León 
G. 2011. Endohelminth parasites of the freshwater fish 
Zoogoneticus purhepechus (Cyprinodontiformes: Goodeidae) 
from two springs in the Lower Lerma River, Mexico. Revista 
Mexicana de Biodiversidad 82: 1132-1137. 
Martínez-Aquino A, Pérez-Rodríguez R, Hernández- 
Mena DI, Garrido-Olvera L, Aguilar-Aguilar R, Pérez- 
Ponce de León R. 2012. Endohelminth parasites of seven 
goodein species (Cyprinodontiformes: Goodeidae) from Lake 
Zacapu, Michoacán, Central Mexico Plateau. Hidrobiológica 
22: 88-91. 
Martínez-Aquino A, Reyna-Fabián ME, Rosas-Valdez R, 
Razo-Mendivil U, Pérez-Ponce de León G, García- 
Varela M. 2009b. Detecting a complex of cryptic species 
within  Neoechinorhynchus  golvani  (Acanthocephala: 
Neoechinorhynchidae) inferred from ITSs and LSU rDNA 
gene sequences. Journal of Parasitology 95: 1040-1047. 
Martínez-Aquino A, Salgado-Maldonado G, Aguilar- 
Aguilar R, Cabañas-Carranza G, Mendoza-Palmero 
CA. 2007. Helminth parasite communities of Characodon 
audax and C. lateralis (Pisces: Goodeidae), endemic fresh- 
water fishes from Durango, Mexico. Southwestern Natural- 
ist 52: 125-130. 
Martínez-Aquino A, Salgado-Maldonado G, Aguilar- 
Aguilar R, Cabañas-Carranza G, Ortega-Olivares MP. 
2004. Helminth parasites of Chapalichthys encaustus 
(Pisces: Goodeidae), an endemic freshwater fish from Lake 
Chapala, Jalisco, Mexico. Journal of Parasitology 90: 889— 
890. 
Mejía-Madrid H, Domínguez-Domínguez O, Pérez- 
Ponce de León G. 2005. Adult endohelminth parasites of 
Goodeinae (Cyprinodontiformes: Goodeidae) from México 
with biogeographical considerations. Journal of Parasitol- 
ogy 72: 200-211. 
Miller RR, Smith ML. 1986. Origin and geography of the 
fishes of Central Mexico. In: Hocutt CH, Wiley EO, eds. The 
zoogeography of North American freswater fishes. New York: 
John Wiley and Sons, Inc., 487-517. 
Miura O, Kuris AM, Torchin ME, Hechinger RF, 
Dunham EJ, Chiba S. 2005. Molecular-genetic analyses 
reveal cryptic species of trematodes in the interdial gastro- 
pod, Batillaria cumingi (Crosse). International Journal for 
Parasitology 35: 793-801. 
Miura O, Torchin ME, Kuris AM, Hechinger RF, Chiba 
S. 2006. Introduced cryptic species of parasites exhibit 
different invasion pathways. Proceedings of the National 
Academy of Sciences of the United States of America 103: 
19818-19823. 
Monaghan MT, Wild R, Elliot M, Fujisawa T, Balke M, 
Inward DJG, Lees DC, Ranaivosolo R, Eggleton P, 
Barraclough TG, Vogler AP. 2009. Accelerated species 
inventory on Madagascar using coalescent-based models of 
species delineation. Systematic Biology 58: 298-311. 
Morgan JAT, Blair D. 1998. Relative merits of nuclear 
ribosomal internal transcribed spacers and mitochondrial 
CO1 and ND1 genes for distinguishing among Echinostoma 
species (Trematoda). Parasitology 116: 289-297. 
Nadler SA, Pérez-Ponce de León G. 2011. Integrating 
molecular and morphological approaches for characterizing 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 125 
 
 
 
MOLECULAR PHYLOGENY OF MARGOTREMA 15  
parasite cryptic species: implications for parasitology. Para- 
sitology 13: 1688-1709. 
Nee S, Mooers AO, Harvey PH. 1992. Tempo and mode of 
evolution revealed from molecular phylogenies. Proceedings 
of the National Academy of Sciences of the United States of 
America 89: 8322-8326. 
Nei M, Kumar S. 2000. Molecular evolution and phylogenet- 
ics. Oxford: Oxford University Press. 
Nieberding CM, Durette-Desset M-C, Vanderpoorten A, 
Casanova JC, Ribas A, Deffontaine V, Feliu C, Morand 
S, Libois R, Michaux JR. 2008. Geographic and host 
biogeography matter for understanding the phylogeography 
of a parasite. Molecular Phylogenetics and Evolution 47: 
538-554. 
Page RDM. 2003. Tangled trees: phylogeny, cospeciation, and 
coevolution. Chicago: University of Chicago Press. 
Page RDM, Charleston MA. 1997. From gene to organismal 
phylogeny: reconciled trees and the gene tree/species 
tree problem. Molecular Phylogenetic and Evolution 7: 231— 
240. 
Page RDM, Charleston MA. 1998, Trees within trees: phy- 
logeny and historical associations. Trends in Ecology and 
Evolution 13: 356-359. 
Parenti LR. 1981. A phylogenetic and biogeographic analysis 
of cyprinodontiform fishes (Teleostei: Atherinomorpha). Bul- 
letin of the American Museum of Natural History 168: 
340-557. 
Peresbarbosa-Rojas E, Pérez-Ponce de León G, García- 
Prieto L. 1994. Helmintos parásitos de tres especies de 
peces (Goodeidae) del Lago de Pátzcuaro, Michoacán. Anales 
del Instituto de Biología, UNAM, Serie Zoología 65: 201— 
204. 
Pérez-Ponce de León G. 2001. Margotrema guillerminae n. 
sp. (Trematoda: Macroderoididae) from two species of fresh- 
waters fishes in Lake Zacapu, Michoacan state, Mexico, and 
new records of Margotrema bravoae Lamothe, 1970. Journal 
of Parasitology 87: 1112-1114. 
Pérez-Ponce de León G, Choudhury A. 2005. Biogeogra- 
phy of helminth parasites of freshwater fishes in Mexico: 
the research for patterns and processes. Journal of Bioge- 
ography 32: 645-649. 
Pérez-Ponce de León G, Choudhury A. 2010. Parasites 
inventories and DNA-based taxonomy: lessons from 
helminths of freshwater fishes in a megadiverse country. 
Journal of Parasitology 96: 236-244. 
Pérez-Ponce de León G, García-Prieto L, León- 
Régagnon V, Choudhury A. 2000. Helminth communities 
of native and introduced fishes in Lake Pátzcuaro, Micho- 
acán, México. Journal of Fish Biology 57: 303-325. 
Pineda-López R, Salgado-Maldonado G, Soto-Galera 
E, Hernández-Camacho N, Orozco-Zamorano A, 
Contreras-Robledo S, Cabañas-Carranza G, Aguilar- 
Aguilar R. 2005. Helminth parasites of viviparous fishes in 
Mexico. In: Uribe MC, Grier H, eds. Viviparous fishes: 
genetics, ecology, and conservation. Homestrad, FL: New 
Life Publications, 437-456. 
Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, 
Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler 
AP. 2006. Sequence-based species delimitation for the DNA 
taxonomy of undescribed insects. Systematics Biology 55: 
595-609. 
Posada D. 2008. ¡ModelTest: phylogenetic model averaging. 
Molecular Biology and Evolution 25: 1253-1256. 
Poulin R, Krasnov BR, Mouillot D. 2011a. Host specificity 
in phylogenetic and geographic space. Trends in Parasitol- 
ogy 27: 355-361. 
Poulin R, Krasnov BR, Mouillot D, Thieltges DW. 2011b. 
The comparative ecology and biogeography of parasites. 
Philosophical Transactions of the Royal Society B 366: 
2379-2390. 
Powell JR. 2012. Accounting for uncertainty in species 
delineation during the analysis of environmental DNA 
sequence data. Methods in Ecology and Evolution 3: 1-11. 
Rambaut A, Charleston M. 2002. TreeEdit: phylogenetic 
tree editor v1.0 alpha 10. Available at: http://tree.bio. 
ed.ac.uk/software/treeedit/ 
Rannala B, Yang Z. 2003. Bayes estimation of species diver- 
gence times and ancestral population sizes using DNA 
sequences from multiple loci. Genetics 164: 1645-1656. 
Razo-Mendivil U, Rosas-Valdez R, Pérez-Ponce de León 
G. 2008. A new cryptogonimid (Digenea) from the Mayan 
cichlid, Cichlasoma urophthalmus (Osteichthyes: Cichli- 
dae), in several localities of the Yucatán peninsula, Mexico. 
Journal of Parasitology 94: 1371-1378. 
Razo-Mendivil U, Vázquez-Domínguez E, Rosas-Valdez 
R, Pérez-Ponce de León G, Nadler SA. 2010. Phyloge- 
netic analysis of nuclear and mitochondrial DNA reveals 
a complex of cryptic species in Crassicutis cichlasomae 
(Digenea: Apocreadiidae), a parasite of Middle-American 
cichlids. International Journal of Parasitology 40: 471-486. 
Rosas-Valdez R, Choudhury A, Pérez-Ponce de Léon G. 
2011. Molecular prospecting for cryptic species in Phyllo- 
distomum lacustri (Platyhelminthes, Gorgoderidae). Zoo- 
logica Scripta 40: 296-305. 
Sánchez-Nava P, Salgado-Maldonado G, Soto-Galera E, 
Jaime-Cruz B. 2004. Helminth parasites of Girardinich- 
thys multiradiatus (Pisces: Goodeidae) in the upper Lerma 
River sub-basin, Mexico. Parasitology Research 93: 396-402. 
Sanderson MJ. 1997. A nonparametric approach to estimat- 
ing divergence times in the absence of rate constancy. 
Molecular Biology and Evolution 14: 1218-1231. 
Satler JD, Starrett J, Hayashi CHY, Heidin M. 2011, 
Inferring species tree from gene trees in a radiation of 
California trapdoor spiders (Araneae, Antrodiaetidae, Ali- 
atypus). Public Library of Science Biology One 6: e25355. 
Schwarz G. 1978. Estimating the dimension of a model. The 
Annals of Statistics 6: 461464. 
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, 
Kumar S. 2011. MEGA5: molecular evolutionary genetics 
analysis using maximum likelihood, evolutionary distance, 
and maximum parsimony methods. Molecular Biology and 
Evolution 28: 2731-2739. 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 126 
 
 
 
16 A. MARTÍNEZ-AQUINO ET AL. 
SUPPORTING INFORMATION 
Additional Supporting Information may be found in the online version of this article at the publisher's web-site: 
Figure S1. Phylogenetic tree obtained with MrBayes for COI. 
Figure S2. Phylogenetic trees obtained with MrBayes for IT'S1. 
Appendix S1. Localities sampled for freshwater fishes (Goodeinae), host species of Margotrema from México. 
Appendix S2. Margotrema and hosts species, localities analysed, with codes referring to each terminal taxa in 
the phylogenetic analyses, voucher reference, and accession numbers for each specimen and sequence. 
O 2013 The Linnean Society of London, Zoological Journal of the Linnean Society, 2013, 168, 1-16
 127 
 
 
 
 128 
 
SUPPORTING INFORMATION 
 
 
TLAP Iwh2
AHUA Azo1
Wallinia chavarriae
MINT Zqu8
CUZA Xre3
MINT Zqu7
CUZA Xre9
AHUA Azo2
CHAP Adi6
TOBO Cha5
Allocreadium lobatum
Wallinia chavarriae
AHUA Azo11
TOCU Ifu2
AHUA Azo8
AHUA I fu4
CHAP Adi12
CHAP Adi4
CHAP Adu5
CUZA Xre5
CUZA Xre1
RICO Are8
PINO Cha5
PINO Cha6
TLAP Iwh10
TOBO Cha6
PINO Cha7
RICO Are7
TOCU Chp
AHUA Ifu2
TOBO Cha1
MINT Zqu6
PINO Cha2
TLAP Iwh12
AHUA Azo10
CHAP Adu4
GUAG Cha2
RICO Are5
CHAP Adi7
CUZA Xre6
TLAP Iwh8
AHUA Azo5
TLAP Iwh9
OPOP Ame2
TLAP Iwh5
TLAP Iwh4
CHAP Adu5
AHUA Azo9
TLAP Iwh11
TOBO Cha7
RICO Are3
OPOP Ame8
Prosthenhystera sp.
CHAP Adi3
CUZA Xre10
OPOP Ame10
AHUA I fu6
AHUA I fu5
MINT Zqu4
CHAP Adi1
OPOP Ame7
RICO Are2
CHAP Adi6
AHUA I fu3
ZACA Zqu10
TLAP Iwh1
MINT Zqu5
CHAP Adu2
AHUA Azo3
RICO Are4
CHAP Adu3
ZACA Aza
AHUA Azo7
AGON Cha
CHAP Adi8
OPOP Ame9
MINT Aro
CHAP Adi2
OPOP Ame6
RICO Are6
TLAP Iwh6
CHAP Adu1
RICO Are9
CUZA Xre4
GUAG Cha3
TOCU I fu1
Wallinia chavarriae
PINO Cha1
RICO Are10
ZACA Zqu1
CUZA Xre2
AHUA Ifu8
CHAP Adi10
OPOP Ame1
PINO Cha4
Prosthenhystera sp.
AHUA Ifu7
TLAP Iwh13
MINT Zqu2
CHAP Adi13
OPOP Ame3
TLAP Iwh7
GUAG Cha1
Prosthenhystera sp.
CHAP Adu8
AHUA Azo4
MINT Zqu1
CUZA Xre8
CHAP Adu7
TOBO Cha4
TOBO Cha3
RICO Are1
OPOP Ame4
LLUZ Zpu
TLAP Iwh3
MINT Zqu3
AHUA Azo6
TOBO Cha2
CHAP Adi9
CUZA Xre7
BOCO  Cor
AHUA I fu9
PINO Cha3
AHUA Ifu1
OPOP Ame5
2.0 subst./site
Supporting Figure S1
COI
 129 
 
 
Pros thenhys tera sp.
Pros thenhys tera sp.
Allocreadium lobatum
Wallinia chavarr iae
Wallinia chavarr iae
CUZA Xre5
CUZA Xre6
C UZA Xre1
C UZA Xre3
C UZA Xre4
CUZA Xre2
AHUA Az o11
AHUA Azo12
AHUA Azo5
T OC U Ifu2
T OC U Ifu1
BOC O Cor
AHUA Az o10
AHUA Az o2
AHUA Ifu9
AHUA Az o7
AHUA Az o3
T LAP Iwh2
AHUA Azo6
AHUA Azo9
AHUA Azo13
AHUA Azo4
AHUA Ifu6
AHUA Ifu7
AHUA Ifu8
T OCU C hp
AHUA Ifu10
AHUA Ifu1
AHUA Ifu4
AHUA Ifu2
AHUA Ifu3
T LAP Iwh3
T LAP Iwh1
AHUA Azo1
AHUA Ifu5
AHUA Azo8
CHAP Adi3
CHAP Adi6
C HAP Adi6
OPOP Ame2
C HAP Adi8
OPOP Ame4
MINT  Aro2
OPOP Ame1
ZAC A Aza5
ZAC A Zqu6
MINT  Zqu3
MINT  Zqu6
MINT  Zqu4
RIC O Are4
RIC O Are2
ZAC A Zqu2
OPOP Ame3
ZAC A Zqu3
MINT  Zqu9
ZAC A Zqu4
MINT  Zqu8
MINT  Zqu5
MINT  Zqu7
MINT  Zqu1
RIC O Are5
R IC O Are9
RIC O Are6
RIC O Are1
RIC O Are3
LLUZ Zpu
ZACA Zqu2
RIC O Are10
R IC O Are8
RIC O Are7
CHAP Adi2
C HAP Adi5
C HAP Adu1
CHAP Adi9
CHAP Adi1
MINT  Aro1
MINT  Zqu2
ZAC A Zqu7
C HAP Adu4
C HAP Adu2
C HAP Adu5
C HAP Adu3
CHAP Adi7
PINO Cha4
T OBO Cha3
GUAG Cha1
T OBO Cha2
AGON Cha
T OBO Cha6
GUAG Cha3
PINO Cha3
PINO Cha2
T OBO Cha4
T OBO Cha1
PINO Cha5
PINO Cha1
T OBO Cha5
GUAG Cha2
0.7 subst./site
Supporting Figure S2
ITS1
 130 
 
Appendix S1. Localities sampled for freshwater fishes (Goodeinae), host species of Margotrema 
from México. NH = sample size of hosts collected; NM = sampled size of individuals of 
Margotrema collected by locality; M = total number of individuals of Margotrema used for 
morphological analyses; DNA = total number of individuals of Margotrema used for molecular 
analyses; DV = total number of digital vouchers of individuals of Margotrema obtained by 
locality. The asterisks (*1, *2) refer to previously published data by Pérez-Ponce de León et al. 
(2009) and Aguilar-Aguilar et al. (2010), respectively, in studies of helminth parasites of 
freshwater fishes from Mexico, but correspond to the same samplings. The host from locality 44 
corresponds to a species of the family Cypriinidae.   
Locality Host species NH NM  M DNA VD 
1.  Stream in Ahuacapán, Jalisco Allodontichthys zonistius 11 80 37 43 0 
 
Ilyodon furcidens 11 50 17 33 0 
2.  Spring in Canal Magdalena, Michoacán Chapalichthys pardalis 3 0 − − − 
3.  Channel Magdalena, Michoacán Ilyodon furcidens 2 0 − − − 
 
Zoogoneticus purhepechus 7 0 − − − 
4.  Channel Santiago Tiacaque, Estado de México Girardinichthys multiradiatus 12 0 − − − 
5.  Spring Chapultepec, Michoacán Allotoca diazi 21 31 9 22 1 
 
Allotoca duguesi   22 6 1 5 1 
6.  Spring Chilchota, Michoacán Skiffia multipunctata 10 0 − − − 
7.  Spring Cupatziro, Michoacán Skiffia multipunctata 13 0 − − − 
 
Zoogoneticus purhepechus 16 0 − − − 
8.  Arroyo Durazno in Cuzalapa River, Jalisco Xenotaenia resolanae  35 131 68 63 0 
9.  El Tule (River), Jalisco Allodontichthys tamazulae 19 0 − − − 
10. Estanque en Río del Canal Santiago Tiacaque, Girardinichthys multiradiatus 6 0 − − − 
      Estado de México 
   
   11.  La Angostura, Zacapu Lake (balneario), Michoacán Skiffia lermae 11 0 − − − 
 
Allotoca zacapuensis 32 1 0 1 1 
 
Goodea atripinnis 20 0 − − − 
 
Hubbsina turneri 16 0 − − − 
 
Skiffia lermae 19 0 − − − 
 
Zoogoneticus quitzeoensis 30 18 4 14 8 
12.  La Luz spring, Jacona de Plancarte, Michoacán Zoogoneticus purhepechus  32 1 0 1 1 
 
Zoogoneticus purhepechus  12 0 − − − 
 
Chapalichthys encaustus 8 0 − − − 
 
Skiffia multipunctata 4 0 − − − 
 
Alloophorus robustus 35 0 − − − 
13.  La Mintzita spring, Michoacán, Michoacán Zoogoneticus quitzeoensis 22 5 1 4 3 
 
Alloophorus robustus 14 3 0 3 − 
14.  Camecuaro Lake, Michoacán  Alloophorus robustus 2 0 − − − 
 131 
 
 
Zoogoneticus purhepechus  11 0 − − − 
15. Opopeo Lake, Michoacán Goodea atripinnis 4 0 − − − 
 
Allotoca meeki 4 45 29 16 4 
16.  Las Adjuntas (River), Michoacán  Skiffia multipunctata 2 0 − − − 
 
Zoogoneticus purhepechus  5 0 − − − 
17.  Los Negritos spring, Michoacán Chapalichthys encaustus 2 0 − − − 
 
Zoogoneticus purhepechus  19 0 − − − 
 
Zoogoneticus purhepechus  9 0 − − − 
 
Zoogoneticus purhepechus  8 0 − − − 
18.  Cutzaróndiro spring, Michoacán Ilyodon whitei 31 0 − − − 
19.  La Estancia spring, Michoacán Zoogoneticus purhepechus  21 0 − − − 
20. Parque Ecológico Chicnahuapan (Lake),  Girardinichthys multiradiatus 44 0 − − − 
      Estado de México Girardinichthys multiradiatus 29 0 − − − 
21.  Pátzcuaro Lake, Michoacán Goodea atripinnis 31 0 − − − 
 
Alloophorus robustus 2 0 − − − 
22.  Predio Porfirio, La Angustura, Zacapu Lake, Michoacán Allotoca zacapuensis 3 2 − − − 
 
Xenotoca variata 1 0 − − − 
 
Alloophorus robustus 2 0 − − − 
23.  Dam in Santiago Chanel, Tiacaque, Estado de México Girardinichthys multiradiatus 2 0 − − − 
24.  Dam Ignacio Ramírez, Estado de México Girardinichthys multiradiatus 14 0 − − − 
25.  Dam Salazar, Estado de México Girardinichthys multiradiatus 35 0 − − − 
26.  Rico spring, Michoacán Allotoca regalis 39 61 30 31 − 
26.  Ahuehuello River in Santo Domingo, Puebla Ilyodon whitei 51 0 − − − 
28.  Ángulo River close to Zacapu Lake, Michoacán Alloophorus robustus 9 0 − − − 
 
Xenotoca variata 20 0 − − − 
 
Zoogoneticus quitzeoensis 11 0 − − − 
 
Allotoca goslinei 2 0 − − − 
29.  Tamazula River, Jalisco Allodontichthys zonistius 32 0 − − − 
 
Ilydon furcidens 56 0 − − − 
30.  Tributary of San Idelfonso River, Querétaro Goodea atripinnis 10 0 − − − 
31.  San Jerónimo, Pátzcuaro Lake, Michoacán Alloophorus robustus 5 0 − − − 
32.  Santa Maria del Oro (River), Jalisco Ilydon furcidens 15 0 − − − 
33.  Bordo or man-made pond in Tlapetlahuaya, Puebla Ilyodon whitei 34 62 29 33 7 
34.  Spring in park of Tocumbo, Michoacán Chapalichthys pardalis 38 4 2 2 1 
 
Goodea atripinnis 16 0 − − − 
 
Ilydon furcidens 18 3 1 2 2 
35.  Ucasanastaua, Pátzcuaro, Michoacán Alloophorus robustus 11 0 − − − 
36.  Puente en el poblado de Pino Suárez,  Characodon audax*
1
 21 45 30 15 − 
       carretera Durango-Mezquital, Durango 
   
   37.  Spring in Abraham González, Durango  Characodon audax*
1
 12 16 11 5 0 
38.  Spring in the Unidad de Manejo Ambiental Characodon audax*
1
 14 8 5 3 0 
       de caza, Guadalupe Aguilera, Durango 
   
   39.  Spring el Toboso, Durango Characodon audax*
1
 42 28 15 13 0 
 132 
 
40.  Manantial en el poblado Amado Nervo, Durango  Characodon lateralis*
1
 9 0 − − − 
41.  Ojo de Agua de San Juan, Durango  Characodon lateralis*
1
 11 0 − − − 
42.  Ojo de Agua del poblado de los Berros, Durango  Characodon lateralis*
1
 23 0 − − − 
43. Río Potrero Grande, Jalisco Ilydon furcidens 10 1 0 1 − 
 
Allotoca goslinei 2 0 − − − 
44.  Upper Piaxtla River, Municipio San Dimas, Durango Codoma ornata*
2
 21 6 − − − 
              
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 133 
 
Appendix 2. Margotrema and host species. Tribe of each host species. Code for each individual of Margotrema sequenced, as shown 
in the terminal taxa names of figures 2, 3, S1 and S2 (4 capitals for locality, 3 letters for species host and number, respectivelity). 
Country, state / región, name of locality, type of habitat, altitude (m) of sampled locality, GPS location, date collected, collection 
method for fishes, names of collectors of fishes, names of collector of digeneans, additional info (digital vouchers of sequencing 
individuals), vouchers deposited numbers at Colección Nacional de Helmintos (CNHE) [National Helminth Collection]. The asterisks 
(*, **, ***) after the voucher numbers refer to previously published data by Martínez-Aquino et al. (2009a, 2012) and Pérez-Ponce de 
León et al. (2009), respectively, in studies of helminth parasites of freshwater fishes from Mexico, but correspond to the same 
samplings. Number of sequences (in ascending order) and GenBank accession for COI and ITS1 for Margotrema spp.    
Part A 
     
Species Host species Tribe of Host 
Taxa Terminal 
Code Country State/Region 
Margotrema bravoae sensu lato Characodon audax1 Characodontini AGON Cha México Durango 
Margotrema bravoae sensu lato Allodontichthys zonistius1 Ilyodontini AHUA Azo1 México Jalisco 
Margotrema bravoae sensu lato Allodontichthys zonistius2 Ilyodontini AHUA Azo2 México Jalisco 
Margotrema bravoae sensu lato Allodontichthys zonistius3 Ilyodontini AHUA Azo3 México Jalisco 
Margotrema bravoae sensu lato Allodontichthys zonistius4 Ilyodontini AHUA Azo4 México Jalisco 
Margotrema bravoae sensu lato Allodontichthys zonistius5 Ilyodontini AHUA Azo5 México Jalisco 
Margotrema bravoae sensu lato Allodontichthys zonistius6 Ilyodontini AHUA Azo6 México Jalisco 
Margotrema bravoae sensu lato Allodontichthys zonistius7 Ilyodontini AHUA Azo7 México Jalisco 
Margotrema bravoae sensu lato Allodontichthys zonistius8 Ilyodontini AHUA Azo8 México Jalisco 
Margotrema bravoae sensu lato Allodontichthys zonistius9 Ilyodontini AHUA Azo9 México Jalisco 
Margotrema bravoae sensu lato Allodontichthys zonistius10 Ilyodontini AHUA Azo10 México Jalisco 
Margotrema bravoae sensu lato Allodontichthys zonistius11 Ilyodontini AHUA Azo11 México Jalisco 
Margotrema bravoae sensu lato Allodontichthys zonistius12 Ilyodontini AHUA Azo12 México Jalisco 
Margotrema bravoae sensu lato Allodontichthys zonistius13 Ilyodontini AHUA Azo13 México Jalisco 
Margotrema bravoae sensu lato Ilyodon furcidens1 Ilyodontini AHUA Ifu1 México Jalisco 
Margotrema bravoae sensu lato Ilyodon furcidens2 Ilyodontini AHUA Ifu2 México Jalisco 
 134 
 
Margotrema bravoae sensu lato Ilyodon furcidens3 Ilyodontini AHUA Ifu3 México Jalisco 
Margotrema bravoae sensu lato Ilyodon furcidens4 Ilyodontini AHUA Ifu4 México Jalisco 
Margotrema bravoae sensu lato Ilyodon furcidens5 Ilyodontini AHUA Ifu5 México Jalisco 
Margotrema bravoae sensu lato Ilyodon furcidens6 Ilyodontini AHUA Ifu6 México Jalisco 
Margotrema bravoae sensu lato Ilyodon furcidens7 Ilyodontini AHUA Ifu7 México Jalisco 
Margotrema bravoae sensu lato Ilyodon furcidens8 Ilyodontini AHUA Ifu8 México Jalisco 
Margotrema bravoae sensu lato Ilyodon furcidens9 Ilyodontini AHUA Ifu9 México Jalisco 
Margotrema bravoae sensu lato Ilyodon furcidens10 Ilyodontini AHUA Ifu10 México Jalisco 
Margotrema bravoae sensu lato Allotoca diazi1 Girardinichthyini CHAP Adi1 México Michoacán 
Margotrema bravoae sensu lato Allotoca diazi2 Girardinichthyini CHAP Adi2 México Michoacán 
Margotrema bravoae sensu lato Allotoca diazi3 Girardinichthyini CHAP Adi3 México Michoacán 
Margotrema bravoae sensu lato Allotoca diazi4 Girardinichthyini CHAP Adi4 México Michoacán 
Margotrema bravoae sensu lato Allotoca diazi5 Girardinichthyini CHAP Adi5 México Michoacán 
Margotrema bravoae sensu lato Allotoca diazi6 Girardinichthyini CHAP Adi6 México Michoacán 
Margotrema bravoae sensu lato Allotoca diazi7 Girardinichthyini CHAP Adi7 México Michoacán 
Margotrema bravoae sensu lato Allotoca diazi8 Girardinichthyini CHAP Adi8 México Michoacán 
Margotrema bravoae sensu lato Allotoca diazi9 Girardinichthyini CHAP Adi9 México Michoacán 
Margotrema bravoae sensu lato Allotoca diazi10 Girardinichthyini CHAP Adi10 México Michoacán 
Margotrema bravoae sensu lato Allotoca diazi11 Girardinichthyini CHAP Adi11 México Michoacán 
Margotrema bravoae sensu lato Allotoca diazi12 Girardinichthyini CHAP Adi12 México Michoacán 
Margotrema bravoae sensu lato Allotoca duguesi1 Girardinichthyini CHAP Adu1 México Michoacán 
Margotrema bravoae sensu lato Allotoca duguesi2 Girardinichthyini CHAP Adu2 México Michoacán 
Margotrema bravoae sensu lato Allotoca duguesi3 Girardinichthyini CHAP Adu3 México Michoacán 
Margotrema bravoae sensu lato Allotoca duguesi4 Girardinichthyini CHAP Adu4 México Michoacán 
Margotrema bravoae sensu lato Allotoca duguesi5 Girardinichthyini CHAP Adu5 México Michoacán 
Margotrema bravoae sensu lato Allotoca duguesi6 Girardinichthyini CHAP Adu6 México Michoacán 
Margotrema bravoae sensu lato Allotoca duguesi7 Girardinichthyini CHAP Adu7 México Michoacán 
Margotrema bravoae sensu lato Allotoca duguesi8 Girardinichthyini CHAP Adu8 México Michoacán 
Margotrema resolanae Xenotaenia resolanae1 Ilyodontini CUZA Xre1 México Jalisco 
Margotrema resolanae Xenotaenia resolanae2 Ilyodontini CUZA Xre2 México Jalisco 
Margotrema resolanae Xenotaenia resolanae3 Ilyodontini CUZA Xre3 México Jalisco 
 135 
 
Margotrema resolanae Xenotaenia resolanae4 Ilyodontini CUZA Xre4 México Jalisco 
Margotrema resolanae Xenotaenia resolanae5 Ilyodontini CUZA Xre5 México Jalisco 
Margotrema resolanae Xenotaenia resolanae6 Ilyodontini CUZA Xre6 México Jalisco 
Margotrema resolanae Xenotaenia resolanae7 Ilyodontini CUZA Xre7 México Jalisco 
Margotrema resolanae Xenotaenia resolanae8 Ilyodontini CUZA Xre8 México Jalisco 
Margotrema resolanae Xenotaenia resolanae9 Ilyodontini CUZA Xre9 México Jalisco 
Margotrema resolanae Xenotaenia resolanae10 Ilyodontini CUZA Xre10 México Jalisco 
Margotrema bravoae sensu lato Characodon audax1 Characodontini GUAG Cha1 México Durango 
Margotrema bravoae sensu lato Characodon audax2 Characodontini GUAG Cha2 México Durango 
Margotrema bravoae sensu lato Characodon audax3 Characodontini GUAG Cha3 México Durango 
Margotrema bravoae sensu lato Zoogoneticus purhepechus1 Chapalichthyini LLUZ Zpu México Michoacán 
Margotrema bravoae sensu lato Alloophorus robustus1 Chapalichthyini MINT Aro1 México Michoacán 
Margotrema bravoae sensu lato Alloophorus robustus2 Chapalichthyini MINT Aro2 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis1 Chapalichthyini MINT Zqu1 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis2 Chapalichthyini MINT Zqu2 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis3 Chapalichthyini MINT Zqu3 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis4 Chapalichthyini MINT Zqu4 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis5 Chapalichthyini MINT Zqu5 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis6 Chapalichthyini MINT Zqu6 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis7 Chapalichthyini MINT Zqu7 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis8 Chapalichthyini MINT Zqu8 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis9 Chapalichthyini MINT Zqu9 México Michoacán 
Margotrema bravoae sensu lato Allotoca meeki1 Girardinichthyini OPOP Ame1 México Michoacán 
Margotrema bravoae sensu lato Allotoca meeki2 Girardinichthyini OPOP Ame2 México Michoacán 
Margotrema bravoae sensu lato Allotoca meeki3 Girardinichthyini OPOP Ame3 México Michoacán 
Margotrema bravoae sensu lato Allotoca meeki4 Girardinichthyini OPOP Ame4 México Michoacán 
Margotrema bravoae sensu lato Allotoca meeki5 Girardinichthyini OPOP Ame5 México Michoacán 
Margotrema bravoae sensu lato Allotoca meeki6 Girardinichthyini OPOP Ame6 México Michoacán 
Margotrema bravoae sensu lato Allotoca meeki7 Girardinichthyini OPOP Ame7 México Michoacán 
Margotrema bravoae sensu lato Allotoca meeki8 Girardinichthyini OPOP Ame8 México Michoacán 
Margotrema bravoae sensu lato Allotoca meeki9 Girardinichthyini OPOP Ame9 México Michoacán 
 136 
 
Margotrema bravoae sensu lato Allotoca meeki10 Girardinichthyini OPOP Ame10 México Michoacán 
Margotrema bravoae sensu lato Characodon audax1 Characodontini PINO Cha1 México Durango 
Margotrema bravoae sensu lato Characodon audax2 Characodontini PINO Cha2 México Durango 
Margotrema bravoae sensu lato Characodon audax3 Characodontini PINO Cha3 México Durango 
Margotrema bravoae sensu lato Characodon audax4 Characodontini PINO Cha4 México Durango 
Margotrema bravoae sensu lato Characodon audax5 Characodontini PINO Cha5 México Durango 
Margotrema bravoae sensu lato Characodon audax6 Characodontini PINO Cha6 México Durango 
Margotrema bravoae sensu lato Characodon audax7 Characodontini PINO Cha7 México Durango 
Margotrema bravoae sensu lato Neoophorus regalis1  Girardinichthyini RICO Nre1 México Michoacán 
Margotrema bravoae sensu lato Neoophorus regalis2 Girardinichthyini RICO Nre2 México Michoacán 
Margotrema bravoae sensu lato Neoophorus regalis3 Girardinichthyini RICO Nre3 México Michoacán 
Margotrema bravoae sensu lato Neoophorus regalis4 Girardinichthyini RICO Nre4 México Michoacán 
Margotrema bravoae sensu lato Neoophorus regalis5 Girardinichthyini RICO Nre5 México Michoacán 
Margotrema bravoae sensu lato Neoophorus regalis6 Girardinichthyini RICO Nre6 México Michoacán 
Margotrema bravoae sensu lato Neoophorus regalis7 Girardinichthyini RICO Nre7 México Michoacán 
Margotrema bravoae sensu lato Neoophorus regalis8 Girardinichthyini RICO Nre8 México Michoacán 
Margotrema bravoae sensu lato Neoophorus regalis9 Girardinichthyini RICO Nre9 México Michoacán 
Margotrema bravoae sensu lato Neoophorus regalis10 Girardinichthyini RICO Nre10 México Michoacán 
Margotrema bravoae sensu lato Ilyodon whitei1 Ilyodontini TLAP Iwh1 México Puebla 
Margotrema bravoae sensu lato Ilyodon whitei2 Ilyodontini TLAP Iwh2 México Puebla 
Margotrema bravoae sensu lato Ilyodon whitei3 Ilyodontini TLAP Iwh3 México Puebla 
Margotrema bravoae sensu lato Ilyodon whitei4 Ilyodontini TLAP Iwh4 México Puebla 
Margotrema bravoae sensu lato Ilyodon whitei5 Ilyodontini TLAP Iwh5 México Puebla 
Margotrema bravoae sensu lato Ilyodon whitei6 Ilyodontini TLAP Iwh6 México Puebla 
Margotrema bravoae sensu lato Ilyodon whitei7 Ilyodontini TLAP Iwh7 México Puebla 
Margotrema bravoae sensu lato Ilyodon whitei8 Ilyodontini TLAP Iwh8 México Puebla 
Margotrema bravoae sensu lato Ilyodon whitei9 Ilyodontini TLAP Iwh9 México Puebla 
Margotrema bravoae sensu lato Ilyodon whitei10 Ilyodontini TLAP Iwh10 México Puebla 
Margotrema bravoae sensu lato Ilyodon whitei11 Ilyodontini TLAP Iwh11 México Puebla 
Margotrema bravoae sensu lato Ilyodon whitei12 Ilyodontini TLAP Iwh12 México Puebla 
Margotrema bravoae sensu lato Ilyodon whitei13 Ilyodontini TLAP Iwh13 México Puebla 
 137 
 
Margotrema bravoae sensu lato Characodon audax1 Characodontini TOBO Cha1 México Durango 
Margotrema bravoae sensu lato Characodon audax2 Characodontini TOBO Cha2 México Durango 
Margotrema bravoae sensu lato Characodon audax3 Characodontini TOBO Cha3 México Durango 
Margotrema bravoae sensu lato Characodon audax4 Characodontini TOBO Cha4 México Durango 
Margotrema bravoae sensu lato Characodon audax5 Characodontini TOBO Cha5 México Durango 
Margotrema bravoae sensu lato Characodon audax6 Characodontini TOBO Cha6 México Durango 
Margotrema bravoae sensu lato Characodon audax7 Characodontini TOBO Cha7 México Durango 
Margotrema bravoae sensu lato Chapalichthys pardalis1 Chapalichthyini TOCU Chp1 México Michoacán 
Margotrema bravoae sensu lato Ilyodon furcidens1 Ilyodontini TOCU Ifu1 México Michoacán 
Margotrema bravoae sensu lato Ilyodon furcidens2 Ilyodontini TOCU Ifu2 México Michoacán 
Margotrema bravoae sensu lato Allotoca zacapuensis1 Girardinichthyini ZACA Aza México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis1 Chapalichthyini ZACA Zqu1 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis2 Chapalichthyini ZACA Zqu2 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis3 Chapalichthyini ZACA Zqu3 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis4 Chapalichthyini ZACA Zqu4 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis5 Chapalichthyini ZACA Zqu5 México Michoacán 
Margotrema bravoae sensu lato Zoogoneticus quitzeoensis6 Chapalichthyini ZACA Zqu6 México Michoacán 
Margotrema bravoae sensu lato Codoma ornata1 
 
BOCO Cor México Chihuahua 
Allocreadium lobatum Semotilus atromaculatus 
  
Canada 
 Prostenhystera sp. Gephyrocharax sp. 
  
Panama Gamboa 
Prostenhystera sp. Gephyrocharax sp. 
  
Panama Gamboa 
Prostenhystera sp. Gephyrocharax sp. 
  
Panama Gamboa 
Wallinia chavarriae Gephyrocharax sp. 
  
Panama Gamboa 
Wallinia chavarriae Gephyrocharax sp. 
  
Panama Gamboa 
Wallinia chavarriae Gephyrocharax sp. 
  
Panama Gamboa 
            
 
Part B 
   Locality Habitat Altitude (m) GPS Location 
Spring in Abraham González Spring 1865 24º12´45´´N; 104º31´48´´W 
 138 
 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Stream in Ahuacapán Stream 842 19º39´52´´N; 104º19´19.1´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
 139 
 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Spring Chapultepec Spring  2072 19º34´20´´N; 101º31´18.7´´W 
Arroyo Durazno in Cuzalapa River Stream 825 19º30´32.1´´N; 104º17´45.6´´W 
Arroyo Durazno in Cuzalapa River Stream 825 19º30´32.1´´N; 104º17´45.6´´W 
Arroyo Durazno in Cuzalapa River Stream 825 19º30´32.1´´N; 104º17´45.6´´W 
Arroyo Durazno in Cuzalapa River Stream 825 19º30´32.1´´N; 104º17´45.6´´W 
Arroyo Durazno in Cuzalapa River Stream 825 19º30´32.1´´N; 104º17´45.6´´W 
Arroyo Durazno in Cuzalapa River Stream 825 19º30´32.1´´N; 104º17´45.6´´W 
Arroyo Durazno in Cuzalapa River Stream 825 19º30´32.1´´N; 104º17´45.6´´W 
Arroyo Durazno in Cuzalapa River Stream 825 19º30´32.1´´N; 104º17´45.6´´W 
Arroyo Durazno in Cuzalapa River Stream 825 19º30´32.1´´N; 104º17´45.6´´W 
Arroyo Durazno in Cuzalapa River Stream 825 19º30´32.1´´N; 104º17´45.6´´W 
Spring in the Unidad de Manejo Ambiental de caza, Guadalupe Aguilera Spring 1941 24º25´59.5´´N; 104º38´29´´W 
Spring in the Unidad de Manejo Ambiental de caza, Guadalupe Aguilera Spring 1941 24º25´59.5´´N; 104º38´29´´W 
Spring in the Unidad de Manejo Ambiental de caza, Guadalupe Aguilera Spring 1941 24º25´59.5´´N; 104º38´29´´W 
La Luz spring, Jacona de Plancarte Spring 1616 19º56´10.4´´N; 102º17´57.8´´W 
La Mintzita spring Spring 1895 19°38'40.3''-19°38'52.3''N; 101°16‟28.20‟‟-101°16‟13.0‟‟W 
La Mintzita spring Spring 1895 19°38'40.3''-19°38'52.3''N; 101°16‟28.20‟‟-101°16‟13.0‟‟W 
La Mintzita spring Spring 1895 19°38'40.3''-19°38'52.3''N; 101°16‟28.20‟‟-101°16‟13.0‟‟W 
La Mintzita spring Spring 1895 19°38'40.3''-19°38'52.3''N; 101°16‟28.20‟‟-101°16‟13.0‟‟W 
La Mintzita spring Spring 1895 19°38'40.3''-19°38'52.3''N; 101°16‟28.20‟‟-101°16‟13.0‟‟W 
 140 
 
La Mintzita spring Spring 1895 19°38'40.3''-19°38'52.3''N; 101°16‟28.20‟‟-101°16‟13.0‟‟W 
La Mintzita spring Spring 1895 19°38'40.3''-19°38'52.3''N; 101°16‟28.20‟‟-101°16‟13.0‟‟W 
La Mintzita spring Spring 1895 19°38'40.3''-19°38'52.3''N; 101°16‟28.20‟‟-101°16‟13.0‟‟W 
La Mintzita spring Spring 1895 19°38'40.3''-19°38'52.3''N; 101°16‟28.20‟‟-101°16‟13.0‟‟W 
La Mintzita spring Spring 1895 19°38'40.3''-19°38'52.3''N; 101°16‟28.20‟‟-101°16‟13.0‟‟W 
La Mintzita spring Spring 1895 19°38'40.3''-19°38'52.3''N; 101°16‟28.20‟‟-101°16‟13.0‟‟W 
Opopeo Lake Lake 2268 19°24'20.2''N; 101°36‟08.2‟‟W 
Opopeo Lake Lake 2268 19°24'20.2''N; 101°36‟08.2‟‟W 
Opopeo Lake Lake 2268 19°24'20.2''N; 101°36‟08.2‟‟W 
Opopeo Lake Lake 2268 19°24'20.2''N; 101°36‟08.2‟‟W 
Opopeo Lake Lake 2268 19°24'20.2''N; 101°36‟08.2‟‟W 
Opopeo Lake Lake 2268 19°24'20.2''N; 101°36‟08.2‟‟W 
Opopeo Lake Lake 2268 19°24'20.2''N; 101°36‟08.2‟‟W 
Opopeo Lake Lake 2268 19°24'20.2''N; 101°36‟08.2‟‟W 
Opopeo Lake Lake 2268 19°24'20.2''N; 101°36‟08.2‟‟W 
Opopeo Lake Lake 2268 19°24'20.2''N; 101°36‟08.2‟‟W 
Puente en el poblado de Pino Suárez, carretera Durango-Mezquital Spring 1911 23°52'43.5''N; 104°31‟54.7‟‟W 
Puente en el poblado de Pino Suárez, carretera Durango-Mezquital Spring 1911 23°52'43.5''N; 104°31‟54.7‟‟W 
Puente en el poblado de Pino Suárez, carretera Durango-Mezquital Spring 1911 23°52'43.5''N; 104°31‟54.7‟‟W 
Puente en el poblado de Pino Suárez, carretera Durango-Mezquital Spring 1911 23°52'43.5''N; 104°31‟54.7‟‟W 
Puente en el poblado de Pino Suárez, carretera Durango-Mezquital Spring 1911 23°52'43.5''N; 104°31‟54.7‟‟W 
Puente en el poblado de Pino Suárez, carretera Durango-Mezquital Spring 1911 23°52'43.5''N; 104°31‟54.7‟‟W 
Puente en el poblado de Pino Suárez, carretera Durango-Mezquital Spring 1911 23°52'43.5''N; 104°31‟54.7‟‟W 
Spring Rico Spring 1842 19°49'51.85''N; 102°30‟7.98‟‟W 
Spring Rico Spring 1842 19°49'51.85''N; 102°30‟7.98‟‟W 
Spring Rico Spring 1842 19°49'51.85''N; 102°30‟7.98‟‟W 
Spring Rico Spring 1842 19°49'51.85''N; 102°30‟7.98‟‟W 
Spring Rico Spring 1842 19°49'51.85''N; 102°30‟7.98‟‟W 
Spring Rico Spring 1842 19°49'51.85''N; 102°30‟7.98‟‟W 
Spring Rico Spring 1842 19°49'51.85''N; 102°30‟7.98‟‟W 
Spring Rico Spring 1842 19°49'51.85''N; 102°30‟7.98‟‟W 
 141 
 
Spring Rico Spring 1842 19°49'51.85''N; 102°30‟7.98‟‟W 
Spring Rico Spring 1842 19°49'51.85''N; 102°30‟7.98‟‟W 
Spring in Tlapetlahuaya Spring 1681 18°45'20.40''N; 98°34‟28.8‟‟W 
Spring in Tlapetlahuaya Spring 1681 18°45'20.40''N; 98°34‟28.8‟‟W 
Spring in Tlapetlahuaya Spring 1681 18°45'20.40''N; 98°34‟28.8‟‟W 
Spring in Tlapetlahuaya Spring 1681 18°45'20.40''N; 98°34‟28.8‟‟W 
Spring in Tlapetlahuaya Spring 1681 18°45'20.40''N; 98°34‟28.8‟‟W 
Spring in Tlapetlahuaya Spring 1681 18°45'20.40''N; 98°34‟28.8‟‟W 
Spring in Tlapetlahuaya Spring 1681 18°45'20.40''N; 98°34‟28.8‟‟W 
Spring in Tlapetlahuaya Spring 1681 18°45'20.40''N; 98°34‟28.8‟‟W 
Spring in Tlapetlahuaya Spring 1681 18°45'20.40''N; 98°34‟28.8‟‟W 
Spring in Tlapetlahuaya Spring 1681 18°45'20.40''N; 98°34‟28.8‟‟W 
Spring in Tlapetlahuaya Spring 1681 18°45'20.40''N; 98°34‟28.8‟‟W 
Spring in Tlapetlahuaya Spring 1681 18°45'20.40''N; 98°34‟28.8‟‟W 
Spring in Tlapetlahuaya Spring 1681 18°45'20.40''N; 98°34‟28.8‟‟W 
Spring El Toboso Spring 1890 24° 16' 30.7'' N; 104° 34' 52.8'' W 
Spring El Toboso Spring 1890 24° 16' 30.7'' N; 104° 34' 52.8'' W 
Spring El Toboso Spring 1890 24° 16' 30.7'' N; 104° 34' 52.8'' W 
Spring El Toboso Spring 1890 24° 16' 30.7'' N; 104° 34' 52.8'' W 
Spring El Toboso Spring 1890 24° 16' 30.7'' N; 104° 34' 52.8'' W 
Spring El Toboso Spring 1890 24° 16' 30.7'' N; 104° 34' 52.8'' W 
Spring El Toboso Spring 1890 24° 16' 30.7'' N; 104° 34' 52.8'' W 
Spring in park of Tocumbo Spring 1010 19°42'8.9''N; 102°30‟55.6‟‟W 
Spring in park of Tocumbo Spring 1010 19°42'8.9''N; 102°30‟55.6‟‟W 
Spring in park of Tocumbo Spring 1010 19°42'8.9''N; 102°30‟55.6‟‟W 
La Angostura, Zacapu Lake (balneario) Lake with spring 1990 19°49'35''N; 101°47‟10‟‟W 
La Angostura, Zacapu Lake (balneario) Lake with spring 1990 19°49'35''N; 101°47‟10‟‟W 
La Angostura, Zacapu Lake (balneario) Lake with spring 1990 19°49'35''N; 101°47‟10‟‟W 
La Angostura, Zacapu Lake (balneario) Lake with spring 1990 19°49'35''N; 101°47‟10‟‟W 
La Angostura, Zacapu Lake (balneario) Lake with spring 1990 19°49'35''N; 101°47‟10‟‟W 
La Angostura, Zacapu Lake (balneario) Lake with spring 1990 19°49'35''N; 101°47‟10‟‟W 
 142 
 
La Angostura, Zacapu Lake (balneario) Lake with spring 1990 19°49'35''N; 101°47‟10‟‟W 
Tributary of Conchos River, Bocoyna River 2261 27°51'30.32''N; 107°36‟3.01‟‟W 
Tobacco Creek, Manitoba River 
  Quebrada Juan Grande Stream 
 
9°8'50.5''N; 79°43‟21.1‟‟W 
Quebrada Juan Grande Stream 
 
9°8'50.5''N; 79°43‟21.1‟‟W 
Quebrada Juan Grande Stream 
 
9°8'50.5''N; 79°43‟21.1‟‟W 
Frijolito River Stream 
 
9°8'58.1''N; 79°43‟53.8‟‟W 
Frijolito River Stream 
 
9°8'58.1''N; 79°43‟53.8‟‟W 
Frijolito River Stream 
 
9°8'58.1''N; 79°43‟53.8‟‟W 
        
 
Part C 
  Date collected Collection method of fishes Collector of fishes 
1-7.12.2008 Seine nets A. Martínez-Aquino & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
 143 
 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
15.07.2009 Minnow traps and seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
 144 
 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
18-24.08.2008 Electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets and electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets and electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets and electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
23.07.2009 Seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
30.07.2009 Electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
30.07.2009 Electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
30.07.2009 Electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
30.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
30.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
30.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
30.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
30.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
30.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
30.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
30.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
16.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
16.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
16.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
16.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
16.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
16.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
16.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
16.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
16.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
16.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
 145 
 
1-7.12.2008 Seine nets and electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets and electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets and electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets and electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets and electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets and electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets and electrofishing A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
25.07.2009 Seine nets and electrofishing D.I.Hernández-Mena & R. Pérez-Rodríguez 
25.07.2009 Seine nets and electrofishing D.I.Hernández-Mena & R. Pérez-Rodríguez 
25.07.2009 Seine nets and electrofishing D.I.Hernández-Mena & R. Pérez-Rodríguez 
25.07.2009 Seine nets and electrofishing D.I.Hernández-Mena & R. Pérez-Rodríguez 
25.07.2009 Seine nets and electrofishing D.I.Hernández-Mena & R. Pérez-Rodríguez 
25.07.2009 Seine nets and electrofishing D.I.Hernández-Mena & R. Pérez-Rodríguez 
25.07.2009 Seine nets and electrofishing D.I.Hernández-Mena & R. Pérez-Rodríguez 
25.07.2009 Seine nets and electrofishing D.I.Hernández-Mena & R. Pérez-Rodríguez 
25.07.2009 Seine nets and electrofishing D.I.Hernández-Mena & R. Pérez-Rodríguez 
25.07.2009 Seine nets and electrofishing D.I.Hernández-Mena & R. Pérez-Rodríguez 
02.07.2010 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, F.J. Alcantar & R. Pérez-Rodríguez 
02.07.2010 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, F.J. Alcantar & R. Pérez-Rodríguez 
02.07.2010 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, F.J. Alcantar & R. Pérez-Rodríguez 
02.07.2010 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, F.J. Alcantar & R. Pérez-Rodríguez 
02.07.2010 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, F.J. Alcantar & R. Pérez-Rodríguez 
02.07.2010 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, F.J. Alcantar & R. Pérez-Rodríguez 
02.07.2010 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, F.J. Alcantar & R. Pérez-Rodríguez 
02.07.2010 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, F.J. Alcantar & R. Pérez-Rodríguez 
02.07.2010 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, F.J. Alcantar & R. Pérez-Rodríguez 
02.07.2010 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, F.J. Alcantar & R. Pérez-Rodríguez 
02.07.2010 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, F.J. Alcantar & R. Pérez-Rodríguez 
02.07.2010 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, F.J. Alcantar & R. Pérez-Rodríguez 
02.07.2010 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, F.J. Alcantar & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
 146 
 
1-7.12.2008 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
1-7.12.2008 Seine nets A. Martínez-Aquino, R. Aguilar-Aguilar, R. Rosas-Valdez & R. Pérez-Rodríguez 
22.07.2009 Seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
22.07.2009 Seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
22.07.2009 Seine nets A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
17-24.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
17-24.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
17-24.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
17-24.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
17-24.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
17-24.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
17-24.07.2009 Seine nets and electrofishing A. Martínez-Aquino, D.I.Hernández-Mena & R. Pérez-Rodríguez 
- -  R. Rosas-Valdez 
   15-17.01.2010 Seine nets A. Choudhury, A. Martínez-Aquino, & G. Pérez-Ponce de León  
15-17.01.2010 Seine nets A. Choudhury, A. Martínez-Aquino, & G. Pérez-Ponce de León  
15-17.01.2010 Seine nets A. Choudhury, A. Martínez-Aquino, & G. Pérez-Ponce de León  
15-17.01.2010 Seine nets A. Choudhury, A. Martínez-Aquino, & G. Pérez-Ponce de León  
15-17.01.2010 Seine nets A. Choudhury, A. Martínez-Aquino, & G. Pérez-Ponce de León  
15-17.01.2010 Seine nets A. Choudhury, A. Martínez-Aquino, & G. Pérez-Ponce de León  
      
 
Part D 
       Genebank  Genebank 
Collector of digeneans Additional info Vouchers number  ITS1 COI 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 6493*** KC900074 KC899971 
 147 
 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8320 KC899983 KC899864 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8320 KC899984 KC899865 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8320 KC899985 KC899866 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8320 KC899986 KC899867 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8320 KC899987 KC899868 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8320 KC899988 KC899869 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8320 KC899989 KC899870 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8320 KC899990 KC899871 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8320 KC899991 KC899872 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8320 KC899992 KC899873 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8320 KC899993 KC899874 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8320 KC899994 - 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8320 KC899995 - 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8321 KC899996 KC899875 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8321 KC899997 KC899876 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8321 KC899998 KC899877 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8321 KC899999 KC899878 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8321 KC900000 KC899879 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8321 KC900001 KC899880 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8321 KC900002 KC899881 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8321 KC900003 KC899882 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8321 KC900004 KC899883 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 8321 KC900005 - 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_223 Akin CNHE 8323 KC900010 KC899898 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8323 KC900011 KC899899 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8323 KC900012 KC899900 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8323 KC900013 KC899901 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8323 KC900014 KC899902 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8323 KC900015 KC899903 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8323 KC900016 KC899904 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8323 KC900017 KC899905 
 148 
 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8323 KC900018 KC899906 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8323 - KC899907 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8323 - KC899908 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8323 - KC899909 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_261 Akin CNHE 8324 KC900019 KC899910 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8324 KC900020 KC899911 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8324 KC900021 KC899912 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8324 KC900022 KC899913 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8324 KC900023 KC899914 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8324 - KC899915 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8324 - KC899916 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8324 - KC899917 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 6880* KC899977 KC899854 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 6880* KC899978 KC899855 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 6880* KC899979 KC899856 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 6880* KC899980 KC899857 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 6880* KC899981 KC899858 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 6880* KC899982 KC899859 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 6880* - KC899860 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 6880* - KC899861 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 6880* - KC899862 
A. Martínez-Aquino & R. Aguilar-Aguilar - Akin CNHE 6880* - KC899863 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 6498*** KC900071 KC899968 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 6498*** KC900072 KC899969 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 6498*** KC900073 KC899970 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_480 - KC900024 KC899918 
A. Martínez-Aquino & D.I.Hernández-Mena - - KC900025 KC899919 
A. Martínez-Aquino & D.I.Hernández-Mena - - KC900026 - 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_208 Akin CNHE 8325 KC900027 KC899920 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_214 Akin CNHE 8325 KC900028 KC899921 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_222 Akin CNHE 8325 KC900029 KC899922 
 149 
 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8325 KC900030 KC899923 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8325 KC900031 KC899924 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8325 KC900032 KC899925 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8325 KC900033 KC899926 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8325 KC900034 KC899927 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8325 KC900035 - 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_246_a Akin CNHE 8326 KC900036 KC899928 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_246_b Akin CNHE 8326 KC900037 KC899929 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_247 Akin CNHE 8326 KC900038 KC899930 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_249 Akin CNHE 8326 KC900039 KC899931 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8326 - KC899932 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8326 - KC899933 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8326 - KC899934 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8326 - KC899935 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8326 - KC899936 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8326 - KC899937 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8327 KC900066 KC899961 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8327 KC900067 KC899962 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8327 KC900068 KC899963 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8327 KC900069 KC899964 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8327 KC900070 KC899965 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8327 - KC899966 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8327 - KC899967 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8328 KC900040 KC899938 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8328 KC900041 KC899939 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8328 KC900042 KC899940 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8328 KC900043 KC899941 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8328 KC900044 KC899942 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8328 KC900045 KC899943 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8328 KC900046 KC899944 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8328 KC900047 KC899945 
 150 
 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8328 KC900048 KC899946 
A. Martínez-Aquino & D.I.Hernández-Mena - Akin CNHE 8328 KC900049 KC899947 
A. Martínez-Aquino, R. Aguilar-Aguilar & F.J. Alcantar 
Digital Voucher_1269_21-
25 Akin CNHE 8322 KC900006 KC899884 
A. Martínez-Aquino, R. Aguilar-Aguilar & F.J. Alcantar 
Digital Voucher_1269_26-
29 Akin CNHE 8322 KC900007 KC899885 
A. Martínez-Aquino, R. Aguilar-Aguilar & F.J. Alcantar 
Digital Voucher_1269_11-
20 Akin CNHE 8322 KC900008 KC899886 
A. Martínez-Aquino, R. Aguilar-Aguilar & F.J. Alcantar 
Digital Voucher_1277_30-
31 Akin CNHE 8322 - KC899887 
A. Martínez-Aquino, R. Aguilar-Aguilar & F.J. Alcantar 
Digital Voucher_1277_34-
35 Akin CNHE 8322 - KC899888 
A. Martínez-Aquino, R. Aguilar-Aguilar & F.J. Alcantar Digital Voucher_1280 Akin CNHE 8322 - KC899889 
A. Martínez-Aquino, R. Aguilar-Aguilar & F.J. Alcantar - Akin CNHE 8322 - KC899890 
A. Martínez-Aquino, R. Aguilar-Aguilar & F.J. Alcantar - Akin CNHE 8322 - KC899891 
A. Martínez-Aquino, R. Aguilar-Aguilar & F.J. Alcantar - Akin CNHE 8322 - KC899892 
A. Martínez-Aquino, R. Aguilar-Aguilar & F.J. Alcantar - Akin CNHE 8322 - KC899893 
A. Martínez-Aquino, R. Aguilar-Aguilar & F.J. Alcantar - Akin CNHE 8322 - KC899894 
A. Martínez-Aquino, R. Aguilar-Aguilar & F.J. Alcantar - Akin CNHE 8322 - KC899895 
A. Martínez-Aquino, R. Aguilar-Aguilar & F.J. Alcantar - Akin CNHE 8322 - KC899896 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8329 KC900060 KC899954 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8329 KC900061 KC899955 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8329 KC900062 KC899956 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8329 KC900063 KC899957 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8329 KC900064 KC899958 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8329 KC900065 KC899959 
A. Martínez-Aquino, R. Aguilar-Aguilar & R. Rosas-Valdez - Akin CNHE 8329 - KC899960 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_532 - KC900050 KC899948 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_541_a Akin CNHE 8330 KC900051 KC899949 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_541_b Akin CNHE 8330 KC900052 KC899950 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_181 Akin CNHE 7811** KC900053 KC899951 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_118 Akin CNHE 7812** KC900054 KC899952 
 151 
 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_121 Akin CNHE 7812** KC900055 KC899953 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_124 Akin CNHE 7812** KC900056 - 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_131.1 Akin CNHE 7812** KC900057 - 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_135 Akin CNHE 7812** KC900058 - 
A. Martínez-Aquino & D.I.Hernández-Mena Digital Voucher_139 Akin CNHE 7812** KC900059 - 
 R. Rosas-Valdez - Akin CNHE 8331 KC900009 KC899897 
A. Choudhury 
  
KC899972 KC899847 
A. Choudhury, A. Martínez-Aquino, & G. Pérez-Ponce de León  
 
KC899973 KC899848 
A. Choudhury, A. Martínez-Aquino, & G. Pérez-Ponce de León  
 
KC899974 KC899849 
A. Choudhury, A. Martínez-Aquino, & G. Pérez-Ponce de León  
 
- KC899850 
A. Choudhury, A. Martínez-Aquino, & G. Pérez-Ponce de León  
 
KC899975 KC899851 
A. Choudhury, A. Martínez-Aquino, & G. Pérez-Ponce de León  
 
KC899976 KC899852 
A. Choudhury, A. Martínez-Aquino, & G. Pérez-Ponce de León  
 
- KC899853 
          
 
 
 
 
 
 
 
 
 
 
 152 
 
 
 
 
 
 
 
 
 
 
 
CAPÍTULO III 
DOES THE HISTORICAL BIOGEOGRAPHY AND COPHYLOGENY OF THE DIGENEAN 
MARGOTREMA SPP. ACROSS CENTRAL MEXICO MIRRORS THAT OF THEIR FRESHWATER FISH 
HOSTS (GOODEINAE)? 
 
 
 
 
 
 
 
 
 
 
 
 
 
 153 
 
Para concretar este proyecto, se planteo como objetivo integrar la historia evolutiva de 
Margotrema spp., influenciada por la evolución de Goodeinae y la geología del centro de 
México, a través de la identificación de patrones biogeográficos y cofilogenéticos. Para ello, se 
pusieron a prueba las hipótesis biogeográficas y cofilogenéticas detectadas con base en la 
reconstrucción genealógica de Margotrema propuestas por Martínez-Aquino et al. (2013), a 
través de análisis biogeográficos paramétricos (Ree & Sanmartín, 2009; Sanmartín, 2010; 
Ronquist & Sanmartín, 2011). Para evaluar hipótesis biogeográficas y cofilogenéticas 
considerando variables espacio-temporales, se realizó un análisis de Species Tree multispecies 
coalescent con el objetivo de estimar las edades de divergencia de los linajes de Margotrema, 
usando métodos de reloj molecular bayesianos (Drummond et al., 2006) calibrado a partir de 
eventos geológicos sobre la región occidental de la Faja Volcánica Transmexicana (FVT) (Ferrari 
et al., 1999; Mateos et al., 2002; Ferrari, 2004). 
  Los patrones de distribución geográfica de Margotrema fueron estudiados a través de 
análisis de DEC (por sus siglas en inglés Dispersal-Extinction-Cladogenesis; Ree et al., 2005; 
Ree & Smith, 2008), usando como unidades de estudio los sistemas hidrológicos previamente 
considerados para análisis biogeográficos de Goodeinae por Domínguez-Domínguez et al. 
(2010). Como primer paso, evaluamos la similitud de las áreas a utilizar a partir de los datos 
filogenéticos de Margotrema (Martínez-Aquino et al., 2013), usando métodos binarios 
bayesianos a través de la reconstrucción de estados ancestrales en filogenias (RASP, por sus 
siglas en inglés Reconstruct Ancestral State in Phylogenies; Nylander et al., 2008; Yu et al., 
2010, 2011). Este análisis fue realizado para describir la concordancia biogeográfica entre las 
unidades de análisis hidrológicas tanto para peces como para sus digéneos parásitos. 
Propiamente, la reconstrucción de la biogeografía histórica de Margotrema se realizó con base en 
medios biogeográficos paramétricos tomando en cuenta tres variables: a) distancia geográfica; b) 
eventos geológicos; c) patrones y fechas de diversificación del ancestro común más reciente 
(MRCA, por sus siglas en inglés Most Recent Common Ancestor), para cada especie de huésped 
con respecto a cada una de las tribus de Goodeinae, es decir, Chapalichthyini, Characodontini, 
Girardinichthyini e Ilyodontini. 
  Como es posible realizar analogías entre los procesos biogeográficos y cofilogenéticos 
(Page, 1994a; Page & Charleston, 1998; Matzke, 2010), seleccionamos como unidades de 
 154 
 
análisis a las especies de goodeinos en los que están asociados los digéneos Margotrema, 
implementando un modelo de DEC. Para este análisis también consideramos a) la probabilidad 
de dispersión de las individuos de Margotrema, en función a la vagilidad y dispersión registrada 
para las especies explícitas de goodeinos a los que están actualmente asociados en cada una de las 
localidades muestreadas, y tomando en cuenta la distancia geográfica entre las áreas analizadas 
(sistemas hidrológicos); b) las edades de divergencia de cada especie / género de huésped, así 
como las relaciones genealógicas entre Margotrema y sus áreas de distribución. Se realizó una 
prueba estadística (“p”) implementada en el programa TreeMap 3b (Charleston, 2013), para 
proveer de una medida de confianza (intervalo de confianza = 95%) a aquellos grupos 
pertenecientes a Goodeinae y Margotrema que reflejaban cierto grado de congruencia 
filogenética (correspondencia topológica entre dos o más arboles filogenéticos). Con base en los 
patrones biogeográficos y cofilogenéticos observados para Margotrema, se interpretó la historia 
evolutiva de este taxón para comprender como es el origen de los procesos de diversificación de 
los organismos parásitos en peces dulceacuícolas endémicos de México. 
  A continuación se presenta un manuscrito en formato de articulo en extenso intitulado 
“Does the historical biogeography and evolutionary history of the digenean Margotrema 
spp. across central Mexico mirrors that of their freshwater fish hosts (Goodeinae)?”, el cuál 
será sometido para su publicación en una revista arbitrada e indizada (ISI / SCI), referente a los 
patrones biogeográficos y cofilogenéticos de Margotrema.  
 
 
 
 
 
 
 
 
 
 155 
 
Manuscrito para ser sometido para su publicación en la revista Journal of Biogeography  
Original Article 
Running header: Margotrema biogeography: cophylogeny and history  
 
Does the historical biogeography and evolutionary history of the digenean Margotrema spp. 
across central Mexico mirrors that of their freshwater fish hosts (Goodeinae)?  
 
Andrés Martínez-Aquino1,2*, Fadia Sara Ceccarelli3, Luis E. Eguiarte4, Ella Vázquez-Domínguez5 
and Gerardo Pérez-Ponce de León1 
 
1Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, 
Apartado Postal 70-153, C.P. 04510, México, D.F., México.  
2 Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Av. Ciudad 
Universitaria 3000, C.P. 04360, Coyoacán, Distrito Federal, México.  
3 Institut für Biogeographie, Klingelbergstrasse 27 CH-4056 Basel, Switzerland. 
4 Laboratorio de Evolución Molecular y Experimental, Departamento de Ecología Evolutiva, 
Instituto de Ecología, Universidad Nacional Autónoma de México. Apartado Postal 70-275, C.P. 
04510 México, D.F., Mexico. 
5Departamento de Ecología de la Biodiversidad, Instituto de Ecología, Universidad Nacional 
Autónoma de México, Apartado Postal 70-275, C.P. 04510 México D.F., 04510, México. 
 
Correspondence: Andrés Martínez-Aquino, 1Departamento de Zoología, Instituto de Biología, 
Universidad Nacional Autónoma de México, Apartado Postal 70-153, C.P. 04510, México, D.F., 
 156 
 
México; 2 Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Av. 
Ciudad Universitaria 3000, C.P. 04360, Coyoacán, Distrito Federal, México. 
E-mail: maandres@ibiologia.unam.mx 
 
ABSTRACT 
Aim To use recently published phylogenies of Goodeinae and those of their digenena parasite 
(Margotrema spp.) to uncover biogeographical and cophylogenetic patterns and to describe the 
processes that determined them over 6.5 Ma. The key questions addressed in this study is: Was 
the evolution of Margotrema spp. influenced by the complex geographical scenario of central 
Mexico, by the close association with their goodeinae hosts, or both? 
Location Hydrological systems of central Mexico.  
Methods A species tree for Margotrema spp. was obtained using DNA sequence data from two 
molecular markers, and a molecular dating looking for divergence events within the genus was 
performed. A dispersal-extinction-cladogenesis (DEC) model was used to describe the historical 
biogeography of digeneans. Meanwhile, DEC was used to uncover cophylogenetic events 
between Margotrema and their goodeines hosts. 
Results This study shows a response of the parasite taxa in a geographical context, followed by 
establishing host specificity at three distinct levels of the historical association with their hosts: a) 
Species-Species, i.e., a historical association represented by Xenotaenia resolanae-M. resolanae 
exclusively at the Cuzalapa River Basin; b) Species-Lineage, i.e., a historical association 
represented by Characodon audax-M. bravoae Linaje III, exclusively distributed along the Upper 
and Middle Mezquital River Basin and c) Tribe-Lineage, i.e., two instances of historical 
associations among parasites and hosts at taxonomical level of Tribe, one represented by 
Ilyodontini-M. bravoae Lineage I, which are mainly distributed across the Ayuquila and Balsas 
River Basins, and the second represented by Girardinichthyini / Chapalichthyini-M. bravoae 
Lineage II, only distributed in the Lerma River Basin.  
Main conclusions The parasite evolutionary history is congruent with the phylogenetic and 
biogeographical history and of their hosts, showing instances of coespeciation and several 
 157 
 
colonization events via host-switching and vicariant plus dispersal events at different times 
during the diversification history of both associates, related with tecto-volcanic events that 
occurred in the area. 
Keywords 
Codivergence, cospeciation, DEC model, divergence times, host switch, host-parasite 
evolution, lineage loss, Parametric biogeography, vicariance, dispersal. 
 
INTRODUCTION 
The evolutionary biology of host-parasite associations can be analogized to biogeographical 
processes in terms of events such as codivergence, duplication, horizontal transfer and lineage 
sorting (Page, 1994a; Page & Charleston, 1998; Matzke, 2010). The study of a host-parasite 
association focuses in the effects of geographical distribution in combination with the 
phylogenetic relationships of the hosts, on the evolution of the parasitic organisms. These two 
elements can be analysed by event-based biogeography methods (Ronquist & Sanmartín, 2011), 
as well as through evolutionary tangled trees of hosts and parasites (Page, 2003). Parametric 
biogeography methods (Ree et al., 2005; Ree & Smith, 2008, Sanmartín et al., 2008), coupled 
with dated species-tree estimation (Maddison, 1997; Edwards, 2009; Heled & Drummond, 2009), 
and contrasting the phylogenetic relationships between two groups (Charleston, 2011) with a 
narrow biological association in a particular geographical area, allow for hypotheses of 
evolutionary history and biogeography to be tested explicitly in time and space (see Sanmartin et 
al., 2008; Cowman & Bellwood, 2013; Ceccarelli & Zaldivar-Riverón, 2013). 
 Biogeographical reconstruction with parametric methods is implemented through 
models such as dispersal-extinction-cladogenesis (DEC) (Ree et al., 2005; Ree & Smith, 2008), a 
method that permit uncovering dispersal and extinction events along branches of a phylogeny, 
while estimating the ranges of the most recent common ancestor (MRCA) and descendent species 
at each node. DEC can be used to test hypotheses of origin of areas as well as geographical 
species within lineage formation scenarios, and dispersal (expansion routes), by incorporating 
 158 
 
both, historical and contemporary information for a particular region and the organisms 
associated to that region. 
  Previous studies have shown that geographical features may be influential in shaping 
genealogical relationships by causing a codifferentiation of parasitic organisms in relation to the 
evolutionary history of their hosts (Nieberding et al., 2008, Mizukoshi et al., 2012). However, it 
is difficult to find a biological model of parasitism capable to explain the process of 
diversification between hosts and parasites. The biogeographical “core” parasite fauna, i.e. 
species widely distributed and characteristically associated with and restricted to a monophyletic 
group of hosts species, in freshwater fishes across central Mexico (see Pérez-Ponce de León & 
Choudhury, 2005) offers a unique opportunity to test diversification processes between parasites 
and hosts, because they show high levels of host-specificity, are distributed in a restricted 
geographical area, and do not disperse naturally across water; therefore, there is no gene flow 
among individuals parasitising host species other than goodeines, or among goodeines occurring 
in different hydrological systems (Martínez-Aquino et al., 2013).  
  Additionally, central Mexico, and particularly the so-called Trans Mexican Volcanic 
Belt (TMVB), has been considered as a model of biodiversification, as it is a transitional area 
between the Neotropical and Nearctic biogeographical regions (Luna-Vega et al., 2005; Morrone, 
2010; Luna-Vega & Contreras-Medina, 2012). The TMVB is considered an area of endemism for 
several taxa, as a result of a complex hydro-geomorphological history; particularly, this is a 
remarkable area of endemism for the freshwater fish fauna (Miller et al., 2005). 
 Among the endemic elements of the central Mexico freshwater fish fauna are the 
goodeines, a monophyletic group of cyprinodontiforms that experienced a diversification in the 
area (Domínguez-Domínguez et al., 2010 and references therein). On the other hand, the genus 
Margotrema represents the model of this study since their species are relatively common as 
parasites of goodeines across Mexico (Martínez-Aquino et al., 2013). Since the evolutionary and 
biogeographical history of goodeines in central Mexico was influenced by the tecto-volcanic 
activity and events such as river piracy (Parenti, 1981; Miller  Smith, 1986, Domínguez-
Domínguez et al., 2010), Martínez-Aquino et al. (2013) recently demonstrated that the 
genealogical structure of Margotrema (i.e., M. resolanae and three independent genetic lineages 
of M. bravoae) shows a particular geographical distribution pattern across hydrological systems 
 159 
 
in central Mexico, and also that each lineage of Margotrema apparently shows some specific 
association with their hosts, at the goodeine tribe level, as monophyletic group. These results 
shed light on the hypothesis that the distribution patterns, as well as host associations of each 
lineage of Margotrema, would be concordant with the hydrogeomorphological events that 
occurred in central Mexico, and that the vicariant and dispersal events that caused the goodein 
diversification promoted at the same time the diversification of each Margotrema lineage. In this 
context, two general patterns in the evolution of Margotrema were uncovered: 1) Restricted 
geographical distribution in hydrological systems, i.e., M. resolanae is exclusively found in the 
Cuzalapa River Basin, meanwhile M. bravoae Lineage I is only found in the Ayuquila, Balsas 
and Conchos rivers, M. bravoae Lineage II is only found in the Lerma River, and M. bravoae 
Lineage III is exclusive to the Mezquital River. And the second pattern: 2) Host specificity at 
host-species and host-tribe level, e.g., M. resolanae is associated only to Xenotaenia resolanae 
(Tribe: Ilyodontini) while M. bravoae Lineage I is found in hosts belonging to Ilyodontini; M. 
bravoae Lineage II is associated to hosts of Girardinichthyini and Chapalichthyini, and finally, 
M. bravoae Lineage III is exclusive to Characodon audax (Tribe: Characodontini).  
 In the present study, biogeographical and phylogenetic analyses of goodeines, as well as 
the phylogenetic relationships of Margotrema spp. were explicitly used to explore the 
evolutionary process that may have driven the diversification of the host-parasite association, and 
to determine the potential role that geographical distribution had on the evolutionary history of 
both, goodeines and their digenean parasites. To accomplish that goal, phylogenetic 
reconstructions of both fish and parasites, along with novel probabilistic algorithms as a means of 
providing more objective outcomes, were used. This study was then designed to answer the 
following four questions: 1. What is the divergence time for each lineage of Margotrema? 2. Is 
there a biogeographical congruence between the genealogical history of Margotrema and the 
hydro-geomorphological history of central Mexico which is supported by the historical 
biogeography of their goodein hosts? 3. Is there a congruence (i.e., cophylogeny) between the 
evolutionary histories of the tribes of Goodeinae and those of Margotrema?, and finally, 4. Is 
there a congruence between the divergence time among the main clades of Goodeinae and each 
species (or Lineage) of Margotrema? 
 
 160 
 
MATERIALS AND METHODS 
Taxa, molecular dataset and phylogenetic analyses 
The taxa used for phylogenetic analyses comprised samples of Margotrema spp. used already in a 
previously study; two molecular markers were sequenced, fragments of COI (mitochondrial 
DNA) and ITS1 (nuclear DNA). Analyses included two outgroups (i.e. Allocreadium lobatum and 
Walliniae chavarriae). The software RASP version 2.1 (Nylander et al., 2008; Yu et al., 2010, 
2011) was used for biogeographic analyses of the first phylogeny (see below). We used the same 
combined dataset (COI + ITS1) to perform a multispecies coalescent analysis as implemented in 
*BEAST (version 1.7.2, Drummond  Rambaut, 2007; Heled  Drummond, 2010), resulting in 
a Species Tree (ST) to infer the genealogical relationship between M. resolanae and the three 
lineages of M. bravoae (see Martínez-Aquino et al., 2013). 
Divergence Dating 
To propose an accurate time frame for phylogenetic divergence processes between the areas 
(localities) for each lineage of Margotrema spp. (see Appendix 1 in Supporting Information), we 
estimated mean node ages and their 95% highest posterior densities (HPDs) using a Bayesian 
relaxed molecular clock method (Drummond et al., 2006) as implemented in *BEAST v. 1.7.4 
(Drummond et al., 2012). In this method, test of evolutionary hypotheses are not conditioned to a 
single tree topology, which allows for simultaneous evaluation of topology and divergence times 
while incorporating uncertainty in both. A uniform Yule tree prior was specified, as appropriate 
for hierarchical rather than reticulate relationships, and a sub-sampling of one representative 
specimen for every lineage was included to avoid over-representation of certain individual 
lineages. We applied the same optimal model as obtained by Martínez-Aquino et al., (2013), of 
data partitioning and DNA substitution, identified by BIC for using jModelTest 0.1.1. (Posada, 
2008), for each gene COI with HKY+I+G and ITS1 with HKY+G invariant sites in *BEAST 
package (BEAUti v 1.7.4; Drummond et al., 2012). An uncorrelated relaxed log normal 
molecular clock was applied to model rate variation across branches. Were introduced uniform 
prior distributions because of the lack of evidence to justify a specific distribution of rates in our 
data. Based on geographical distribution (localities where with published records) of Margoterma 
(Pérez-Ponce de León et al., 2007, 2009, 2013; Martínez-Aquino et al., 2007, 2009, 2011, 2012, 
 161 
 
2013; Aguilar-Aguilar et al., 2010), a geological calibration was applied, based on the uplifting 
of the western part of the TMVB, which began around 11 million years ago (Ma) (Ferrari et al., 
1999; Ferrari, 2004). This age was set, as a maximum for the MRCA of Margotrema spp. 
Monophyly was not enforced for any of the other nodes. Analyses were run for 50 million 
generations with a sampling frequency of one in every 1000 generations. Branch support for the 
different tree topologies was evaluated by Posterior Probability (PP) of the inferred relationships, 
where PP > 0.95 was considered to provide strong nodal support. The trees with the highest 
lineage PP were chosen from *BEAST output files using the program TreeAnnotator v.1.7.4 
(Drummond et al., 2012). The phylogenetic divergence processes were run in the aforementioned 
programs in the Bioportal of the University of Oslo (http://www.bioportal.uio.no/). 
Historical biogeography 
To test the naturalness of 12 hydrological systems as a single biogeographical unit we explored – 
as a first step – the PP values of the ancestral areas of the main clades recovered within the 
lineages of Margotrema spp. using a Bayesian method for biogeographical and ancestral state 
reconstructions implemented in the program RASP version 2.1. Bayesian binary MCMC analyses 
performed on the last 10, 000 trees obtained from both MrBayes runs, were set to 10, 000, 000 
cycles, coding the geographic distribution of the terminal taxa into 12 different areas following 
Domínguez-Domínguez et al. (2006, 2010), delimited based on the Mexican hydrological basins 
and sub-basins map produced by the Comisión Nacional para el Conocimiento y Uso de la 
Biodiversidad (CONABIO 1998; www.conabio.gob.mx). Furthermore, for this first analysis we 
used two plus areas correspond to distribution area of outgroups (see Appendix 1). 
To uncover the events that influenced the historical biogeography and diversification 
processes (i.e. Ronquist  Sanmartín, 2011; Sanmartín, 2012) of M. resolanae and M. bravoae 
(the three lineages), we performed Dispersal-Extinction-Cladogenesis (DEC) analyses using the 
program Lagrange v. 20120508 (Ree  Smith, 2008) on the dated ultrametric tree of areas 
obtained from *BEAST (see below). Once we obtained the probability values from the Bayesian 
binary MCMC analyses (not show results), we selected a new set of hydrological systems and 
built a second matrix of eight areas (basins and sub-basin rivers), without outgroups, to tested a 
DEC model (see Appendix S2A-C). The input file for the analysis was constructed using the 
web-based Lagrange configurator (http://www.reelab.net/lagrange/configurator/index). The 
 162 
 
maximum range size for ancestral areas was set to two. Dispersal probabilities were constrained 
based on the following three factors. I) Geographical distance. II) Geological events, i.e. uplifting 
of the western part of the TMVB (6 – 10 Ma) (Ferrari et al., 1999; Ferrari, 2004), Tamazula 
failure (5 – 4.2 Ma) (Rosas-Elguera et al., 1996; Ferrari  Rosas-Elguera, 1999), connection / 
disconnection of Cuitzeo-Aztlán paleolakes (5.8 Ma) (Israde-Alcántara and Garduño-Monroy, 
1999; Silva-Romo et al., 2002), main course of the ancient El Naranjo-Verde River (De Cserna  
Álvarez, 1995), El Salto waterfall failure (1.5 Ma) (Albitron, 1958). III) Patterns and dates of 
diversification of the most recent common ancestor (MRCA) of particular taxa of each tribe of 
goodein hosts; i.e. Xenotaenia resolanae (5.1 Ma) and the genus Allodontichthys (5.6 Ma), both 
of the tribe Ilyodontini (6.9 Ma); Neoophorus regalis (6.9 Ma), of the tribe Girardinichthyni (8 – 
7 Ma) and to Characodon audax (1.8 Ma) of the tribe Characodontini (15.5 Ma) (for more details 
see Domínguez-Domínguez et al., 2006, 2010). 
A second DEC was carried out to detect the biogeographical events in several localities 
of M. bravoae Lineage III (Martínez-Aquino et al., 2013), in the area and particular timing of the 
plio-pleistocenic lakes from central Mexico (< 1 Ma). For this analysis, we built a third matrix of 
six areas (i.e. sub-basin) (Appendix S3A-B). The maximum range size for ancestral areas was set 
to two. Also, dispersal probabilities were constrained based on the three factors mentioned above; 
i.e. geographical distances, dates of connection / disconnection of Zacapu-Villa Morelos-Cuitzeo 
paleolakes (Plio-Pleistocene < 1 Ma) (Israde-Alcántara, 1999), patterns and dates of 
diversification of the MRCA of the tribes Girardinichthyini and Chapalichthyini, respectively (for 
more details see Domínguez-Domínguez et al., 2010). 
Cophylogeny 
To test the evolutionary associations, i.e., codivergence between goodein fishes and their 
digenean parasites, a DEC model using the software Lagrange was implemented. Trees involving 
the association of two taxa are used to infer their common evolutionary history, both in a 
geographic (area and organism trees) and in a cophylogenetic scenario (host and parasite) 
(Matzke, 2010). Since the biogeographical interpretations can be analogized to cophylogenetic 
ones, the following analogies, as study units, were used in accordance with Matzke (2010): area / 
host; organism / parasite, dispersal / host switch; vicariance / cospeciation; sympatric speciation / 
parasite speciation on one host; extinction / parasite extinction (lineage loss). Also, in this study 
 163 
 
the following terms were used following Charleston (2011): Codivergence, which also referred as 
cospeciation, implies an event where a parasite lineage (e.g., species) infecting a host lineage 
diverges into two new lineages at the same moment that its host does. Duplication is the event 
where the parasite lineage diverges into two new lineages, independently of its host, and both 
new lineages remain on that host lineage. Host switching is defined as the event where the 
parasite diverges by switching to establishing on another host lineage (Charleston, 2011); 
following Choudhury (2002), parasite speciation may either be concomitant with and resulting 
from host speciation (cospeciation) or follow the colonization of a „„new‟‟ host from an existing 
one (host-switching). 
 In this context, to test when cophylogenetic events in a particular time and space occurred 
between association Goodeinae-Margotrema spp., we performed a DEC using the species‟ hosts 
as areas and the parasites as organisms distributed in the areas. For this analysis, we built a third 
matrix of 15 areas as a single biogeographical unit (host species) (Appendix S4A-B). The 
maximum range size for ancestral areas was set to two. The dispersal probabilities were 
constrained considering geographical distances, similar events as the ones for the geographical 
DEC analyses, plus divergence timing of genus / species of hosts (Appendix S4B) and the 
genealogical relationships between Margotrema spp. and their geographical areas. 
 Additionally, to determine whether there is a significant match between host and parasite 
trees, the phylogenies of the subfamily Goodeinae and Margotrema were compared using a 
statistic test of p values with a 95% of confidence intervals through TreeMap 3b (Charleston, 
2011). We employed the tree topologies obtained from the cytochrome b gene sequence from the 
hosts and COI+ITS1 sequences from four lineages of Margotrema spp. The consensus trees from 
the Bayesian Inference analyses (dated with Maximum Likelihood approach) of Goodeinae (see 
Domínguez-Domínguez et al., 2010), were edited through the program Mesquite Modular 
System for Evolutionary Analysis (MESQUITE) version 2.72 (Maddison  Madisson, 2011) to 
select the terminal taxa that can be found in a host-parasite association with Margotrema, and to 
remove the remaining terminal taxa from the tree. Similarly, the dated molecular phylogeny of 
Margotrema spp. was also edited in MESQUITE, in that samples of each locality were trimmed 
to a single terminal taxon. This was done because TreeMap 3b only reconciles strictly 
dichotomous trees.  
 164 
 
RESULTS 
Divergence times 
The divergence time estimates, based on the tree reconstructed using *BEAST, for the MRCA of 
M. resolanae + M. bravoae clade was 6.53 Ma. The divergence time between the ancestor of 
Lineage I and the ancestor of lineages II and III was dated 3.20 Ma, and finally, lineages II and 
III diverged 1.03 Ma. (Appendix S5). 
Historical Biogeography 
The results of the reconstruction of ancestral areas through the Bayesian MCMC algorithm in 
RASP, considering the same dataset for the main lineages of Margotrema spp. uncovered eigth of 
the 18 river sub-basins across central Mexico (not show results), as defined by Domínguez-
Domínguez et al. (2006, 2010). The same areas were used for carrying out the DEC analysis.  
 We used two distinct matrices of areas to test the biogeographical events of the Lineages 
of Margotrema spp. in each locality. The most clear-cut summary of the data of the geographical 
distribution of each Margotrema lineage (Fig. 1), was recovered by analysis of the combined 
dataset matrix of DEC to 0 – 6.5 Ma (i.e. Appendix S2C) and DEC to 0 – 1 Ma (i.e. Appendix 
S3C) and is presented next.  
 The analysis in Lagrange show that the MRCAs of M. resolanae and M. bravoae were 
distributed in a geographical range which apparently spanned the North-Western Central in 
Cuzalapa River, Upper and Middle Mezquital River and Armería-Ayuquila Rivers (areas I, B and 
H, respectively). The first diversification event occurred when this MRCA was isolated by a 
vicariant event in the Cuzalapa River, from the ancestor of M. bravoae (B, H) producing an 
allopatric speciation for M. resolanae in this river (Fig. 1a). Once in areas B and H, the MRCA of 
the three lineages of M. bravoae underwent dispersion to the Cotija area [J] and the Lower Balsas 
River [K], and apparently it was lost in the Armería-Ayuquila River [H]. This MRCA, through a 
vicariant event, experienced cladogenesis separating the MRCA of Lineage I (in Area K) from 
the MRCA of Lineages II and III in areas B and J (Fig. 1a). 
Margotrema bravoae Lineage I 
 165 
 
The MCRA of Lineage I (distributed in the Lower Balsas River, K) exhibited two dispersal 
events, in one, the ancestor dispersed back into the Armería and Ayuquila Rivers (H), and in the 
second, to a tributary of Conchos River (A). A vicariant event then separated areas H and A from 
K and finally, the areas H and A, and K and L (Upper Balsas River) were separated by vicariant 
events, respectively (Fig. 1b).  
Margotrema bravoae Lineage II & III 
Once in areas B and J, the MRCA of Lineages II and III dispersed into Lower Lerma River (C). 
Later, a vicariant event separated the Upper and Middle Mezquital River (B) from the Lower 
Lerma River (C) + Cotija (J) (Fig. 1a). Lineage III of M. bravoae is exclusively found in the 
Mezquital River (B). 
Margotrema bravoae Lineage II 
The MRCA of M. bravoae Lineage II distributed in C and J (Fig. 1a) deserved further 
consideration, since it experienced several vicariant and dispersal events. This ancestor dispersed 
to Cuitzeo Lake (E) and Zirahuén Lake (G) (Fig. 1c). A vicariant event separated Cotija (J) from 
the other areas of the Lerme River (C, E, and G). A posterior vicariant event isolated Zirahuén 
Lake (G) from Cuitzeo Lake and Lower Lerma River which were subsequently separated by 
another vicariant event. A population from Zirahuén Lake (G) dispersed into Zacapu Lake (D) 
and Pátzcuaro Lake (F) and later, these areas were geographically separated.  
Cophylogenetic patterns 
A DEC analysis was performed using all host species – areas – of Margotrema in all recorded 
localities in our phylogenetic study (Fig. 2). These analyses show that the MRCA of M. 
resolanae and M. bravoae was associated to Allodontichthys zonistius (g) and Codoma ornata 
(h), giving rise to a lineage duplication in one host (i.e. into “g”) (akin to a allopatric speciation 
event) and a posterior cospeciation in Xenotaenia resolanae (m), plus lineage loss in A. zonistius 
because to extinction of this host (Fig. 2a). The MRCA of the three lineages of M. bravoae sensu 
lato (Martínez-Aquino et al., 2013) was associated to A. zonistius and C. ornata since 6.53 – 3.20 
Ma (Fig. 2a). In total, in the three lineages of M. bravoae was found five events of duplication 
 166 
 
following of host-switching + lineage loss, and only one more without lineage loss; plus six of 
codivergence events (Fig. 2). 
Margotrema bravoae Lineage I 
Particularly, the MRCA of the M. bravoae Lineage I was associated to A. zonistius (g) + C. 
ornata (h) (Fig. 1a), and posteriorly, colonised several host species belonging to the Ilyodontini 
(Fig. 2b). For example the parasite associated with A. zonistius experienced a host switching 
event into Ilyodon furcidens (k) (in Armería Ayuquila Rivers [H]) (Fig. 1, 2), followed by 
dispersal into I. whitei (l) (hypothetically, in a same area as Lower and Upper Balsas Rivers [K] 
and [L]). After, a codivergence event separated the populations associated to I. furcidens (k) (in 
the Lower Balsas River [K]) and I. whitei (l) (in the Upper Balsas River [K]). Finally, M. bravoae 
Lineage I occurring in the Lower Balsas River (K) (Fig. 1b) experienced a host switching event 
into Chapalichthys pardalis (j) with both hosts occurring in sympatry (Fig. 2b). 
Margotrema bravoae Lineages II & III 
The possible differentiation of the MRCA of Lineages II and III of M. bravoae was due to a host 
switching event that separated Lineage II from III. Previously, DEC uncovers a dispersal event of 
the ancestor into Characodon audax, and a concomitant vicariant event separated the populations 
of C. audax in the Mezquital River from the other ancestor that colonised Chapalychthyini and 
Girardinychthyini in the Lerma River (Fig. 2a, 2c). 
Margotrema bravoae Lineage II 
Particularly, in Lineage II, the ancestor experienced colonisation via host switching into 
Neoophorus regalis (d) and Zoogoneticus quitzeoensis (n) in the Lerma River Basin (Fig. 2c). 
Posteriorly, other host switching events occurred once the ancestor was in that particular 
geographical area. For instance a host switching event allowed the colonisation of Alloophorus 
robustus (e), while another five host switching events allowed the colonisation of Allotoca meeki 
(c), A. duguesi (b), A. diazi (a), and A. zacapuensis (f) (Fig. 1c). 
 Finally, cophylogenetic results show three general patterns bewteen the two associated 
taxa, through a reconciliation phylogenetic analysis using TreeMap 3b. These patterns are shown 
in the form of a Tanglegram, were the topology of the phylogenetic trees of both groups can be 
 167 
 
compared (Fig. 3). The resulting three shows all three levels of host-parasite association between 
Goodeinae and Margotrema: Level 1 is Species-Species, interpreted as cospeciation; Level 2 is 
Species-Lineage, interpreted as Codivergence Type I, when the host experience a speciation 
process and a parasite lineage colonised posteriorly reaching some level of intraspecific genetic 
divergence; and Level 3 is Tribe-Lineage, interpreted as Codivergence Type II, when divergence 
occurs at deeper level of the phylogenetic history of the hosts (tribes) and parasites colonised 
these hosts acquiring some level of intraspecific genetic divergence (Fig. 3). 
DISCUSSION 
Most Recent Common Ancestor of the genus Margotrema 
The divergence date of the most recent common ancestor (MRCA) of the genus Margotrema was 
estimated in 6.53 Ma, and apparently it was distributed in northern Mexico in the Upper and 
Middle Mezquital and in the Cuzalapa and Armería-Ayuquila Rivers (Fig. 4a). This MRCA was 
associated with A. zonistius (Goodeinae) and C. ornata (Cyprinidae) (Fig. 2a). Recent reports on 
the presence of Margotrema spp. in hydrological systems of Northern Mexico parasitising 
freshwater fish species belonging to the Cyprinodontidae and Cyprinidae are strong evidence of 
the possibility that these parasites colonised goodeids from other freshwater fish groups, either 
from the Nearctic cyprinids or the Neotropical cyprinodontids. For instance, records of 
Margotrema spp, albeit with low relative prevalence and abundance values, have been established 
for Cyprinodon nazas (Cyprinodontidae) in the Nazas River Basin, and more frequently, in the 
following cyprinids: C. ornata in the Piaxtla River Basin and Cyprinella lutrensis in the Santa 
María River Basin (Pérez-Ponce de León et al., 2009, 2013; Aguilar-Aguilar et al., 2010) (Fig. 
4a, Appendix 6).  
         Based on the recovered ancestral area through the analyses conducted in this study, some 
support is provided for the Nearctic affinity of this digenean, as previously suggested by Pérez-
Ponce de León et al. (2007) and Curran et al. (2011), even though these authors found a close 
sister group relationship between Margotrema and Crepidostomum, both members of the 
Allocreadiidae, with the latter being a common parasite of centrarchids. The divergence date, 
ancestral associations and distribution of Margotrema, in addition to the biogeographical and 
cophylogenetic patterns uncovered by the DEC-model, allows us to propose that the ancestral 
 168 
 
area of the MRCA extended across hydrological systems currently occupied by the Sierra Madre 
Occidental (SMOc), and western regions of the Altiplano Mexicano (AM) (biogeographical 
provinces sensu lato, Morrone, 2005) (Fig. 4a).  
          In terms of host-association, two competing historical scenarios could have occurred:  
a) Goodeidae-Margotrema. This scenario is explained by an ancestral relationship between 
Margotrema and goodeines ocurring in northern Mexico. The ancestral area of Margotrema, as 
shown in this study, is similar to that of the MRCA´s for Goodeinae (divergence dated as 15.5 to 
8 Ma, see Domínguez-Domínguez et al., 2010). A goodeid fossil (Empetrichthys erdisi) was 
found in the Yaqui River, Sonora, in Northwestern Mexico, a locality close to the area where 
goodeids are currently distributed (Uyeno & Miller, 1962; Parenti, 1981; Minckley et al., 1986). 
The sister group of Goodeinae is Empetrichthyinae, and the diversification event that gave rise to 
both subfamilies is recognized to have occurred in the Great Basin in southwestern USA (Parenti, 
1981). The result of the overlap on the distribution range of both ancestors was the establishment 
of a close evolutionary relationship with strong host-specificity, and it was latter dispersed into 
2003), even though goodeines experienced a diversification in river basins of northern Mexico, 
and more intensively in central Mexico. An important question that remain unresolved is where 
the goodeids inherited the ancestral Margotrema from, since no records of the helminth fauna are 
available for empethrychthyines, and no record of an allocreadiid like Margotrema has been 
established for other cyprinodontiforms.  
b) Cyprinidae-Margotrema. The ancestral association of Margotrema with the cyprinid C. ornata, 
as shown in this study, could have been established in hydrological systems of northern Mexico 
at 6.5 Ma (Figs. 1a, 2a). The implication of this scenario is that goodeines began the association 
with the ancestor of Margotrema in northern areas of Mexico, previous to the diversification, as a 
result of a host sharing (ecological host extension) event from other freshwater fish groups, such 
as cyprinids, with a subsequent specialization in goodeines, where the digenean developed a 
strong host specificity. We recently collected a few specimens of Margotrema in a species of 
cyprinid in three river basins of northern Mexico (Santa María River, Conchos River and 
Pagigóchic River, unpublished data) and clearly this may reflect the shadow of the ancestral 
distribution of extinct goodeids in northern hydrological systems, where cyprinids are common 
 169 
 
and very abundant (Fig. 4a). The same results of low prevalence and abundance values of 
Margotrema in cyprinids from Chihuahua (and even in Cyprinodon from Durango) may indicate 
the transfer of the ancestor between cyprinids and goodeids. Considering that phylogenetic 
hypothesis of allocreadiids place Margotrema as the sister taxa of Crepidostomum (a genera 
predominantly parasitic in centrarchids, but also found in other freshwater fish groups such as 
cyprinids, see Hoffman, 1999), it is likely that the origin of Margotrema is the result of a host 
sharing event from centrarchids to cyprinids, and from there to goodeines, or from centrarchids to 
goodeines. Once in goodeines, Margotrema experienced events such as cospeciation and several 
instances of host switching. Clearly, the diversification rate of the parasite was slower that that of 
their host, an idea originally proposed by Manter (1966). 
          It is noteworthy that distinct aquatic taxa currently distributed in central Mexico possessing 
a Nearctic biogeographical affinity, show an ancestral distribution pattern similar to that proposed 
in this study for the MRCA of Margotrema, including Cyprinidae (Chernoff & Miller 1986: 
Schönhuth et al., 2008: Pérez-Rodríguez et al., 2009); and crayfish of the subfamily 
Cambarellinae (Pedraza-Lara et al., 2012). Clearly, future collections of specimens of 
Margotrema in other host species across northern Mexico, and also survey work for helminths in 
Empetrychthynae in Southwestern USA will be instrumental in providing further support for one 
of the competing scenarios.  
Xenotaenia resolanae-Margotrema resolanae: an allopatric cospeciation model 
According to our results, the first cladogenetic event during the evolutionary history of 
Margotrema was the separation of M. resolanae from the ancestor of M. bravoae an event dated 
6.53 Ma. The restricted distribution range of both species seem to be the result of an allopatric 
speciation by peripheral isolates, where populations of both, hosts and parasites, were isolated at 
the edge of the distributional range of the MRCA, in the Cuzalapa River Basin, resulting in a 
strong host-specificity pattern of association illustrating a classical model of cospeciation 
reflecting reciprocal selection, i.e., coevolution. This hypothesis is supported by the divergence 
date of the MRCA of A. zonistius (6.9 Ma) and the posterior diversification process of X. 
resolanae, exclusive to the Purificación-Mascota River basin (between 5.6 to 5.1 Ma) (see 
Domínguez-Domínguez et al., 2010). Unfortunately, geological information of this region is 
 170 
 
scarce and only the volcanic activity of the Talpa-Mascota graben dated ca. 4.6 Ma has been 
documented (Carmichael et al., 1996; Bandy et al., 2001).  
Patterns of regional codivergence of Goodeinae-Margotrema bravoae across central Mexico 
Most Recent Common Ancestor of Margotrema bravoae  
The MRCA of M. bravoae, after the split from M. resolanae underwent phylogenetic 
codivergence through a dispersal process in areas such as Upper and Middle Mezquital River, 
Cotija and the Lower Balsas River (Fig. 4b) and subsequently, this ancestor experienced a 
secondary lineage loss in goodeines of the the Armería and Ayuquila Rivers. Interestingly, the 
pattern of regional codivergence seems to be closely tied to the evolutionary history of Goodeinae 
regarding the formation of what currently represents each tribe of the subfamily, i.e., 
Chapalichthyini, Characodontini, Girardinichthyni and Ilyodontini (Domínguez-Domínguez et 
al., 2010). 
          The historical biogeography of the Goodeinae, as described by Domínguez-Domínguez et 
al., (2006, 2010), was instrumental to explain the diversification process of the parasite fauna in 
this complex area. For instance, the erosion of the river tributaries from the Pacific and Atlantic 
slopes (i.e., Balsas, Ameca, and Pánuco River Basins) promoted the capture of water bodies of 
the Central Altiplano, with the subsequent dispersal of species that were characteristic of that 
region. Apparently, the Tamazula fault and the Sayula graben (dated 5 – 4.2 Ma), are two of the 
main causes that promoted the diversification of the MRCA´s of the each Tribe of goodeines by a 
series of vicariance and dispersal events represented by isolation processess, and connection-
disconnection of river basins with ancestral paleolakes such as Cuitzeo-Aztlán (dated 6 – 3.2 Ma) 
(Smith et al., 1975; Rosas-Elguera et al., 1996; Ferrari & Rosas-Elguera, 1999; Domínguez-
Domínguez et al., 2006, 2010). In this context, the differentiation process of each of the three 
lineages of M. bravoae resulted from geological events that changed the geographical 
configuration of the area and, apparently, with a posterior diversification of their hosts. Next, we 
describe the hypothetical scenarios that explain the evolutionary history of the three M. bravoae 
lineages. 
Ilyodontini-Margotrema bravoae Lineage I 
 171 
 
The differentiation process of the MRCA of M. bravoae Lineage I was dated 3.2 Ma. A 
geographical barrier caused the split the ancestral area of the MRCA of M. bravoae (Upper and 
Middle Mezquital River, Cotija and Lower Balsas River), and what currently represents Lineage I 
was isolated in the Lower Balsas River. The origin of M. bravoae Lineage I is apparently 
associated with the isolation and posterior diversification of the MRCA of Allodontichthys (dated 
3.6 to 2.9 Ma) in the Ameca, Ayuquila-Armería, and Coahuayana-Tamazula River Basins (see 
Domínguez-Domínguez et al., 2010). The entire tribe Ilyodontini diversified in these river basins, 
and Lineage I of M. bravoae codiversified through a horizontal transmission pattern (see Rannala 
& Michalakis, 2003) into other illiodontins, in addition to a member of the Chapalichthyini 
inhabitant of the same river drainages. According with Domínguez-Domínguez et al. (2010) the 
MRCA of Allodontichthys and Ilyodon (dated 5.6 Ma), dispersed from the Ayuquila-Armería 
river into several hydrological systems in central Mexico such as Ameca, Balsas, Coahuayana-
Tamazula, Armería-Ayuquila and Purification-Mascota river basins.  Previous published records 
of Margotrema (see Mejía-Madrid et al., 2005) in ilyodontins in the Coahuayana River Basin (in 
Allodonthichthys hubbsi in El Tule, Jalisco, and A. tamazulae in Río Tamazula, Jalisco, are 
congruent with the hypotheses of area expansion of M. bravoae Lineage I related with the  
diversification process of the Tribe Ilyodontini. Similarly, these records also support the ancestral 
connection between the Armería-Ayuquila and Coahuayana hydrological systems where the 
MRCA of the Ilyodontini was distributed (Webb, 2002; Domínguez-Domínguez et al., 2010).  
 The evolutionary history and divergence date of M. bravoae Lineage I (3.2 Ma), is 
congruent with the hypothesis of the origin of the diversification of the genus Allodontichthys 
(3.6 – 2.9 Ma) influenced by vicariance and dispersal events (Domínguez-Domínguez et al., 
2010) associated with geological events that shaped the biogeographical history of several 
freshwater fish taxa, i.e., the uprising of the Sierras de Manantlán and Cacoma, the volcanic 
activity of the Talpa-Mascota graben (dated 3.6 Ma), and the reactivation of the Colima and 
Tamazula graben in the Pliocene  (Allan, 1986; Carmichael et al., 1996; Garduño-Monroy et al., 
1998; Mateos et al., 2002; Pérez-Rodríguez et al., 2009; Domínguez-Domínguez et al., 2010). 
Girardinichthyini / Chapalichthyini-Margotrema bravoae Lineage II: a pleistocenic model? 
The genealogical differentiation of the MRCA of M. bravoae Lineages II and III that occurred 
between 3.2 and 1.03 Ma presumably in the Transmexican Volcanic Belt, particularly in the 
 172 
 
Lower Lerma River and Cotija (Fig. 4c), is related with the patterns of dispersal and isolation of 
the MRCAs of the goodeids Zoogoneticus quitzeoensis and Allotoca zacapuensis in Cuitzeo and 
Zacapu Lakes dated at 3.3 – 2.8 Ma, and the divergence date and expansion process of Z. 
purhepechus into the river basins of the Lower Lerma and the Ameca Rivers as well as Chapala 
Lake (2.8 Ma and 2 – 1.9 Ma, respectively) (Domínguez-Domínguez et al., 2006, 2007c, 2008, 
2010). 
 The evolutionary history of Lineage II occurred between 1 and 0.0167 Ma (Appendix S5), 
which corresponds with events that took place during the Pleistocene, and because of that, a DEC 
model was specifically conducted to describe the separation events for this lineage. (Appendix 
S3).  The results of the DEC model, support the idea of the dispersion of M. bravoae Lineage II 
during Pleistocene across hydrological systems of the Lower Lerma River, the Cuitzeo Lake and 
the Zirahuén Lake, and apparently the dispersion and vicariant events occurred in concordance 
with the diversification processes of their hosts. Two area relationships are recovered from this 
model, the first one between the Zacapu, Pátzcuaro and Zirahuén Lakes which further support the 
idea of ancestral connections between these water bodies (see Domínguez-Domínguez et al., 
2006, 2010) (Fig. 4e), and that of Cuitzeo Lake and the Lower Lerma River which explains the 
ancestral connection of this river basin.  These area relationships are also supported by the current 
distribution patterns of several freshwater fish taxa, an idea originally proposed by Alvarez del 
Villar (1972) and more recently by particular phylogenetic and biogeographical analyses 
(Domínguez-Domínguez et al., 2007a; 2010; Pérez-Rodríguez et al., 2009).  
Characodon audax-Margotrema bravoae Lineage III 
Our results indicate that the MCRA of M. bravoae Lineages II and III was associated with the 
ancestor of the Characodontini in the Upper and Middle Mezquital Rivers, Cotija and Lower 
Lerma River, an event dated between 3.2 and 1.03 Ma. The posterior isolation caused the 
codiversification of Lineage III with Ch. audax. The presence the ancestor of the Characodontini 
in Cotija and the Lower Lerma River is incongruent with the distribution patterns established for 
the genus Characodon, which occupies a basal position in the phylogeny of the Goodeinae 
(Domínguez-Domínguez et al., 2010). Even tough, the phylogenetic history of goodeines shows 
that the vicariant event that caused the allopatric speciation of Ch. audax and Ch. lateralis dated 
1.8 Ma was the formation of the Salto waterfall (Domínguez-Domínguez et al., 2006, 2010) (Fig. 
 173 
 
4d), however, no records of Margotrema spp. have been established for C. lateralis, even though 
several surveys have been conducted in the area (Mejía-Madrid et al., 2005; Martínez-Aquino et 
al., 2007; Pérez-Ponce de León et al., 2009). Apparently, the codiverence process detected in this 
study, related with the association of Ch. audax and M. bravoae Lineage III (exclusive to the 
Upper and Middle Mezquital River) can be explained by an extinction event of non-viable 
ancestral populations of the Lineage III in the Lower Mezquital River, following the event of 
cladogenesis in the host caused by the Salto waterfall.  
 The results of this study show that the diversification process of the genus Margotrema is 
the result of a combination of geography and host specificity at three distinct levels: a) Species-
Species (cospeciation), b) Species-Lineage (Codivergence Type I); c) Tribe-Lineage 
(Codivergence Type II) (Fig. 3). In this context, the allopatric cospeciation process proposed 
between X. resolanae-M. resolanae is a classic model of cospeciation of type one by one (Ehrlich 
and Raven, 1969). On the other hand, the cophylogenetic process we uncovered between 
Goodeinae and Margotrema bravoae (Lineages I, II and III), support Manter´s parasitological 
rule in that "the parasites evolve more slowly than their hosts" (Brooks, 1979). As a result, a 
general pattern we discovered is that parasites are relatively younger than their hosts, i.e., 
divergence times do not coincide for parasites and their hosts.  For example, divergence date of 
C. audax is dated 1.5 Ma, meanwhile for M. bravoae Lineage III it was estimated in 1.03 Ma. 
Nevertheless, the coevolutionary scenary follows a geographical mosaic in which the populations 
differ in their characteristics and specializations with respect to the species with which they 
interact (see Thompson, 2005). Therefore, the patterns of codivergence uncovered for the 
Goodeinae-M. bravoae association occur at three aforementioned levels, and are thus congruent 
with the geographical mosaic theory. 
CONCLUSION 
This study provides empirical evidence that demonstrates that the historical biogeography and 
evolutionary history of the digenean Margotrema spp. across central Mexico mirrors that of their 
goodein freshwater fish hosts. Evidence of coespeciation and a series of vicariant and dispersal 
events were found as the main causes that explain the codivergence patterns, first between 
Margotrema resolanae and Xenotaenia resolanae, second between Margotrema bravoae 
Lineages I, II (codivergence type I at goodein tribe level), and finally, Lineage III (codivergence 
 174 
 
type II at goodein species level). These results clearly show a cophylogenetic pattern for this 
host-parasite association, even though these taxa show independent evolutionary histories.  
Divergence times for each host and parasite lineage are relatively congruent and demonstrate the 
concordance of the evolutionary and biogeographical history between the two taxa, both in time 
and space. In this context, the geographical scenario molded by the complex geological and 
climatic history of the region, is the most important determinant that drives the evolution of the 
digenean, followed by the cophylogenetic association that this parasite established with their 
goodein hosts. 
AKNOWLEDGEMENTS 
We thank C. Pedraza-Lara for facility the information of phylogenetic analysis and molecular 
evolution of Goodeinae; J. Rozas, A. Sánchez-Gracia and R. Pérez-Rodríguez for earlier 
discussions of this manuscript. B. Mendoza for processing some of the specimens, and L. García 
for providing specific scientific literature. A.M.A. and F.S.C. special thanks to Swiss Systematics 
Society to permit take the course Model-based methods in Biogeography given by Dr. Isabel 
Sanmartin, celebrity during the 5. Scientific meeting of the Swiss Systematics Society. A.M.A. 
was supported by a scholarship from the Consejo Nacional de Ciencia y Tecnología 
(CONACyT). This paper fulfills the requirements of A.M.A. to obtain his Ph.D. degree within 
Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México. This study was 
supported by grants from the Consejo Nacional de Ciencia y Tecnología (CONACyT 83043), and 
Programa de Apoyo a Proyectos de Investigación e Innovación Tecnologíca (PAPIIT-UNAM IN 
202111) to G.P.P.L. 
REFERENCES 
Aguilar-Aguilar, R., Rosas-Valdez, R., Martínez-Aquino, A., Pérez-Rodríguez, R., Domínguez-
Domínguez, O. & Pérez-Ponce de León, G. (2010) Helminth fauna of two cyprinid fish 
(Campostoma ornatum and Codoma ornata) from the upper Piaxtla River, Northwestern 
Mexico. Helminthologia, 47, 251–256. 
Albitron, C.C. (1958) Quaternary stratigraphy of the Guadiana valley, Durango, Mexico. 
Geological Society of America Bulletin, 69, 197–216. 
 175 
 
Aldous, D.J. (2001) Stochastic models and descriptive statistics for phylogenetic trees, from Yule 
to today. Statistatistical Science, 16, 23–34. 
Allan, J.F. (1986) Geology of the northern Colima and Zacoalco grabens, southwest Mexico: 
Late Cenozoic rifting in the Mexican volcanic belt. Geologicall Society American 
Bulletin, 97, 473–485. 
Bandy, W.L., Urrutia-Fucugauchi, J., McDowell, F.W. & Morton-Bermea, O. (2001) K-Ar ages 
of four mafic lavas from the Central Jalisco Volcanic Lineament: supporting evidence for 
a NW migration of volcanism within the Jalisco block, western Mexico. Geofisica 
Internacional, 40, 259–269. 
Blair, D. (2006) Ribosomal DNA variation in parasitic flatworms. In (A. Maule, Ed.) Parasitic 
Flatworms: Molecular Biology, Biochemistry, Immunology and Control CABI. pages 96-
123. 
Brooks, D.R. (1979) Testing the context and extent of host-parasite coevolution. Systematic 
Zoology, 28, 299–307. 
Canning, E.U. & Madhavi, R. (1977) Studies on two new species of Microsporida hyperparasitic 
in adult Allocreadium fasciatusi (Trematoda, Allocreadiidae). Parasitology, 75, 293–300. 
Carmichael, I.S.E., Lange, R.A., & Luhr, J.F. (1996) Quaternary minettes and associated volcanic 
rocks of Mascota, western Mexico: a consequence of plate extension above a subduction 
modified mantle wedge. Contribution to Mineralogy and Petrology, 124, 302–333. 
Ceccarelli, F.S. & Zaldívar-Riverón, A. (2013) Broad polyphyly and historical biogeography of 
the Neotropical wasp genus Notiospathius (Braconidae, Doryctinae). Molecular 
Phylogenetics and Evolution.  
Charleston M.A. (1998) Jungles: a new solution to the host/parasite phylogeny reconciliation 
problema. Mathematical Biosciences, 149, 191–223. 
Charleston, M.A. (2011) TreeMap 3b. URL http://sites.google.com/site/cophylogeny 
 176 
 
Chernoff, B. & Miller, R.R. (1986) Fishes of the Notropis calientis complex, whit a key to the 
southern shiners of Mexico. COPEIA, 1, 170–183. 
Conow, C., Fielder, D., Ovadia, Y. & Libeskind-Hadas, R. (2010) Jane: a new tool for the 
cophylogeny reconstruction problem. Algorithms for Molecular Biology 5, 16. 
Cowman, P.F. & Bellwood, D.R. (2013) The historical biogeography of coral reef fishes: global 
patterns of origination and dispersal. Journal of Biogeography, 40, 209–224. 
Criscione, Ch.D. & Blouin, M.S. (2004) Life cycles shape parasite evolution: comparative 
population genetic of salmon trematodes. Evolution, 58, 198-202. 
Curran S.S., Tkach, V.V., & Overstreet, R.M. (2011) Phylogenetic affinities of Auriculostoma 
(Digenea: Allocreadiidae), with descriptions of two new species from Peru. Journal of 
Parasitology, 97, 661-670. 
De Alba, E. & Reyes, M.E. (1998) El contexto físico. La diversidad biológica de México: Estudio 
de país, 1998. (Ed. by CONABIO), pp. 4–22. Comisión Nacional para el Conocimiento y 
uso de la Biodiversidad, México. 
De Cserna, Z., & Álvarez, R. (1995) Quaternary drainage development in Central Mexico and the 
threat of and environmental disaster: A geological appraisal. Environmental & 
Engineering Geosciences, 1, 29–34. 
Domínguez-Domínguez, O., Doadrio, I., & Pérez-Ponce de León, G. (2006) Historical 
biogeography of some river basins in central Mexico evidenced by their goodeine 
freshwater fishes: apreliminary hypothesis using secondary Brooks parsimony analysis. 
Journal of Biogeography, 33, 1437–1447. 
Domínguez-Domínguez, O., Pompa-Domínguez, A. & Doadrio, I. (2007a) A new species of the 
genus Yuriria Jordan & Evermann, 1896 (Actinopterygii, Cyprinidae) from the Ameca 
basin of the Central Mexican Plateau. Graellsia, 63, 259–271. 
Domínguez-Domínguez, O., Boto, L., Alda, F., Pérez-Ponce de León., G. & Doadrio, I. (2007c) 
Human impacts on drainages of the Mesa Central of Mexico, and its genetic effects on an 
endangered fish, Zoogoneticus quitzeoensis. Conservation Biology, 21, 168–180. 
 177 
 
Domínguez-Domínguez, O., Alda, F., Pérez-Ponce de León, G., García-Garitagoitia, J.L. & 
Doadrio, I. (2008) Evolutionary history of the endangered fish Zoogoneticus quitzeoensis 
(Bean, 1898) (Cyprinodontiformes: Goodeidae) using a sequential approach to 
phylogeography based on mitochondrial and nuclear DNA data. BMC Evolutionary 
Biology, 8, 161. 
Domínguez-Domínguez, O., Pedraza-Lara, C., Gurrola-Sánchez, N., Pérez-Rodríguez, R., Israde-
Alcántara, I., Garduño-Monroy, V.H., Doadrio, I., Pérez-Ponce de León, G., & Brooks, 
D.R. (2010) Historical biogeography of the Goodeinae (Cyprinodontiforms). In: Uribe-
Aranzabal, M.C. & Grier, H. (Eds). Viviparous Fishes II, New Life Publications, 
Homestead, Florida, 33-74.  
Drummond, A.J., Ho, S.Y.W., Phillips, M.J. & Rambaut, A. (2006) Relaxed phylogenetics and 
dating with confidence. PLoS Biology, 4, 699–710. 
Drummond, A.J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, 
J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T. & 
Wilson, A. (2010) Geneious v5.0.4 Available from http://www.geneious.com/ 
Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with 
BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973. 
Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling 
trees. BMC Evolutionary Biology, 7. 
Edwards, S.V. (2009) Is a new and general theory of molecular systematics emerging? Evolution, 
63–1, 1–19. 
Ehrlich, P.R. & Raven, P.H. (1964) Butterflies and Plants: a study in Coevolution. Evolution, 18, 
586–608.  
Esch, G.W., Kennedy, C.R., Bush, A.O., & Aho, J.M. (1988) Patterns in helminth communities 
in freshwater fish in Great Britain: alternative strategies for colonization. Parasitology, 
96, 519–532. 
 178 
 
Ferrari, L. (2004) Slab detachment control on volcanic pulse and mantle heterogeneity in Central 
Mexico. Geology, 32, 77–80. 
Ferrari, L. & Rosas-Eleguera, J. (1999) Late Miocene to Quaternary extension at the northern 
boundary of the Jalisco block, western Mexico: the Tepic-Zacoalco rift revised. 
Geological Society of America, Special Paper 334, 1–23.  
Ferrari, L., Lopez-Martinez, M., Aguirre-Diaz, G. & Carrasco-Nunez, G. (1999) Space-time 
patterns of Cenozoic arc volcanism in central Mexico: From the Sierra Madre Occidental 
to the Mexican Volcanic Belt. Geology, 27, 303–306. 
Ferrari, L., López-Martínez, M. & Rosas-Elguera, J. (2002) Ignimbrite flareup and deformation 
in the southern Sierra Madre Occidental, western Mexico–implications for the late 
subduction history of the Farallon Plate. Tectonics, 21, 10.1029/2001TC001302. 
Garduño-Monroy, A., Saucedo-Girón, R., Jiménez, Z., Gavilanes-Ruiz, J.C., Cortés-Cortés, A. & 
Uribe-Cifuentes, R.M. (1998) La falla Tamazula, límite suroriental del bloque de Jalisco y 
sus relaciones con el complejo volcánico de Colima. Revista Mexicana de Ciencias 
Geológicas, 15, 132–144. 
Gesundheit P., Macias-García C. 2003. Biogeografía cladísta de la familia Goodeidae 
(Cyprinodontiformes). En: Morrone, J. y J. Llorente (eds). Una perspectiva 
latinoamericana de la biogeografía. CONABIO, México D.F. 319–337.   
Heled, J. & Drummond, A.J. (2010) Bayesian inference of species trees from multilocus data. 
Molecular Biology and Evolution, 27, 570–80. 
Huidobro, L, Morrone J.J., Villalobos J.L. & Álvarez, F. (2006) Distributional patterns of 
freshwater taxa (fishes, crustaceans and plants) from the Mexican Transition Zone. 
Journal of Biogeography, 33, 731–741. 
Israde-Alcántara, I. & Garduño-Monroy, V.H. (1999) Lacustrine record in a volcanic intra-arc 
setting: the evolution of late Neogene Cuitzeo basin system (central-western Mexico, 
Michoacan). Palaeogeography, Palaeoclimatology, Palaeoecology, 151, 209–227. 
 179 
 
Luna-Vega, I. & Contreras-Medina, R. (2012) Contributions of Cladistic Biogeography to the 
Mexican Transition Zone. In: L. Stevens (Ed): Global Advances in Biogeography. ISBN: 
978-953-51-0454-4, InTech, Available from: http://www.intechopen.com/books/global-
advances-in-biogeography/contributions-ofcladistic-biogeography-to-the-mexican-
transition-zone 
Luna-Vega, I., Morrone, J.J. & Espinosa, D. (Eds) (2005) Biodiversidad de la Faja Volcánica 
Transmexicana. Las Prensas de Ciencias, Universidad Nacional Autónoma de México. 
pp. 514. 
Libeskind-Hadas, R. & Charleston, M.A. (2009) On the computational complexity of the 
reticulate cophylogeny reconstruction problema. Journal of Computational Biology, 16, 
105–117. 
Maddison, W.P. (1997) Gene trees in species trees. Systematic Biology, 46, 523–536. 
Madhavi, R. (1978) Life history of Allocreadium fasciatusi Kakaji, 1969 (Trematoda: 
Allocreadiidae) from the freshwater fish Aplocheilus melastigma McClelland. Journal of 
Helminthology, 52, 51–59. 
Manter, H.W. (1963) The zoogeographical affinities of trematodes of South American freshwater 
fishes. Systematic Zoology, 12, 45–70. 
Martínez-Aquino, A., Aguilar-Aguilar, R., Santa Anna del Conde Juárez, H.O. & Contreras-
Medina, R. (2007a) Empleo de herramientas panbiogeográficas para detectar áreas para 
conservar: un ejemplo con taxones dulceacuícolas. In: Luna I., Morrone, J.J., & Espinosa., 
D. (Eds). Biodiversidad de la Faja Volcánica Transmexicana. Las Prensas de Ciencias, 
Universidad Nacional Autónoma de México. Pp. 449–460. 
Martínez-Aquino, A., Salgado-Maldonado, G., Aguilar-Aguilar, R., Cabañas-Carranza, G., & 
Mendoza-Palmero, C.A. (2007b) Helminth parasite communities of Characodon audax 
and C. lateralis (Pisces: Goodeidae), endemic freshwater fishes from Durango, Mexico. 
The Southwestern Naturalist, 52, 125–130. 
 180 
 
Martínez-Aquino, A., Aguilar-Aguilar, R., Pérez-Rodríguez, R. & Pérez-Ponce de León, G. 
(2009) Helminth parasite of Xenotaenia resolanae (Osteichthyes: Cyprinodontiformes: 
Goodeidae) from the Cuzalapa hydrological system, Jalisco, México. Journal of 
Parasitology, 95, 1221–1223. 
Martínez-Aquino, A., Hernández-Mena, D., Pérez-Rodríguez, R., Aguilar-Aguilar, R. & Pérez-
Ponce de León, G. (2011) Endohelminth parasites of the freshwater fish Zoogoneticus 
purhepechus (Cyprinodontiformes: Goodeidae) from two springs in the Lower Lerma 
River, Mexico. Revista Mexicana de Biodiversidad, 82, 1132–1137. 
Martínez-Aquino, A., Pérez-Rodríguez, R., Hernández-Mena, D.I., Garrido-Olvera, L., Aguilar-
Aguilar, R. & Pérez-Ponce de León, G. (2012) Endohelminth parasites of seven goodein 
species (Cyprinodontiformes: Goodeidae) from Lake Zacapu, Michoacán, Central Mexico 
Plateau. Hidrobiológica, 22, 88–91. 
Martínez-Aquino, A., Ceccarelli, F.S., & Pérez-Ponce de León, G. (2013) Molecular phylogeny 
of the genus Margotrema (Digenea: Allocreadiidae), parasitic flatworms of goodeid 
freshwater fishes across central Mexico: species boundaries, host-specificity and 
geographical congruence. Zoological Journal of the Linnean Society, 168, 1–16.  
Mateos, M., Sanjur, O.I. & Vrijenhoek, R.C. (2002) Historical biogeography of the livebearing 
fish genus Poeciliopsis (Poeciliidae: Cyprinodontiformes). Evolution, 56, 972–984.  
Mejía-Madrid, H., Domínguez- Domínguez, O. & Pérez-Ponce de León, G. (2005) Adult 
endohelminth parasites of Goodeinae (Cyprinodontiformes: Goodeidae) from México 
with biogeographical considerations. Journal of Parasitology 89, 356–361. 
Mejía-Madrid, H., Vázquez-Domínguez, E., & Pérez-Ponce de León, G. (2007) Phylogeography 
and freshwater basins in central Mexico: recent history as revealedby the fish parasite 
Rhabdochona lichtenfelsi (Nematoda). Journal of Biogeography, 34, 787–801. 
Miller, R.R. & Smith, M.L. (1986) Origin and geography of the fishes of Central Mexico. In: 
Hocutt, C.H. & E.O. Wiley (Eds). The Zoogeography of North American Freshwater 
Fishes. John Wiley and Sons, Inc. New York. pp. 487–517. 
 181 
 
Minckley, W.L.D., Hendrickson, D.A. & Bond, C.E. (1986) Goegraphy of western North 
American Freshwater fishes: Description and relationships to intracontinental tectonism. 
In: Hocutt C.H. & E.O. Wiley (Eds). The Zoogoegraphy of North Amercian Freshawater 
Fishes. John Wiley y Sons, New York, 516–613 pp.   
Mizukoshi, A., Johnson, K.P. & Yoshizawa, K. (2012) Co-phylogeography and morphological 
evolution of sika deer lice (Damalinia sika) with their hosts (Cervus nippon). 
Parasitology, 139, 1614–1629. 
Morales-Hojas, R., Reis, M., Vieira, C.P. & Vieira, J. (2011) Resolving the phylogenetic 
relationships and evolutionary history of the Drosophila virilis group using multilocus 
data. Molecular Phylogenetics and Evolution, 60, 249–258. 
Morrone, J.J. (2010) Fundamental biogeographic patterns across the Mexican Transition Zone: an 
evolutionary approach. Ecography, 33, 355–361. 
Morrone, J.J. (2005) Hacia una síntesis biogeográfica de México. Revista Mexicana de 
Biodiversidad, 76, 207–252. 
Murty, A.S. (1975) Studies on Indian cercarie II. Allocreadioid cercarie. Journal of Parasitology, 
61, 418–420. 
Nieberding, C.M., Durette-Desset, M.-C, Vanderpoorten, A., Casanova, J.C., Ribas, A., 
Deffontaine, V., Feliu, C., Morand, S., Libois, R. & Michaux, J.R. (2008) Geography and 
host biogeography matter for understanding the phylogeography of a parasite. Molecular 
Phylogenetics and Evolution, 47, 538–554. 
Nylander, J.A.A., Olsson, U., Alström, P., & Sanmartín, I. (2008) Accounting for Phylogenetic 
Uncertainty in Biogeography: A Bayesian Approach to Dispersal-Vicariance Analysis of 
the Thrushes (Aves: Turdus). Systematic Biology, 57, 257–268. 
Page, R.D.M. (1994a) Maps between trees and cladistic analysis of historical associations among 
genes, organisms, and areas. Systematic Biology, 43, 58–77. 
Page, R.D.M. (2003) Tangled Trees: Phylogeny, Cospeciation, and Coevolution. Chicago: 
University of Chicago, Press. 378 p. 
 182 
 
Page, R.D.M. & Charleston, M.A. (1998) Trees within trees: phylogeny and historical 
associations. TREE, 13, 356–359. 
Parenti, L.R. (1981) A phylogenetic and biogeographic analysis of cyprinodontiform fishes 
(Teleostei: Atherinomorpha). Bulletin of the American Museum of Natural History, 168, 
340–557. 
Pedraza-Lara, C., Doadrio, I., Breinholt, J.W., & Crandall K.A. (2012) Phylogeny and 
evolutionary patterns in the dwarf crayfish subfamily (Decapoda: Cambarellinae). PLoS 
ONE, 7, (11): e48233. doi:10.1371/journal.pone.0048233 
Pérez-Ponce de León, G. & Choudhury, A. (2005) Biogeography of helminth parasites of 
freshwater fishes in Mexico: the research for patterns and processes. Journal of 
Biogeography, 32, 645–649. 
Pérez-Ponce de León, G., Mendoza-Garfias, B., Rosas-Valdez, R. & Choudhury, A. (2013) New 
host and locality records of freshwater fish helminth parasites in river basins north of the 
Transmexican Volcanic Belt: another look at biogeographical patterns. Revista Mexicana 
de Biodiversidad. 
Pérez-Ponce de León, G., García-Prieto, L. & Mendoza-Garfias, B. (2011) Describing parasite 
biodiversity: the case of the helminth fauna of wildlife vertebrates in Mexico. In: O. 
Grillo (Ed.), Changing Diversity in Changing Environment, ISBN: 978-953-307-796-3, 
InTech, Available from: http://www.intechopen.com/books/changing-diversity-in-
changing-environment/describing-parasitebiodiversity-the-case-of-the-helminth-fauna-of-
wildlife-vertebrates-in-mexico 
Pérez-Ponce de León, G., García-Prieto, L. & Mendoza-Garfias, B. (2007a) Trematode parasites 
(Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa, 1534, 1–247. 
Pérez-Ponce de León, G., Choudhury, A., Rosas-Valdez, R. & Mejía-Madrid, H. (2007b) 
Systematic position of Wallinia spp. and Margotrema spp. parasites of Middle-American 
and Neotropical freshwater fishes based on 28S ribosomal RNA gene. Systematic 
Parasitology, 68, 49–55. 
 183 
 
Pérez-Ponce de León, G., Rosas-Valdez, R., Mendoza-Garfias, B., Aguilar-Aguilar, R., Falcón-
Ordaz, J., Garrido-Olvera, L. & Pérez-Rodríguez, R. (2009) Survey of the endohelminth 
parasites of freshwater fishes in the upper Mezquital River Basin, Durango State, Mexico. 
Zootaxa, 2164, 1–20. 
Pérez-Rodríguez., R., Domínguez-Domínguez, O., Pérez-Ponce de León, G., & Doadrio, I. 
(2009) Phylogenetic relationships and biogeography of the genus Algansea Girard 
(Cypriniformes: Cyprinidae) of central Mexico inferred from molecular data. BMC 
Evolutionary Biology, 9, 223. 
Posada, D. (2008) jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution, 
25, 1253–1256. 
Poulin, R. (2007) Evolutionary ecology of parasites  (2nd ed.). Princeton University Press, 
342 p. 
Poulin, R., Blanar, Ch.A., Thieltges, D.W., & Marcogliese, D.J. (2012) Scaling up from 
epidemiology to biogeography: local infection patterns predict geographical distribution 
in fish parasites. Journal of Biogeography, 39, 1157–1166. 
Ramanjaneyulu, J.V. & Madhavi, R. (1984) Cytological investigations on two species of 
allocreadiid trematodes with special reference to the occurrence of triploidy and 
parthenogenesis in Allocreadium fasciatusi. International Journal of Parasitology, 14, 
309–316. 
Rannala, B. & Michalakis, Y. (2003) Populations genetics and cospeciation: from process to 
pattern. In: Page R.D.M. 2003. Tangled Trees: Phylogeny, Cospeciation, and 
Coevolution. The University of Chicago Press: Chicago y London, U.S.A. 120-143 pp. 
Ree, R.H. & Smith, S.A. (2008) Maximum likelihood inference of geographic range evolution by 
dispersal, local extinction, and cladogenesis. Systematic Biology, 57, 4–14 
Ree, R.H., Moore, B.R., Webb, C.O. & Donoghue, M.J. (2005) A likelihood framework for 
inferring the evolution of geographic range on phylogenetic trees. Evolution, 59, 2299–
2311. 
 184 
 
Ronquist, F. & Sanmartín, I. (2011) Phylogenetic methods in biogeography. Annual Review of 
Ecology, Evolution, and Systematics, 42, 441–464. 
Rosas-Elguera, J., Ferrari, L., Garduño-Monroy, V.H. & Urrutia-Fucugauchi, J. (1996) 
Continental boundaries of the Jalisco block and their influence in the Pliocene-Quaternary 
kinematics of western Mexico. Geology, 24, 921–924. 
Sanmartín, I. (2012) Historical Biogeography: Evolution in Time and Space. Evolution: 
Educationa and Outreach, 5, 555–568. 
Sanmartín, I., Van derMark, P. & Ronquist, F. (2008) Inferring dispersal: a Bayesian approach to 
phylogeny based island biogeography, with special reference to the Canary Islands. 
Journal of Biogeography, 35, 428–449. 
Schönhuth, S., Doadrio, I., Domínguez-Domínguez, O., Hillis, D.M., & Mayden, R.L. (2008) 
Molecular evolution of southern North American Cyprinidae (Actinopterygii), with the 
description of the new genus Tampichthys from central Mexico. Molecular Phylogenetics 
and Evolution, 47, 729–756. 
Silva-Romo, G., Martiny, B., Mendoza-Rosales, C., Nieto-Samaniego, A. & Alaniz-Álvarez, S. 
(2002) La Paleocuenca de Aztlán, Antecesora de la Cuenca de México. GEOS-Boletin 
Informativo de la Unión Geofísica Mexicana, 22, 75–76. 
Smith, M.L., Cavender, T.M. & Miller, R.R. (1975) Climatic and biogeographyc significance of 
fish fauna from the Late Pliocene-Early Pleistocene of the Lake Chapala Basin, Jalisco, 
Mexico. In: Smith G.R. & Friedland (Eds). Studies on Cenozoic paleontology and 
stratigraphy in honor of Claude W. Hibbard,Vol. 12. Pp 29-38. 
Thompson, J.N. (2005) The Geographic Mosaic of Coevolution. University of Chicago Press, 
Chicago. p. 443. 
Uyeno, T. & Miller, R.R. (1962) Summary of Late Cenozoic freshwater fish records for North 
America. Occasional papers of the Museum of Zoology University of Michigan. 36 p. 
Webb, S.A. (2002) Molecular systematics of the genus Allodontichthys (Cyprinodontiformes: 
Goodeidae). Reviews in Fish Biology and Fisheries, 12, 193–205. 
 185 
 
Willis, M.S. (2001) Population biology of Allocreadium lobatum Wallin, 1909 (Digenea: 
Allocreadiidae) in the Creek Chub, Semotilus atromaculatus, Mitchill (Osteichthyes: 
Cyprinadae), in a Nebraska Creek, USA. Memórias do Instuto Oswaldo Cruz, 96, 331-
338. 
Yu, Y., Harris, A.J. & He, X. (2010a) S-DIVA (Statistical Dispersal- Vicariance Analysis): a tool 
for inferring biogeographic histories. Molecular Phylogenetics and Evolution, 56, 848–
850. 
Yu, Y., Harris, A.J. & He, X. (2010b) S-DIVA (Statistical Dispersal-Vicariance Analysis), 
version 1.9 beta. Available at: http://mnh.scu.edu.cn/S-diva/ 
FIGURE LEGENDS 
Figure 1 Biogeographical events of the evolution of Margotrema spp. from Central 
Mexico associated to Goodeinae; (a) shows a general pattern of the evolution of M. resolanae 
and of each of the Lineages of M. bravoae; (b) shows the specific events that influenced the 
evolution of M. bravoae Lineage I; (c) shows the specific events that influenced the evolution of 
M. bravoae Lineage II.  
   Figure 2 Host-parasite events of the evolution of Margotrema spp. from Central 
Mexico associated to Goodeinae; (a) shows a general pattern of the evolution of M. resolanae 
and of each of the Lineages of M. bravoae; (b) shows the specific events that influenced the 
evolution of M. bravoae Lineage I; (c) shows the specific events that influenced the evolution of 
M. bravoae Lineage II. 
Figure 3 Tanglegram show the levels three of parasitic associations between Goodeinae-
Margotrema. Level 1 (L1-L1, green = Species-Species; represent with the association Xenotaenia 
resolanae-M. resolanae). Level 2 (L2-L2, red = Species-Lineage; represent with the association 
Characodon audax-M. bravoae Lineage III), Level 3 (L3-L3, blue = Tribe-Lineage; represent 
with the associations between Ilyodontini-M. bravoae Lineage I and Girardinichthyini / 
Chapalichthyini-M. bravoae Lineage II). Colours patterns in the curvigram of Goodeinae 
correspond to each tribe; i.e. blue = Girardinichthyini; green = Chapalichthyini; yellow = 
Ilyodontini; red = Characodontini. Colours patterns in the curvigram of Margotrema correspond 
 186 
 
to each independent evolutionary lineage; i.e. yellow = M. bravoae Lineage I; blue = M. bravoae 
Lineage II; red = M. bravoae Lineage III. The gray polygons under the curvigrams correspond to 
specific lineage of Goodeinae and M. bravoae, respectively. The capital letters correspond to the 
each locality where specimens of Margotrema were collected, for details see Appendix S1. 
Figure 4 Schematic description of the areas and dispersal routes of generating alternative 
biogeographic / cophylogenetic hypotheses using dispersal-extinction-model (DEC) analysis of 
Margotrema spp., in function an evolutionary time and hydrogeomorphology historical from 
Central Mexico and Goodeinae. (a) Ancestral area, green shadow, of Margotrema genus detected 
based on ours results. The red shadow represents an ancestral hypothetical area potential 
associate to north records from Mexico of Margotrema and the distribution area of fossil records 
of species of Goodeidae. (b) Fragmentation of the ancestral area of most recent common ancestral 
(MRCA) of Margotrema spp. represent by two green shadow. Diversification process of the 
MRCA of the tribe Ilyodontini and Margotrema, respectively, influence for events of vicariance-
dispersal on Cuzalapa River (I) and Armería Ayuquila River (H). (c) Geographic scenery of the 
diversification of M. bravoae Lineage I [L1] and M. bravoae Lineage II [L2] associate to 
Goodeinae tribes, based on hypothetical expansion routes. Yellow arrows due reference to 
dispersal of L1 influence by the dispersal of the Ilyodontini [I]; blue arrows due reference to 
dispersal of L2 influence by the dispersal of the Chapalichthyini [Ch] and Girardinichthyini [G]. 
(d) Geographic scenery of the diversification of M. bravoae Lineage III associate to a vicariant 
event (El Salto waterfall) that caused the diversification of Characodon audax. Red shadow 
covers the hypothetical area of the pleistocenic paleolakes. (e) Hypothetical area of the 
pleistocenic paleolakes when is distributed M. bravoae Lineage II; the orange, blue and green 
shadows correspond to phylogenetic relationships of areas. Polygons in intensity different of gray 
correspond to biogeographic provinces (sensu lato Morrone, 2005): SMOc = Sierra Madre 
Occidental; AM = Altiplano Mexicano; MTVB = Mexican Transvolcanic Belt; BRB = Balsas 
River Basin; hydrological systems in green and yellow correspond to the records of Margotrema 
collected and no collected in this study, respectively; filled circles green with a capital letter 
correspond to localities analysed in this study; filled circles red together with the number, 
indicate Margotrema records not collected in this study, for details see Appendix S1 and S6. 
 
 187 
 
SUPPORTING INFORMATION 
Additional Supporting Information may be found in the online version of this article: 
Appendix S1 Table with the areas and area codes, localities and locality codes and parasite 
species and terminal codes used in the RASP analyses (MCMC), Dispersal-Extinction-
Cladogenesis (DEC) analyses and divergence date of Margotrema spp. Also show each area, 
locality and terminal lineage associate to host species. 
Appendix S2 Supplementary tables and figures of DEC analyses, Modelo I, general geographic 
areas. 
Appendix S3 Supplementary tables and figures of DEC analyses, Modelo II: pleistocenic events. 
Appendix S4 Dispersal matrix used for Lagrange, Modelo III: cophylogenetical events.  
Appendix S5 Divergence date of Margotrema spp.  
Appendix S6. Additional Margotrema records in freshwater fish species from Mexico. 
BIOSKETCH  
Andrés Martínez-Aquino is interested in parasite evolutionary biology using molecular and 
distributional data analysis, with a particular focus on helminth parasite taxa of wildlife. 
Author contributions: All authors conceived and discussed the ideas. A.M-A. and F.S.C. 
performed the analyses. L.E.E., E.V-D. and F.S.C. contributed to data interpretation. A.M-A. and 
G.P-PL led the writing. All authors contributed to led the writing. 
 
 
 
 
 
 
 
 188 
 
Figure 1 
 
(a) 
7.0 6.0 5.0 4.0 
Biogeographic events 
• Vicariance 
4 Dispersal 
........ Dispersal 
~ + lineage 1055 
Areas (Sub-basins) 
A " Lower Conchos River 
B " Upper and Middle 
Mezquital River 
e " Lower Lerma River 
(e) 
Legend 
o " Zacapu lake 
E " Cuitzeo lake 
F " Pátzcuaro lake 
G " lirahuén Lake 
H " Annerla-Ayuquila Rivers 
I "Cuzalapa River 
J "Colija 
K " l ower Balsas River 
3.0 2.0 1.0 
(b) 
1.0 0.5 
M. resolanae 
Lineage I 
~ 
~ 
.Q 
lineage 11 E 
lineage 111 
0.0 Millions of years ago 
e 
(; 
e> :;: 
0.0 Millions of years ago 
~Ir---------'--------------------'--------------------, 
900 200 100 0.0 Thousands of years a90 
 189 
 
Figure 2 
 
(a) 
KD -: . ~ M. resolanae 
K2» m ---c 
~ ~ ~ Lineage I 
I_ h" ..!' 
L (b) • • o 
~ ~ 
> 
~ 
" ~ " .. r lineage 11 • E 
L .1: 
-'hX . .. 
o 
~ 
e> 
~ ..;;. ;;.: ~ 
~~ -- " (e) .. .. Lineage 111 
7.0 6.0 5.0 4.0 3.0 2 .0 1.0 0.0 Mill ions of years a90 
Legend 
(b) 
Host-Parasite events Hosts 
~ -~ Lineage codivergence 
Ityodontini ~ - ~~ (Xenofaenia resoJanae) 
~ - ." ~ Lineage duplica/ion Ilyodontin; 
~ h 
In one hos! 
(Le. Allodontichythys zonistius) ~~ X l ineage 1055 in hosl -Chapalichthyini ... 
~ - Hasl switch (i.e. Zoogonelicus purhepechus) 
~ ... ~ ., Characodontini .. 
Hasl switch (Le Characodon audax) 
+ lineage 1055 --
I ~ Cospeciation 
Girard inichthyini ,1 . " ~ 
..... 
vía hos! switch (Le AI/otoca diaZl) ...,-< ~ L.....- ~ + lineage 1055 -Cyprinidae j j j 
(Codoma oma/a) 1.0 0.5 0.0 Millions of years a90 
(e) ... ... 
~ ... . 11 ... - ...... 
~ - ~ ... ~ ... ~ 
~ 
... ... ... 
" ti) .1 .... 
" ... -- ..... ... ~ ... ... ... --- ~ .... ... ... 
,---11 j j j 
900 200 100 0.0 Thousands of years ago 
 190 
 
Figure 3 
 
 
 
 
 
 
 
 
 191 
 
Figure 4 
 
> 6.6 m.y.a. 
4 - 2 m.y.a. 
1- O m.y.a. 
G=' "'"O" :::::r= ~ G 
" 
Margolremo 
M. resolanae 
Fragmentatlon 01 ""ceslral 
a'ea 01 M RCA 01 Marg o l rema 
genus 
6.6 - 4 m.y.a. 
Diversiflcatkm 01 MRCII 
01 M. bruvoue U ne"ge 111 
(L3) assoclale lo a vlca,j .. " , 
speclaUon even l 0 1 
Characodon Re neos 
(Le. Ch. Gudox ) 
Goode in a" 
M argo/remo 
El Salto water/a ll 
6.9 Oi"e"ific<~t;;on 01 
M RCA 0 1 lIyodontinni 
Ion 0 1 
Ch. n udox 
, 
G 
" 
'"m,'e" .. " ~ ---.:= ~ ~ plesiloo:cn k 
paleolak.,. 
2 - O m.y.a. 
T 
Victoria 
oe OGG>o 
 192 
 
Appendix S1 Codes employed for the RASP analyses (MCMC) (not show results), Dispersal-
Extinction-Cladogenesis (DEC) analyses (akin Fig. 1), following Domínguez-Domínguez et al. 
(2006, 2010) hydrological systems (areas). Areas delimited based on the Mexican hydrological 
basins and sub-basins map produced by the Comisión Nacional para el Conocimiento y uso de la 
Biodiversidad (CONABIO, 1998; www.conabio.gob.mx). Also show species and lineages of 
Margotrema included found in each area, locality (and code) and host taxa following Martínez-
Aquino et al., 2013. The localities was used to test the divergence date of each lineage of 
Margotrema spp., at locality level (akin Appendix S5). 
Locality 
Locality 
code 
Tributary of Conchos River, Bocoyna, Chihuahua, México BOCO 
Spring in Abraham González, Durango, México AGON 
Spring in the Unidad de Manejo Ambiental de caza, Guadalupe Aguilera, Durango, México GUAG 
Puente en el poblado de Pino Suárez, carretera Durango-Mezquital, Durango, México PINO 
Spring El Toboso, Durango, México TOBO 
La Luz spring, Jacona de Plancarte, Michoacán, México LLUZ 
La Angostura, Zacapu Lake (balneario), Michoacán, México ZACA 
La Mintzita spring, Michoacán, México MINT 
Spring Chapultepec, Michoacán, México CHAP 
Opopeo Lake, Michoacán, México OPOP 
Stream in Ahuacapán, Jalisco, México AHUA 
Arroyo Durazno in Cuzalapa River, Jalisco, México CUZA 
Spring Rico, Michoacán, México RICO 
Spring in park of Tocumbo, Michoacán, México TOCU 
Spring in Tlapetlahuaya, Puebla, México TLAP 
 193 
 
River Chagres at the Frijolito River,  Panama   
Tobaco creek, Canada   
 
Continued appendix 1. 
Area (sub-basin) 
Area 
code  
Lower Conchos River  A 
Mezquital River Upper and Medium B (1) 
Mezquital River Upper and Medium B (2) 
Mezquital River Upper and Medium B (3) 
Mezquital River Upper and Medium B (4) 
Lower Lerma River C 
Zacapu Lake D 
Cuitzeo Lake E 
Pátzcuaro Lake F 
Zirahuén Lake G 
Armería-Ayuquila Rivers H 
Cuzalapa River I 
Cotija  J 
Lower Balsas River K 
Upper Balsas River L 
River Chagres   
Tobaco creek   
 194 
 
  Continued appendix 1. 
Parasite species  
Terminal 
Hosts taxa 
code 
Margotrema bravoae Lineage I IA Codoma ornata 
Margotrema bravoae Lineage III IIIB Characodon audax 
Margotrema bravoae Lineage III IIIB Characodon audax 
Margotrema bravoae Lineage III  IIIB Characodon audax 
Margotrema bravoae Lineage III IIIB Characodon audax 
Margotrema bravoae Lineage II IIC Zoogoneticus purhepechus 
Margotrema bravoae Lineage II IID 
Allotoca zacapuensis,  
Zoogoneticus quitzeoensis 
Margotrema bravoae Lineage II IIE 
Alloophorus robustus,  
Zoogoneticus quitzeoensis 
Margotrema bravoae Lineage II IIF 
Allotoca diazi,  
Allotoca duguesi 
Margotrema bravoae Lineage II IIG Allotoca meeki 
Margotrema bravoae Lineage I IH 
Allodontichthys zonistius, 
Ilyodon furcidens 
Margotrema resolanae M. resolanae Xenotaenia resolanae 
Margotrema bravoae Lineage II IIJ Neoophorus regalis 
Margotrema bravoae Lineage I IK 
Chapalichthys pardalis, 
Ilyodon furcidens 
Margotrema bravoae Lineage I IL Ilyodon whitei 
Walliniae chavarriae 
  
Gephyrocharax sp. 
  
Allocreadium lobatum 
  
Semotilus atromaculatus 
  
 
 
 195 
 
 
 
Appendix S2A Table with codes employed for the Dispersal-Extinction-Cladogenesis (DEC; 
Model I: 0-6.5 Ma), analyses following Domínguez-Domínguez et al. (2006, 2010) hydrological 
systems (areas). Areas delimited based on the Mexican hydrological basins and sub-basins map 
produced by the Comisión Nacional para el Conocimiento y uso de la Biodiversidad (CONABIO, 
1998; www.conabio.gob.mx). Each lineage of Margotrema included found in each area, locality 
and host species.  
Area (sub-basin) 
Code 
area 
Lineage Margotrema 
spp. by area Locality by area Host species by area 
Lower Conchos River  A 
Margotrema bravoae 
Lineage I 
Tributary of Conchos River, Bocoyna, 
Chihuahua, México Codoma ornata 
Mezquital River Upper 
and Medium B 
Margotrema bravoae 
Lineage III 
Spring in Abraham González, Durango, 
México Characodon audax 
Mezquital River Upper 
and Medium B 
Margotrema bravoae 
Lineage III 
Spring in the Unidad de Manejo Ambiental de 
caza, Guadalupe Aguilera, Durango, México Characodon audax 
Mezquital River Upper 
and Medium B 
Margotrema bravoae 
Lineage III 
Puente en el poblado de Pino Suárez, carretera 
Durango-Mezquital, Durango, México Characodon audax 
Mezquital River Upper 
and Medium B 
Margotrema bravoae 
Lineage III Spring El Toboso, Durango, México Characodon audax 
Lower and Medium 
Lerma and Central 
Lakes  C 
Margotrema bravoae 
Lineage II 
La Luz spring, Jacona de Plancarte, 
Michoacán, México 
Zoogoneticus 
purhepechus 
Lower and Medium 
Lerma and Central 
Lakes  C 
Margotrema bravoae 
Lineage II 
La Angostura, Zacapu Lake (balneario), 
Michoacán, México 
Allotoca zacapuensis, 
Zoogoneticus 
quitzeoensis 
Lower and Medium 
Lerma and Central 
Lakes  C 
Margotrema bravoae 
Lineage II La Mintzita spring, Michoacán, México 
Alloophorus robustus, 
Zoogoneticus 
quitzeoensis 
Lower and Medium 
Lerma and Central 
Lakes  C 
Margotrema bravoae 
Lineage II Spring Chapultepec, Michoacán, México 
Allotoca diazi, Allotoca 
duguesi 
Lower and Medium 
Lerma and Central 
Lakes  C 
Margotrema bravoae 
Lineage II Opopeo Lake, Michoacán, México Allotoca meeki 
Armería Ayuquila 
River D 
Margotrema bravoae 
Lineage I Stream in Ahuacapán, Jalisco, México 
Allodontichthys 
zonistius, Ilyodon 
furcidens 
Cuzalapa River E Margotrema resolanae 
Arroyo Durazno in Cuzalapa River, Jalisco, 
México Xenotaenia resolanae 
Cotija F 
Margotrema bravoae 
Lineage II Spring Rico, Michoacán, México Neoophorus regalis 
Lower Balsas River G 
Margotrema bravoae 
Lineage I 
Spring in park of Tocumbo, Michoacán, 
México 
Chapalichthys pardalis, 
Ilyodon furcidens 
Upper Balsas River H 
Margotrema bravoae 
Lineage I Spring in Tlapetlahuaya, Michoacán, México Ilyodon whitei 
 196 
 
Appendix 2SB Figure of the hydrological systems (areas) and collection sites for Margotrema 
spp. in Mexico. The capital letters correspond to each hydrological system for each locality 
(black point) where specimens of Margotrema spp. were collected from (for details see Table of 
Appendix S2A). 
 
 
 
 
 
-115 -105-110 -110 -95 -90
-30
-20
-15
-115 -105 -100 -95 -90
-30
-25
-20
-15
-25
-110
100 0 100Kilometers
D
E H
C
 B
 A
G
F
C C
C
C
N
2
 M
 197 
 
Appendix S2C Matrix used for Lagrange dispersal constrains for different time slices (Model I: 
0-6.5 Ma). 
 
Time: 0 – 2 Ma. 
 A B C D E F G H 
A - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
B 1  10-6 - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
C 1  10-6 1  10-6 - 1  10-6 0.5 1  10-6 1  10-6 1  10-6 
D 1  10-6 1  10-6 1  10-6 - 1  10-6 1  10-6 1  10-6 1  10-6 
E 1  10-6 1  10-6 1  10-6 1  10-6 - 1  10-6 1  10-6 1  10-6 
F 1  10-6 1  10-6 0.5 1  10-6 1  10-6 - 0.95 0.5 
G 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 0.95 - 1 
H 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 0.5 1 - 
 
Time: 2 – 4 Ma. 
 A B C D E F G H 
A - 0.1 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
B 1  10-6 - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
C 0.1  1  10-6 -0. 0.1 1  10-6 1  0.1  0.1 
D 1  10-6 1  10-6 0.5 - 0.5 0.95 1 0.95 
E 1  10-6 1  10-6 0.4 0.5 - 0.4 0.5 0.4 
F 1  10-6 1  10-6 1 0.5 0.5 - 0.6 0.6 
G 1  10-6 1  10-6 0.5 0.5 1  10-6 0.6 - 0.95 
H 1  10-6 1  10-6 0.1 0.3 1  10-6 0.5 0.95 - 
 
Time: 6.5 – 4 Ma. 
 A B C D E F G H 
A - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
B 1  10-6 - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
C 1  10-6 1  10-6 - 1  10-6 1  10-6 1  1  10-6 1  10-6 
D 1  10-6 1  10-6 0.9 - 1 0.9 0.95 0.9 
E 1  10-6 1  10-6 1  10-6 0.5 - 1  10-6 1  10-6 1  10-6 
F 1  10-6 1  10-6 1 1  10-6 1  10-6 - 1  10-6 1  10-6 
G 1  10-6 1  10-6 1  10-6 0.3 1  10-6 1  10-6 - 1 
H 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1 - 
 
 
 198 
 
Appendix S3A Table with codes employed for the Dispersal-Extinction-Cladogenesis (DEC; 
Model I: 0-1 Ma), analyses following Domínguez-Domínguez et al. (2006, 2010) hydrological 
systems (areas). Areas delimited based on the Mexican hydrological basins and sub-basins map 
produced by the Comisión Nacional para el Conocimiento y uso de la Biodiversidad (CONABIO, 
1998; www.conabio.gob.mx). Appendix also shows locality and host taxa associated to each area 
where Margotrema bravoae Lineage III is distributed. 
 
Area (subasin) Code area Locality Hosts 
Lower Lerma C 
La Luz spring, Jacona de Plancarte, Michoacán, 
México Zoogoneticus purhepechus 
Zacapu Lake D 
La Angostura, Zacapu Lake (balneario), 
Michoacán, México 
Allotoca zacapuensis,  
Zoogoneticus quitzeoensis 
Cuitzeo Lake E La Mintzita spring, Michoacán, México 
Alloophorus robustus,  
Zoogoneticus quitzeoensis 
Pátzcuaro Lake F Spring Chapultepec, Michoacán, México 
Allotoca diazi,  
Allotoca duguesi 
Zirahuén Lake G Opopeo Lake, Michoacán, México Allotoca meeki 
Cotija J Cotija, Michoacán, México Neoophorus regalis 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 199 
 
Appendix S3B Figure of the hydrological systems (areas) for Margotrema bravoae Lineage III 
from Central Mexico. The capital letters correspond to each water body of the locality where 
specimens of Margotrema spp. were collected from (for more details Appendix S3A). 
 
 
J
C
D
G
E
F
C
N
 200 
 
Appendix S3C Matrix used in Lagrange dispersal constrains for different time slices (mirrow 
matrix) (Model II: 0-1 Ma). 
 
Time: Plio-Pleistocen (> 1 Ma) 
 C D E F G J 
C - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
D  - 0.85 0.85 0.85 1  10-6 
E   - 0.85 0.85 1  10-6 
F     - 0.9 1  10-6 
G     - 1  10-6 
J      - 
 
Time: 0 m.y.a 
 C D E F G J 
C - 1 1  1  1  1  
D  - 1 1 1 1  
E   - 1 1 1  
F     - 1 1  
G     - 1  
J      - 
 
 
 
 
 
 
 
 
 
 
 
 
 201 
 
Appendix S4A Table with codes employed for the Dispersal-Extinction-Cladogenesis (DEC) 
using the host species as areas and divergences timing, in million years ago (Ma) based on 
Domínguez- Domínguez et al., 2010, used in the dispersal matrix for cophylogenetical analysis 
Lagrange, of the most recent common ancestral (MRCA) of genus / species of hosts of 
Margotrema spp. 
Host species (Areas) Code areas Age of MRCA of genus / species 
Allotoca diazi A 7.5 / < 1 
Allotoca duguesi B 7.5 / 3.9 
Allotoca meeki C 7.5 / < 1 
Neoophorus regalis D 6.9 / < 1 
Alloophorus robustus E 4 / 2.8 
Allotoca zacapuensis F 7.5 / 3.9 
Allodontichthys zonistius G 6.9 / 3.6 
Codoma ornata H ? 
Characodon audax I 15.5 / 1.8 
Chapalichthys pardalis J 4 / ? 
Ilyodon furcidens K 5.1 / ? 
Ilyodon whitei L 5.1 / ? 
Xenotaenia resolanae M 6.9 / 5.6 
Zoogoneticus quitzeoensis N 6.9 / 3.9 
Zoogoneticus purhepechus O 6.8 / 2.8 
 
 
 
 
 
 
 
 
 
 
 
 202 
 
Appendix S4B Matrix used for Lagrange dispersal constrains for different time slices (mirrow matrix) (cophylogenetic model). 
Time: 0 – 2 Ma. 
 a B c d e F g h i j k l m n 0 
a - 1  1  1 1  1  1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  1 
b  - 1  1 1  1  1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1 1 
c   - 1 1 1  1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1 1 
d    - 1 1  1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1 1 
e     - 1  1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1 1 
f      - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1 1 
g       - 1  10-6 1  10-6 1 1 1 1  10-6 1  10-6 1  10-6 
h        - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
i         - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
j          - 1 1 1  10-6 1  10-6 1  10-6 
k           - 1 1  10-6 1  10-6 1  10-6 
l            - 1  10-6 1  10-6 1  10-6 
m             - 1  10-6 1  10-6 
n              - 1 
o               - 
 
Time: 2 – 4 Ma. 
 a b c d e F g h i j k l m n O 
a - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
b  - 1  10-6 0.5 1  1  1 1  10-6 1  10-6 0.5 1  10-6 1  10-6 1  10-6 1 1 
c   - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
d    - 0.5 0.5 0.5 1  10-6 1  10-6 0.25 1  10-6 1  10-6 1  10-6 0.5 0.5 
e     - 1  1 1  10-6 1  10-6 0.5 1  10-6 1  10-6 1  10-6 1 1 
f      - 1 1  10-6 1  10-6 0.5 1  10-6 1  10-6 1  10-6 1 1 
g       - 1  10-6 1  10-6 0.5 1 1 0.1 1 1 
h        - 0.1 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
i         - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
j          - 1  10-6 1  10-6 1  10-6 0.5 0.5 
k           - 1 1  10-6 1  10-6 1  10-6 
l            - 1  10-6 1  10-6 1  10-6 
m             - 1  10-6 1  10-6 
n              - 1 
o               - 
 203 
 
 
Time: 6.6 – 4 Ma. 
 a B c d e F g h i j k l m n O 
a - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
b  - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
c   - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
d    - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
e     - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
f      - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
g       - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1 1  10-6 1  10-6 
h        - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
i         - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
j          - 1  10-6 1  10-6 1  10-6 1  10-6 1  10-6 
k           - 1  10-6 1  10-6 1  10-6 1  10-6 
l            - 1  10-6 1  10-6 1  10-6 
m             - 1  10-6 1  10-6 
n              - 1  10-6 
o               - 
 
 
 
 
 
 
 
 
 204 
 
Appendix S5 Ultrametric tree resulting from the dating analysis of Margotrema spp. Mean ages are indicated in each node, the 
terminal codes are (localities) as in Appendix 1. 
 
 
 
IIIB
IIF
0.0167
IID
0.0503
IIG
0.1324
IIE
0.07150.1789
IIC
IIJ
1.0355
0.1881
IL
IK
0.9015
IA
0.3892
IH
Margotrema resolanae
3.2032
6.5353
0.7
0.01.02.03.04.05.06.07.0
Lineage III
Lineage II
Lineage I
M
a
rg
o
tr
e
m
a
 b
ra
v
o
a
e
 205 
 
Appendix S6 Additional records of Margotrema in freshwater fish species from Mexico. The 
locality number (LN) corresponds in the Figure 4. For more details see text in the manuscript. * = 
Unpublished data. 
 
LN  Host species  Locality  Georreferences 
1 Cyprinella lutrensis Buenaventura, Chihuahua 29° 50' 16.94'' N; 107° 28' 24.86'' 
W 
2* Cyprinidae Conchos River, Chihuahua Unpublished data 
3* Cyprinidae Pagigochic River, Chihuahua Unpublished data 
4 Cyprinodon nazas Río Guatimape in the Sofía town, Durango 24° 54‟ 41.1‟‟N; 104° 32‟ 7.4‟‟W 
5 Codoma ornata Río Piaxtla, Municipio de San Dimas, 
Durango 
24°21'59'' N; 105°31‟7.8‟‟ W 
6 Allodontichthys hubbsi El Tule, Jalisco 19° 19' 34.2'' N; 103° 22' 15'' W 
7 Allodontichthys tamazulae Río Tamazula, Jalisco 19° 43' 22.7'' N; 103° 12' 08.5'' W 
8 Goodea atripinnis Verde River, Jalisco 21º 49'' 12.0'' N; 101º 46' 21.3'' W 
9 Allotoca maculata Río San Marcos, Jalisco 20° 46' 35.7'' N; 104° 09' 52.6'' W 
10 Ilyodon furcidens Río Potrero Grande, Jalisco 19° 43' 22.7'' N; 103° 12' 08.5'' W 
11 Neoophorus regalis Los Reyes, Michoacán 19° 33' 43.5'' N; 102° 27' 39'' W 
12 Goodea atripinnis Ignacio Allende, Guanajuato 20° 55' N; 100° 50' W 
13 Ilyodon cortesae Manantial Cutzaróndiro, Michoacán 19° 10' 59'' N; 101° 30' 13'' W 
14 Girardinichthys 
multiradiatus 
Canal el Porvenir, Michoacán 19° 40' 29'' N; 100° 38' 25'' W 
15 Girardinichthys 
multiradiatus 
Villa Victoria, Estado de México 19° 27' 30'' N; 99° 59' 39'' W 
16 Girardinichthys 
multiradiatus 
Ciénega La Lagunilla, Estado de México 19° 08' 30'' N; 99° 30' 12'' W 
 
 
 
 
 
 
 
 
 
 
 206 
 
DISCUSIÓN GENERAL  
La asociación Goodeinae-Margotrema, representa un modelo biológico potencial para poner a 
prueba hipótesis acerca de la evolución de los helmintos parasitarios de peces dulceacuícolas de 
México, debido a que se distribuye sobre áreas geográficas restringidas y no puede dispersarse 
por fenómenos naturales a través de sistemas hidrológicos epicontinentales del centro de México, 
lo que impide el flujo génico entre huéspedes o sistemas hidrológicos (Martínez-Aquino et al., 
2013). Por tanto, es posible recuperar una estructura genealógica de los organismos parásitos 
capaz de reflejarse tanto sobre el escenario geográfico en el que se distribuyen como con la 
historia evolutiva de sus huéspedes. En este contexto, el presente estudio tuvo como objetivo 
general detectar los patrones biogeográficos y cofilogenéticos que configuraron la asociación 
Goodeinae-Margotrema, grupos endémicos y con historia evolutiva estrechamente relacionada y 
ocurrida en sistemas hidrológicos del centro de México.   
Implicaciones taxonómicas y patrones filogenéticos 
Con base en los distintos análisis filogenéticos se detectó que la especie Margotrema 
guillerminae es sinónima de M. bravoae (Martínez-Aquino et al., 2013). Por tanto, M. bravoae 
representa una especie polimórfica en términos de ciertos rasgos morfológicos, tales como la 
distribución de los ciegos intestinales en relación a la posición de los testículos. A su vez, M. 
bravoae incluye tres linajes con evolución independiente, aparentemente asociados a sistemas 
hidrológicos y grupos particulares de huéspedes: a) Margotrema bravoae Linaje I, distribuido en 
los sistemas hidrológicos de los ríos Ayuquila, Balsas y Conchos, y asociado primordialmente a 
huéspedes de las tribus Ilyodontini. b) Margotrema bravoae Linaje II, distribuído en sistemas 
hidrológicos del río Lerma y asociado a huéspedes de las tribus Girardinichthyini y 
Chapalichthyini. c) Margotrema bravoae Linaje III, distribuido en sistemas hidrológicos del río 
Mezquital y asociado a un único huésped de la tribu Characodontini. 
Con base en caracteres morfológicos y moleculares, y como parte de los análisis de la 
reconstrucción filogenética de Margotrema, se determinó y describió una especie nueva para la 
ciencia, Margotrema resolanae Pérez-Ponce de León, Martínez-Aquino & Mendoza-Garfías, 
2013, asociada exclusivamente para Xenotaenia resolanae y microendémica para el río Cuzalapa, 
Jalisco (Pérez-Ponce de León et al., en prensa). Este reordenamiento taxonómico sin implicar un 
 207 
 
incremento en el numero de especies descritas para el género Margotrema, apoya la hipótesis de 
que la helmintofauna de peces dulceacuícolas de México esta cerca de ser completada (Pérez-
Ponce de León  Choudhury, 2010). Sin embargo, es importante resaltar que la delimitación de 
los linajes intraespecíficos de M. bravoae nos acerca a entender cómo ocurren los procesos de 
diversificación parasitaria en helmintos parásitos de peces dulceacuícolas de México. 
Patrones biogeográficos 
La siguiente hipótesis biogeográfica se puso a prueba: “si existe congruencia biogeográfica entre 
la historia genealógica de Margotrema y la historia hidrogeomorfológica del centro de México, 
entonces se puede reflejar con la historia biogeográfica de sus huéspedes”. De manera general, se 
observó que los patrones de distribución geográfica de Margotrema están asociados con las 
barreras biogeográficas que fragmentaron los sistemas hidrológicos del centro de México y que, a 
su vez, influenciaron también en el patrón de distribución de sus huéspedes a través de eventos de 
vicarianza. Por otra parte, el proceso de dispersión causado por sus huéspedes goodeinos juega un 
papel relevante en la estructura biogeográfica de Margotrema, debido a la vagilidad que 
presentaron históricamente los MRCA de cada una de las tribus de Goodeinae, mismos que 
expandieron el área de distribución de Margotrema sobre los sistemas hidrológicos del centro de 
México. 
  Con base en los resultados del análisis de DEC, se observó que el área ancestral de 
Margotrema estuvo ubicada en sistemas hidrológicos del Norte de México y que presentó una 
conexión relativamente ancestral (6.6 millones de años -ma-) con los sistemas hidrológicos del 
centro de México. Este resultado es apoyado con base en el patrón de distribución ancestral 
inferido para otros peces dulceacuícolas (Barbour, 1973; Chernoff & Miller, 1986; Domínguez-
Domínguez et al., 2010). Al parecer, la expansión del área de distribución del MRCA de 
Margotrema, ocurrió debido a un evento de transmisión vertical (Rannala  Michalakis, 2003), de 
tipo Goodeinae-Margotrema. Esto indica que esta asociación ancestral ocurrió entre un huésped 
basal de la tribu Ilydontini, y su posterior expansión geográfica causada por eventos de 
vicarianza-dispersión, seguida de asociaciones cofilogenéticas sobre el centro de México. En este 
contexto, los patrones de diversificación de M. resolanae y cada uno de los tres linajes de M. 
bravoae pueden reflejarse en primera instancia en los procesos de fragmentación de los sistemas 
 208 
 
hidrológicos del Centro de México y, como resultado de ello, pueden reflejarse en los patrones de 
distribución y diversificación de sus huéspedes Goodeinos. 
  Los patrones de distribución geográfica de M. bravoae Linaje II, datados en < 1 ma, 
muestran una relación espacio-temporal con los grandes paleolagos que existieron en el centro de 
México durante el pleistoceno. Futuros estudios con análisis de tipo Isolation with migration 
model (Nielsen & Wakeley, 2001; Hey & Nielsen, 2007; Hey, 2010), usando distintas localidades 
de distribución de M. bravoae Linaje II, podrán poner a prueba posibles rutas de expansión 
poblacional contrastadas con los de otros taxa dulceacuícolas en la región en donde ocurrieron. 
En este escenario, podrá detectarse como los taxa dulceacuícolas respondieron ante los eventos 
pleistocénicos ocurridos en el centro de México. 
Patrones cofilogenéticos 
Las siguientes hipótesis cofilogenéticas se pusieron a prueba: a) Hay congruencia filogenética 
entre Goodeinae (a nivel de especies y tribus) reflejada en la historia genealógica de Margotrema 
(a nivel de linajes y especies). b) Los tiempos de divergencia entre los principales clados de 
Goodeinae (Tribus) corresponden con los de cada especie / linaje de Margotrema. Con base en la 
congruencia biogeográfica detectada con las asociaciones especificas de huéspedes de Goodeinae 
y apoyada con los resultados de los análisis cofilogenéticos y con los tiempos de divergencia de 
los principales linajes para Margotrema, se identificaron tres niveles de asociaciones históricas 
distintas donde se apoyan dichas hipótesis cofilogenéticas. A continuación se menciona de 
manera general cada uno de estos tres niveles de asociación histórica.  
a) Especie-Especie. Esta asociación representa un proceso de coespeciación (≈ 
coevolución), ocurrido entre Xenotaenia resolanae-Margotrema resolanae. El MRCA de 
Margotrema asociado a este evento fue datado hace 6.5 ma y es apoyado estadísticamente por los 
análisis cofilogenéticos de TreeMap. Por otra parte, esta hipótesis se sustenta por la edad de 
divergencia del MRCA del goodeino A. zonistius (6.9 ma), y el posterior evento de 
diversificación de X. resolanae, exclusivo para la región hidrológica del Río Purificación-
Mascota (Domínguez-Domínguez et al., 2010), lo que corresponde con la edad de divergencia 
del MRCA de Margotrema. 
 209 
 
b) Especie-Linaje. Esta asociación implica un proceso de especiación de huésped y una 
codiferenciación de linajes parasitarios que corresponde tanto con un evento de separación y 
aislamiento (Falla del Salto sobre el Río Mezquital, Durango, datado hace 1.8 ma), como para el 
tiempo de divergencia de M. bravoae Linaje III (1.0355 ma). Este evento causó la especiación 
alopátrica vicariante de los caracodontinos; Ch. audax y Ch. lateralis (Domínguez- Domínguez et 
al., 2006, 2010). Characodon audax actualmente está registrado como huésped exclusivo de M. 
bravoae Linaje III. Con base en esta evidencia biogeográfica y cofilogenética, se infiere que 
ocurrieron procesos de codiferenciación mediados por la vicarianza del Río Mezquital (entre el 
Río Mezquital Alto-Medio y el Río Mezquital Bajo), lo que promovió la codiferenciación entre el 
MRCA de Ch. audax y el MRCA de sus parásitos (M. bravoae Linaje III). Por otra parte, es 
posible que la asociación ancestral Characodon-M. bravoae Linaje III se perdiera en Ch. lateralis 
quizá por extinción natural de las poblaciones de M. bravoae Linaje III sobre el Río Mezquital 
Bajo; o bien, debida a una diferenciación ecológica mediada por los hábitos alimentarios 
herbívoros que presenta actualmente Ch. lateralis, lo que pudo causar la pérdida de la asociación 
con M. bravoae Linaje III. Futuros estudios podrán esclarecer ambos procesos de diversificación.  
c) Tribu-Linaje. Esta asociación histórica representa patrones de codivergencia a nivel de 
tribu, históricamente asociados con una codiferenciación de parásitos a nivel de linajes. Este 
patrón fue observado empíricamente por Martínez-Aquino et al., (2013), donde se infirió que las 
asociaciones entre las tribus de Goodeiane y los tres linajes de M. bravoae están estrechamente 
relacionados tanto por la historia hidrogeomorfológica del centro de México como por los 
procesos de diversificación filogenética de Goodeinae. En el Capítulo III, se puso a prueba esta 
hipótesis y se descubrió que M. bravoae Linaje I esta estrechamente relacionado con la historia 
de los sistemas hidrológicos de los ríos Ayuquila y Balsas que a su vez moldearon la 
diversificación de la tribu Ilyodontini. Del mismo modo se detectó una estrecha relación entre la 
la diversificación de M. bravoae Linaje II y el Rio Lerma, en donde también existió una 
diversificación de Girardinichthyini y Chapalichthyini. 
Con base en estos resultados se infiere que la divergencia de los linajes de Margotrema, 
en primera instancia, se debe a eventos vicariantes seguidos de los procesos de diversificación de 
los sus huéspedes goodeinos (i.e. Tribus). En este contexto, nuestros resultados se suman a otros 
trabajos donde se propone que el escenario geográfico rige, en primer orden, los procesos de 
 210 
 
diversificación de los organismos parásitos y, en segundo, las asociaciones con sus huéspedes 
(Nieberding et al., 2008, Mizukoshi et al., 2012). Los resultados de los análisis cofilogenéticos 
obtenidos en el presente trabajo nos permiten detectar que los procesos de codivergencia pueden 
actuar en tres niveles distintos, representado claramente que la evolución de los helmintos 
parásitos puede ocurrir de manera independiente, aún cuando están estrechamente relacionados 
filogenéticamente. En este contexto, es posible postular que la historia evolutiva del género 
Margotrema ocurrió sobre un mosaico geográfico, en el cual las poblaciones de parásitos difieren 
en sus características y especializaciones con respecto a las especies de huéspedes con las que 
están asociadas (Thompson, 2005).      
El área de distribución observada para M. bravoae y M. resolanae, así como la datación 
de la divergencia molecular, sus relaciones filogenéticas, patrones biogeográficos y 
cofilogenéticos, en contraste con la datación de los eventos hidrogeomorfológicos sobre el centro 
de México, apoyan las hipótesis que se generaron en este trabajo. Estos resultados sugieren que al 
aplicar distintos medios de análisis filogenéticos, biogeográficos y cofilogenéticos, con 
información detallada tanto del área de distribución de los taxa a estudiar, como de las edades 
geológicas del escenario geográfico en cuestión, permiten definir con mayor objetividad la 
historia evolutiva de los helmintos parásitos de peces dulceacuícolas de México.  
Implicaciones evolutivas 
La historia evolutiva de Margotrema propuesta en este estudio es congruente con la regla de 
Manter, la cual infiere que los parásitos evolucionan más lentamente que sus huéspedes (Brooks 
& McLennan, 1993). La tasa de diversificación observada para Goodeinae refleja una radiación 
biológica relativamente alta ya que cuenta con 42 taxa taxonómicamente válidos (Domínguez-
Domínguez et al., 2010). Actualmente se han registrado 55 taxa de helmintos parásitos para peces 
goodeinos (Capítulo I), sin embargo, solo 10 de estos pueden definirse como especialistas de 
Goodeinae: Margotrema bravoae, M. resolanae, Phyllodistomum sp., Saccocoeloides sp., 
Gyrodactylus lamothei, G. mexicanus, Gyrodactylus  sp. 1, Gyrodactylus  sp. 2, Rhabdochona 
ahuehuellensis y R. lichtenfelsi. La baja riqueza de especies del género Margotrema en goodeinos 
sugiere una tasa de especiación baja. Algo similar ha sido registrado en las especies de 
monogéneos de cíclidos de México, donde se ha sugerido que las tasas de diversificación de sus 
huéspedes han sido más rápidas que las de sus parásitos, por lo que el patrón de distribución 
 211 
 
huésped / parásito es desigual, es decir, pocas especies de monogéneos en muchas especies de 
huéspedes (Vidal-Martínez et al., 2001). 
El área de distribución ancestral de Margotrema coincide con la hipótesis de que 
Goodeinae divergió en sistemas hidrológicos del norte de México (Parenti, 1981). Con base en 
ello, en este trabajo se infiere la hipótesis de un área ancestral de Margotrema más amplia sobre 
sistemas hidrológicos del norte del país, lo que puede ser coherente con los patrones de 
distribución de los fósiles de Empetrichthyinae, grupo hermano de la subfamilia Goodeinae 
(Parenti, 1981; Minckley et al., 1986). Futuros estudios, con base en análisis filogenéticos 
moleculares de Margotrema distribuidos en sistemas hidrológicos del norte del país, podrán 
apoyar o contrastar esta posible asociación histórica entre Margotrema y peces empetríctinos. 
Los patrones biogegráficos y cofilogeneticos descubiertos en este trabajo para 
Margotrema dan pauta para generar nuevas preguntas. Por ejemplo, si mapeamos como 
caracteres los hábitos alimentarios de los peces goodeinos sobre su filogenia, se puede observar 
que aquellos peces que presentan carnivoría presentan están parasitados por Margotrema. Con 
base en esta observación, tiene sentido formular cuestionamientos como: ¿existe un efecto 
ecológico-evolutivo en el hecho de presentar un hábito alimentario de tipo carnívoro, capaz de 
reflejarse en un patrón de transmisión parasitaria horizontal o vertical? ¿la transmisión parasitaria 
es regida por el tipo de hábito alimentario del huésped definitivo y esta asociado a sus relaciones 
filogenéticas? Los patrones cofilogenéticos detectados entre Goodeinae-Margotrema fueron 
interpretados sobre el marco teórico del mosaíco geográfico (Thompson, 2004). Sin embargo, es 
posible apoyar nuestras hipótesis con evidencia coadaptativa si exploramos estudios 
metagenómicos respondiendo preguntas como: ¿el complejo mayor de histocompatibilidad 
(MHC, por sus siglas en ingles major histocompatibility complex) de Goodeinae y el de 
Margotrema, puede reflejar una asociación coadaptativa en parte de su genoma? En este proyecto 
se cuantificó la variación genética de Margotrema sobre los huéspedes definitivos. Algunos 
autores han descubierto que el origen de la variación genética en digéneos de la familia 
Allocreadiidae ocurre en los huéspedes definitivos debido a que es ahí donde ocurren las fases 
meióticas de los digéneos adultos (Murty, 1975; Canning & Madhavi, 1977; Madhavi, 1978; 
Ramanjaneyulu & Madhavi, 1984; Willis, 2001). Para este estudio en Margotrema, resulta 
interesante preguntarnos ¿que porcentaje de la variación observada en los sitios nulceotídicos 
 212 
 
polimórficos, tanto a nivel inter e intrapoblacionales, se originó en cada uno de los huéspedes 
involucrados en su ciclo de vida? Modelar estudios de selección natural dependiente de la 
frecuencia para organismos parásitos (Poulin, 2007), permitirá observar este tipo de información 
por descubrir. El comportamiento identificado para las asociaciones históricas intrínsecas (gen-
organismo, huésped-parásito y área-organismo) del modelo biológico Goodeinae-Margotrema 
permitió comprender los procesos de diversificación de los organismos parásitos de México. Este 
trabajo representa la arquitectura central a considerar para otros modelos biológicos (v. gr. 
helmintofaunas principales de México), en el sentido de expandir nuevas pautas de conocimiento 
sobre la vida parasitaria. 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 213 
 
CONCLUSIONES GENERALES 
  < La subfamilia Goodeinae (Osteichthys: Cyprinodontiformes: Goodeidae), incluye un 
total de 55 taxones de helmintos parásitos para 36 especies de goodeinos de las 42 que existen, de 
los cuales 10 son categorizados como especies especialistas (principales, desde el punto de vista 
biogeográfico) a esta subfamilia.  
  < El género Margotrema representa un grupo monofilético, en el cual se incluyen dos 
especies: M. bravoae Lamothe-Argumeto, 1970 y M. resolanae Pérez-Ponce de León, Martínez-
Aquino & Mendoza-Garfías, 2013.  
< Margotrema bravoae presenta una estructura genealógica que comprende tres linajes 
con evolución independiente asociados estrechamente a sistemas hidrológicos y a grupos 
particulares de huéspedes: a) Margotrema bravoae Linaje I, distribuido sobre los sistemas 
hidrológicos de los ríos Ayuquila, Balsas y Conchos y estando asociados a huéspedes de las 
tribus Ilyodontini, Chapalichthyini y a una especie de ciprínido (Codoma ornata). b) Margotrema 
bravoae Linaje II, distribuído sobre sistemas hidrológicos del río Lerma y asociado a huéspedes 
de la tribu Girardinichthyini y Chapalichthyini. c) Margotrema bravoae Linaje III, distribuído 
sobre sistemas hidrológicos del río Mezquital y asociado a un único huésped de la tribu 
Characodontini (Characodon audax). 
  < Los patrones de distribución geográfica de Margotrema están asociados con los eventos 
que fragmentaron a los sistemas hidrológicos del centro de México y que, a su vez, influenciaron 
también el patrón de distribución de sus huéspedes goodeinos. Por tanto, existe congruencia 
biogeográfica entre la historia genealógica de las poblaciones de Margotrema y la historia 
hidrogeomorfológica del centro de México, así como con la historia biogeográfica de Goodeinae. 
  < El proceso de dispersión causado por los huéspedes goodeinos jugó un papel relevante 
en el patrón de distribución actual de Margotrema, debido a la vagilidad que presentó 
históricamente el ancestro común más reciente de cada una de las tribus de Goodeinae, mismos 
que expandieron el área de distribución de Margotrema sobre los sistemas hidrológicos del 
centro de México. 
 214 
 
  < Existe congruencia entra las relaciones filogenéticas de Goodeinae (a nivel de especies 
y tribus) y la historia genealógica de Margotrema (a nivel de linajes y especies). A su vez, este 
patrón cofilogenético se observa en los tiempos de divergencia estimados para Goodeinae (a nivel 
de especies y tribus), y para especies y linajes de Margotrema.  
  < La relación Goodeinae-Margotrema representa tres niveles de asociaciones históricas 
distintas que reflejan que los procesos de codivergencia de los taxones de Margotrema, en 
primera instancia, son debidos a eventos vicariantes seguidos de los procesos de diversificación 
de los grupos monofiléticos de goodeinos: a) Especie-Especie. Representada por la asociación 
histórica Xenotaenia resolanae-Margotrema resolanae, exclusivo del Río Cuzalapa. b) Especie-
Linaje. (Codivergencia Tipo I). Representada por la asociación histórica Characodon audax-
Margotrema bravoae Linaje III, exclusivo del Río Mezquital Medio-Alto. c) Tribu-Linaje. 
(Codivergencia Tipo II). Representado, a su vez, por dos tipos de asociaciones históricas 
distintas: 1) Ilyodontini-Margotrema bravoae Linaje I, distribuido en los sistemas hidrológicos 
de los Ríos Ayuquila y Balsas. 2) Girardinichthyini / Chapalichthyini -Margotrema bravoae 
Linaje III, distribuido en el Río Lerma. 
 
 
 
 
 
 
 
 
 
 
 215 
 
LITERATURA CITADA  
Aguilar-Aguilar R., Rosas-Valdez R., Martínez-Aquino A., R. Pérez-Rodríguez, Domínguez-
Domínguez O. y G. Pérez-Ponce de León. 2010. Helminth fauna of two cyprinid fish 
(Campostoma ornatum and Codoma ornata) from the upper Piaxtla River, Northwestern 
Mexico. Helminthologia 47: 251–256. 
Barbour C. D. 1973. A biogeographical history of Chirostoma (Pisces: Atherinidae): A species 
flock from the Mexican Plateau. Copeia 3:533-556. 
Brooks D. R. 1979. Testing the context and extent of host-parasite coevolution. Systematic 
Zoology 28:299-307. 
Brooks, D. R. y D. A. McLenann. 1993. Parascript. Parasites and the Language of Evolution. 
Smithsonian Institution Press, Washington y Londres. 429 p.  
Canning E.U. y R. Madhavi. 1977.  Studies on two new species of Microsporida hyperparasitic 
in adult Allocreadium fasciatusi (Trematoda, Allocreadiidae). Parasitology 75: 293-300 
Charleston M.A. 2011. TreeMap 3b. URL http://sites.google.com/site/cophylogeny 
Chernoff B. y R.R. Miller. 1986. Fishes of the Notropis calientis complex, whit a key to the 
southern shiners of Mexico. COPEIA 1:170-183. 
Conow C., Fielder, D., Ovadia, Y. y R. Libeskind-Hadas. 2010. Jane: a new tool for the 
cophylogeny reconstruction problem. Algorithms for Molecular Biology 5: 16. 
Curran S.S., V.V. Tkach V.V. y R.M. Overstreet. 2011. Phylogenetic affinities of Auriculostoma 
(Digenea: Allocreadiidae), with descriptions of two new species from Peru. Journal of 
Parasitology 97: 661–670.  
Darwin Ch. 1859. On the origin of the species. The ilustrated edition 2008, Sterling Publishing, 
Co., Inc, China 544 p. 
Domínguez-Domínguez O., I. Doadrio y G. Pérez-Ponce de León. 2006. Historical biogeography 
of some river basins in central Mexico evidenced by their goodeine freshwater fishes: 
 216 
 
apreliminary hypothesis using secondary Brooks parsimony analysis. Journal of 
Biogeography. 33: 1437-1447. 
Domínguez-Domínguez O., C. Pedraza-Lara, N. Gurrola-Sánchez, R. Pérez-Rodríguez, I. Israde-
Alcántara, V. H. Garduño-Monroy, I. Doadrio, G. Pérez-Ponce de León y D.R. Brooks. 
2010. Historical biogeography of the Goodeinae (Cyprinodontiforms). En: Uribe-
Aranzabal M. C. and H. Grier. (Eds.). Viviparous Fishes II, New Life Publications, 
Homestead, Florida, 33-74.  
Drummond A.J., Ho S.Y.W., Phillips M.J. y A. Rambaut. 2006. Relaxed phylogenetics and 
dating with confidence. PLoS Biology 4: 699–710. 
Edwards S.V. 2009. Is a new and general theory of molecular systematics emerging? Evolution. 
63-1: 1–19. 
Ehrlich P.R. y P.H. Raven. 1964. Butterflies and Plants: a study in Coevolution. Evolution 18: 
586-608. 
Ferrari L. 2004. Slab detachment control on volcanic pulse and mantle heterogeneity in Central 
Mexico. Geology 32:77-80. 
Ferrari L., Lopez-Martinez M., Aguirre-Diaz G. y G. Carrasco-Nunez. 1999. Space-time patterns 
of Cenozoic arc volcanism in central Mexico: From the Sierra Madre Occidental to the 
Mexican Volcanic Belt. Geology 27: 303–306. 
Fontaneto D., Herniou E.A., Boschetti C., Caprioli M., Melone G., Ricci C., y T.G. Barraclough. 
2007. Independently evolving species in asexual bdelloid rotifers. PLoS Biology. 5, 914-
921. 
Gesundheit P. y Macias-García C. 2005. Biogeografía cladísta de la familia Goodeidae 
(Cyprinodontiformes). En: Morrone, J. y J. Llorente (eds). Una perspectiva 
latinoamericana de la biogeografía. CONABIO, México D.F. 319-337. 
Hey J. 2010. Isolation with Migration Models for More Than Two Populations. Molecular 
Biology and Evolution 27: 905–920. 
 217 
 
Hey J. y R. Nielsen. 2007. Integration within the Felsenstein equation for improved Markov 
chain Monte Carlo methods in population genetics. PNAS 104: 2785-2790. 
Huelsenbeck J.P. y F. Ronquist. 2001. MRBAYES: Bayesian inference of phylogenetic tres. 
Bioinformatics 8: 754-755. 
Huelsenbeck J.P., F. Ronquist, R. Nielsen y J.P. Bollback. 2001. Bayesian Inference of 
Phylogeny and Its Impact on Evolutionary Biology. Science. 294: 2310-2314. 
Huidobro L., Morrone J.J., Villalobos J.L. y F. Álvarez. 2006. Distributional patterns of 
freshwater taxa (fishes, crustaceans and plants) from the Mexican Transition Zone. 
Journal of Biogeography 33: 731–741. 
Lamothe-Argumedo R. 1972. Tremátodos de peces VI. Margotrema bravoae gen. nov.sp. nov. 
(Trematoda: Allocreadiidae) parásito de Lermichthys multiradiatus Meek. Anales del 
Instituto de Biología, UNAM, Serie Zoología 41: 87-92. 
Libeskind-Hadas R. y M. A. Charleston. 2009. On the computational complexity of the reticulate 
cophylogeny reconstruction problema. Journal of Computational Biology 16: 105-117. 
Luna-Vega I. y R. Contreras-Medina. 2012. Contributions of Cladistic Biogeography to the 
Mexican Transition Zone. En: L. Stevens (Ed.): Global Advances in Biogeography. 
ISBN: 978-953-51-0454-4, InTech, Available from: 
http://www.intechopen.com/books/global-advances-in-biogeography/contributions-
ofcladistic-biogeography-to-the-mexican-transition-zone 
Luna-Vega I., J.J. Morrone y D. Espinosa (Eds). 2005. Biodiversidad de la Faja Volcánica 
Transmexicana. Las Prensas de Ciencias, Universidad Nacional Autónoma de México. 
514 p. 
López-Ramos E. 1982. Geología de México. Tomos II y III. México, D.F. 454 p. 
Maddison W.P. 1997. Gene trees in species trees. Systematic Biology 46: 523–536. 
 218 
 
Madhavi R. 1978. Life history of Allocreadium fasciatusi Kakaji, 1969 (Trematoda: 
Allocreadiidae) from the freshwater fish Aplocheilus melastigma McClelland. Journal of 
Helminthology 52: 51-59. 
Martínez-Aquino A., G. Salgado-Maldonado, R. Aguilar-Aguilar, G. Cabañas-Carranza y M.P. 
Ortega-Olivares. 2004. Helminth parasites of Chapalichthys encaustus (Pisces: 
Goodeidae), an endemic freshwater fish from Lake Chapala, Jalisco, México. Journal of 
Parasitolology. 90: 889-890. 
Martínez-Aquino A., Aguilar-Aguilar R., Santa Anna del Conde Juárez H.O. y R. Contreras-
Medina. 2007a. Empleo de herramientas panbiogeográficas para detectar áreas para 
conservar: un ejemplo con taxones dulceacuícolas. En: Luna I., J.J. Morrone y D. 
Espinosa (Eds). Biodiversidad de la Faja Volcánica Transmexicana. Las Prensas de 
Ciencias, Universidad Nacional Autónoma de México. Pp. 449-460. 
Martínez-Aquino A., G. Salgado-Maldonado, R. Aguilar-Aguilar, G. Cabañas-Carranza y C.A. 
Mendoza-Palmero. 2007b. Helminth parasite communities of Characodon audax and C. 
lateralis (Pisces: Goodeidae), endemic freshwater fishes from Durango, Mexico. The 
Southwestern Naturalist 52: 125-130. 
Martínez-Aquino A., Aguilar-Aguilar R., Pérez-Rodríguez R. y G. Pérez-Ponce de León. 2009. 
Helminth parasite of Xenotaenia resolanae (Osteichthyes: Cyprinodontiformes: 
Goodeidae) from the Cuzalapa hydrological system, Jalisco, Mexico. Journal of 
Parasitology 95: 1221-1223. 
Martínez-Aquino A., D. Hernández-Mena, R. Pérez-Rodríguez, R. Aguilar-Aguilar y G. Pérez-
Ponce de León. 2011. Endohelminth parasites of the freshwater fish Zoogoneticus 
purhepechus (Cyprinodontiformes: Goodeidae) from two springs in the Lower Lerma 
River, Mexico. Revista Mexicana de Biodiversidad 82: 1132-1137. 
Martínez-Aquino A., R. Pérez-Rodríguez, D.I. Hernández-Mena, L. Garrido-Olvera, R. Aguilar-
Aguilar and G. Pérez-Ponce de León. 2012. Endohelminth parasites of seven goodein 
species (Cyprinodontiformes: Goodeidae) from Lake Zacapu, Michoacán, Central Mexico 
Plateau. Hidrobiológica. 22: 88-91. 
 219 
 
Martínez-Aquino A., F.S. Ceccarelli and G. Pérez-Ponce de León. 2013. Molecular phylogeny of 
the genus Margotrema (Digenea: Allocreadiidae), parasitic flatworms of goodeid 
freshwater fishes across central Mexico: species boundaries, host-specificity and 
geographical congruence. Zoological Journal of the Linnean Society. 168: 1-66. 
Manter H.W. 1963. The zoogeographical affinities of trematodes of South American freshwater 
fishes. Systematic Zoology 12: 45-70. 
Mateos M., O. I. Sanjur y R. C. Vrijenhoek. 2002. Historical biogeography of the livebearing fish 
genus Poeciliopsis (Poeciliidae: Cyprinodontiformes). Evolution 56: 972–984.  
Mejía-Madrid H., Domínguez- Domínguez O. y G. Pérez-Ponce de León. 2005. Adult 
endohelminth parasites of Goodeinae (Cyprinodontiformes: Goodeidae) from México 
Mizukoshi A., Johnson K.P. y K. Yoshizawa. 2012. Co-phylogeography and morphological 
evolution of sika deer lice (Damalinia sika) with their hosts (Cervus nippon). 
Parasitology 139: 1614-1629. 
Minckley W.L.D., D.A. Hendrickson y C.E. Bond. 1986. Goegraphy of western North American 
Freshwater fishes: Description and relationships to intracontinental tectonism. En: Hocutt 
C.H. y E.O. Wiley (Eds). The Zoogoegraphy of North Amercian Freshawater Fishes. John 
Wiley y Sons, Nueva York 516-613 pp.      
Morrone J.J. 2010. Fundamental biogeographic patterns across the Mexican Transition Zone: an 
evolutionary approach. Ecography 33: 355-361. 
Morrison D.A. 2006. Phylogenetic Analyses of Parasites in the New Millennium. Advances in 
Parasitology. Vol 63. 124 p. 
Murty A.S. 1975. Studies on Indian cercarie II. Allocreadioid cercarie. Journal of Parasitology 
61: 418-420. 
Nieberding C.M., Durette-Desset M.-C, Vanderpoorten A., Casanova J.C., Ribas A., Deffontaine 
V., Feliu C., Morand S., R. Libois & J.R. Michaux. 2008. Geography and host 
biogeography matter for understanding the phylogeography of a parasite. Molecular 
Phylogenetics and Evolution 47: 538–554. 
 220 
 
Nielsen R. y J. Wakeley. 2001. Distinguishing Migration From Isolation: A Markov Chain Monte 
Carlo Approach. Genetics 158: 885–896. 
Nylander J.A.A., Olsson U.,  Alström P., e I. Sanmartín. 2008. Accounting for Phylogenetic 
Uncertainty in Biogeography: A Bayesian Approach to Dispersal-Vicariance Analysis of 
the Thrushes (Aves: Turdus). Systematic Biology 57: 257–268. 
Page R. D. M. 1994a. Maps between trees and cladistic analysis of historical associations among 
genes, organisms, and areas. Systematic Biology 43: 58-77. 
Page R.D.M. 2003. Tangled Trees: Phylogeny, Cospeciation, and Coevolution. The University of 
Chicago Press: Chicago y Londres, E.U.A. 378 p. 
Page R.D.M. y M.A. Charleston. 1998. Trees within trees: phylogeny and historical associations. 
TREE. 13: 356–359. 
Page R.D.M. y E.D. Holmes. 1998. Molecular Evolution: A phylogenetic approach. Blackwell 
Science Ltd, Inglaterra 346 p. 
Parenti L. R. 1981. A phylogenetic and biogeographic analysis of cyprinodontiform fishes 
(Teleostei: Atherinomorpha). Bulletin of the American Museum of Natural History 
168:340-557. 
Pérez-Ponce de León G. 2001. Margotrema guillerminae n. sp. (Trematoda: Macroderoididae) 
from two species of freshwaters fishes in Lake Zacapu, Michoacan state, Mexico, and 
new records of Margotrema bravoae Lamothe, 1970. Journal of Parasitology 87: 1112-
1114. 
Pérez-Ponce de León G. y A. Choudhury. 2005. Biogeography of helminth parasites of 
freshwater fishes in Mexico: the research for patterns and processes. Journal of 
Biogeography 32: 645-649. 
Pérez-Ponce de León G. y A. Choudhury. 2010. Parasite inventories and DNA-based taxonomy: 
Lessons from helminths of freshwater fishes in a megadiverse country. Journal of 
Parasitology 96: 236-244. 
 221 
 
Pérez-Ponce de León G., García-Prieto L., León-Régagnon V. y A. Choudhury. 2000. Helminth 
communities of native and introduced fishes in Lake Pátzcuaro, Michoacan, Mexico. 
Journal of Fish Biology 57: 303-325. 
Pérez-Ponce de León G., García-Prieto L. y B. Mendoza-Garfias. 2007a. Trematode parasites 
(Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa 1534: 1-247. 
Pérez-Ponce de León G., Choudhury A., Rosas-Valdez R. y H. Mejía-Madrid. 2007b. Systematic 
position of Wallinia spp. and Margotrema spp. parasites of Middle-American and 
Neotropical freshwater fishes based on 28S ribosomal RNA gene. Systematic 
Parasitology 68: 49-55. 
Pérez-Ponce de León G., R. Rosas-Valdez, B. Mendoza-Garfias, R. Aguilar-Aguilar, J. Falcón-
Ordaz, L. Garrido-Olvera y R. Pérez-Rodríguez. 2009. Survey of the endohelminth 
parasites of freshwater fishes in the upper Mezquital River Basin, Durango State, Mexico. 
Zootaxa 2164: 1–20. 
Pérez-Ponce de León G., Mendoza-Garfias B., Rosas-Valdez R. y A. Choudhury. 2013. New host 
and locality records of freshwater fish helminth parasites in river basins north of the 
Transmexican Volcanic Belt in northern Mexico: Another look at biogeographical 
patterns. Revista Mexicana de Biodiversidad. 84. 
Pérez-Ponce de León G., A. Martínez-Aquino & B. Mendoza-Garfias. 2013. A new species of 
Margotrema (Digenea, Allocreadiidae) from the leopard splitfin Xenotaenia resolanae 
(Cyprinodontiformes, Goodeidae) from west-central Mexico. Zootaxa. 3670: 94-96.  
Pineda-López R., Salgado-Maldonado G., Soto-Galera E., Hernández-Camacho N., Orozco-
Zamorano A., Contreras-Robledo S., Cabañas-Carranza G. y R. Aguilar-Aguilar. 2005. 
Helminth parasites of viviparous fishes in Mexico. En: H. Grier y M.C. Uribe (Eds.). 
Viviparous Fishes: Genetics, Ecology, and Conservation. New Life Publications 
Homestrad, Florida. pp. 437-456. 
Plaisance L., Rousset V., S. Morand y D.T.J. Littlewood. 2008. Colonization of Pacific islands by 
parasites of low dispersal ability: phylogeography of two monogenean species 
 222 
 
parasitizing butterflyfishes in the South Pacific Ocean. Journal of Biogeography. 35: 76-
87. 
Pons J., Barraclough T.G., Gomez-Zurita J., Cardoso A., Duran D.P., Hazell S., Kamoun S., 
Sumlin W.D. y Vogler A.P. 2006. Sequence-based species delimitation for the DNA 
taxonomy of undescribed insects. Systematic Biology 55: 595–609. 
Poulin R. 2007. Evolutionary ecology of parasites  (2nd ed.). Princeton University Press, 342 
p. 
Ramanjaneyulu J.V. y R. Madhavi. 1984. Cytological investigations on two species of 
allocreadiid trematodes with special reference to the occurrence of triploidy and 
parthenogenesis in Allocreadium fasciatusi. International Journal of Parasitology 14: 
309-316.   
Rannala, B. & Michalakis, Y. (2003) Populations genetics and cospeciation: from process to 
pattern. In: Page R.D.M. 2003. Tangled Trees: Phylogeny, Cospeciation, and 
Coevolution. The University of Chicago Press: Chicago y London, U.S.A. 120-143 pp. 
Ree R.H. y S.A. Smith. 2008. Maximum Likelihood Inference of Geographic Range Evolution 
by Dispersal, Local Extinction, and Cladogenesis. Systematic Biology 57: 4–14. 
Ree R.H., Moore, B.R., C.O. Webb y Donoghue, M.J. 2005. A likelihood framework for 
inferring the evolution of geographic range on phylogenetic trees. Evolution 59: 2299–
2311. 
Ree R.H., e I. Sanmartín. 2009. Prospects and challenges for parametric models in historical 
biogeographical inference. Journal of Biogeography 36: 1211–1220 
Ronquist F. e I. Sanmartín. 2011. Phylogenetic methods in biogeography. Annual Review of 
Ecology, Evolution, and Systematics. 42: 441-464. 
Rosenberg N.A. y M. Nordborg. 2002.Genealogical trees, coalescent theory and the analysis of 
genetic polymorphisms. Nature. 3: 380-390. 
 223 
 
Sanmartín I. 2010. Breaking the chain of parsimony: parametric approachesin historical 
biogeography. En: Cox C.B. y P.D. Moore (Eds) Biogeography,an ecological and 
evolutionary approach. 8th ed. Hoboken Nueva Jersay: Wiley, pp. 213–4. 
Sanmartín I. 2012. Historical Biogeography: Evolution in Time and Space. Evolution: 
Educationa and Outreach. 5: 555-568. 
Thompson J.N. 1994. The coevolutionary process. University of Chicago Press, Chicago. 376 p. 
Thompson J.N. 2005. Coevolution: the geographic mosaic of coevolutionary arms races. Current 
Biology 15: 992-994. 
Thompson J.N. 2013. Relentless Evolution. University of Chicago Press, Chicago (upcoming, 
spring 2013). approx. 496 pp. 
Uyeno T. y R.R. Miller. 1962. Summary of Late Cenozoic freshwater fish records for North 
America. Occasional papers of the Museum of Zoology University of Michigan. 36 p. 
Vidal-Martínez, V. M., T. Scholz y L. Aguirre-Macedo. 2001. Dactylogyridae of cichlid fishes 
from Nicaragua, Central America, with descriptions of Gussevia herotilapiae sp. n. and 
three new species of Sciadicleithrum (Monogena: Ancyrocephalydae). Comparative 
Parasitology 68: 76-86. 
Willis M.S. 2001. Population biology of Allocreadium lobatum Wallin, 1909 (Digenea: 
Allocreadiidae) in the Creek Chub, Semotilus atromaculatus, Mitchill (Osteichthyes: 
Cyprinadae), in a Nebraska Creek, USA. Memórias do Instuto Oswaldo Cruz 96: 331-338. 
Yu Y., Harris, A.J. y He, X. 2010. S-DIVA (Statistical Dispersal-Vicariance Analysis): a tool for 
inferring biogeographic histories. Molecular Phylogenetics and Evolution 56: 848–850. 
Zietara M.S. y J. Lumme. 2002. Speciation by host switch and adaptive radiation in a fish 
parasite genus Gyrodactylus (Monogenea, Gyrodactylidae). Evolution 56: 2445-2458. 
 
 
 224 
 
 
 
 
 
 
 
 
 
 
 
APÉNDICE 
HELMINTH PARASITES OF FRESHWATER FISHES FROM CUATRO CIÉNEGAS, COAHUILA, IN  
THE CHIHUAHUA DESERT OF MEXICO: INVENTORY AND  
BIOGEOGRAPHICAL IMPLICATIONS   
 
 
 
 
 
 
 
 
 
 
 
 225 
 
Durante el transcurso del presente proyecto doctoral (financiado por el Consejo Nacional de 
Ciencia y Tecnología a través de una beca para estudios de doctorado dentro del Programa de 
Posgrado en Ciencias Biológicas, de la Universidad Nacional Autónoma de México), de manera 
paralela, se genero un artículo en extenso referente a la biodiversidad de helmintos parásitos de 
peces dulceacuícolas del norte de México el cuál se muestra a modo de apéndice en este trabajo. 
A continuación se presenta la galera de este articulo en extenso aceptado para su publicación, 
intitulado:  
Helminth parasites of freshwater fishes from Cuatro Ciénegas, Coahuila, in the 
Chihuahua, desert of Mexico: Inventory and biogeographical implications (Aguilar-
Aguilar et al., 2013). 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 226 
 
 
 
1<11 , 1I "aoi. , ~1 .1 fl .~" . , C . .... C"" I<'" 
1I, '_i.,. po ..... " . , I ..... ~ . '" fl .... 1.-. .. C .... . C"' .... ~ C_ • • ilL io ,.< 
R,,¡d .. AGU'LAK_AGUlLAR'. ,,",M, M,\RTiNEZ-AQUINo" ' , 11<rt", 
ESP I:<OSA_p rREZ' . ....l C,."..;, I'tREZ- I'ONCE DE '-"Ó,;' 
" u"""" ",, J, M".oo, Apdo 1'0"" 1oJ.-l1~ . C_ P_ 0.5 10 Mo' .. ", D_F __ M,,",o. E_m. ", 
"C. il-b "",i ... "",m . ,," 
o. MixKO. Apdo_ P .... l 70- 1 53. C . P_ 0.11 Q ~li,~o D.F .. M,,~o 
o. Mhiro. Apdo_ Po"" 10- \ 53. C r _ 0.1\ Q M i,~" D.F .. M,,"," 
n •• """' ....... "'--"'" """"M_'" __ "''''' ,~~ ...... "" .... -.. .. _ ..... ___ _ ...... ~ •• ' • ___ ..... ~ .. Ka-.. ... ~ 
... ,~ ..... ,' ...... "'0" .. ' . n-..<o~ h _ " _ ... _ 10." 1 ",,_ -r,-,;o;' 
ABSTRACT. As a partofan ongoing inventory of hs hclminih parasitos of reswater 
fishes in Mexico, 570 individual Fish were collected between April 2008 and October 
2011 126 locals along the Cuatro Ciéne as region in Coahuila State, northern 
México, Seventeen species of hosts, mosly corresponding to Neareticfrshwater 
elements, were studied. A total 08324 individual worms wee collected dering this 
y representing 25 species of helminih of which 9 were digencan, 3 
monogencans, | cestodo, 3 acantboccphalans, and 9 nematodos, Most of th records in 
this chccklisreprescot new host or locelity records. The information provided in his 
hcklis may be helpful for our understanding of lc biodiversity und historical 
biogcography of his hst-paraste system, since in the Cuatro Ciénegas region occur a 
Nearetcfreshwater fish fauna, along wilh Neotropical and endemic clements and from. 
a biogcographical point of icw, may represents tranitonal arca 
  
KEY WORDS. Monogenca, Digenca, Cestoda, Acanthocephala, Nematoda, 
Fresincatr fishes, Cuatro Ciénegas, Mexico
 227 
 
 
 
A~ ST Il AC T . "" • pm~h" "";"'" ; ' '''~'''''Y f tOo ... .." .. ¡¡, f"' ..... 01 f=IM· ... , 
r,.¡",. '" ,úoo, j7<J o.! X!"oI I >  ~ .., , Ilm«l "'''''=- Ap<i 1200~ o d ü<t t.... 
1 .. 2' "'oIit"" ""' ... I>< e ....o ;¡"'.p' ,,; "" ..  • .t..;1o , ••. rtOom 
,,;"o. ".-.. """'" .fho.o~ ".,>tly .. ""',.,.,...,,,, .. ~ · '"ITt;" f=j,,,,,,, 
d<m<n< ~ ~ .., ~ud>«l . Ioul .fl)24 .... ,"'j"l """"'" ~= r lo«« wml 'o;' 
~. ",,«><nI "'; 1 . <e;" . l>o. ,.,,,,o. . f ~hKO  ~ ..., ,V"' .. ~ 1 
""''''''''., .... 1 , .. .00., 1 ..... ho <¡'hol ..... '"  .."..,ü<lo• . oo! . ftOo ",,,, o. .. 
¡¡'¡, <""k~" ,...,. .. <nI ",  u,,", .... Iioy ... roro._ h< , nno! m ~",,'od« .. ¡¡,,, 
ct.. ,k l ,~ ... y 1>< Oolrful ..- "'" ....... "-" ¡ .r"" oo.i".,, ;ty od Im>o","¡ 
"V"rrby.r ¡¡,;, oo'-f"''' ' ' ' 1""". ,¡"'< .. tOo ""'" C Oin<~ ",p .. .,,, .... 
<.,-c'K [,.,.n-.-.<" ,,. ........, ' '' s ",;¡¡' N..~ . I o d md",,~ <I< <nt. , O  
• "V",'''f'IIK oI PO" .h;"". m")' ,...,.",,, •• ,,.,...,,,,,,,j ""~ 
 228 
 
 
 
I.'lTRODllCTION 
e """, e;¡"., .... , "",11 "' .. ",,"'_ ", I i<~ "'i< of,~ SkITo Mad« Oriontal in 
e .... óIL """~m M,,"o. no. ~~ I ) ' I 000 "1"'" km ..... " "oIk)' ofe ..... 
eK' .. ~ po ..... "'" p .... " .... mI><r of...km" """;,, of .. y ~ ... , in North Amn", 
(S .. , ,,, 01. 20001 . .. ¡¡in, • -.. oiOO;, .... y .... IDO« ,tw. 7(1 ''''¡ <m~ 'f'<C"" l. 
th" ",Iky. ""."" "' .... 'K .nO ""» __ Io ~ "' " _b .. "'.;", ~ "'"""'~ m-m 
...,j l. ... m fouAoj (M_ 19U). ~'IO< " "PI"'" '" """ ... Iy dom" f .... f .... f ... 
Nortb A""",.., ....." "i"". ,,,,,fo,,,,," oy" 1 ... , 16 ",",., f6b >p<ri,~ , of ~-t.;,h 
., <n<km" I~hnül<y 1_1- n.o f"'",.. .... r ... h<Irn, .. h p"' .... , f""", ofe .. "" 
eK' .. ".. o... bo<n "'""dy ,,"dkd (eO<ttT<n.< 2()(1.1). Publ,ohNI =",", ",Iod. ti>< 
d;¡<"' .... &o.o<~el¡" ;"I>.¡ ... (Lomoth<_A<p....oo. 1971). e . 1vK;,., c;,!I;J"", .. 
"l""", .M"odo .l: Sc¡"'k 2005. ü"" ... ~ , ,dk=_. r.t.nt ... 1930. ond 
.\.m"_ '1'. (."",,,, onvWl)' d",.-k<l _ t"-,...,,..Ji, ¡. ".,¿Ji. s"cro<",¡ioid,~ 
'1' .• en",""''' "'.,""c, .... '«ari"_,.,,¡J,, '1' .. '''¡O«"'''''', = p .. ""_r",,,,", 
l<óo" .1. 1001). 011 orlh<m r_;,u,"S C.cltl"" ... '1'1'. (.h""""" .1. 19I11 
0w~OO-M,";"" lo¡g.,l. Oth.. = ..... ,..--.~ .. """"', ..... ,,. of"'" 6un~. 
D.<')lo~)"nd .. .. ~ ..... " 01 e"u,-,,,",,, "f'I'. "'" EI~....,_. "'. W-",,_M.mnn 
19"'1. t ~ "' ... ...,<pIu.w., P • .!_,., '1' . .. c .. ,.¡,.,,,, "",,,1Ii (Md\', 19I11 ~ ,,,.j 
""""' .nid.,.W"'¡ '1""'" of mI""'''' ud ",m"odd I"rom Ello""",.., "" 
c,'pri"'''¡''. "'jon"' ... Mill«. 1%11 .... ea"", .. ", ..,nM MUtckky '" Dad...,. •. 
1%11CO • ...,-.L-M.rtina I <¡g.(; Mdf, 19i5). Add;,.,,,,1 ,,,.,.-d, of ¡"kn, .. h p"'''' '' 
of ",,,,., "","", ... , r,,¡,,. orCoobu;¡' ;" ...my 1", .. , .. , .fe ...... e;¡".,,, ,.<1 .... 
"" ""'''''i<''''. m¡,ku",,. ... idu 'p""'"'" MO«: ,IJum. 1911 ~ _ '«"'"""',,1, 
 229 
 
 
 
."u.;c;"",¡,,,, .... ¡;Il. or Aplrn¡"'''.g __ ~"".I<aIl , ,,,,'l''' ' 1119 (Bnm,_lloa;,. " 
JimIno, 1 \11th .... ~i,<n<" .. /J;plo,_¡"", '1'_ ."j Alloglru.;d'_ ",ro (t-.o,.. 
'~l J I ",r"","; k",I."" p"'''''''' (kalh,,"'1Y'. ¡ i Ji) (ü.¡"lkn>-Pa,hh. '''''1 ;" 
P"",_l'ooc<'" l<OO" O/. 2001~""¡ tOo "",",,,,,ario< OrÜ"_"'fH--'.' 
(N~h~O<i. 18N) ... ,.....i1< oH)p_U. "'''''''H (S.mI " Gi,.,-d. Illl) (A~ib. _ 
.o.pd",""J. 200'it) 
c-..tro c;¡".,v' o .... ,.. ....... o"-;'¡" ,.. ..... yof &, ... ~." r_, ~,oh . 
b .. ¡:<oppbocol offinOy ",,"Iy" .... N,,,,,,,, .. ,;"n , ¡,." ;, .. io<ot<d '" """",", 
M,,",o, ro.. ...... bonko- ~.;.¡, .... USA .. bot""'" "" """" N«><ropcol ,km<"" 
(M •• .,¡,",y 19S4) "'" "",b thd. mo" """brrn d~ """t.,. IOn .. '" ,h< L""". f"Dooin; 
.... ...-... .. , modd .. otu<ly _ .... 1 pz»"" fowul "'"'"S'. Fa, oh" '..- .... 
I"=- ~"'¡y Oom;' '0;<1"" ~""·,,, ... 11 putol6h«l mlonru .... .",j "'''' d ... "'" ",-,., 
pth=d oom& = .... """'''Y ;" dw f>Mti'" ~ K<'. ;" ,h< '0""'" ur . """" 
"" ...... '""""v, "'-xl ~., ""., """,""t<d .. """""'" M, .. ,o (S<, M"""""_A,,,,"'" " 
.1. 1007, Morti"",_A'I""'" " """ .... -AJO"I .. 200II , M.ruou_V""",o " A"' .... _ 
"",iloo 1001< , """ ..... _A"'i .... ".1. lOO'it, ;,QI &; rm ... pOftC<.., L<ón".1. 100'it. 
10101. n.o ..... ofoh .. I"'f"" "'" ID ="'" .... ¡", ..... O PO"'''' &un... oh"",al ro ... 
'!'<''''' rrom Cuotro C"''''P' ;. ook"o ,on'''''''' t~ .... """nkH)' orm"..,,,,,, 
,....,i ... i. rr. ... ~"'" ow.., from no"""" M,,,,,, """ .. ¡'n.fly d,,,,, .. ,h< 
b .. "",ppbocol ~I~ .. .,.,. uf"". findiop. 
MI. HRIALS ASD METIIODS 
A 10loi of IJO fun., from lo !oc.1;'~ ... Cuo"" c;¡".,~ h¡d.-olopo. I.)"',,,,, ...d 
"'" ....... , ,.,..." ""'''' ",11ffi<O ¡"""'UO Al"'l 200Jl """ Oc..-, lG11 (F~ l. T'¡'k 
'1_ S-<>,_ ..... off ... """" """,,,..¡, a.o,""";'¡ .. , Cm"' ........ '1'-10 _ l~ 
 230 
 
 
 
C,n<=chod.,,, i.".-u _I;"""u IR, f",,"I"" 1~2úl (. - 7, """''''''"'' .. iM<>i<h. 
IUc~,. 1802) lo _ i~ C" .... "d. " "'~"'...,. _ • ., ...... 10. F, .... , 1111) (.o _ 11) 
C"'bI,d." 1I""",1om .. ,. bi""" .... ,.. Gill L &02 1" _ 2'). 11 __ " ,_ ~"' ... 
(11';'0 & ........ 11141 l ' _ 1, 11. .. "'11.,. (K"",ro,(d" lo)l..-. 1911) (. _ ii \ 
C:<!,,,om., ül'riodl. ¡,,, ...... ¡, lB..ird & Go...d. 1111)1. _ 1'). C. """0.".,,, 
(M ... ki<y " l¡.<i<. '%'JI l' _ l< 1.l)i".,a" .";""",, (t'n,,!. 1 ~ 5I.1 l' _ .'01 . .v"""Pi. 
"'. l' _ l); ~xI .. , C.priooda< ."""" Mil¡"'. 1 %81' _ 101); e ."""" x 
b.J.=W"'I' - 6\. c. bifoc"""' M;¡k<. '%1 l. _ 281. ["' .... i."""", 1M b. & 
Mili«. 1 '1M (. - 2r k .. hai d." 1< .. 1",", '''_1'''''''' 1851) l' _ < ); """ 1'o«;li .... , 
'",_,i. """,.ii Mi .. "ky & Cn.do,,". L %2 (. _ 119). Fo.h "'= ,oIkrt,d "' ~ 
TI"' ... " ......... """ "''''' ........ w= " ,. .li,·,.nd ....,¡;,.¡ .... h,bm n' ~ "" ...... , ,""" 
4 In ,11<, ,"" ...... F;o/, W<'I' ...,,,f,,,,I "'" i......tiotdy .. ud...! fo» "'I"nn'm. AII 
"""''''' "" ... -..= plo<od "I'".t<1r .. 0 .611'. ..J'" .... ,,&mi ",d .nJ", tho 
"=o",,,,,,. no. "':11. ¡",m , ,,,b ~ ~ . = d~ o<c,," . plo<..! .. Poi .. da"" ~-. " "'" 
-.._.".¡ < ..... ...d foc "" ... V"' , n~ ~b " ~~'" fi , od .. JI),"" __ r""'" 
(GAPI ¡" onk. ., .. udy u.,;, .d""."od a"""",,,. Aft" ,'" ''"''1' I>0I0;,,'' ".1" ... ,,,,-
"""""'"' ro,," ",th GAP ... ", ......,.,,,od ¡" C."..... o.l>am r.uo..· .. E~," , 11%9) 
"""'" '<'"""""'" ~ .... , f" od "' ¡"" ' .. ' .... n ~ ¡""",h ... 4<4 . ... ;....¡ wi.h , ...,..,.; •• 
"" ~. "' '' ond """' .. ..t in C."..¡, b.t..m '" >tudy .Iu ¡ ........ I ........ ~~ ... 
"'= " '""..! .. ... ond """,,,,j , •• l'« ri ,jo.;, ~ ' ;,h O . M ~ . .. ,'" pn..- ro ....... 
PIot)k ..... '" wm ¡"od ~ i th loo< I .. ~.,') 4··' fonn.olin.. A .... """'""~ ~= 
""' .......... ~ 'C fe, 11 h .. d", dW " ....... .".. t ~. fi • .J .. ,.Id 10'4 .......... 
N""" ....... .....-. fu..! _ "'" ( . t< ..ru "~i 4 \. fonrulin ... 00' (",,,,:~ 10"4 "banal 
AII l>dm;"u" ""'" P""'''''" f.II" ,,· ~ ound..-.l p "",«Iw-<.I Lo mo"" _ ~do 
 231 
 
 
 
I mi. kI,"" r. ... "'" ~'" """!' l<t<O u~ " ; ."..,,, ¡¡",I I "".tu c< • ..,.¡ "."",, '!'<''''''''' 
of"..,,, b<1m" .. .... ~ . ,", 0'1",,, .. d ., ti>< eolo<,OIn N","-I "' 1I, 1m ¡ .... (CNIlE). 
1 ... """,, "' B .. Io~ U.i"",doO N .. ,,-" A utónomo <k M""-"o. Mw", e.)·. 
M".,o. F;'¡' '1""""="-'"" d""",,«I .. ti>< eol=OIn N",,,-I <k PO<'<' (CNPm. 
!mt;tuto "' B;'¡"~ lku,.",idod N",;""'¡ A...ru.. ... <k Mi<"o. M",,," COy, 
M""o. n.o, u .. orl''''-.I<"" (0, ,""",todl. "",n .... m"y 1""""'" 01 r ...... " ofti>< 
""'" 'r>«;" .. ' "f",,«I fi'¡') ,..t obund""" (......o.r ofp ..... " ord" ,,,,,,, "",0<, 
1'" , ...... ..,¡ r,.¡,) foJlo~·, Bu"'''.1. (''1'>7). 
IlESULTS 
l. tho> ""''''y, 110 no ;,·"",,, ro,¡, !mm Cwtro e"",g.» N." , nd "" rh""'~ 
..-. ... ,.....,.,.,ndin¡ '" 11 'm """ ...... ,,<1. ..."h • ...."Iin, ~'" 1'" ""''''' ,.")i~ 
i-om 1 ., 119 m ;" ....... F;,t, from 16 10 .. 1;, ,,, ~-.., ""'1',," , , 00,,,,,, , """" 
""~ ....... IIod;d , """ .. '1''''''' &nd ".nd.o, bu, , 1>0 ,~ = and ............. ,~, 
(T""" l. r ~ IJ. lb< ho., '!""'" ~·"h ti>< w¡,~ _ pi< ,,"',.-....... 100, .. _"ó;, 
"'h",b . ''' .... 10 b< ti>< ""'" ""'"""'" mU mu_ fuh 'P"'" ,n ~ . _ 1Iodi<, of,Oo 
e .. ..., C""'I" " ' '''" 1'" ,,,,,,n«! """,'" of,.,." ("''1'''' ' Ca"',"'""" 'f' . .",j 
C]p,¡oo.Io. bijoHU,OH. ~bh ... .", ",pO,., ro.- Oo lm"" b pa=¡'''1 -..t.oml brt-." 
I mU 10 b<1m, .. , opa';'" ,.·.h ti>< ",t .... , ;ori>w;' G . ... ""'b<"", , b< "". '1''''''' 
n.m..- ~ ,00 1 .. , ,,, "",,"', or l><lrninlh -... Jo. ",", ofiJl< !nd;v""'oI wcnru ~.= 
col",tod .1 ..... oh .. 4-)" .... ,<y. ~on, II .... "" oroo l .... '" oh·hod, 9 ~ . "" 
o; ;,..,.. ~ J m"""V"""",- 1 ,,,toó<. J ""'"'"""'I't..w... .... 9 ......... ... 
n.. ",,,,1,, or,),,, " " '~r '" p"" • .""j " ,,..,, ''''''' ~ n.o fnl 00<,, ' ~ 
!,",""I<-""" ¡,,, (T'¡'" 1), "' .. ·hU, ,... .. 0" ..... 8 "'P'OZ'" Oy .. 1m .... ,,_o .,., 
"P«'" ,.-0" .. <~¡, P""!'''' h>t<d oIp~ , i<. ll r· 11>< ",lo .. ,f~ "'''''' .,., """'''y 
 232 
 
 
 
.. ~,......ed. 10 110 .... by .... &bb<,,"'.,. indk" ml t h< hab'''(' 1 ... """ '"' "lml",b 
, .. ,," ..... fuu ...... ·.b,. '"' ro",. N,,,. ,'" ho" ..... '" "' .. ""h '"' "'''"""b .... ¡¡'W><l 
• ¡, ... d. follo .... br'''' 1oc,I . r . .... '"' " 1,,,. "fp«> ~ """ ...... .......... "'. ,00 
"" .. , .. ..m'y ofml«1 ..... W .... mo« ,hon o", _ 'f'<';" bOomi ,'" """" 
h<b", .. k ""~ thoo< "" 1Ht.,j alpIW><o~.lIy. and """ 'P"'''' 100- " ',,,b mo« ,tu", """ 
1oc . I ~r n , "c.roed "" I"',d "",""'. n.. 1000'_ ...... , I ~ t (T"'1o JI ~ .. gmizod 
oIph.l.,,,,,.lIy by f"k f ... il,·. Wdo .. ...,¡, fomily. '<"""'''-' 01", 1",Ni ;" .1o~ 1 
oro..-. Eoch fi,¡' 'P"'" Im l..l " , tIm, .'" p", . .. ,,,d). 6 follo .. ·od byth< 1 .. of" 
f'M";'''' .. ·,,,10 ""ko,dn "><Iopm<oul "'iI' ."j." .b!"-",.,,,.., oft h< "',,"ondo 
"""1' '" .. 1>o<h tIut ~ .... "' "'loop . ,...., pa=' " pon .,,,, ly ",ororo .. ,'" ...... 
"""""",,.1 "lI"'" ." ok .. ,r>«l .... do.., ",m. ... ·i .. '"' ~"'P'" mm"" .. 
~­
DISCliSSION 
n..:, " ''''''')' 1""""" h= .. «f"<""''' '"' ""o;."" ... of.,.. ,fIO,,, ro 
d=nb< .... ¡"ooi"", ityof"'lm""h 1'"',.;,., •• 1 11-< ........ .,. f .... " In M,';",. ;" tOd 
...., 10110,,,",, VOC ,~,~ · .I """" ~proo<h (o« N",_!'ono. <k Lro. oni 
a....¡¡,.'y 1010). """oI<rin~ =""llocoI . ... ; . u.., .... " yoll<)'ofC.wro c;¡"",,,. 
In .. ~ SU""y ... , =",okd 15 >p«'" 01 h<lm .. ho. bnn¡jn, th< .... 1 ... mi>« of 
h<1m".o '1""" "' Cwtro C\i.."" fro ....... t<T f"",,, '" W . Mo" .f"" ''''''''"' .. ~ 
""bk"'lo= ~ """. Ioc.loy., Ioo.t «<OOili. WOlo ,'" ""pO''''' of .,m< "'.." i .. 1o 
=- 1<·, " I""".di .... ¡< "- '1' .. ""',l"""'I'Iu.I .... S""- "' .. ond ~II""", 'P. ). 
" 'koch ,,"W'" ,h. roO,,' ... . 1 """" 'P"''''''' ond ""''''' Ioxonom" .. " " 'o ",,"'I~ h 
'"'~ "x""""'o< <knt.y . • 00 ........ ~. CJu."'CUM<,_ ",-".ricnuU, ,,'0..10 ,.,.. ...... 
• ,.;& d ,~rib u'",." th< N,_"ol "', .... frum ..,.''''m Mu, .. tu Soudo Am<rio. 
 233 
 
 
 
i5
ll
"
-
.
1l
g,
 
..
 
q
,
;
¡
 
..
 
,
,
-
..
 
,.
-r
-
-
',
é
l.
 1I
-;
r 
Q
 
~ 
tí-
~ 
"'l
o 
¡> 
~ 
'" 
~"~, 
¡' 
J 
i 
~;:: 
O'!l~J"~Z
W 
~"'·2" 
" 
.. 
" 
~~-~i;~~i~"'~~~,i~~f.=
' 
¡.w.~~t 
if,qli!
'
t~,!,!tHl 
!
í
'
¡
 
i"
-
<
'<
 
~.:r 
~'
l' 
L~ 
¡ 
i
.
;
 
i' 
ii'
 
E"'-~":"'1" 
'~2 
..
,:
 
3
:Z:~;;
'
:::-~ 
~ 
-
i
!
'
:
:
'
;
r
 
.~ 
~ 
[ t
 ~ 
~. 
g 
~ 
~ 
j 
~ 
r 
:. 
t 
~ 
1 
l 
l 
-~ 
l 
~ 
~ 
~ ~ 
~ 
r(
 
8 
';;'l2-
~,
"
.
"
;' 
~;¡. 
__
 
;
.
 
'!
' 
¡
',
" 
if
.9
, 
I 
,
-
·
'1
 
l
"
"
"
 
! 
_,
o
. 
~!Jlf" 
~ 
a~!
'
'='¡;:'''-E 
t-
S-
¡¡~~-; 
'>~if"~"" 
¡;;::
.
~
.~~
,
t
.
~~,..~.:,,~
-
-
~ 
r 
[ 
~ ~ 
l 
~ 
[ 
~,~ 
~ 
r 
~ 
~ 
! 
:: 
~-
f 
~ 
~ 
E
 
.~ 
~ 
t= 
~ 
8
0
-
"
[
 
~l_~'~!'-!C' 
•
•
 
.¡,¡a.fi-~; 
.. 
=r~ 
~ 
.. 
~~~" 
~""'~~[·h.
" 
~ 
~,. 
;r
 
8 
t 
! 
~ 
~ 
~ 
g 
JO"
 
1 
;' 
!.
 
-~ 
i 
1 
f'· 
~ 
~ 
; 
! 
,¡:
 
~ 
¡r
 
..
 
:s
-;
 
.. ,
l"
_
a~ 
"~!'¡ 
o.,.--~, 
.~ 
:<
. 
..
 
r
"
l"
"
 
o
-
"
l
O
-
tlt~.~;¡~~;;¡(~~il 
i."i~a.:f~ 
'<
 
" 
!.
 
•
• >
 
~ 
il 
!!..
 
'i1 
1 
I 
.!l 
"-
a. 
f 
l 
~ 
41 
1. 
' •
• 
§ 
.,.. 
r 
l"'fi-¡~~¡¡~~
= 
~~i
-~.8-2{.!~"~[
-'" 
2
C
 
'5~ 
~.
'-
"
' 
~ 
a
;
1
 
,
'¡
 
,1
-,
-
"~-"-,,,~,,,,-
"
1
-'
, 
, 
" 
a 
":<~oj(;¡::: 
,
"
"
_
 
~
h 
il.
'"
 
1it·~-~~a."~ 
... 
8 
~~ 
..
 
f~"-
f ~ 
~ 
11
 !
 1 i
 1 
t 1
 l~ 
·f 
t 1
 r ¡
 !
 1
 ! i
 ~ ~ 
1 
~.;¡ 
¡¡-~!;r¡¡l~ 
.. 
~ 
~ 
""·!f~S 
' 
•
•
 
,
[
;
r
 
r""~ 
, 
, 
velas one pecios of Homalometror were recognized based on a combiation ol 
molecular and morphological data. Inti espect, molecular date wee instrumental 
“and necessary to establish more robust species delimitan criteria for these helmint 
pecis. Inte case oftbe digencans Crassicuis pp. we recognized lineage | from 
Razo-Mendivil era. Q010) (an undeseribed cry species) ss paras 08% 
canagatats, adC. cichlasomae (sensu lao) sa paras OE múncllsi. ln 
omalometron,scquences of te FTS and 265 nucicarrbNA were used o recognize 
tt our specimens actual correspond vis 4 pallidum, species oigially described 
from fndadid in severa parts o North America (Hoffman. 1999), The record of 1 
pallidum in endemic fish species in Cutro Ciénegas (Gambusio marshi) poses an 
interesting question tar deserve fur investigation to actually demonstas they are 
«omspecifis, or hey may represent epic species, but other molecular murkcrs such 
as COL ae needed to have conclasive dat 
On sl reuals that some tspical Neotropical helminth species vic are part 
ft biogcographial core fuma o characins and cichlids were found, eg. he 
digencans Crasscutscchlasomae and Crassictis.(inege Y) and Rhabdochona 
Adri as paras   es of cichlids while Creptotrematinanguirrepequenol, 
Characihecium avstaricensis, aná Procamellans neocaballerai in characns, 
Likcwvise, some typical Nearctichelminh species were found, Heli species wit 
Ncareis afitis recorded here a he monogencass of th gens Salinas, th 
Aigencans 4. palm and Microphallx e. opacur and he acamtboccplalans 
Leplorhynchaidesthecatus and Pomphorkonchus hulbocolli Monogencans of gens 
Salseginus have been recorded i he Nearctic portion of Mexico in guodcids and 
pupfishes (Maninez-Aquino et af. 2004, 2007: Mendoza-Palmero 2007; Martnez-
 234 
 
 
 
",~ 1I .. "'"' 'f'O<"" of ''''_t-""", .,,'" "",&",,«1 "-<1 ... , ,,,,,,,,,,,0>," f 
rook"' ... 'OO """""""",,,1 ol __ l. h ' <>f'<'< """""1 ...... , "' .... """""""",1 
...  """"""Y '  ........... """" ...... ,....,,,. d."' .... "'" ,n""" r .. ..,'" ),.I ".h 
'1'<";'" 1".., " •• , ur,),. i""""", ="",,, 'PI' .. ~ . , ,,,..,,,,i=l ,,,.,, 1 l  
u · ",j,"¡1 ".1. {20IOH" .... <",ril><d ''Yf'''' '1'<"".) .. . ~ .... " of 11. 
" .... ,p,." ••. ...d C. ,HI""_{...,,,. ""'1 " 'I"'''¡'' 01 11. "';"'~¡; . 1" 
11""",1"""" ..... """",<> .r"" I S .00 18S ... <1...- ,DS  «' ><d ., t r ",;'" 
tIu< .... ~ ....... orno. Uy '''''«f'''''" ..-oh I/.I'"II;J .... . "f>«i<> ... , .. lIy "",iI><d 
rn  tw.Iul'4< '" =<.-.1 ... rt. r ortk m",,,, II ffnw>. '19). k ",..,..j Df 1. 
,.,lIiJ.",  , " ...a. k ~,¡, ,....,,,.  e ....... C;m.~ I o,,_~. "",,,~.11""" "" 
int<",~ ¡ ~" , ,,>t.," ,bot O<><n'" urt'" "''''''fOt.,. l  ... -.u.lIy<l<monol,,,, '),.y ..' 
"''''f''<;r~ . .. '),.r mor "'f'<"'''' , crl1"~ ~i<> bo<, t'" oI<c"lo, """'"" ""'  
.. Ol ..., «<I«I .. bo" ,""' ....... .t__ 
o..- . udy ",· .. h '" """'" ')'I'k,1 N<o "",, ~ ~ od ,"' O '1'<" .... .. -h"'o "'" "'" 
of.., b""l!<o~hi<.1 ,<>« ..."".r ,.....,¡", . ,.l< k li'" = d. '.J .. "" 
i" ", .., r..,i.-.,;'- ,H,"",,,,,,," "'" """""";"p. (1""." 1) ...d N¡"'¡"¡"¡"'"" 
/.¡JJen· ..  .........f mhbd ~ ~-I"k ü'P''''''_''' ~g.;""_, .. ". 
/oo"",i1¡'_ .. ,,,,,,,,,,,.ru. .00 roc_II",,,, ."""¡,,,JI_ .. , Iw-.. in>. 
l  ... ·...,. ""'" ')'1',,,, 1 N,.,.,,", o. .",. ,_'" <<< r.-I. IHm",h op«"" ",ito 
N"'IT'~ ,ff "";", "" .. .Jod ..., "'" to. "", ... "", ... r,),. 11"""" a".p"" ti>< 
oi" ....... 1I <dl;'¡".. "'" i""'''' ll=<f. .,., ... ...d "" .. ..,Ihoc'l'_ 
u"",,"¡,,,,J.oNJ,,, ,..,..."" ..... o..pw,*¡"d..., b llxoroll;. """&, ... ,. ... r"" t"'"
Sal .. g ..... fw," .,." ,«onl<d ., ""  .. ",", ~ 01 m." ,".,.,..., ... "'" 
l"'f'fal><.  .... ;,.,' _ A ~ " i"" ....1. 0... 07; mdo,.·P. 1m<ro 1 07, ""¡,,,,_ 
velas one pecios of Homalometror were recognized based on a combiation ol 
molecular and morphological data. Inti espect, molecular date wee instrumental 
“and necessary to establish more robust species delimitan criteria for these helmint 
pecis. Inte case oftbe digencans Crassicuis pp. we recognized lineage | from 
Razo-Mendivil era. Q010) (an undeseribed cry species) ss paras 08% 
canagatats, adC. cichlasomae (sensu lao) sa paras OE múncllsi. ln 
omalometron,scquences of te FTS and 265 nucicarrbNA were used o recognize 
tt our specimens actual correspond vis 4 pallidum, species oigially described 
from fndadid in severa parts o North America (Hoffman. 1999), The record of 1 
pallidum in endemic fish species in Cutro Ciénegas (Gambusio marshi) poses an 
interesting question tar deserve fur investigation to actually demonstas they are 
«omspecifis, or hey may represent epic species, but other molecular murkcrs such 
as COL ae needed to have conclasive dat 
On sl reuals that some tspical Neotropical helminth species vic are part 
ft biogcographial core fuma o characins and cichlids were found, eg. he 
digencans Crasscutscchlasomae and Crassictis.(inege Y) and Rhabdochona 
Adri as paras   es of cichlids while Creptotrematinanguirrepequenol, 
Characihecium avstaricensis, aná Procamellans neocaballerai in characns, 
Likcwvise, some typical Nearctichelminh species were found, Heli species wit 
Ncareis afitis recorded here a he monogencass of th gens Salinas, th 
Aigencans 4. palm and Microphallx e. opacur and he acamtboccplalans 
Leplorhynchaidesthecatus and Pomphorkonchus hulbocolli Monogencans of gens 
Salseginus have been recorded i he Nearctic portion of Mexico in guodcids and 
pupfishes (Maninez-Aquino et af. 2004, 2007: Mendoza-Palmero 2007; Martnez-
 235 
 
 
 
",~ 1I .. "'"' 'f'O<"" of ''''_t-""", .,,'" "",&",,«1 "-<1 ... , ,,,,,,,,,,,0>," f 
rook"' ... 'OO """""""",,,1 ol __ l. h ' <>f'<'< """""1 ...... , "' .... """""""",1 
...  """"""Y '  ........... """" ...... ,....,,,. d."' .... "'" ,n""" r .. ..,'" ),.I ".h 
'1'<";'" 1".., " •• , ur,),. i""""", ="",,, 'PI' .. ~ . , ,,,..,,,,i=l ,,,.,, 1 l  
u · ",j,"¡1 ".1. {20IOH" .... <",ril><d ''Yf'''' '1'<"".) .. . ~ .... " of 11. 
" .... ,p,." ••. ...d C. ,HI""_{...,,,. ""'1 " 'I"'''¡'' 01 11. "';"'~¡; . 1" 
11""",1"""" ..... """",<> .r"" I S .00 18S ... <1...- ,DS  «' ><d ., t r ",;'" 
tIu< .... ~ ....... orno. Uy '''''«f'''''" ..-oh I/.I'"II;J .... . "f>«i<> ... , .. lIy "",iI><d 
rn  tw.Iul'4< '" =<.-.1 ... rt. r ortk m",,,, II ffnw>. '19). k ",..,..j Df 1. 
,.,lIiJ.",  , " ...a. k ~,¡, ,....,,,.  e ....... C;m.~ I o,,_~. "",,,~.11""" "" 
int<",~ ¡ ~" , ,,>t.," ,bot O<><n'" urt'" "''''''fOt.,. l  ... -.u.lIy<l<monol,,,, '),.y ..' 
"''''f''<;r~ . .. '),.r mor "'f'<"'''' , crl1"~ ~i<> bo<, t'" oI<c"lo, """'"" ""'  
.. Ol ..., «<I«I .. bo" ,""' ....... .t__ 
o..- . udy ",· .. h '" """'" ')'I'k,1 N<o "",, ~ ~ od ,"' O '1'<" .... .. -h"'o "'" "'" 
of.., b""l!<o~hi<.1 ,<>« ..."".r ,.....,¡", . ,.l< k li'" = d. '.J .. "" 
i" ", .., r..,i.-.,;'- ,H,"",,,,,,," "'" """""";"p. (1""." 1) ...d N¡"'¡"¡"¡"'"" 
/.¡JJen· ..  .........f mhbd ~ ~-I"k ü'P''''''_''' ~g.;""_, .. ". 
/oo"",i1¡'_ .. ,,,,,,,,,,,.ru. .00 roc_II",,,, ."""¡,,,JI_ .. , Iw-.. in>. 
l  ... ·...,. ""'" ')'1',,,, 1 N,.,.,,", o. .",. ,_'" <<< r.-I. IHm",h op«"" ",ito 
N"'IT'~ ,ff "";", "" .. .Jod ..., "'" to. "", ... "", ... r,),. 11"""" a".p"" ti>< 
oi" ....... 1I <dl;'¡".. "'" i""'''' ll=<f. .,., ... ...d "" .. ..,Ihoc'l'_ 
u"",,"¡,,,,J.oNJ,,, ,..,..."" ..... o..pw,*¡"d..., b llxoroll;. """&, ... ,. ... r"" t"'"
Sal .. g ..... fw," .,." ,«onl<d ., ""  .. ",", ~ 01 m." ,".,.,..., ... "'" 
l"'f'fal><.  .... ;,.,' _ A ~ " i"" ....1. 0... 07; mdo,.·P. 1m<ro 1 07, ""¡,,,,_ 
 236 
 
 
 
Aqu ... & Apn .. _AgoilH !OO:i). ~ 1010 l' hM'-"Ili .. I'-'dr'" 10<. f"",",.f 
""'.,,~ ~ · .b ,,"'''' "",<do in"' .... ti," p""!" (lloilin>. 1 '1\>9 , Pm-L_ Pon<, <k 1-""' " 
al. 2Q()g). n.. ""un!.f 11. pallNJ_ .... .\1~II., d. "I"""'~""" , N"""", 
¡"fko."" ",." bott. 'f>«i ..... f.,.,..,j ¡" .. "'" "f>'<;" off ... bw_, fi<h,. fmm No.do 
"-,,,, 1= Hoffinoo. IWI~ '-«'''.J'y. """""'''' orM~II",d ._"" 
.............. "'" ''''m'' ....... 'W""" .",,.¡ ¡" ,h< ut<ru~ """"¡lo 'yrnm,,,' ,,1 
"" .. .,-"j o .. ,-y Ioc .. ", en ,j, .. ,.1 ,..¡ _, .. ~ul .. po>rt..., """ obon-,''''' >till ti-.< 
I"'"'-booly obor<. "' .... booly ""¡"". ,..¡ 'n< .. F"""'" .110 .... '" 10 """' ¡"<ly 
<kl""""" ÚUO '1"""" Dfd,~""",- N"" .... "',.,> '" tb. ¡o""h'y Ioo¡';'~ f., """"" 
".... 'p"''''' ..:"', .... ,,",'''''' .rtl-.< "," oo.. '"" ron"",,'" .. oh ,h< di.""" .. of 
ti-.< ~" .. ~ l..k<w.,. ,,,,,.¡, of L Ih"""" 1"' ..... '" """ ""lud< 6 """ ' p«;"~ 
""",>t .. , , lo .. ",",,;f""r. h'w"·<r. oo.ly IV"'" r"",1oo .¡ L ",,'"'''' ~'" ""' ... 
...... tt., """im< ........... fro m ti-.< ""'51 ... ofM'""I""'" .. ¡ .. >Niu. ,,""" 
. " .. ¡ly fo .. ·.0 f .... '"p m,,,k by L,,,,,,,,,,,,, uod V.oCla" (1'149) . .,·tu .......... """ 
oIItuo.¡¡h 1. <MNO" u. "1"'rt«! ¡rom , Ion, l i~ of""" ~ ,h< !<molo, do _~, 
<u' ...... , .... ... ".,ty.rtl-.< ¡, ..... , .... ...., _ """"', ..... o..- oo..n",., .. . rtb. 
'1"' ''''''' ~~ ,001o..,od mm>too"" , .... 01 .. ",,,,.,,, _,,'h< "'W~'""' o¡ 
"""'" ac,hon .. 'tu ¡",, ~ 1'<0.0'" • do., . _, ...... 01 'O" ",,,,,,iM><q>lu.w-. ...... "",¡"-",, 
iS" .... '" ,,01. 1001). Th< "ron~" ,..., orho.< """,f,city ~ ,,¡,;o.«I by ti-.< 
.. _"","Ion Am_ ... "''''' d"","¡, .. ""i~ " 'h"h ,.... t..m «,ot<kd .... , .... >Iy .. 
I'"~(.h< •• (Ib. V"'" C'pn ...... (G""ia_I'n<t." .1. 1010). .... by 0..,,,,,,110...;,, .. 
""","'ric,,,," ...... ~k '1'1"'-" "' "" onl)' ....,<0 .. '" " 'itb ,ho",,,j f~b.. oftl-.< V.,,, 
A ,~".ax i"'<n<lou·f,,,",o" 01. lOO<, F..-"'" ,o..,.. both b.lom .. b ",ocio. con lo< 
 237 
 
 
 
ro ... , .......... """ of .... ¡.;,,~ .. c"'. r... ... of ,)'f',¡",.¡" .......... , ............ 
"''l'",';"dy 
n...~ .. m, ,ornobo,., .... , C .. ,"'Gi"'p . ...... i, • ~b ,,; "''' 
",rt" ... >tu", of N<Ot<'~ .... N""n'l' i,,1 1 .... '0"l"'''''''~ ~'¡';'h ~ «11«, .. ¡" •• 
o.bo" • • ro ...... 11o~ · " · ,, ..... ~I DI .ro"""", u f ,ho ftilo hobo".h &.un.t ;" ,ki> 
"';"'" ......... ,ft." ,Ita! O I .... K Ii>. Ito.o~ Up ., dot, ... mokm" '1""" ofholnuntb 
ha," h«n =onk<l ;. tb .. .... , Itow,,· ... V""" ,.fonnoot"" ... y.oo ... " •••• uf 
"}~ ' K 'f'<"'''' (moopholop,.11y , im ilo. ¡"', ;,,,,,,,·.lly d .. ''''dI1 .... P .... , -P""' ... 
león &: o.,odiI>'Y 20101_ Lilt,~, .. , lWttw.- ... 1)"< • • ,,, "'1"." ¡" uro.. tu ,,,"oli" 
"" ' "",,,,,m~ itknutyof"" "'''''1'''''''' klm"ft«l .. ,,"')fl'< .......... ; , n. '1' 
!mm lI..ricltlit" .. ;'.,.'I,,·¡ ond 11. ? ~""l,)~"""" (du.h proNbl,· holon¡ ,. '" 
...d=.-ibod ;<"". ",";'"_hbo",, ~'" ""mnL~ . noI ,ho ....... od< _ ... 11,,_ 
'" fmm .... _" ... uf le,""'""""",, 
l><>r it< .... &." th.o, .... C .. tro C ;m.~ " "'f"'. ¡, .. . " ... , 01 rnd", ..... "'" 
di",,,, "'''. no """,,1 ho'-" ... ,,"" ,okc" " S m,,J,,,_ ro .. ~ . "" f""'¡ .. 'OH _le 
""!Ocb "'rnXoon." .... ~",n maok b y r .... , _po"', ... l<Ón'noI Chootdlu-y 1201 O) 
",1», ¡,...o "" .... " ,,,. uf"" .. ,-....,.yor .... m,oJn._ fi'" 'dm_d .. , 01 M .. ~" 
V"""<d ~ .. 1010, ..-,¡uod ...... """"''''' "'" ""'''''''''' . ... , .... in""",,y ~ " ".n"~ 
"""",kt.,n ro. ..,., p ....,.~ .,.¡ ¡¡,. tht • .....,.. f, ... ...,." .. 1 n.",1 .... ,,,,,MI be 
"'f""" ID h< r...,noI. TIr" ... 100,.. al., , u",,, .. d • _P" "'''~y ",,,.1. """""'in¡ 
........... '"'11<' """""",, """1" "'''''' ul .... loo .. ""," .. m ~'iIb ,ho ,hoK' of 
"",..,..;.., d, .. ",~ . o.>«I.n '''_ ""R·. r ... ,,,",, ...J ),¡<Imlo"" ..... .. ..-d .. 1o 
mtw." .... o;oo;'=;,y "''''''_y. l. ,b6 "' ...... oh" ~-...1. ~"',,>k> fu_, d .... on 
"" h<_h f ..... of f«<ho.'Otff r.,¡,.. ¡" • "<ry ""f"' ..... "'""' of .... ru_ytlw 
 238 
 
 
 
hao b«n ,.".«1, .. ,dd ro. O" ..... h 1"'"' ¡"". 
l_ t"", of ", " ~ >¡>«"" of l,,,bw .. ,, , ... '0 h)'lrolop,.l .Y'" ......... 
o,,,.,,,,d u-.q.." .. l, .. M""o. n.o eu..ro O"", .. b";n en "", .. """1"'00.00 
<U""'~ Y' m ... 1 .,trodoccd >P«'" 01 f.n. ... ~-dl .. d,m" "'1""" .. " ........ " 
"'" b<foW>l (C""""u_A"",""" I m, Mm' '" M","":>O(1). n .. inIrodudioo "'" 
¡.,,,,,,.!<d , o., ,~I; >hm< ", .r ... "" ""',, hdrnen'" '1"';"" .. th< d.f<"<". 
C ....... "'"'-"'-'''' ....... ,'" ,<>too. B"'.ri<>«pJu>J.. ""*''',,,,_,., wlx' .. , 
""~ . W ..... 1" .... · .. " r" .... ufCwtro CK'''''p' .... "' ;.-, ...... "1""'''''"11 
'ro"", .. I".. fo< th< "' ..... k "''''''' ..... n . 1 ... " r~ h 'f'<"n Both o., lrrUntb .... 
"' .... ,,,,,oduo« lo h)do-olo ~ ". 1 'Y" ..... of M,noo ~·.tIu " tI>< ~ t.. .... and """'" , 1><;'-
..... bost .,...,r",.y and ¡t<"" , ... "'il.y .. a ~ .. difk" ..... ,;.-.-.-.. .. 01 00,,";""'" 
u... allo-o' ,h<m ,. tb .... , .... ""'"." ""~ """ .... d.~,"',"""- I .. n~,. ""y ",,"'¡Iy 
." .«oro" p .... ;,~ "' ; ............. &"",",,,,,, fi<h,....,,,,, oc M ... .,. \S<t..l, &< 
SoIgodo-M._ 1000, S. lpdo-MoIOOnaOO &< p...w_liop<z 200), C"',,¡"",_ 
C""'"=o"..J. 2OOj; I'in-z_P""", <k loóa '" .1.l007. lOO9. :W'O; R..¡..-S.b .. ·h<z & 
G"dt¡-';"'o 1000: A,¡uil .. -Apd..- ",.1. 20011.1010 •. 101<»0; 0...1' .... 1. 100'1; 
M<n.l .. ",.i 1010) 
11>< d.,. , I»! ~ . , "«><nO ;, th~ "''''''y "!"'''''' • f'IT'''""''Y """" of 
inkmru ............ "'km .. h "..-, . .. ". 01 c....... C;¡"." . ~ <:k..-1y. """" ..,.¡ ... .. , 
n«OOl .. ro .... ", ti>< ""'<nO")'. ho",,, ... "'" fnd .. p' ,_rib"" .. ,o., "', .. '" 
de.mp''' •• f"" 'p";'" ""bn<.. p ........ of"" &,,¡,,, ... ,, fi ... "'lminoh r .... "' 
....... m M"~,, r-t><u!.o-Iy I'rurn ti>< ........ "" "I' .... .,..¡ '" .".;, .. " ,h>. "'fu ..... '." 
;. ''''y =1101 lo f"""", , .... nt.uo< ,, ;!h "" <bao!" ... or,,,, ",,1""''''')' ,00 
boo",,¡t<a¡>Iu<oI r.' .. '< .... th .. o<t""""" '" ""',-" .... "" .""" ...... 
 239 
 
 
 
REFERESCfS 
~,Io< _ """w R. Ce"""' .. _M' ..... lO:. Slopio-M"¡........, G (1003,. PU"""'''l' 
A .. I)' ... of .. "k"",O)' IrAE! of M ... " .. hyJro"T'" ... .., b.oN "" bckn, .. h 
P"' ';'''' 01 &, ,,¡,,,~,.,. f""', . .40"","1 "III"'I!"W"'I'I ... Jt. 1 86 1 _1"2. 
~,¡" _ A",,1o< R. Jo .... Ah.-<'" A. Pha_P""" ... l<óa G (WIOo). C...oo.. 
H.otIIOOC<!'hohd ... II",h~, """";/"1(-' Yznoll''' ' 1930, N ...... ...... 
RO ..... od""' ..... k """,."... .. ,-../,.,,, Mo'",,"<C O<>d A"". 1911 N .... =..--d. ro.-
......... 01 p,,'¡'ko. M"KO, and , ,,,,,,. r"h bo ... O .... w, •. 431-4l8 
~,¡,, _ ~,Io< R. M ........ Aqu ... A. P"" ... P""", <k l.<ón D, P¡",. ltOOri",,,, R 
(200\1) . D,V """ 1I .. <>""o,iclo<. C ......... ,,"',""""" .... , ""',.",,,,.,,,,,, D,,'-;bu_ 
,,''''','''' for M",,". ,."" ..... ,<=ni .. ~ ""JO,!,h" ~ ... _ .... ""'1'. O",t U" 
S,3l 7_1l9. 
~,¡,, _ ~,Io< R. Ro ... _V.1<kz R. M ... i..,,_Aqu_ A. P¡",. R<>dri",,, R, 
¡""""'II'",_Domi"p" O. P¡",_I'c",,, oc l.o. G (lO lúb). H,¡." .. h " , "" Df .... 
'lI'"",d r»h le ... !"",,,.., 0,"0"""'" C",",- O"""') fmm .... ~ p",u.. ""'. 
Nooh ...... "" M, .. ,o.IM";.'''Iog'' n . 1l l_llb 
~,¡,, _ ~,Io< R. Solp>o.-.\.dd" ....... G, C_ ..... ·MNliN R .\ .. "in<z _A~" "'" A 
!lOOR). R ~""',.oo <nd",,~m orl><lmiroh """"'. of fr<dro-.... r~b ¡" M,xko 
8iol&g;'-'1 )".,..1 of'"' U_"'. SOOffi' ~. , . Jl_4H . 
B ... · o-U" I I~ M. 1"""", r 1\ '1111). Roi .... ~ir<;,;.,¡, ,tI;,-""",)'" ..... i,'"'" M ... 
C, II"m. 19 11. Anol" J.J I.,,;¡ • ., J. B;"Jq;;,,- u..;,,,,,iJaJ 1k",,,,,I.l.";"',.. J. 
,ti"' ..... Seri. :rootogia 53. 19_16 
 240 
 
 
 
B ... AO. t.. fkrty KD. Lo<.< l M. Sho>tai A W ~ ''I9n P" .. ' olu.,. m"," ""<>l)' '''' 
"" o"'~ '''''''' ' 1>1",01 .. " .1. ", .. rt.d . .k"",,,,1 O¡Po""''''1ov . , . ""7 __ 
Cuprta-M ..... ¡..., lM ~20IOI . N_Iod, p"'""i", o[fr" ''''''" fi ,. i • . ' ''xiro K,,· 
10 '1""'''' M"'i!,,"''''''¡ J ulrir.. .... AGT '.,h.". S. A.. M .. "". D. F 
C,,,,1rau S ~100-1). r~,", ;"" ..... y"""''''' "". ".,. •. lo, I<odino G. !knu.on T. d, 
V;", A , "",,,'0 " So", ... G. ro. &.j. ,1 <h ... "". El ",HI_ d, "" "P'" J, C .. "'o 
C¡;o.g"'- ,,,,,,,.to C...t..¡",..., ... Ct. 1t"",- C ..... ; ... 1'1'. ~ -I {lS. 
C""n" ... An¡"~" A 01 'I9\j). N< ... «ro" J¡ of"" .... ,IJId ......... .. r.m-. la., (Mil'",", 
1774) (G ... ropod .. Tbi ... <dtt);" '"' Cu"'" C;.".C" b";,, ..... oh.o-ibu ..... ¡" th< 
","" orc".¡., .. , .~b~" . T'" &"""""',,,, Nolorol .. ,.). 28.!_1!\6 
E'V"" k ~ 1%9~ Tto. ",;ub¡';'y of.....,,,,,,m 1"",-,"'''''' "' F"""rioJ ....... of 
lo ...... """"'V ....... . Fol .. P.ro,'IoIugk<, l •. J20 
Gud .. p,."," L. Goo-<i. _V..-d. M. M,odu. -Gorf .. , B. P<ra_P,,,.,, ... LoO." (2{lIO) 
CIo«I.Ii>< of ,to. A< .. "",,<¡,Ioo" .. ,, ¡ Id , ;r~ """0"'" of M",,,, WoI",o 2.", 1_ 
Gwja.-do-M.rt;""z " ~ ''Ill<1 "'d,m ¡" " y '''''''Y of p.,..;t<> or C .. tro Cói"'i'" 
C".¡.,¡¡ ~ M,,~o . .I"",..,lofl'" Ari,.,.. ·N,,"¡" Ac",ü .. vo[Sri",,, " , II-.8J 
("""~IT<z-<-Obm- . A ~ Puhoo_fio.-<. G. M • .a. S. G.,,,,,..()~.,,;,, lC (1005). 
I't-=o>o .. ... B"~",.w'lap",l'; V"""",,,," 1 ~) 4 IC,~"""'" 
Botlnx<¡,hoI>lx) '" F""" <k M"".lón. 11.&1", M<' .. m . lI"'roh;oI6gico " . 211_ 
281. 
lIoffman G L (1 <¡Ol'h 1'0ro,;l" of ,'IoriIt A .. , ,;..-[n'¡"""" ¡,.¡, .. , 2.J d (0",<1 1 
U .. ,..ni'y _ ~ ,_ .. NV 
 241 
 
 
 
Ji"""" . p, e ....... .., G. o".",.., C 11911). T __ <l< f>«'<' ooh..,uioolao ... 
C~.~ Mi .. ,. l. IJ-lri,../W" lviJI..J.Ji .. ~ " 'f'- "" . (1', ..... _, Ik ... ;..-.... ' 
po .......... dd";'" md<ro"",. <l< c., .... c;<m,s"_ T"" ,<;o.M"",,,,. N ... ",I", 1._ 
409-41l 
~"' - Ar¡wnodo R_( 11I91) M."...I"< """" .. P"'I"'I"'. Y .. '"d .... n, po'''oo, 
......... 1<. " I" .'m. A_G .T_ Ed .. ,,", S."" MhKO 
ün, ~ · """, DR. V .. CI",,·. IU (1 .... 9). Do_"""" .r L'P •• ri,~< .. .,¡" I ,,"~"~ • 
"""""" "'''''~ ' " pan"~ ;" f"""~ ~"'-.o !>lid""'" ,\'a .. ",liJt 11 41 1_ 
. )1. 
M.m. IJ. Morti..,z M (<<k) 12007). ü,..(jEJ i.,-"""",", .1", ¡O"""", Q Jo 
,","¡i,...,~ .- Pri",id"",,,~ M',i«>_ 1 M T "..('0""",,,.(;[C1 _ AridA""""'_ Tho 
N .. "", C"""""'",')'. M"i,,, 
M...h pe, ''184)_ O .... ufCuono C;¡""P'- Coahu;a,. M,,~u.- PmK<. ,k,¡""u of"'" 
~ ri""",_ S",.d" A""'",,!, o[ Se .. "", " . 1_1_ 
M"""""_"",,",,, " , A ...... _ ~..., ~ (lOO!!} lid ..... "...~ ... of'" """r~ h 
0-";0"""" .. m¡ (P,m., C)T'ri ....... ,furnr'). ... nokm" ¡...te ... " .. fi.h ¡rum 
Noob_C. .... 1 M,mo. '''I .. '"~a .! . .(lI _jl. 
M"""""_"q'"", ". SoIpIo_M.ldono<lo G. A"'¡!ao- _ "~¡.- R, C~C .. n ",. G. 
M,,,d,,,,._P.mo-o CA 120(7). IHm,,", 1"""'.' oo"""""".of a",-"""""" .oJax 
.... C. 1""",lu (_<OC, C""¡,m<, ","."oc h.h ..... " r ..... from Do""'&"_ 
M<XKO_ n.s,."In.",.,,~ Nao".I", SI. I lj_,.lI) 
M"""",,_Aq'''''' A. S .. pIo_M.W.no<lo G. A"'¡!ao- _ A~J. R, C~C,",,,,,, G. 
Ortop-Ob,,,,. MP (200<1_ IIdm ""h ~ .. ; .... (C¡.,,,.lrlMH .. """', .. (Pi",,, 
 242 
 
 
 
G",,<I'"'''I.''' .... ""'"' fr<>h",,,,,," r,.¡, OTo m ~ Chopal .. )'1",. M"", •. ;....n..1 
ufP""" i~-", ,89-l<00. 
Mdf, GK ( Ins). lif, loo . .. ., p ........ o, G."¡"". _,,., Il'o<óli"",1 from Cuotro 
~ Mm",,_ Coprio "'5. i'lt-90S 
Mml .. O. Ssl¡odo-M.1do<wlo G. C~~ I ...aujuo J.~( C"'_C~ G 
(1010). 110m,,". pan"" .f"""" &,'¡'n' .. fidoo, from O.jo. Colo_ s., . 
.\1,,", •. 7-=. 1311, -14-50 
M<OO~F"""., F.. F .. R, ... RG. l.",.", ME (1009 ). Dac'y!o"rn. (M""""""Ok.) 
po< .. ";,in~ ,1>0 ~ i ll •• , .... 9"""-' '1'1'_ (0...«001 .. ) f,om P ....... .,.¡ . oo<i><M, 
.\1"",,,, • """ -""'"" ., Im.pIu>rod .... r ,,,,j , ""'1"'...,) lo. Ch."',.; ...... ; . .. "- ""-
.1.,,,,,,,1 .¡ P"''''''"'''J;)' os. -1M s. 
M<OO~P.m.ro CA (1001). M""" ~"",, po<lo.,,' "' J'<"""' ... ubf .... ~;, 
C.ood,"'" (P ..... , 0T<inotIonIi"""",) "'" tE< .,,;:~,¡, "' ... d ....... "O\. , ,,,,rifKO 
IM& <1-..,;'). ro."oOO '" C.,." .. Biol tW,, ~ U.,..rnd.od N", .... I A .. ónomo <lo 
M<OO~P.m.ro CA. A, .iIoo-_A", il" R (2001). R"",d.f Urock;¿";'¡,, 
,,,,,_¡,,,,,,,, .. Iop>oo,i. lútt>lr""¡ v"' ... , ............. , 2OCJ.I (M""",,,,,,,, 
o.,;,'Y!OIY".1o'l rn.-n • f",ho.-"", f"¡' .. M " ~ ,,. P",.,i"¡"g;}' R",.,," IOJ, 11J5-
1B6. 
Mili", RR, .\I¡""~ Wl. No" 6 S.\I 1 1 00S~ F,..m.-_ r61d " f .~",ioro. 0 " -",,, 
u."-""¡'y P"" ... Oun", 
M""kky WL (1'Ill4~ C"'tu C""'l" r,,¡,., R,""uch "'-",,-...,j • ..,al ,,,,.f 
do"".)-,-""', bWo ... "". Jo.."",1 _/ IIog Ari"",._SnwJ. Ac"'¡'..,' o¡ Se;"'" " , 
\l_JI 
 243 
 
 
 
• 
• 
• 
• 
• 
• 
• 
4 
, 
~ 
, 
1 
, ,
 i •
 ,
 , 1
 
, t
 
• 
,. 
• 
r , , 
~ 
, , 
l 
, 
, 
• 
¡ 
, 
, 
j 
• 
, 
~ 
! 
, 
, 
, 
, ,
 , ,
 , 
, 
, j
 
" 
, 
• 
• 
" 
! 
¡ 
• 
, 
• 
, •
 ! 
! 
, ! 
• 
• 
! 
" 
, 
.' 
r , 
, 1 
" 
, 
.~ 
f 
• 
r 
• 
• 
, 
, 
, 
, 
t 
, 
, 
i , 
¡ 
• 
, 
, 
, 
• 
, 
, 
F
 
, 
, 
¡ 
¡ 
, 
• 
.' 
• 
• 
¡ 
• 
• 
! 
¡ 
• 
• 
, •
 
• 
o 
, 
o 
.o
 
¡ 
¡ 
• 
" 
, 
, 
I 
• 
" 
~ 
• 
¡ 
, 
; 
1 ." 
• 
• 
, 
• 
• 
o 
f 
, 
, 
.o 
, 
.o 
¡ 
, 
, 
.o 
, ,
 ,
 
1 • 
; 
¡ 
¡ 
¡ 
, 
• 
J 
! 
¡ 
• 
J: 
¡ 
" 
J ¡ 
J 
" 
, ~ 
, 
~ 
, 
, 
• 
r 
, 
, 
• 
• 
! 
¡ 
! 
.o
 
• 
, 
¡ "
 , 
t 
! 
, 
¡ 
I 
! 
• 
, 
, ~ 
~ 
¡ 
, 
• 
, 
! 
; 
~ 
• 
j 
! 
• 
• 
, o
 
• 
¡ 
, 
• 
, 
, 
1 
1 
, 
, 
• 
, 
• 
, 
• 
, •
 
• 
r • 
I 
, 
• 
• 
, 
• 
• 
! 
• 
¡ 
• 
, 
• 
! 
, 
• 
• 
, 
1 
, 
, 
, 
I 
• 
¡ •
 i
 
• 
, 
, 
1 
o 
r 
i 
l 
t 
t 
~ 
O
> 
, 
, 
f 
~ 
, -
, 
, 
, 
¡ 
, •
 
• 
• 
• 
• 
• 
• 
, 
" 
1 
¡ 
1 
, ,
 
• 
• 
r , 
t 
• 
• 
, 
• 
¡ 
¡ 
! 
} 
• 
• 
¡ 
l 
!1 
• 
• 
• 
, 
, 
! 
• 
, 
¡ 
! 
• 
~ 
, 
~ 
~ 
! 
! 
; 
• 
, 
, 
• 
• 
• 
1 
, 
, 
, 
, •
 
• 
, 
; 
" 
¡ 
¡ 
r 
, 
• 
¡ 
, 
~ 
, ! 
• 
, 
• 
, 
, 
¡ 
, 
¡ 
• 
! 
¡ 
, 
, ;
 
~, 
• 
, 
• 
l 
, 
• 
l 
• 
1
 
! 
; 
• 
• 
! 
• 
¡ 
o 
, 
• 
1 
¡ 
, 
, 
'0
 
, 
, 
¡ 
, 
• 
¡ 
, 
¡ 
.o
 
, ,
 
l 
.o
 
, 
• 
, 
, 
1 
, 
z 
, 
¡ 
• 
¡ 
• 
• 
, 
• 
.~ 
, 
¡ 
r 
• 
t 
, 
, 
• 
, 
, 
• 
1 
¡ 
l 
¡.
 
• 
, 
• 
i: 
, 
• 
, 
t 
• 
, 
1 
, 
, 
, 
[ 
.o 
, 
• 
, 
• 
• 
, 
• 
• 
 244 
 
 
 
"""f'h Dr ")pi;' ""'><> ,n Cn=¡,,"," ~ .. ;I=_.(D,&""", """'",,.d, .... ) . • 
pan>>t< Df MMId"_Am .. ~." ,"",I" ~ 1.,,,.,,,,,,,,,1 J .. "",lfo- f""'''''''''I!J, .w. ~1 1 _ 
~ i" . 
k D .... _SOno .... A. Gu"l.-I'ri< .. l (2003) 0; ,,, .. ,,,01 . .. , ... 1.., 1 ",,_ 
Bu<hrioc'PIoaIOd .do"!og.,,", "" M'UD_ M,,,.,.... XXV S....." .. "'""" F", .. 
3 ;1",,.,.. Unmn,doJ N ........ Autb""mo'" Mi,,.. ... Mluo_ ' 9_91 rr 
S . I~M ._ . G_ P ....... LOr« RF (2ooR lb< A,"m ro ... _"""" 
8u<hri",,,,.,,1,,, .... "I.>pa'", A 1""_ .. 1 ,tu-< .. ID "";" ( ... h., .... fi ... 'f'O";" ;n 
M",oo_ B"'¡"g"~II"m"'"' S. 261 _261_ 
s..,t.olz l , .s.lpdo _ ~ I . _ G (20001_ n., "" ...... " .. '" ,.-.l d;,p..-...l DI C ... """",,,,-, 
¡on.....""' (N"'~n.. I~ l .) (0;S""''' U .. «Of>Io>ido<) ¡" M"ioo A """'W_ 
A"mc. • .lIiJl""¡ ,1'.",,,,liJl la 1 ,QOO 
s .......... Ml . N;' .. I D, oro G (2007). c,YI"'" .,..., ... "",.ro 1"n""" ofrlx-noll1'~ 
,-";"'"n of. ho~ly "" ....... ", .. to«pIu.l ... p ...... _ M,*,.'" Eruu't.>' 1 •. ..-...,_ 
4109_ 
S, .... HA, Ku'.." LS_ Ad.m> JS (.o,) (lOOO). P",iooa II,,;'~I;' . - 10, SI,toa",-
BioJ;,~"u, ' '" ¡J" ~"';".¡ ,'ól,I<._ 0, ...... lJn" .... "y ...... , O.fuod 
VOiol_"","', I'M . Ap;',...Mocroo ML. Sol>ol<. l . C .. n.ála_s" " D. Mmoo,"_ 
r.""o H (2001 j . Al"" of'"' 1w1 .. ;.,io",,'.';1< ofridoliJfuJ. ofu .. _ Aca<krni ~ 
,-
  
   SIERRA 
DE 
MENCHACA 
  
   
    
   
SIERRA 
Río 
Mezquites 
   
   
   
20| 0 
25 5 
SIERRA 
DE LA 
FRAGUA ss a 
a AS     
   
 
  
 245 
 
Figure 1. 
 
 246 
 
 
 
eoo< l.o<at.y G",,,,,,,,,, ",1",,,,,, 
,fi¡,l) , Conal Son 1uo.Ilo<¡.oIlu 1 • . _S. IOU91 1 W , C .... I "." l. V<vyd V, ...... U .'Iú06 N 101 .9192'1.' , 1'0", PlaY"" lb.'I09j N. 101 .0 1J9W 
• Chorr .. p,,,,,,, 1~ . 9O'I'J N. 101 .0360 W , 1-", 11..,...,.,. 101 .0 1\10'1.' , RiD M,,'I""" 101 .10)1 W , N......,,,,, I 101 .6%0 \\' 
• N-..1 (lI ,izaohal) 101.1071 \\' 
• RiD "" C,!.m .... (Coo",,,) 11.(14'1 N. 101 .6""JW .. llioonC,k..-. 11(l.\.l6 N. IOI .69i JI\' 
" f'uont, S ... J'" <k In A"" ... 11.(14)9 N. 101.61.11 W 
" Po .. '""'1""'1 """"'" • Pla)"" lU'2J N. 101 .00hl \\' 
" """yo -",",o • E..t,,·oón !~ . 9JOj N. 101 .1191 W 
" M ........ I <n 0..,,,,,, 16.II44lJ N. 101 .1.>41 W 
" Lo_ I .. <m>«lia 20.B4¡j N. 101 .1434 W 
" .... "'1" s.." ...... 20.%94 N. IOl . l2{)S W 
" El Mo¡.,.1 10.9110 N. 101 . I177W 
" ""'"'jo 10.%94 N. IOl . I2l~W 
" C""¡"" h,d. Lo T",1o 10.7\0)(1 N. 101 .0000 W 
W _T,d. 1~ . 7'JOa N. 101.9\1)2 \\' 
" L, f,d .. !&.1:N2 N. 101 ._'1.' 
11 1'0", Lo B«,,,. lUliO N. 101 . I300W 
" Po,," TOo cónO'" 20.1704 N. 101 .07114 W 
" Cam"., ..... Pl.o" ... 2'.9'.0 N. IOlW% \\' 
" Po,. Lo., .. "" 10 .• 8' 1 N. 101 .""80 W 
_2. H _ ~.J 1'.9,011'. )0, .1104 W 
 247 
 
 
 
1>1 ... .. 
AU .. .... di .. " ... ",. 111 
G.""",,," ... "¡i 
............ I .. p. (IWoll) 
G • ..a.,,, ... "¡i 
Lu. lluni-w. (1) 
C-I""", Lo \'0l" yol Vonodc 
'" I..& T« I;" OI 
c..nóno hao .. l. Tod. (6) 
s ..... Tod.(JI 
e"""""""f~_" IS;'¡';",ri. 1 ~14IIG) 
A,(>~"". _ ..... n.' C-I mI>< Lo V" . Y rI Vonodc 
'" R;" <n Cric .... ",. ( I ~) A_ So" "' .. 17) 
Po" Lo e..,=n (4) 
0'!'ri",,11a .. " .. ,¡, P ... o< s..., )ud "d .. Á;"'''' oJ 1) 
IB I O_ll l l 
.. _61 10 ... " 1 
""_61 16 .3lf 9.S 
,,,_61 10JJ/l 
"';_61 1 I.3J / 1 
5.16 10 .31 16 
IU9 1 ' . ~ lI S'iI 
1l 1! / 4 
Rom .. ", lb;' «con.! "'''' do"ribod "l' .. .,oly by ~;I..- - A¡¡u;g,,, ~1. (100\1) 
e' '!'ri""lIu",,'ó,;.,. C-I ""'" Lo Vol" y 01 Vonodc 100 1 ~ I i 
'" C¡'!'ri- a""",, x bijuú."" 1..&11""" ; .. <m>«l'" (S', 
G.""",,," ... "¡i Pumo s..n lo>i <k la. Á"".., 11 , 
Pon 1..& e..,,,,.,. (7) 
L'P" .. i"'<J!~lo'u Rio '" erl.....,,;.121 
M,;,,,p""" ",1 ...... , P"" .. , s..., )ud "d .. Á;"il .. (J) 
,~'.In>p'¡ '1' Rio .. CrI ........ (JI 
e "" ";'M';' ",1<1 ... _, M_.".o 19J6 (1) 
I/,ric"'" ", ,, ,~; a...."" Pri<t .. I") 
I..&¡¡u .. ; .. <m>«l'" (J, 
Rio "',,""" .. W 1 
Po,," 1..& B«"". (O> 
e .... ,,"",;, "'. (1 .... ,< 11 (1) 
I/<ric¡'¡,,,, "'"""l/u"""" P"" .. , s..., )ud", ¡,. Á;"il .. (1) 
e""._¡; •• ' ~.;""P"I.,-, (Jrn<n<'",,""""'o 1913) (1) 
A"' ..... ' _ ...... '" R;" <n Cdcm.n .. ( I ~) 
1/ __ '-."",. ".¡¡;~. '" 5 .. ''1<".,1
0 
''>(4 11) 
G ... Io.,., .... ,,'" lo< 1I",,,hw. (1) 
a....". 1'.""0' ( ~ I 
Po," T....."ru ""°io PU)'"'' 11) 
Mm)" <n t... E .... ;,;" (5) 
M....,,1i,,1 <k Ch."""" «91 
.'/""", •• 11. , d. opo ..... (lI'zolo 11'14) 
e,'!'ri_ a""",, Po," Lo. C .. ." (2)) 
Fl~allh) 
"~"~_,,,.,, ",,,;,,, ... (MO<Üol"m, 191'1 (M I 
e , ,,.;_~",,,,,, Po," ""'f'<'.J bocio plo)Ó'''( 111 
Po" Lo. ".to> (2)) 
10 / 17_6 1 811 
100 11 11 
1B lI 44!lS4 
100 1 1iO I W 
100 1 14 / 14 
"';_61 1!hl / l\4_l 
,J.JJI 1HJ I 2U 
)3_JJ I II .67 I Jj 
41_'" 1 L<J I UJ 
'1.11 / 0 .50 1 5 
5.16 / 0 .11 11 
6B I G_1S 1 1.2 
H I G_?l I J 
5?_ 1< 10 .gG ¡ l .j 
10 / 0.1 1 1 
)0.4 1 GOl l 1 
4 .Jj I O. LJ I J 
'6_61 10.111 1 
7 .• 9 10 .0i / 1 
1L14 1B2 / IL6 
 248 
 
 
 
M ...... .. ".<} ........ ~ ....... 'P' (G , 
'''riel,l,.. "~'"'I< "lta"" 
JI,ric!'!", .... dk.; 
a..."'pn....(4¡ 
R" Mm","" ('O) 
Com;", ...., .. P!.Y"" (JI 
c.m,,,,, ¡,.., .. Puyo .. (1 1 
Rio .. Cd.....,,;. i2! 
CIuo<o< P"",o, 16) 
Po," u 1k«rr.19) 
Pon ro> Cln<hd .. (1) 
e~ .,. ,ifII",¡ ... .......... "" ... (l'T"" &; B ... ¡o-" 1% 7) 1(;) 
A,(>~"", _' .... n.' c....1 mI>< Lo y" . Y d Vonodc 
s.hM~¡ • • , 'p. (G) 
<),..;,."""" ~"""" 
0,..;""""" Q""",, X Infi=i ... , 
Cn' .... 
'" ,,_ s.." Ju" I') 
Pozo u B",,,..,.14) 
Pozo PIo¡i' ''I41 ' 
M~ , ,,,l <k a.,,,,,,,, ('~I 
up .. I",'"""'"~ (J) 
•• /."'ur".' .,¡,.;¡",,_ tIo¡ v ..... p,;. 1 ~J41 1 ) 
e,"';""l/u",,'!;Co,o Rio M",I""" (1' 
Go .. ,,",", ""mI; c.n.J s.... Ju,," &q.oIlo. (1 1) 
~ ' ... ,,,,,. 
e ..... ,."' •• 'f'. (OC) 
1I_I,.p .. "~; 
E"""",~l ik> .... IOC) 
G ... t.. ...... n.I, 
IIme",.p ",""I.¡; 
L"",,, .. , "<gU¡'''~ 
L",,.,,,, " ",.i",u 
,.,..,.. ... II ••• ,.p. (1) 
s-. T« I"ól 
R" M,zqu"" (111 
Po" lO, Cónd.Jo (1) 
Nad ...... , (1') 
Nadodo"" • H."",-¡"'I (1) 
Po", u ~"'<TI.I~) R" M",,,,,,,, (11 
c.m,,,, hoo .. P!.)"I» m 
,"""",,, ..,... CIuo<"" ",;n., (l¡ 
,.,..,..,..11 ••• , .""_""; (e .... II<ro-Ddo)". 1'1711 (11 
A .... ~"""' _x ...... , R" '" Cd .......... (19) 
tthM><h_ .... (I ) 
R;. M,,'I""" (2) 
u¡¡wu.~ ... (l1) 
le"'""",""" El ",""')0 rl) 
L""",,'" ............ u c.m.., ¡,." .. PUY"" (2) 
IUoI.Jod.".. liJJm (P,....,. 19361 (1 1 
G ... Iou;~ .... n.I, c....J m'" Lo Y'l" yrl y, ..... 
IImel"",.. ~. lta "" 
IlmeN.p .... ~; 
'" a-.""",;., ... (~¡ 
R;o '" ed""",,;.121 
c....1 m17< Lo y" . Y d Vonodc 
'" 
1!1 • . 2HI .J) 
10 10.1 11 
)J.J) 1 1."1/l 
10011 / 1 
100 11.l l 1.l 
16.61/0.J) 11 
12.22 1l.l"1 16 
100 / H I , ) 
1L4J 121 .11 I JI.! 
l1. 1 "~.11 I i.2l 
lO I Ulnl 
4.ll I 0 .117 / U 
11.22 1 0..5 I 2.21 
16 10.1 11 
100 11.1 12.1 
IL7<"O.IHI 
16.61 10.1111 
4.1. I O.0l / 1 
10011 11 
~ . 16/0 . 0l 1 1 
1 ~ .2'l / O-' ~ / 1 
IUI I0.l6 / l 
1001[11 
lO I O.H I 
lOIl12 
"L<l / 1 11 / 1.6, 
lO / 0..511 
l .IIIO.I ! I! 
100 1l/ ! 
100 / 4.l14 .1 
B.JJ 10.6111 
lO l lll 
100 1111 
100 I :>O 110 
 249 
 
 
 
a...",pn....(6) 
R" M",,,,,,,{, l I 
Po," Lo B..",nI9) 
S~ ..... 'n.,.;"" .... IL,o<Iy, l~l2¡ ti) 
¿q>'''''' -tlalo", Riu M"".,¡.,. {II 
Mk"'P""" ",I"",¡,j,,, 
S".;",,,., 'p. (II 
Microp'''''' ",1"'-, 
S,,""')', "'_ (MI 
..... Q~ .. ,_x ..... ., 
1Ji-i. q>""_ 
G._';Q ... "Ii 
MiCrop""," ",1_Ok. 
N~tropU '1'. 
"".'~"p"''' 
M ........ I "" cta.,;"." (. ¡ 
Clo_"" 1";"" (() 
R;G<nCd ........ ( I ~1 
Cmu"" ba." .. Lo T,d, m 
PG" Lo Ikc ..... 141 
Po .. T" Cindido 1161 
Lopu. ,,,,,,,,,,,,, .. 117) 
S .... T,d. iJI 
Po .. PIo¡it ul4-1I 
Pon '''''fK''.J !t.<;, pla"".{ 111 
lo, 11 o..!; .... (Ji)) 
c-....I " " " la \'" . r d \'<na<lo 
'" Po .. PIo¡i· "IUI 
Po," _0I!.a<;' pla);,U (71 
Lo T« I¡" (l) 
M~ .. l en Clarrin<, (1) 
Lopu.lntem",d;' 1201 
a....", f"Ó«o' (6) 
R" M"'p';',,(211 
s ..... f « la ,ó\ 
Po .. Lo BO<""'I~) 
Cmu", ru.-.. P!.yu. (1) 
R;G<nCd.....,,;.121 
Riu M",,,,,,,, (II 
c.m ... !too .. Pbyo<a> (3) 
'''.61 10.11 1 1 
41.l!6 l l l Hl 
IU1 103J1l 
100 1 1 1 1 
ll l 0.'1 11 
100 / J I l 
100 / 10110 
41.11 1 1.6if4 
10 10.1 1 1 
11 / H I I~ 
100 1 IUJ / tI .ll 
1.31 10 .06 1 1 
"".61 10.67 1 1 
0.8210.071 1 
JO.TI 10 .<6 1 U 
l I O.O! 11 
Jl.JJ IO.JJ/1 
7 . <i9 1 0 . ~ l l 
1 ~ .l'l 1 0-'911 
"" .671633 1 1 
100 / 4 14 
11lüll1.4 
~ll l lO 
~ . H I 2.J1 I U . l 
16.67 103l / 1 
IUI I O.'l ! l 
100 / 111 
100/1.1 / 1.1 
looll l l 
"';.61 10 .61 / 1 
13.3l I0 .61 / 1 
..... _h}" ,h. , J .... ~ ."',¡ , S.lpio-M • ..,""OO, A"' .... _A"'¡ ... & C_ ... c. ..-.nz ~ 
lOOl (l) 
C'pri""¡"" a"""'" Po,," P;,¡it .. ( .... ) 
Po .. ,~. l!.a< ;' ~ Ia )' .. , (!JI 
MmD;'! en CIorrin<, (1 i ) 
Lopu. ,",o"","" ,3, 
Po .. Lo. c..ro. ,1ll 
C¡".-i""¡'" Q""",,, IH¡",á.'., Lopu. , ........... (S) 
~ ¡ "clu>M" ,¡,,,.,.>l.'"'''' I~~I (1) 
C}!";_ Q'""", Po .. PIo¡it u 14< ' 
G."""";Q _nli Pon P;'¡it .. (1J1 
a...."'f";., ... H) 
Poza ,....-,1 1>0< .. pla)it .. (7) 
a...."" 1";"'" (6) 
4,HI I0.M 1 U" 
JO.TI 10 .TI / B 
JI .89 10-" 1 1 U1 
"';.61 10 .61 / 1 
12.11 1 1.11 1 1.,3 
10 1 14 11.J5 
15.91 10 .18 / 1.1. 
7.69 10 .0> / 1 
11 10.21 1 1 
".l'l 10 .111 4 
IUl l J I H 
 250 
 
 
 
1"""",,, hqo<> 
Lepo •• " "'l"k>" 
100 / lH IS 
SO I ~ . 5 1 1 
75 1 ~_1S I I 
100 16 16 
ll.13 10.61/1 
 251 
 
 
 
c •• ,,,,,,Oó<l .. 
"<pO,"" _alofU 
c"'''''''''"'fo ___ ''''''' ,M~<IT""'_ D) 
E"""",~"iJ" 'l'. jLan.-.." N) 
L'1',"m ) ~ cI.oiJ ... '."a"" (Adull. A) 
S"l''''''''riJpi''''''''' (1.",_, Ni 
Sp_." 'l'-(~ ' ''', N) 
M;cr-"p""" ",1_, 
e," ""'"""'-'JO""""'""' 1 M<Ii<m· ...... D) 
L'1''''m,~, Ioo;'¡" 1Io ... ~,", ,Adu! '. A) 
f'ru,Md."m.-." .......... (M«o.= ..... D) 
S"'P""-'''-'P'""",",(L."",." N¡ 
Spi';'''''' "'. 'A .... It_ N) 
Sp;",X¡' 'l'_(l .. ", •. NI 
Ch_ida, 
C"""""''''-'fo'-'''""' ,.~,~"' .... ,. D) 
0,0'."-'0"'''''' ,ruto"'",,;' (Aduk. M) 
C .. ". __ ' 1",""""",...,[ 1-'00" N) 
P"","""It-w . ""ol>aJl_IAduk. N) 
.Ifo''''X¡''r_ (u",''''' N) 
Ck .J;da< 
JI, .. ;,-OlO .. ;' /,;-..10"" 
.Ifo''''''!"' -'f'. (u",''''' N) 
11_111.)" C"'''''8.''O"" 
An<)TOC<pI..,j'- V "- 'l'_IAtlult. M) 
C=>K>I¡" n.-U._. (A .... lt. DI • ( .. C . • "'..- b, (""",j.do-.\_brt~"'"' 19S-I1 
R""bdoc¡""o . ;'¡'¡m IAdule ~1 
IImchllop .... d I.¡; 
An<¡roc'pI..J"'" ,<"- 'l'_IAduIl. M) 
C"'nlCO"'" .. "'. Il "" .... ~) 
 252 
 
 
 
c.w,ü"tu- ,;.~I,u" •• " IAdule D) 
E .. t"",~Hd" 'r- (~-... N) 
L'I"""') ~rlto"''' ¡J,,,,o". (AduI ' . A) 
R¡'"bdod"",o ¡w.¡m (Adule t-.) 
.I¡o''''')''f'- (l-U> .... N) 
C,·pri"id .. 
('-,pri", ,/Q .,,"' .. ~ 
c ....... " ... fo_ ..... ¡M"'o<"" ....... D) ' (A,¡u'.-A",¡I.-" 01_ 20091 
P_"''''')"do., ¡"iI;>.>roIIi (Adult". Al 
C )1";",11. """~;..,. 
8","';""","",," oc.ri!op>thi (A<loIt. C) 
c..-.",,, fo" "'''''''''' (. ~'""«<"",,,_ D) 
R ¡"'~ 'I'_(L",u". NI 
Sp;""" 'r_ (l-U> .... NI 
w.-Jo "'''''_ 
Sp'",.!, 'r_ (l-U> .... NI 
So""!';' '1'_ 
e .. tr.x<, IU, fo __ oa •. ~'<IO«.,,, .n ,,,_ DI 
Sp ....... " '1'_ (lM> .... N) 
C'·p'i ...... ,w< 
C)pri_ ."""'" 
A""",,,,.,,,,, ••• .t..nu,go""'" (Aduk. Al 
G)=do,~'''' '1'- (Adu ~. M ) 
L 'I''''''')~rlto''''' ¡J,,,,o". (A"'I,. A) 
Mi<ropIwl'" , 1. """",.'Adult. A) 
So""'g;"'" '1'_ (Adok. M) 
Sp ....... " 'I'_IlM>· ... N) 
C)pri_ o"""'. x Info"'.'" 
A"""''')''''""''' .t..""'g>'''' '" ("-<Lb Al 
e .... "",",,hU fo"""-" • M"",=,,,~,_ D) 
So","g;"" '1'_ (Adob. MI 
Khabdochona sp. (Larvac, N) 
letaluridac: 
Aetalarus lupus 
Leptorlynchoides hecatus (Adult, A) 
Procumallanus sp. (Adult, N) 
Rhuabdochona sp. (Larvac, N) 
Poeci 
Gambusia marshi 
Allocreadiidac pen sp. (Adull, DJ 
    
¿seacaple sp. (Metacercariae, D) 
Bothriocephalus achetlognathi (Adult, C) 
Centrocestus formosamus (Metacercarias, D) 
Eustrongolides sp. (Larvac, N) 
Homalomerron pallidum (Adult, D) 
Leptorlunchoides necatus (Adal, A) 
Posthodiplostomum minimum (Metacercarias,D) 
Rhabdochona kidderi (Adult N) 
Spirossssp. (Larva,      
A=Acanhoceptalan, C= Cestoda, D= Digencan, M= Monogencan. N =Nematoda.
 253 
 
 
 
R~'I'.(L .. ",<. I 
,,,.1."" .. 
1c",¡""" ""'"' 
<p"'m¡ ~doc ;Ja """"''''' (" .... 10. ) 
,,,,.,,,,II,,,,,,, '1'. duh. I 
R~""'. '1'. 1~'"". I 
t ..,iliid •• 
.""",,,. _n ; 
" ""' ..... ,.¡.. . "" •. ,Aduh, DI 
"""""91. '!'-- ",.",,·..;.. , I 
B<Kh_."Iw"" """,,'~""" Aduk, C) 
c. ...... ,,"'.¡.""""' • ., "'"''''' ....,. I 
 .. ''''"C'Ii.,,,., . (~-... ) 
11""",10 .. ""," I"'IM ... ,"dok. I 
<p"'m,' ~doc;J .. """."" ,,, .... 10. l 
"-,'OOd"."",,..", .... i ..... l _"",.,,..  D) 
/t"t./oc."" . ,,;,Mi,.; dule ~1 
¡¡'''''¡''I'.(u".-... NI 
 _ "'''''.''''p¡''' ... e _ c. .. od..  _ o.~<,,,.,,-  _ 'Io",,~ ...  _ N<ITWodo.