UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO POSGRADO EN CIENCIAS BIOLÓGICAS FACULTAD DE CIÉNCIAS CAMBIOS DE DIVERSIDAD DE FAUNA ASOCIADA A ESPONJAS ARRECIFALES DEL GOLFO DE MÉXICO Y MAR CARIBE TESIS QUE PARA OPTAR POR EL GRADO DE: DOCTOR EN CIENCIAS PRESENTA: M. EN C. ANTAR MIJAIL PÉREZ BOTELLO TUTOR PRINCIPAL DE TESIS: DOCTOR FERNANDO NUNO DIAS MARQUES SIMÕES FACULTAD DE CIENCIAS, UNIDAD ACADÉMICA YUCATÁN, UNAM, SISAL, YUCATÁN MÉXICO COMITÉ TUTOR: DOCTORA GUILLERMINA ALCARAZ ZUBELDIA FACULTAD DE CIENCIAS, UNAM, DEPARTAMENTO DE ECOLOGÍA Y RECURSOS NATURALES DOCTOR FERNANDO ÁLVAREZ NOGUERA INSTITUTO DE ECOLOGÍA, UNAM, COLECCIÓN NACIONAL DE CRUSTÁCEOS CIUDAD UNIVERSITARIA, CD. MX. MARZO DE 2024. 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 FACULTAD DE CIÉNCIAS CAMBIOS DE DIVERSIDAD DE FAUNA ASOCIADA A ESPONJAS ARRECIFALES DEL GOLFO DE MÉXICO Y MAR CARIBE TESIS QUE PARA OPTAR POR EL GRADO DE: DOCTOR EN CIENCIAS PRESENTA: M. EN C. ANTAR MIJAIL PÉREZ BOTELLO TUTOR PRINCIPAL DE TESIS: DOCTOR FERNANDO NUNO DIAS MARQUES SIMÕES FACULTAD DE CIENCIAS, UNIDAD ACADÉMICA YUCATÁN, UNAM, SISAL, YUCATÁN MÉXICO COMITÉ TUTOR: DOCTORA GUILLERMINA ALCARAZ ZUBELDIA FACULTAD DE CIENCIAS, UNAM, DEPARTAMENTO DE ECOLOGÍA Y RECURSOS NATURALES DOCTOR FERNANDO ÁLVAREZ NOGUERA INSTITUTO DE ECOLOGÍA, UNAM, COLECCIÓN NACIONAL DE CRUSTÁCEOS CIUDAD UNIVERSITARIA, CD. MX. MARZO DE 2024. UN 258 POSG Do 4 COORDINACIÓN GENERAL DE ESTUDIOS DE POSGRADO COORDINACIÓN DEL POSGRADO EN CIENCIAS BIOLÓGICAS FACULTAD DE CIENCIAS OFICIO: CGEP/CPCB/FC/0214/2024 ASUNTO: Oficio de Jurado M. en C. Ivonne Ramírez Wence Directora General de Administración Escolar, UNAM Presente Me permito informar a usted que en la reunión ordinaria del Comité de Posgrado en Ciencias Biológicas, celebrada el día 27 de noviembre de 2023 se aprobó el siguiente jurado para el examen de grado de DOCTOR EN CIENCIAS del estudiante PÉREZ BOTELLO ANTAR MIJAIL con número de cuenta 307142838 con la tesis titulada: “Cambios de diversidad de fauna asociada a esponjas arrecifales del golfo de México y mar Caribe”, realizada bajo la dirección del DR. FERNANDO NUNO DIAS MARQUES-SIMOES: Presidente: DR. MICHEL EDMOND HENDRICKX RENERS Vocal: DR. EDGAR JAVIER GONZÁLEZ LICEAGA Vocal: DRA. BRIGITTA INE VAN TUSSENBROEK RIBBINK Vocal: DR. ENRIQUE AVILA TORRES Secretario: DR. FERNANDO ÁLVAREZ NOGUERA Sin otro particular, me es grato enviarle un cordial saludo. ATENTAMENTE “POR MI RAZA HABLARÁ EL ESPÍRITU” Ciudad Universitaria, Cd. Mx., a 04 de marzo de 2024 COORDINADOR DEL PROGRAMA ñ US ! Y COORDINACIÓN 2 DR. ARTURO CARLOS Il BECERRA BRACHO c. c. p. Expediente del alumno ACBB/AAC/GEMF/EARR/mnm COORDINACIÓN DEL POSGRADO EN CIENCIAS BIOLÓGICAS Unidad de Posgrado, Edificio D, 1* Piso. Circuito de Posgrados, Ciudad Universitaria Alcaldía Coyoacán. C. P. 04510 CDMX Tel. (+5255)5623 7002 http://pcbiol.posgrado.unam.mx/ Agradecimientos institucionales. Agradezco al Posgrado en Ciencias Biológicas de la Universidad Nacional Autónoma de México (UNAM). Agradezco al Consejo Nacional de Humanidades Ciencias y Tecnologías (CONAHCTY) por el apoyo económico. Agradezco al Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT IV300123) por el apoyo económico recibido Finalmente, a mi Tutor el Dr. Fernando Nuno Días Marques Simões y a los extraordinarios miembros de mi comité, la Dra. Guillermina Alcaraz Zubeldia y el Dr. Fernando Alvarez Noguera por su guía incondicional, por toda la retroalimentación brindada y por su excelencia académica. Agradecimientos personales A la Unidad Multidisciplinaria de Docencia e Investigación - Sisal, Facultad de Ciencias, Universidad Nacional Autónoma de México (UMDI Sisal-FC-UNAM). A la Secretaría de Marina-Armada de México (SEMAR), 7ma Zona Naval, Ciudad del Carmen y a Manuel Victoria y toda la tripulación del barco Caribbean Kraken por todo el apoyo logístico proporcionado durante el trabajo en altamar. También al Harte Research Intitute, a la Harte Charitable Foundation a la Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO-NE018), y a la Consejo Nacional de Humanidades Ciencias y Tecnologías (CONAHCyT: CB-2012-01-177293) por financiar este trabajo. Agradezco infinitamente a todos los investigadores y especialistas involucrados en la identificación de los diferentes taxones asociados a este trabajo: Anfípodos, M en C. María Muciño y Dr. Carlos Paz; Decápodos Carídeos, M en C. Julio Duarte; Decápodos Porcelánicos, M en C. Gabriel Cervantes; Equinodermos, M en C. Quetzalli Hernández y M en C. Francisco Márquez Borras; Porifera, Biol. Oscar Bocardo. Sin dudarlo este trabajo no sería posible si ustedes no hubiesen participado. De igual manera al Dr. Edlin Guerra por todo el aporte en los análisis estadísticos. Además, agradezco a todo el equipo de trabajo de BDMY involucrado en las campañas de recolecta y elaboración de este manuscrito, porque sin su aporte, apoyo y críticas no sería posible su realización. Agradezco sinceramente a todas esas fuentes de inspiración que me han brindado apoyo y consejo a lo largo de esta aventura. No como seres humanos perfectos, sino más bien aprecio la sutileza de sus imperfecciones y la forma en que enfrentan los diferentes desafíos académicos, lo cual ha sido una constante fuente de inspiración para mí. En particular, a Maite por su habilidad para expresar sus pensamientos de manera precisa y elocuente, a Nuno por su libertad de pensamiento y enfoque crítico, y a Edlin por su mente privilegiada que enriquecen mi pensamiento abstracto. Por último, agradezco a mis padres y hermanos, que sin importar en dónde estemos o qué tan lejos nos encontremos el apoyo y cariño compartido es incondicional. A mi compañera de aventuras Quetzalli, por esos instantes nuestros, por todo el cariño y por todos esos momentos inolvidables. A mis amigos y compañeros del hermoso puerto de Sisal, Xochitl, Deneb, Maria, Tonali, Pedro, Raúl, Diana, Nancy, Gabriel e Isaac. Al grupo de trabajo de Biodiversidad Marina de Yucatán, por ser para mí un espacio de expresión libre y de constante crecimiento. Les agradezco por todos los buenos momentos juntos que más allá de una relación laboral, me acompañaron y apoyaron en risas, en campañas, buceos, muestreos y sobre todo las experiencias únicas que llegamos a vivir juntos tanto en el mar como en tierra firme. Para quien me acompaña entre flores, sabores y canciones Índice Índice ................................................................................................................................ 9 Resumen ........................................................................................................................... 1 Abstract ............................................................................................................................ 2 Introducción ..................................................................................................................... 3 Artículo 1 (Requisito): Sponge-dwelling fauna: a review of known species from the Northwest Tropical Atlantic coral reefs ............................................................................ 8 Artículo 2: (Publicado) Geographic range size and species morphology determines the organization of sponge host-guest interaction networks across tropical coral reefs. .... 27 Artículo 3: (en revisión) A multi-scale analysis of α-diversity and β-diversity spatial variability on living islands ............................................................................................. 51 Discusión ........................................................................................................................ 80 Conclusiones .................................................................................................................. 82 Referencias bibliográficas .............................................................................................. 84 Apéndices ....................................................................................................................... 90 Apéndice I. Artículos publicados adicionalmente durante el programa doctoral. ...... 90 Apéndice II. Generación y mantenimiento del sitio web Marine Species Interactions 92 1 | P a g e Resumen Las esponjas arrecifales son un componente biológico fundamental de la comunidad arrecifal, desempeñando diversas funciones. Entre estas funciones, destacan su papel como generadoras y facilitadoras de microhábitats, los cuales son utilizados por una amplia diversidad de especies, que abarcan desde microorganismos unicelulares hasta vertebrados. Algunas especies de esponjas ofrecen refugio y protección a los organismos asociados, mientras que otras contribuyen a la defensa química mediante la producción de metabolitos secundarios especializados, lo que beneficia a los organismos asociados al reducir su detectabilidad y aumentar su supervivencia. Si nos centramos solo en la fauna asociada a esponjas arrecifales es posible detectar una alta especificidad y variaciones en la diversidad de especies asociadas en función de la distribución y la morfología que presenta cada especie de esponja. En este contexto, la presente tesis tiene tres objetivos fundamentales: i) La integración coherente y estandarizada de la información disponible sobre la fauna asociada a esponjas en los arrecifes de coral del Atlántico Tropical Noroccidental. Este objetivo se cumplió a través de la recopilación de información proveniente de diversas fuentes bibliográficas y la creación de una base de datos estandarizada. ii) Analizar la estructura de la red de interacciones de esponjas arrecifales y su fauna asociada, evaluando la diversidad de interacciones por especie involucrada, la estructura de la red y el papel que cada especie de esponja desempeña en el mantenimiento de la estructura de esa red. Este objetivo se cumplió a través de un análisis de redes complejas el cual nos permitió cuantificar la diversidad de interacciones por especie y evaluar la importancia de cada esponja en la estructura de la red. iii) Analizar la diversidad α y β de la comunidad asociada a la esponja tubular Callyspongia aculeata en tres escalas espaciales, a nivel de ecosistema, a nivel de hábitat y a nivel de microhábitat. Este objetivo se cumplió mediante salidas a campo, muestreos en ocho sistemas arrecifales distintos, identificación en laboratorio de organismos y pruebas de hipótesis estadísticas. Estos análisis revelaron patrones complementarios entre los diferentes componentes de diversidad analizados en función de la escala espacial. En conclusión, esta tesis contribuye significativamente al entendimiento de las complejas redes de interacciones que existen en los arrecifes de coral del Atlántico Tropical Noroccidental, ofreciendo una perspectiva integral de la importancia de las esponjas como especies clave en la estructura de las comunidades en sistemas arrecifales. 2 | P a g e Abstract Reef sponges play a fundamental biological role within the reef community, performing multiple functions. Among these functions, their capability to generate and facilitate microhabitats stands out, which are utilized by a wide range of species, from unicellular microorganisms to vertebrates. Certain sponge species offer shelter and protection to associated organisms, while others contribute to chemical defense through the production of specialized secondary metabolites, benefiting associated organisms by reducing their detectability and enhancing their survival. A high specificity and variations in species diversity based on the distribution and morphology of each sponge species is revealed if we only focus on the sponge’s associated fauna. In this context, this thesis encompasses three fundamental objectives: i) The coherent and standardized integration of available information on sponges- associated fauna within the coral reefs of the Northwestern Tropical Atlantic. This objective was achieved through the compilation of information from various bibliographic items and the creation of a standardized database. ii) Analyzing the structure of the interaction network of reef sponges and their associated fauna, evaluating the diversity of interactions per species involved, the network's structure, and the role that each sponge species plays in maintaining the network's structure. This objective was fulfilled through the analysis of complex networks, allowing us to quantify the diversity of interactions per species and assess the importance of each sponge in the network's structure. iii) Analyzing the α and β diversity of the community associated with the sponge Callyspongia aculeata at three spatial scales: ecosystem, habitat, and micro-habitat. This objective was achieved through fieldwork, sampling in eight different reef systems, laboratory organism identification, and statistical hypothesis testing. These analyses revealed divergent patterns among the different components of diversity analyzed according to the spatial scale under consideration. In conclusion, this thesis significantly contributes to our understanding of the complex interaction networks within the coral reefs of the Northwestern Tropical Atlantic, offering a comprehensive perspective on the importance of sponges as key species in the structure of communities in reef systems. 3 | P a g e Introducción La diversidad biológica, en un lugar y tiempo específicos, es el resultado de procesos históricos como especiación, vicarianza y dispersión, que moldean y regulan la distribución actual de la vida en el planeta Tierra (Holt, 1992). Estos procesos históricos generan una distribución no aleatoria de la vida, donde la heterogeneidad espacial y temporal del entorno físico, junto con la interacción entre organismos y ambiente, conducen a diversos procesos biológicos y ecológicos (Feldman, 1970; Legendre & Robson & Barmuta, 1998; Baselga & Gómez-Rodríguez, 2019; Legendre, 2012). Los factores que influyen en las medidas de diversidad biológica en un lugar y tiempo determinado son, el número de individuos de una comunidad, la distribución y abundancia de las especies de la comunidad y la distribución de cada individuo (Underwood et al., 2000; He & Legendre, 2002; McGlinn & Palmer, 2009; Chase & Knight, 2013; Chase et al., 2018). Cada uno de estos componentes puede interactuar de manera independiente o conjunta dentro de un ecosistema, lo que provocando cambios multidimensionales dependientes de la escala espacial o temporal que se analice (Chase et al., 2018). Entender cómo se organizan millones de especies representa un desafío para cualquier estudio centrado en patrones de diversidad biológica (Dáttilo & Rico-Gray, 2018). Al mismo tiempo, la diversidad biológica tiene muchas facetas, por ejemplo, la diversidad de especies, genética, fenotípica, funcional, filogenética, metabólica y de interacciones (Andresen et al., 2018; Dáttilo & Rico-Gray, 2018; Martínez-Falcón et al., 2019; Pugh & Field, 2022). Para esta tesis utilizamos los conceptos de diversidad de interacciones (ver Artículo 1 y 2 de este escrito) y diversidad de especies (ver Artículo 3 de este escrito) para contestar las preguntas ¿Cuál es el arreglo de la red de interacciones huésped-hospedero de la fauna asociada a 4 | P a g e esponjas arrecifales del Golfo de México y el Mar Caribe?, ¿Qué especies de esponja son claves en el mantenimiento de la estructura de la red de interacciones huésped-hospedero? y ¿Cuáles son los cambios de diversidad de especies de la fauna asociada a las esponjas arrecifales en tres escalas espaciales diferentes? La diversidad de interacciones se puede definir como el número total de relaciones compartidas por todas las especies en un conjunto dado de organismos, también definida como riqueza de interacciones (Tylianakis et al., 2010; Pugh & Field, 2022). No obstante, la diversidad de interacciones suele medirse en términos relativos entre el número de “enlaces” entre especies y el número de especies en la red (Tylianakis et al., 2010). Y al mismo tiempo, las interacciones bióticas pueden ser de diferente tipo y naturaleza, antagonistas (competencia por recursos), mutualistas (polinización), tróficas (depredación) o no tróficas (huésped-hospedero), siendo el tipo y la naturaleza de la interacción dos mecanismos que promueven la especiación de la vida (Wulff, 1997; Watson & Pollack, 1999; Freilich et al., 2018; Pugh & Field, 2022). A su vez, la diversidad de especies se tiene que definir de acuerdo con la escala espacial que se analice, dividida en tres componentes: la diversidad alfa (α), diversidad beta (β) y diversidad gamma (γ) (Whittaker, 1972; Whittaker et al., 2001; Andermann et al., 2022). La diversidad α se refiere a la riqueza de especies dentro de una comunidad o unidad ecológica (Andermann et al., 2022). La diversidad β, por su parte, describe la diferenciación entre comunidades (Baselga & Gómez-Rodríguez, 2019; Andermann et al., 2022). Sin embargo, la interpretación exacta y la cuantificación de la diversidad β varían sustancialmente entre estudios (Tuomisto, 2010). Inicialmente, se definía como la relación entre la diversidad γ y α (β = γ / α, sensu Whittaker, 1972). Actualmente, una medida ampliamente utilizada para evaluar la diversidad β es la similitud entre comunidades, lo que 5 | P a g e mide el recambio o variabilidad de especies entre unidades ecológicas (Anderson et al., 2013; Anderson & Santana-Garcon, 2015). Por último, la diversidad γ, describiendo la suma total de especies dentro de diferentes comunidades en una zona geográfica más extensa (Baselga & Gómez-Rodríguez, 2019; Andermann et al., 2022;). Para esta tesis utilizaremos la diversidad α, medida como la riqueza de especies en diferentes unidades ecológicas y la diversidad β, medida como la similitud entre pares de unidades ecológicas. A pesar de que la diversidad γ se define como un componente de la diversidad de especies, lo único que la diferencia de la diversidad α es la escala espacial de análisis, por tal motivo se decidido no incluir la diversidad γ en esta investigación. La decisión se fundamenta en que la diversidad α medida en diversas escalas espaciales provee la información necesaria para abordar las preguntas de investigación de esta tesis. A nivel mundial, las esponjas destacan como componentes cruciales en los ecosistemas marinos, desempeñando diversas funciones esenciales (Rütlzer, 2004; González-Rivero et al., 2011). Por ejemplo, su capacidad para filtrar grandes volúmenes de agua y facilitar la producción primaria las posiciona como actores clave en la ecología de los sistemas arrecifales, generando un vínculo bento-pelágico entre los nutrientes disponibles en la columna de agua y la energía disponible en el lecho marino (Diaz & Rütlzer, 2001; Bell, 2008; Perea-Blázquez, 2011; Bell et al., 2013; Pawlik et al., 2013; Maldonado et al., 2017). De igual manera, las esponjas pueden ser especies clave como generadoras de hábitats, los cuales son activamente aprovechados por una amplia diversidad de especies, desde microorganismos hasta animales invertebrados y vertebrados (Diaz & Rütlzer, 2001; Ávila et al., 2007; Bell, 2008; Webster & Taylor, 2012; Maldonado et al., 2017; Bell et al., 2013; Pawlik et al., 2013). Por tales motivos, los cambios en abundancia específica y composición 6 | P a g e comunitaria de las diferentes especies de esponjas ejercen impactos significativos en la comunidad arrecifal y en el funcionamiento global de este ecosistema (Bell, 2008). Las esponjas además de ser facilitadoras de hábitats también brindan cierto grado de protección a los organismos que se asocian a ellas, ya sea por el uso directo de diferentes estructuras como refugio o camuflaje o por la protección indirecta derivada de la defensa química de la esponja (Dembowska, 1926; McLay, 1983; Bedini et al., 2003; Pawlik, 2011; Cruz Ferrer, 2014; Maldonado et al., 2017; Harada et al., 2020). Entre las esponjas reportadas, las de la Clase Desmospongiae son las que tienen un mayor número de asociaciones; además, esta es la Clase con mayor riqueza de especies en los arrecifes del mundo (Maldonado et al., 2016; Rossi et al., 2017). En relación con la defensa química, esponjas de los géneros Agelas, Amphimedon, Aplysina e Ircinia producen metabolitos secundarios especializados para su defensa contra la depredación, siendo compuestos tóxicos o poco palatables, que indirectamente protegen también a los organismos que viven asociados a ellas (Pawlik, 2011). Estas condiciones provocan que un tipo de interacción dominante en el Phylum Porifera sean las relaciones huésped-hospedero (Aerts, 1998; Wulff, 2006; Ávila et al., 2007). Este tipo de interacciones tienden a ser especie-específicas en distintos niveles taxonómicos, sin embargo, la naturaleza de la interacción (comensalismo, parasitismo y mutualismo) y la intensidad de la asociación (obligatoria o facultativa) varía considerablemente entre especies (Turon et al., 2000; Thiel & Baeza, 2001; Ďuriš et al., 2011). El análisis de las redes ecológicas facilita el estudio de las interacciones en una comunidad, en otras palabras, facilita el estudio de las conexiones entre especies (Dáttilo & Rico-Gray, 2018). Esta línea de investigación ofrece una perspectiva que integra la estructura de las redes con procesos ecológicos como, el mantenimiento de la diversidad de especies 7 | P a g e en una región, la colonización de nuevas especies, el efecto de que podría tener la extinción local de especies, y la evolución y coevolución de las redes a medida que las especies avanzan en el tiempo (Martínez-Falcón et al., 2019; Dáttilo & Rico-Gray, 2018). Por otro lado, analizar los cambios de diversidad a diferentes escalas espaciales es esencial para comprender la respuesta de la fauna asociada a las esponjas arrecifales con diferentes factores ecológicos que ocurren a nivel ecosistémico, a nivel local y a nivel del microhábitat (Chase et al., 2018). Por tales motivos los objetivos de esta tesis fueron: i) Integrar toda la información disponible sobre fauna asociada a esponjas en un solo sistema coherente y estandarizado, ii) analizar la estructura de la red huésped-hospedero de la fauna asociada a esponja arrecifales para identificar los patrones que determinar el arreglo presente en la red, y iii) analizar los cambios en la diversidad-α y -β de la fauna asociada a Callyspongia (Cladochalina) aculeata (Linnaeus, 1759) en tres escalas espaciales diferentes las cuales son ecosistema, hábitat y microhábitat. 8 | P a g e Artículo 1 (Requisito): Sponge-dwelling fauna: a review of known species from the Northwest Tropical Atlantic coral reefs Revista: Biodiversity Data Journal Autores: Antar Mijail Pérez-Botello; Nuno Simões Estado: Publicado Año: 2021 DOI: 10.3897/BDJ.9.e63372 Resumen En los arrecifes de coral tropicales de aguas someras (menores a 50 m de profundidad), las esponjas marinas desempeñan un papel crucial al proporcionar microhábitats para una amplia diversidad de especies. A pesar de la existencia de numerosos estudios sobre las relaciones hospedero-huésped entre las esponjas y su fauna asociada, esta información ha permanecido dispersa y desconectada. Por lo tanto, el objetivo de este trabajo fue desarrollar y generar una base de datos que compile las interacciones relacionadas con las especies de esponjas marinas y la fauna asociada en los arrecifes de coral del Atlántico Tropical Noroccidental. Con este conjunto de datos compilamos 67 fuentes bibliográficas que reportan 101 especies de esponjas hospederas, agrupadas en 12 órdenes que interactúan con 284 especies huéspedes pertenecientes a seis Phyla. Esta base de datos tiene la característica de tener dos formatos interrelacionados: i) datos legibles por máquina y ii) datos legibles por humanos, lo que mejora su alcance y facilita su uso tanto en plataformas informáticas como para los usuarios. Además, se generó un entorno visual e interactivo de los registros de interacciones y un diagrama de cuerdas dinámico que representa las conexiones entre las especies huéspedes y las esponjas hospederas. Esta herramienta visual permite a los usuarios explorar y filtrar la información de manera intuitiva. De igual manera esta base de datos proporciona una fuente de información centralizada, de acceso libre, pública y de alta calidad sobre la fauna asociada a esponjas arrecifales incluyendo el tipo de interacción (mutualismo, parasitismo, comensalismo) y otros detalles cuantitativos. Además, se resalta la riqueza de especies que dependen de las esponjas arrecifales y se compara la diversidad entre el Mar Caribe y el Golfo de México. Esta base de datos representa una valiosa recopilación de información sobre las interacciones hospedero-huésped en los arrecifes de coral del Atlántico Tropical Noroccidental, facilitando futuros análisis y promoviendo la colaboración para enriquecer esta línea de investigación. Biodiversity Data Journal 9: e63372 07 doi: 10.3897/BDJ.9.e63372 copo 0000 Data Paper Sponge-dwelling fauna: a review of known species from the Northwest Tropical Atlantic coral reefs Antar Mijail Pérez-Botello*, Nuno Simdes*!.1 ji Posgrado en Ciencias Biológicas, Facultad de Ciencias, Puerto de Abrigo sín, C.P. 97356, Sisal, Yucatán, Mexico $ Universidad Nacional Autónoma de México, Merida, Mexico | Laboratorio Nacional de Resiliencia Costera, Mexico, Mexico Y] International Chair for Coastal and Marine Studies, Harte Research Institute for Gulf of Mexico Studies, Corpus Christi, United States of America Corresponding author: Nuno Simóes (nsGHciencias.unam.mx) Academic editor: Dimitris Poursanidis Received: 19 Jan 2021 | Accepted: 02 Mar 2021 | Published: 15 Mar 2021 Citation: Pérez-Botello AM, Simóes N (2021) Sponge-dwelling fauna: a review of known species from the Northwest Tropical Atlantic coral reefs. Biodiversity Data Journal 9: e63372. https:/fdoi.org/10.3897/BDJ.9.e63372 Abstract Background Within tropical shallow-water coral reefs, marine sponges provide microhabitats for a wide range of fauna. Although there have been numerous studies and reports of symbiotic relationships amongst sponges and their associated fauna, those pieces of information are isolated and disconnected. For this reason, based on the available literature, we compiled a species-interaction dataset of coral reef marine sponge-associated fauna known to date. New information We introduce a dataset that includes 67 literature items that report 101 species of sponge hosts clustered in 12 Orders having a host/íguest interaction with 284 guest species from six Phyla present in the Northwestern Tropical Atlantic coral reefs. This dataset consists of two types of information: 1. Machine-readable data and 2. Human-readable data. These two types of coding improve the scope of the dataset and facilitate the link between machine platforms and human-friendly displays. We also created an interactive O Pérez-Botello A, Simóes N. This is an open access article distributed under the terms of the Greative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 9 | P a g e 2 Pérez-Botello A, Simóes N visualisation of the species-interactions dataset and of a dynamic Chord Diagram of the host-guest species connections to generate a user-friendly link between the user and the dataset. Keywords marine ecology, community ecology, interaction networks, symbiosis, mutualism, parasitism, commensalism Introduction Symbiosis relationships have been recognised as an important speciation mechanism (Wulff 1997, Watson and Pollack 1999, Hagedorn et al. 2015, Brooker et al. 2019, Bauer 2004). A few years ago, Rossi et al. (2017) introduced the term "Marine Animal Forests" in a book with the same name. In this book, the authors compare the function of trees in forests with marine animal communities like corals, sponges and bivalves. These organisms share one particular characteristic: they can create three-dimensional habitat heterogeneity and structural complexity, providing shelter and a secure food source for a wide range of sessile and mobile animals (Tews et al. 2016, Rossi et al. 2017, Brooker et al. 2019). Sponges tend to be particularly abundant and diverse in coral reef ecosystems. Their architecture, morphology and capability to synthesise toxic substances can generate microhabitats where other species may live or have an adaptive advantage to explore (Bruce and Jones 1976, Duffy 1992, Henkel and Pawlik 2011, Pawlik 2011, Maldonado et al. 2017, Reyes-Bonilla and Jordán-Dahlgren 2017, Koukouras et al. 1995, Maldonado and Young 1996, Diaz and Rútzler 2001, Ríos and Duffy 2007). Reef sponges are a well-studied group; however, the available information on marine sponges' intraspecific relationships ¡is scattered, isolated and, in most cases, is only focused on a particular taxonomic group or a reduced geographical area. For this reason and based on published records from the Northwest Tropical Atlantic (NVWYTA) coral reefs, we compiled and created a standardised dataset that brings together information on sponge host/guest interactions in the reagion. Moreover, we also created two dynamic and interactive web visualisation tools to describe and analyse the information. General description Purpose: In a climate change and biological diversity loss scenario, it becomes crucial to have a high-quality open-access baseline dataset on fundamental aspects, such as symbiotic interactions. This dataset provides an updated and standardised matrix of published records on hostíguest interaction between tropical coral reef marine sponges and their associated fauna. Each interaction was codified into a machine- and human- readable format, according to the Global Biotic Interactions (GloBl) standard language (for more information, see Poelen et al. 2014; globalbioticinteractions.org). Furthermore, an 10 | P a g e Sponge-dwelling fauna: a review of known species from the Northwest Tropical ... 3 independent, dynamic, interactive and user-friendly data-visualisation display of this information is provided to maximise outputs in terms of data accessibility and usage. Additional information: In this work, we screened 65 articles and two university theses on the NWTA coral reefs published between 1909 and 2019. The present review includes 101 sponge species divided into 12 Orders from the Demospongiae Class, interacting with 284 guest species from six Phyla. The Haplosclerida and Dyctioceratida orders presented the largest number of associated species. Regarding the host sponges morphologies, the tube, fan and vasiform shapes common to the genera Agelas, Aplisyna, Írcinía and Callyspongía, tended to have more guest species. Írcinta strobilina was the species with the highest number of associated species (dwelling species N = 89) followed by Calfyspongía aculeata (dwelling species N = 63) and /rcinia felix (dwelling species N = 53). According to the sponges-dwelling fauna records, the phylum Arthropoda was dominant on species numbers (164 spp.), followed by Annelida (60 spp.), Mollusca (19 spp.), Chordata (20 spp.), Echinodermata (15 spp.) and Cnidaria (6 spp.). When we compare the hostíguest species richness between the Caribbean and the Gulf of Mexico, the Caribbean has the greatest sponge diversity with 84 sponge species, whereas, the Gulf of Mexico has 38 sponge species. Both regions share 22 sponge species. However, the Gulf of Mexico has 191 guest species against 145 guest Caribbean species. At the guest species richness part, both regions shared 52 guest species. lf we count the interaction diversity (an integrated binomial of hostíguest species), the current work register 451 hostíguest interaction within the Gulf of Mexico, but only 399 inside the Caribbean coral reefs. Meanwhile, mutualistic associations are a common interaction type with 86 entries, followed by the parasitic interaction with 44 entries and commensal interaction with 36 entries. Nonetheless, most of the literature entries do not classify the type of interaction, remaining at the symbiosis or dwelling-species level. Sponges, like other bio-constructing species, are ecosystem engineers, shaping the environmental complexity and maintaining part of the habitat biodiversity (Jones et al. 1994, Rossi et al. 2017). The present species-interactions' dataset highlights the remarkable diversity of animals that depend on, or take advantage of, the sponges' presence. Besides, it is possible to have a host/guest distribution, hostíguest species richness quantification and a few more quantitative metrics that will help to better understand and model the sponge-dwelling fauna. Sampling methods Sampling description: In order to perform the literature search and compilation of the interaction dataset, based on bibliographic records, it was necessary to define our sampling unit. For this work, we define each article and thesis reviewed as a unit; each of these elements we name as "literature item" and each item could provide one or several interaction report entries. 11 | P a g e 4 Pérez-Botello A, Simóes N First, we compiled all the articles and theses known to us that report a sponge host/guest interaction in the NWTA coral reefs (known literature items). This initial baseline was complemented with a Web of Science, Pub Med, Crossref, Scopus and Google Scholar web search (web literature items) using the "Publish or Perish" software application (Harzing 2007; harzing.comfresourcesfpublish-or-perish). Á specific string of keyword sequences and logic operators was used to simultaneously focus the search without losing inclusiveness and to improve the exploration yield [(Sponge” AND ('dwelling” OR “interaction” OR “association” OR “mutualism” OR “commensalism” OR “parasitism” AND FAnnelida” OR "Arthropoda" OR "Chordata" OR "Cnidaria” OR "Echinodermata" OR "Mollusca" OR "Molluska") AND (coral reef”) AND ("Caribbean” OR “Gulf of Mexico” OR “Northwestern Atlantic”)]. To identify possible duplicate and pseudoreplicate literature items between the web search and the known literature items, we used the "Check for Duplicates” tool implemented in Mendeley software (mendeley.com). This tool compares the publication type (Journal Article or Thesis), the literature title, authors, publisher and publication year for all the literature items within the bibliographic database. With this comparison, it was possible to discriminate both duplicate and pseudoreplicates literature items. A literature item would be validated 1. ¡if it were published in an indexed journal, according to the Science Citation Index Expanded (SCIE) or in a MSc or PhD University theses; 2. if the literature item were an indexed journal, necessarily had to match the geography of interest, contain details of the latitude and longitude information (or a detailed geographical description) and clearly stated the species involved. If the literature item were a University thesis, the previous criteria were used, but it was also indispensable that the species involved were deposited in a scientific collection. VWith this protocol, we ensured that all complied literature items has the minimum essential information to be extracted. Whenever possible, the interaction type presence (commensalism, parasitism, mutualism), the species taxonomy details and the host body part where the guest lived, were also extracted. Finally, with the screened literature items, we compiled the sponge-dwelling fauna dataset. The compiling process consisted of generating independent entries, based on the sponge host/guest interaction reports inside a particular item. Quality control: Data were standardised according to the GloBl standard language. This guideline consists of categorising each entry into different standardised vocabularies. We cross-checked the species scientific names with the World Register of Marine Species webserver (Costello et al. 2013; WoRMS; marinespecies.org/aphia.php?p=match), retrieving the actual classification and the universal identifier, Aphia ID, provided by the UN-Global Biodiversity Information Facility. The geographic information was integrated and codified according to the GeoNames ID platform (geonames.org). The interaction type and host body part name were standardised, according to the OBO Library (obofoundry.org). Lastly, for the reference management and citation style, we used Mendeley software. With this standardisation and quality control process, we ensured a high-quality integrated human-readable and machine-readable dataset. 12 | P a g e Sponge-dwelling fauna: a review of known species from the Northwest Tropical ... 5 Step description: Step 1: Define the sampling universe; this step was designed to mark the geographic and environmental limits. Step 2: Literature search; in this step, we compiled the curated bibliographic database, without duplicates and pseudoreplicates between the known literature items and the web search literature items. Step 3: ltem validation; this step consists of a validation test that we used to select the literature items with the minimum necessary information. Step 4: Entry standardisation; in this step, we homogenised all the sponge iteration entries into the GloBl standard language. Step >: Dataset compilation (Fig. 1) — $ au Figure 1. E Flow diagram of the steps followed to generate this dataset. Geographic coverage Description: According to the large marine ecosystems' classification proposed by Spalding et al. (2007), the Northwestern Atlantic has five regions with major coral reef formations: the Gulf of Mexico, the Caribbean Sea formed by the greater and Lesser Antilles, Central America and the north shores of South America, North America, the Bahamian Archipelago and Bermuda at the north-eastern boundary of this major region. Taxonomic coverage Description: This dataset is composed of the host/guest interaction between coral reef sponges (Pylum: Porifera) and six other major marine Phyla: Arthropoda, Annelida, 13 | P a g e 6 Pérez-Botello A, Simóes N Mollusca, Chordata, Echinodermata and Chnidaria. All the information is at species resolution. Taxa included: Rank Scientific Name Common Name phylum Porifera Sponges phylum Arthropoda Shrimps, crabs, lobsters phylum Annelida Worms, christmas tree worm phylum Mollusca Clams, mussels, oysters and scallops phylum Chordata Fish, goby phylum Echinodermata Sea urchins, sea cucumbers, brittle-stars phylum Cnidaria Sea anemones, hydroids Temporal coverage Data range: 1909-1-01 - 2019-12-31. Usage licence Usage licence: Creative Commons Public Domain Waiver (CC-Zero) Data resources Data package title: Sponge dwelling-fauna from the North-western Tropical Atlantic Ocean: a bibliographic records database. Resource link: https://doi.org/10.5281/zenodo.3333023 Alternative identifiers: https://github.comBDMYRepository/Sponge Interactions Number of data sets: 1 Data set name: Sponge-dwelling fauna from the North-western Tropical Atlantic Ocean: a bibliographic records database. Download URL: https://zenodo.org/record/3333023 Data format: .tsv Data format version: 2.06 14 | P a g e Sponge-dwelling fauna: a review of known species from the Northwest Tropical ... 7 Description: The present database compile 65 articles (Baeza et al. 2016, Carrera- Parra and Vargas-Hernández 1997, Chace 1972, Chavarro et al. 2004, Bóhlke and Robinson 1969, Cházaro-Olvera and Vázquez-López 2014, Christoffersen 1972, Coutiéere 1909, Coutiére 1910, Crocker and Reiswig 1981, Crowe and Thomas 2002, D'Aloia et al. 2011, Dardeau 1981, Dardeau 1984, Dauer 1973, Duffy 1992, Duffy 1996a, Duffy 1996b, Duffy 1996c, Duffy 1998, Duffy and Macdonald 1999, Erdman and Blake 1987, Garcia-Hernández and Hoeksema 2017, Hendler 1984, Henkel and Pawlik 2005, Henkel and Pawlik 2011, Henkel and Pawlik 2014, Herrick 1981, Hultgren and Duffy 2010, Huang et al. 2008, Hultgren et al. 2011, Hultgren et al. 2010, Lattig and Martin 2009, Lattig and Martín 2011, LeCroy 1995, Macdonald and Duffy 2006, Macdonald et al. 2009, Macdonald et al. 2006, Montenegro-González and Acosta 2010, Ortiz et al. 2011, Ortiz et al. 2013, Paerse 1932, Pearse 1950, Pawlik 2011, Pequegnat and Heard 1979, Randall and Lobel 2009, Rebolledo et al. 2014, Reimer et al. 2018, Richards et al. 2007, Rios and Duffy 1999, Robertson and Tassell 2019, Santana-Moreno et al. 2013, Scott et al. 1988, Swain 2012, Swain and Wulff 2007, Thomas and Klebaa 2007, Thomas and Klebba 2006, Tobb and Manning 1961, Toóth and Bauer 2008, Tyler and Bóhlke 1972, Victor and Krasovec 2018, Villamizar and Laughlin 2011, Westinga and Hoetjes 1981, Williams 1984, Winfield et al. 2009, Winfield and Ortiz 2010, Wenat et al. 1985) and two university theses (Ugalde García 2014, Perez-Botello 2019) in a detailed sponge host-guest interaction dataset distributed in the Northwest Tropical Atlantic coral reefs, including a total of 2992 interactions between 101 sponge host species and 284 sponge-dwelling species, over 90 years of publications (Fig. 2). All entries are standardised to the GloBl language. Li te ra Weraq€ temporal COv Figure 2. EX] Distribution of the literature items within the dataset temporal coverage. 15 | P a g e Column label sourceOccurrenceld source Taxonld source TaxonName sourceBodyPartld sourceBodyPartName sourceLifeStageld sourceLifeStageName interactionTypeld interactionTypeName targetOccurrenceld targetTaxonld targetTaxonName targetBodyPartld targetBodyPartName targetLifeStageld targetLifeStageName localityld localityName decimal Latitude decimal Longitude YY YY MM DD HH mm ss observationDateTime referenceDoi Pérez-Botello A, Simóes N Column description Globally unique id to reference the individual source organism. Taxon classification id of originating organism in some taxon name authority. WoRMS AphialD Scientific name of taxon classification of source organism Identifier of description of source body part is interacted with. As described by the OBO Relations Ontology Human-readable description of source body part Identifier of description of source life stage. As described by the OBO Relations Ontology Human-readable description of source life stage Id of interaction. As described by the OBO Relations Ontology Human-readable description of interactions Globally unique id to reference the individual target organism Taxon classification id of target organism. WoRMS AphialD Scientific name of taxon classification of target organism of interaction Identifier of description oftarget body part is interacted with. As described by the OBO Relations Ontology Human-readable description of target body part. Identifier of description of target life stage. As described by the OBO Relations Ontology Human-readable description of target life stage. Identifier ofthe Geo classification. As described by geonames.org Human-readable description of locale Latitude of geographic centre of interaction observation location Longitude of geographic centre of interaction observation location Year of the recorded interaction Month of the recorded interaction Day ofthe recorded interaction Hour of the recorded interaction Minute of the recorded interaction Second of the recorded interaction ISO 8601 formatted date time string of the recorded interaction Digital Object ld used to the papers, datasets or other digital object that validate the interaction 16 | P a g e Sponge-dwelling fauna: a review of known species from the Northwest Tropical ... 9 referenceUrl Some resolvable url that points to information related to species interaction record referenceCitation Human-readable reference related to species interaction record Additional information Interactive display and data visualisation A virtual environment was generated to visual-analyse the dataset. We created a Tableau dashboard (public.tableau.com) and a AmCharts Chord Diagram (amcharts.com/demos/ toggleable-chord-diagram). Both the interactive dashboard and the dynamic Chord Diagram are available at the project official web page: marinespeciesinteractions.org/ projects/visual-database/. The uses of the interactive dashboard are based on different lists that filter the displayed information according to the users' requests. The dashboard shows a map of the NWTA where the records of each interaction are plotted (Fig. 3a). In the middle are 10 filters with host Order, Family and Scientific species name, guest Phyla, Class, Order, Family and Scientific species name, the recorded locality (country) and the information source (Fig. 3b). On the right side, two bar graphics show either the sponge Order vs. guest species richness or the guest Phylum vs. guest Class species richness counts (Fig. 3c, d). The hostíguest matrix is centred in the lower part of the dashboard, with the host sponges as rows and the sponge dwelling-fauna species as columns (Fig. 38). In practice, the interactive dataset aims to be an intuitive step-by-step graphical interface. lt is possible to select the source of information to observe and focus on a particular region or taxonomic group. The Chord Diagram gives a general picture of everything in the universe of registered interactions (Fig. 4a). The thickness of the node represents the number of links that a species has and the colour represents the taxonomic group to which it belongs. The information can be filtered by guest Phylum (¡.e. Annelida, Arthropoda, Chordata, Cnidaria, Echinodermata and Mollusca) (Fig. 4b), but not by the sponge Order (Fig. 4c). If the user wants to return to the original view, they can click on the guest Phylum name or the back button (Fig. 4d). Although the complete dataset ¡is fully accessible for downloading as a whole, with these two interactive visualisation tools, openly available through the internet and hopefully sufficiently intuitive, the user can interact with the dataset and pose questions filtered according to their particular interest. What's next? With this dataset, we provide an updated and clustered report on the symbiotic relationships in coral reef sponges in the NWTA coral reefs. This information opens the door to many numerical and statistical analyses. Finally, we encourage you to collaborate with this project and, if you have any records that are not listed on this dataset, contact us. We will be glad to talk with you and add this information in the next version of the Dataset. 17 | P a g e 10 Pérez-Botello A, Simóes N Figure 3. Example of the dashboard features. Concluding remarks Compiling the available sponge hostíguest interaction data in one place enhances the scope and shareability of the diffused information. Furthermore, the standardisation of the dataset into a global language creates a link between this dataset and several international repositories, such as The Encyclopaedia of Life and communication with other data 18 | P a g e Sponge-dwelling fauna: a review of known species from the Northwest Tropical ... 11 languages, such as Darwin Core. Moreover, with this work, a baseline is generated to compare and structure future works that focused on sponge host/guest relationships. Figure 4, Chord diagram features. A overview of how to use the network plot. In conclusion, the state of knowledge about sponge-associated fauna is on the right path. However, the main obstacle during the data collection process was the lack of reported information. For example, the involved species' taxonomic identity and the interaction type are crucial pieces of information that are missing in several literature items. We suggest that future works make an effort to clearly identify both taxonomic entities, not only the guest or host species. Furthermore, it was possible to analyse the interaction matrix of sponge-dwelling species with a complex network approach identifying connected and key species with this dataset. To better understand possible changes in the sponge host/guest interactions, a niche-modelling approach could also be useful, displaying different future species-interaction scenarios. 19 | P a g e 12 Pérez-Botello A, Simóes N Acknowledgements This work was partially financed by grants to NS by the Harte Institute, the Harte Charitable Foundation, CONABIO-NEO18 and CONACyTCB-2012-01-177293. AMPB was supported by CONACyT doctoral fellowship 2019-000037-O2NACF through the Posgrado en Ciencias de la Biologicas, Facultad de Ciencias, Universidad Nacional Autónoma de México (PCB- FC-UNAM). Jorrit Poelen provided valuable feedback on the biological interactions dataset standards (GloBl). References . Baeza JA, Guéron R, Simpson L, Ambrosio LJ (2016) Population distribution, host- switching, and chemical sensing in the symbiotic shrimp Lysmatfa pedersent. implications for its mating system in a changing reef seascape. Coral Reefs 35 (4): 1213-1224. https:/fdoi. org/10.1007/s500338-016-1467-3 . Bauer RT (2004) Remarkable shrimps: adaptations and natural history of the Carideans. Animal Nat. Oklahoma University Press, Oklahoma, EE.UU. . Bóhlke JE, Robinson R (1969) Western Atlantic Sponge-Dwelling Gobies of the Genus Evermannichthys: Their Taxonomy, Habits and Relationships. Proceedings of the Academy of Natural Sciences of Philadelphia 121: 1-24. . Brooker R, Feeney VY, Sih T, Ferrari MO, Chivers D (2019) Comparative diversity of anemone-associated fishes and decapod crustaceans in a Belizean coral reef and seagrass system. Marine Biodiversity2609-2620. https://doi.org/10.10071 s12526-019-00993-5 . Bruce AJ, Jones AO (1976) Shrimps and prawns of coral reefs, with special reference to commensalism. In: Jones O, Endean R (Eds) Biology and geology of coral reefs. New York: Academic Press, New York, USA, 57 pp. https://doi.org/10.1016/ B978-0-12-395527-2.50009-3 . Carrera-Parra LF, Vargas-Hernández JM (1997) Comunidad críptica de esponjas del arrecife de Isla de Enmedio, Veracruz, México. Revista de Biologia Tropical 44-45 (1-3): 311-321. https://doi.org/10.15517/rbt.v4413,22055 . Chace FA (1972) The shrimps of the Smithsonian-Bredin Caribbean Expeditions with a summary of the West Indian shallow-water species (Crustacea: Decapoda: Natantia). Smithsonian Contributions to Zoology (98)1-179. https://doi.org/10.5479/si.00810282.98 . Chavarro SB, Zea S, Díaz JM (2004) Sponges and other ophiuroid microhabitats (Ophiuroidea: Echinodermata) at reef environments of San Bernardo Archipelago (Colombian Caribbean). Boletin de Investigaciones Marinas y Costeras. . Cházaro-Olvera S, Vázquez-López H (2014) Asociación de Syna/pheus (Decapoda, Alpheidea) con esponjas del Parque Marino Nacional Sinstema Arrecifal Veracruzano, SW del Golfo de México. BIOCYT 7 (25): 465-473. . Christoffersen ML (1972) Campagne de la Calypso au large des cótes Atlantiques de l'Amerique du Sud (1961-1962). |. Decapod Crustacea: Alpheoida. Annales de l'Institut Océanographique 55: 297-377. . Costello MJ, Bouchet P, Boxshall G, Fauchald K, Gordon D, Hoeksema BVWY, Poore GB, van Soest RM, Stóhr S, Walter TC, Vanhoorne B, Decock W, Appeltans VW (2013) 20 | P a g e Sponge-dwelling fauna: a review of known species from the Northwest Tropical ... 13 Global coordination and standardisation in marine biodiversity through the world register of marine species (WoRMS) and related databases. PLOS One 8 (1). hitps://doi.org/ 10.1371fjournal.pone.0051629 Coutiére H (1909) The American Species of Snapping Shrimps of the Genus Synalpheus. Proceedings of the United States National Museum 36: 1-93. https://doi.org/10.5479/si.00963801.36-1659. 1 Coutiére H (1910) The snapping shrimps (Alpheidae) of the Dry Tortugas, Florida. Proceedings of the United States National Museum 37 (1716): 485-487. https://doi.ora/ 10.5479/si.00963801.37-1716.485 Crocker LA, Reiswig HM (1981) Host specificity in spoonge-encrusting Zoanthidea (Anthozoa: Zoantharia) of Barbados, West Indies. Marine Biology 65 (3): 231-236. https:/fdoi.org/10.1007/BF00397116 Crowe SE, Thomas JD (2002) Abundance and Distribution of Commensal Amphipods from Common Marine Sponges of Southeast Florida. In: Escobar-Briones E, Alvarez F (Eds) Modern Approaches to the Study of Crustacea. 1, 1. Springer, 5 pp. https:/fdoi.org/10.1007/978-1-4615-0761-1_17 D'Aloia CC, Majoris JE, Buston PM (2011) Predictors of the distribution and abundance of a tube sponge and its resident goby. Coral Reefs 30 (3): 777-786. https://doi.org/ 10.1007/s500338-011-0755-1 Dardeau MR (1981) Caridea: General collections and observations. In: Rezak R, T.J. B (Eds) Northern Gulf of Mexico topographic features study. Final Report to the U.S. Department of Interior, Bureau of Land Management. 18. 29 pp. Dardeau MR (1984) Syna/pheus shrimps (Crustacea: Decapoda: Alpheidae). |. The gambarelloides group, with a description of a new species. Memoirs of the Hourglass Cruises 7 (2): 1-125. Dauer D (1973) Polychaete fauna associated with Gulf of Mexico sponges. Florida Scientist 36 (2-4): 192-196. Diaz M, Rutzler K (2001) Sponges: An essential component of Caribbean coral reefs. Bulletin of Marine Science 69 (2): 535-546. Duffy JE (1992) Host use patterns and demography in a guild of tropical sponge- dwelling shrimps. Marine Ecology Progress Series 90 (February): 127-138. https:/fdoi.org/10.3354/meps090127 Duffy JE (1996a) Resource-associated population subdivision in a symbiotic coral-reef shrimp. Evolution. Duffy JE (1996b) Synalpheus regalís, new species, a sponge-Dwelling shrimp from the Belize Barrier reef, with comments on host specificity in Syna/pheus. Journal of Crustacean Biology 16 (March 1993): 564-573. https://doi.org/10.2307/1548748 Duffy JE (1996c) Eusociality in a coral-reef shrimp. Nature 381 (June): 512-514. https:/fdoi.org/10.1038/381512a0 Duffy JE (1998) On the frequency of eusociality in snapping shrimps (Decapoda: Alpheidae), with description of a second eusocial species. Bulletin of Marine Science 63 (2): 387-400. Duffy JE, Macdonald KS (1999) Colony Structure of the Social Snapping Shrimp Synalpheus filidigitus in Belize. Journal of Crustacean Biology 19 (2). https://doi.ora/ 10.2307/1549235 Erdman RB, Blake NJ (1987) Population Dynamics of the Sponge-Dwelling Alpheid Synalpheus longicarpus, with Observations on S. brooksi and S. pectiniger, in Shallow- 21 | P a g e Pérez-Botello A, Simóes N Water Assemblages of the Eastern Gulf of Mexico. Journal of Crustacean Biology 7 (2). https:/fdoi.org/10.2307/1548613 García-Hernández JE, Hoeksema BW (2017) Sponges as secondary hosts for Christmas tree worms at Curacao. Coral Reefs 36 (4). https: //do¡.org/10.1007/ s00338-017-1617-2 Hagedorn M, Carter Y, Zuchowicz N, Phillips M, Penfield C, Shamenek B, Vallen Ea, Kleinhans FW, Peterson K, White M, Yancey PH (2015) Trehalose is a chemical attractant in the establishment of coral symbiosis. PLOS One 10: 1-18. https: //doi.orgf 10.1371fjournal.pone.0117087 Harzing AW (2007) Publish or Perish, available from https://harzing.comfresources/ publish-or-perish. Hendler G (1984) The Association of Ophiofhrix fineata and Callyspongía vaginalis: A Brittlestar-Sponge Cleaning Symbiosis? Marine Ecology 5 (1): 9-27. https://doi.org/ 10.1111/1439-0485.1984.tb00304.x Henkel T, Pawlik J (2014) Cleaning mutualist or parasite? Classifying the association between the brittlestar Ophiofhrix fineata and the Caribbean reef sponge Ca/lyspongía vaginalís. Journal of Experimental Marine Biology and Ecology 454: 42-48. https:/fdoi.org/10.1016/|.jembe.2014.02.005 Henkel TP, Pawlik JR (2005) Habitat use by sponge-dwelling brittlestars. Marine Biology 146 (2): 301-313. https://doi.org/10.1007/800227-004-1448-x Henkel TP, Pawlik JR (2011) Host specialization of an obligate sponge-dwelling brittlestar. Aquatic Biology 12: 37-46. https: //doi.org/10.3354/ab00322 Herrick FH (1981) Alpheus: A study in the development of Crustacea. Mem. Natl. Acad. Sci. 5: 370-463. Huang JP, McClintock JB, Amsler CD, Huang YM (2008) Mesofauna associated with the marine sponge Amphimedon viridis. Do its physical or chemical attributes provide a prospective refuge from fish predation? Journal of Experimental Marine Biology and Ecology 362 (2): 95-100. https://doi.org/10.1016/| jembe.2008.06.007 Hultgren K, Duffy JE (2010) Sponge host characteristics shape the community structure of their shrimp associates. Marine Ecology Progress Series 407: 1-12. https://doi.org/ 10.3354/meps08609 Hultgren K, MacDonald K, Duffy JE (2011) Sponge-dwelling snapping shrimps (Alpheidae: Synalpheus) of Barbados VWest Indies, with a description of a new eusocial species. Zootaxa 16 (2834): 1-16. Hultgren KM, MacDonald KS, Duffy JE (2010) Sponge-dwelling snapping shrimps of Curacao, with descriptions of three new species. Zootaxa 262 (2372): 221-262. https://doi.org/10.11646/zootaxa.2372.1.20 Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69 (3): 373-386. https:/fdoi.org/10.2307/3545850 Koukouras A, Russo R, Voultsiadou-Koukoura E, Arvanitidis C, Stefanidou D (1995) Macrofauna associated whit sponge species of different morphology. Marine Ecology 17 (4): 569-582. https: /fdoi.org/10.1111/|.1439-0485.1996.tb00418.x Lattig P, Martin D (2009) A taxonomic revision of the genus Haplosylfís langerhans, 1887 (Polychaeta: Syllidae: Syllinae). Zootaxa 40 (2220): 1-40. Lattig P, Martín D (2011) Sponge-associated Haplosyllis (Polychaeta: Syllidae: Syllinae) from the Caribbean Sea, with the description of four new species. Scientia Marina 75 (4): 733-758. https:/fdoi.org/10.3989/scimar.2011.75n4733 22 | P a g e Sponge-dwelling fauna: a review of known species from the Northwest Tropical ... 15 LeCroy S (1995) Amphipod Crustacea l!!. Family Colomastigidae. Memoirs of the Hourglass Cruises1-139. Macdonald K, Duffy JE (2006) Two New Species of Sponge-Dwelling Snapping Shrimp from the Belizean Barrier Reef, with a Synopsis of the Syna/pheus brooksi Species Complex. American Museum Novitates 3543: 1-22. https://doi.org/10.1206/0003- 0082(2006)3543[1:tnsoss]2.0.c0;2 Macdonald KS, Ríos R, Duffy JE (2006) Biodiversity, host specificity, and dominance by eusocial species among sponge-dwelling alpheid shrimp on the Belize Barrier Reef. Diversity and Distributions 12 (2): 165-178. https://doi.org/10.1111/| 1366-9516. 2005.00213.x Macdonald KS, Hultgren K, Duffy JE (2009) The sponge-dwelling snapping shrimps (Crustacea, Decapoda, Alpheidae, Syna/pheus) of Discovery Bay, Jamaica, with descriptions of four new species. Zootaxa 57: 1-57. Maldonado M, Young C (1996) Effects of physical factors on larval behavior, settlement and recruitment of four tropical demosponges. Marine Ecology Progress Series 138 (1-3). 169-180. https://doi.org/10.3354/meps138169 Maldonado M, Aguilar R, Bannister RJ, Bell JJ, Conway KW, Dayton PK, Díaz C, Gutt J, Kelly M, Kenchington ELR, Leys SP, Pomponi SA, Rapp HT, Rútzler K, Tendal OS, Vacelet J, Young CM (2017) Sponge grounds as key marine habitats: A synthetic review of types, structure, functional roles, and conservation concerns. In: Rossi S, Bramanti L, Gori A, Orejas C (Eds) Marine animal forests the ecology of benthic biodiversity hotspots. Springer Nature, Cham, Switzerland, 39 pp. hitps://do¡.org/10.1007/978- 3-319-17001-5 24-1 Montenegro-González J, Acosta A (2010) Habitat preference of Zoantharia genera depends on host sponge morphology. Universitas Scientiarum 15 (2): 110-121. https://doi.org/10. 11144/javeriana.sc15-2.hpoz Ortiz M, Winfield |, Cházaro-Olvera S (2011) A new sponge-inhabiting leptostracan species of the genus Nebalía (Crustacea: Phyllocarida: Leptostraca) from the veracruz Coral Reef System, gulf of mexico. Zootaxa (3027)52-62. https: //doi.org/10.11646/ zootaxa.3027.1.6 Ortiz M, Winfield |, Barcena-Cisneros M, Cházaro-Olvera S (2013) Species of the genus Periclimenaeus (Decapoda, Caridea, Palaemonidae) associated with sponges from the Veracruz Coral Reef System National Park, SW Gulf of Mexico. Crustaceana 86 (6): 641-650. https:/fdoi.org/10.1163/15685403-00003168 Paerse AS (1932) Inhabitants of certain sponges of Dry Tortugas. Carneige Inst. Wash. 28: 119-122. Pawlik JR (2011) The chemical ecology of sponges on caribbean reefs: natural products shape natural systems. BioScience 61 (11): 888-898. https: //doi.org/10.1525/bio. 2011.61.11.8 Pearse AS (1950) Notes on the Inhabitants of Certain Sponges at Bimini. Ecology 31 (1). https://doi.org/10.2307/1931369 Pequegnat LH, Heard RW (1979) Syna/pheus agelas, new species of snapping shrimp from the Guf of Mexico and Bahamas Islands (Decapoda: Caridea. Alpheidae). Bulletin of Marine Science 29 (1): 110-116. Perez-Botello AM (2019) Cambios de diversidad de fauna asociados a Ca/lyspongía vaginalis, en arrecifes coralinos del Banco de Campeche. MsC Thesis, Posgrado en Ciencias Biologicas, UNAM 23 | P a g e Pérez-Botello A, Simóes N Poelen J, Simons J, Mungall € (2014) Global biotic interactions: An open infrastructure to share and analyze species-interaction datasets. Ecological Informatics 24: 148-159. https://doi.org/10.1016fj.ecoinf.2014.08.005 Randall JE, Lobel PS (2009) A literature review of the sponge-dwelling gobiid fishes of the genus. Zootaxa 2133 (June 2009): 1-19. https://doi.org/10. 11646/zootaxa.2133.1.1 Rebolledo AP, Wehrtmann IS, Felder DL, Mantelatto FL (2014) Embryo production in the sponge-dwelling snapping shrimp Syna/pheus apioceros (Decapoda, Alpheidae) from Bocas del Toro, Panama. ZooKeys 238 (457): 227-238. https://doi.org/10.3897/ zookeys.457.6403 Reimer JD, Wee HB, Garcia-Hernández J, Hoeksema B (2018) Zoantharia (Anthozoa: Hexacorallia) abundance and associations with Porifera and Hydrozoa across a depth gradient on the west coast of Curacao. Systematics and Biodiversity 16 (8): 820-830. https:/fdoi.org/10.1080/14772000.2018.1518936 Reyes-Bonilla H, Jordán-Dahlgren E (2017) Caribbean coral reefs: past, present, an insights into the future. In: Rossi S, Bramanti L, Gori A, Orejas C (Eds) Marine animal forests the ecology of benthic biodiversity hotspots. Springer Nature, 41 pp. https:/fdoi.org/10. 1007/978-3-319-17001-5_2-1 Richards VP, Thomas JD, Stanhope MJ, Shivji MS (2007) Genetic connectivity in the Florida reef system: comparative phylogeography of commensal invertebrates with contrasting reproductive strategies. Molecular Ecology 16 (1): 139-157. https://doi.org/ 10.111111365-294X.2006.03145.x Rios R, Duffy JE (1999) Description Of Synalpheus williams!, A New Species Of Sponge-Dwelling Shrimp (Crustacea : Decapoda : Alpheidae), With Remarks On Its First Larval Stage. Proceedings of The Biological Society of Washington 112: 541-552. Ríos R, Duffy JE (2007) A review of the sponge-dwelling snapping shrimp from Carrie Bow Cay, Belize, with description of Zuza/pheus, new genus, and six new species (Crustacea: Decapoda: Alpheidae). Zootaxa 1602: 1-89. httos://do¡.org/10.11646/ zootaxa.1602.1.1 Robertson DR, Tassell JV (2019) Shorefishes of the Greater Caribbean: online information system. Rossi S, Bramanti L, Gori A, Orejas C (2017) Marine Animal Forests The Ecology of Benthic Biodiversity Hotspots. Springer International Publishing, Cham. [ISBN 978-3-319-21011-7] https:/fdoi.org/10.1007/978-3-319-21012-4 Santana-Moreno LD, Grave SD, Simóes N (2013) New records of caridean shrimps (Decapoda: Caridea) from shallow water along the northern Yucatan peninsula coasts of México. Nauplius 21 (02): 225-238. https://doi.org/10.1590/50104- 64972013000200009 Scott PJB, Reiswing HM, Marcotte BM (1988) Ecology, functional morphology, behaviour, and feeding in coral and sponge-boring species of Upogebia (Crustacea: Decapoda: Thalassinidea). Canadian Journal of Zoology 66(2): 483-495. https: //doi.org/ 10.1139/288-069 Spalding M, Fox H, Allen G, Davidson N, Ferdaña Z, Finlayson M, Halpern B, Jorge M, A. L,L, Lourie S, Martin K, McManus E, Molnar J, Recchia C, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57 (07): 573-583. https: /fdoi.org/10. 164 1 B57 707 Swain TD, Wulff JL (2007) Diversity and specificity of Caribbean sponge-zoanthid symbioses: A foundation for understanding the adaptive significance of symbioses and 24 | P a g e Sponge-dwelling fauna: a review of known species from the Northwest Tropical ... 17 generating hypotheses about higher-order systematics. Biological Journal of the Linnean Society 92 (4): 695-711. https://doi.org/10.11111|.1095-8312.2007.00861.x Swain TD (2012) Context-dependent effects of symbiosis: Zoanthidea colonization generally improves Demospongiae condition in native habitats. Marine Biology 159 (7): 1429-1438. https:/fdoi.org/10.1007/500227-012-1919-4 Tews AJ, Brose U, Grimm Y, Tielbórger K, Wichmann MC, Schwager M, Jeltsch F (2016) animal species diversity driven by habitat heterogeneity / diversity: The importance of keystone structures. Journal of Biogeography 31 (31): 79-92. https:/fdoi.org/10. 10467. 0305-0270.2003.00994 .x Thomas JD, Klebba K (2006) Studies of Commensal Leucothoid Amphipods: Two New Sponge-Inhabiting Species from South Florida and the Western Caribbean. Journal of Crustacean Biology 26 (1): 13-22. https://doi.org/10.1651/C-2624.1 Thomas JD, Klebaa KN (2007) New species and host associations of commensal leucothoid amphipods from coral reefs in Florida and Belize (Crustacea:Amphipoda). Zootaxa 1494 (1): 1-44. https://doi.org/10. 11646/zootaxa.1494.1.1 Tobb DC, Manning RB (1961) A checklist of the flora and fauna of nothen Florida Bay and adjacent brakish waters of the Florida mainland collected during the period July, 1957 through September, 1960. Bull. Mar. Sci. Gulf Caribb. 11 (4): 552-649. Tóth E, Bauer RT (2008) Synalpheus paraneptunus (Crustacea: Decapoda: Caridea) populations with intersex gonopores: Á sexual enigma among sponge-dwelling snapping shrimps. Invertebrate Reproduction and Development 51 (1): 49-59. https:/fdoi.org/10. 1080/07924259.2008.9652255 Tyler JC, Bóhlke JE (1972) Records of Sponge-Dwelling Fishes , Primarily of the Caribbean. Bulletin of Marine Science 22 (3): 601-642. Ugalde García DM (2014) Aspectos ecológicos de los camarones Carídeos asociados a espojas de la costa sureste del Golfo de México. MsC Thesis, Posgrado en Ciencias del Mar y Limnologia Biologicas, UNAM Victor B, Krasovec FH (2018) Facultative cleaning behavior in a western Atlantic sponge goby, Efacatinus xanthiprora (Teleostei: Gobiidae). Journal of the Ocean Science Foundation 31 (2018): 1-7. Villamizar E, Laughlin RA (2011) Fauna Associated with the Sponges Aplysina archeri and Aplysina lacunosa in a Coral Reef of the Archipiélago de Los Roques, National Park, Venezuela. Fossil and Recent Sponges 522-542. https://doi.org/10.1007/ 978-3-642-75656-6_44 Watson RA, Pollack JB (1999) How symbiosis can guide evolution. Advances in Artificial Life 1674: 29-38. https://doi.org/10.1007/3-540-48304-7 7 Wenat PH, Van Dolah RF, O'Rourke CB (1985) A Comparative Study of the Invertebrate Macrofauna Associated with Seven Sponge and Coral Species Collected from the South Atlantic Bight. Journal of the Elisha Mitchell Scientific Society 101 (267_vol_101_pt_003_0003): 187-203. Westinga E, Hoetjes PC (1981) The Intraponge fauna of Spheciospongía vesparia (Porifera, Demospongiae) at Curacao and Bonaire. Mar Biol 62: 139-150. https:/fdoi.org/10.1007/BF00388176 Williams AB (1984) Mud Shrimps, Upogebiidae, from the Western Atlantic (Crustacea: Decapoda: Thalassinidae). San Diego Soc. Nat. Hist Mem 14: 1-60. Winfield |, Ortiz M, Cházaro-Olvera S (2009) A new sponge-inhabiting amphipod species (Crustacea, Gammaridea, Sebidae) from the Veracruz Coral Reef System, 25 | P a g e Pérez-Botello A, Simóes N southwestern Gulf of Mexico. Organisms Diversity and Evolution 9 (1): 1-72. https:/fdoi.org/10.1016/j|. ode.2 08. 12.001 Winfield |, Ortiz M (2010) Colomastigids (Amphipoda: Gammaridea: Colomastigidae) from the Veracruz Coral Reef System, SW Gulf of Mexico, with a description of two new species associated with sponges. Scientia Marina 74 (4): 773-782. https: //doi.org/ 10.3989/scimar.2010.74n4773 Wulff JL (1997) Mutualism among species of coral reef sponges. Ecological Society of America 78 (1): 146-159. https://doi.org/10.2307/2265985 26 | P a g e 27 | P a g e Artículo 2: (Publicado) Geographic range size and species morphology determines the organization of sponge host-guest interaction networks across tropical coral reefs. Revista: PeerJ Autores: Antar Mijail Pérez-Botello; Wesley Dáttilo; Nuno Simões Estado: Publicado Año: 2023 DOI: https://doi.org/10.7717/peerj.16381 Resumen Las esponjas son organismos ampliamente distribuidos en los arrecifes de coral del Atlántico Tropical Noroccidental, brindando servicios como refugio, protección contra depredadores y fuente de alimento para una amplia diversidad de especies tanto de vertebrados como de invertebrados. La alta diversidad de fauna asociada a las esponjas puede generar complejas redes de interacciones a lo largo de gradientes espaciotemporales. Una forma de comenzar a descubrir la organización de las complejas redes de interacción entre las esponjas y sus huéspedes es comprender cómo el área geográfica acumulada, la morfología de las esponjas y la taxonomía de las esponjas contribuyen a la conectividad de las especies involucradas dentro de dichas redes. Este estudio es un metaanálisis basado en la literatura previa sobre interacciones entre esponjas y sus huéspedes recopilados en 65 publicaciones científicas. Esta recopilación resultó en un total de 745 interacciones entre esponjas y fauna asociada en ambientes de arrecifes de coral del Mar Caribe y el Golfo de México. El objetivo de este trabajo fue analizar la contribución de las especies de esponjas a la organización de las redes en los arrecifes de coral del Atlántico Tropical del Noroccidental mediante la combinación de siete descriptores a nivel de especie y la relación de esta contribución con tres rasgos funcionales principales: el área geográfica acumulada de las esponjas, la morfología funcional de las esponjas y el sesgo taxonómico de las esponjas. En general, observamos que las esponjas con una distribución amplia y un área geográfica acumulada mayor tenían una mayor contribución estructural a la red. Del mismo modo, encontramos que las morfologías funcionales en forma de copa y masivas tienden a ser formas con una mayor contribución a la organización de la red de interacciones en comparación con las morfologías erectas e incrustantes. Por último, no detectamos un sesgo taxonómico en la organización de la red de interacciones en relación con los órdenes de las esponjas. Estos resultados resaltan la importancia de una combinación específica de rasgos de las esponjas para promover la diversidad de asociaciones entre las esponjas arrecifales y sus especies huéspedes. MIO 2) PeerJ Hubs Published on behalf of International Association for Cde lr] [TN Submitted 6 February 2023 Accepted 9 October 2023 Published 24 November 2023 Corresponding authors Antar Mijail Pérez-Botello, antarmijailecomunidad.unam.mx Nuno Simóes, nseciencias.unam.mx Academic editor Balu Alagar Venmathi Maran Additional Information and Declarations can be found on page 16 DOI 10.7717/peerj.16381 (5 Gopyright 2023 Pérez Botello et al. Distributed under Creative Commons CC-BY 4.0 [OPEN ACCESS | Geographic range size and species morphology determines the organization of sponge host-guest interaction networks across tropical coral reefs Antar Mijail Pérez-Botello*”, Wesley Dáttilo? and Nuno Simóes'** ' Unidad Multidisciplinaria de Docencia e Investigación, Facultad de Ciencias, Universidad Nacional Autónoma de México, Sisal, Yucatán, Mexico . Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Ciudad de Mexico, Mexico 3 Red de Ecoetología, Instituto de Ecología A.C., Xalapa, Veracruz, Mexico 4 Taboratorio Nacional de Resilencia Costera (LANRESC, CONACYT), Sisal, Yucatan, Mexico 5 International Chair for Coastal and Marine Studies in Mexico, Harte Research Institute for Gulf of Mexico Studies, Texas ARM University, Corpus Christi, TX, United States of America ABSTRACT Sponges are widely spread organisms in the tropical reefs of the American Northwest-Atlantic Ocean, they structure ecosystems and provide services such as shelter, protection from predators, and food sources to a wide diversity of both vertebrates and invertebrates species. The high diversity of sponge-associated fauna can generate complex networks of species interactions over small and large spatial temporal gradients. One way to start uncovering the organization of the sponge host-guest complex networks is to understand how the accumulated geographic area, the sponge morphology and, sponge taxonomy contributes to the connectivity of sponge species within such networks. This study is a meta-analysis based on previous sponge host-guest literature obtained in 65 scientific publications, yielding a total of 745 host-guest interactions between sponges and their associated fauna across the Caribbean Sea and the Gulf of Mexico. We analyzed the sponge species contribution to network organization in the Northwest Tropical Atlantic coral reefs by using the combination of seven complementary species-level descriptors and related this importance with three main traits, sponge-accumulated geographic area, functional sponge morphology, and sponges” taxonomy bias. In general, we observed that sponges with a widespread distribution and a higher accumulated geographic area had a greater network structural contribution. Similarly, we also found that Cup-like and Massive functional morphologies trend to be shapes with a greater contribution to the interaction network organization compared to the Erect and Crust-like morphos. Lastly, we did not detect a taxonomy bias between interaction network organization and sponges” orders. These results highlight the importance of a specific combination of sponge traits to promote the diversity of association between reef sponges and their guest species. Subjects Biodiversity, Biogeography, Ecology, Marine Biology, Zoology Keywords Caribbean reefs, Community ecology, Marine ecology, Gulf of Mexico reefs, Functional traits, Ecology Howto cite this article Pérez-Botello AM, Dáttilo W, Simóes N. 2023. Geographic range size and species morphology determines the organization of sponge host-guest interaction networks across tropical coral reefs. Peer] 11:e16381 DOI 10.7717/peerj.16381 ==> o-7 28 | P a g e PeerJ INTRODUCTION The ecology of a species or community can be studied based on the functional characteristics of organisms (Gagic et al., 2015; Schmitz et al., 2015; Pimiento et al., 2020). A functional trait or characteristic is an organism's distinguishable and quantifiable attribute, typically evaluated at the individual level and comparable across different species (Poff et al., 2006; Weiher, 2011). Classifying biodiversity according to some trait or functional group emphasizes the phenotypic differences between taxa and breaks the species ancestor-descendent phylogenetic link (McGill et al., 2006; Weiher, 2011; Gagic et al., 2015; Bagousse-Pinguet et al., 2019). Some functional traits such as feeding strategies, reproduction, dispersal, species distribution, response to environmental changes, species morphology or the ability of certain species to create microhabitats and vertical complexity, generally determine what, how, where and why we observe different species in an ecosystem (McGill et al., 2006; Weiher, 2011; Costello et al., 2015; Gagic et al., 2015; Beauchard et al., 2017; Pimiento et al., 2020). Sponges, some of the oldest animals on Earth with fossil evidence dating back over 580 million years ago (Chen, 2012), are crucial components of modern marine environments, acting as keystone species in benthic habitats (Rútlzer, 2004; Wulff, 2006, 2016; Bell, 2008; González-Rivero, Yakob e+ Mumby, 201 1; Maldonado et al., 2016; Brusca, Moore ++ Shuster, 2018). In particular, sponges can structure coral reef ecosystem performing multiple functions simultaneously, for example, sponge species are capable of filtering large volumes of water, enhancing primary production, participating in critical processes such as carbon, nitrogen, silicon, and oxygen cycles, and providing habitats for a wide variety of life forms which included organism with simple body plans (microorganisms) to complex ones (invertebrates and vertebrates) (Diaz e Ríitlzer, 2001; Bell, 2008; Bell et al., 2013; Pawlik et al., 2013; Maldonado et al., 2016; Rossi et al., 2017). These previous citated studies have recognized the functional importance of sponges in coral reef ecosystems but this understanding has not always been translated into larger scale efforts (Bell, 2008; Gatizére et al., 2022) and even less into no-trophic interaction networks ecology (i.e., host-guest interactions). Host-guest interactions, refer to the co-occurrence of two different species in both space and time (Watson e Pollack, 1999; Baeza, 2015; Overstreet (> Lotz, 2016). The key attribute of these associations is the use of one organism as habitat by another organism of a different species (Baeza, 2015; Overstreet e> Lotz, 2016). In this context, when we know the costs and benefits inherent to these relationships, it is possible to classify the host-guest interactions into parasitism, mutualism, or commensalism (Thiel, 1999; Watson e> Pollack, 1999; Thiel + Baeza, 2001; Baeza, 2015). While itis well-documented that different sponge species can be habitat facilitators for a wide range of organisms, the specific costs acquired by the sponge species involved in these interactions remain poorly understood (Duffy, 1992; Wulff, 1997; Bell, 2008; Maldonado et al., 2016). In order to maintain consistency in the interactions classification, the term “host-guest interaction” is assumed by this study to describe the relationship between sponges and the fauna that inhabit them. Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 12/23 29 | P a g e PeerJ Coral reefs are a dynamic and complex marine ecosystem involving a wide array of interacting organisms (Knowlton, 2001; Bauer, 2004; Hagedorn et al., 2015). The mutualistic relationship between cyanobacteria (Symbiodinium sp.) and scleractinian corals is crucial for the existence of this ecosystem, yet there are many other interspecific relationships that contribute to its complexity (Bauer, 2004 Hagedorn et al., 2015). One example is the host-guest relationship between sponges and the organisms that inhabit them (Diaz + Rútlzer, 2001; Hooper e van Soest, 2002b; Maldonado et al., 2016; Pérez-Botello > Simóes, 2021). Sponges of class Demospongiae possess the highest number of host-guest associations diversity in coral reefs across the globe, highlighting Agelas, Aplysina, Xestospongia, and Callyspongia as the main hostesses genera (Maldonado et al, 2016). However, the study of ecological interactions in reef environments and even more in sponge-associated fauna focuses on analyzing interactions between paired species or on a small subset of networks. In the Northwest Tropical Atlantic (NWTA) coral reefs (the Caribbean Sea, the Gulf of México, and Bermuda), sponges are a crucial benthic component along with scleractinian corals and macroalgae (González-Rivero, Yakob + Mumby, 2011). Phylum Porifera has a heterogeneous distribution, being Caribbean Sea reefs the ones with the highest species richness, then the Gulf of Mexico reefs, and finally Bermuda reefs (Ocean Biodiversity Information System (OBIS), 2020). These sponges could provide a series of services to several guest organisms; for example, sponges as habitat facilitators, can be a food source to the associated organisms, or can provide a certain degree of protection to the organisms that associate with them, either through the direct use of different structures as shelter or camouflage, or through the indirect protection derived from secondary metabolites produced by the sponge (Dembowska, 1926; McLay, 1983; Bedini, Canali + Bedini, 2003; Pawlik, 2011; Cruz Ferrer, 2014; Maldonado et al., 2016; Harada, Hayashi + Kagaya, 2020). Due to the multifunctionality that sponges present in the NWTA reefs, the community structure of sponge species directly influences other reef organisms (Bell, 2008). The NWTA sponge-associated fauna is incredibly diverse, with over 284 known associated species inhabiting 101 sponge species (Pérez-Botello > Simóes, 2021). The main pattern is that host-guest associations are species-specific at sponge phylam level, meaning that sponges have the potential to maintain part of the biodiversity of reef systems (Maldonado et al., 2016; Pérez-Botello + Simóes, 2021). However, when evaluating the sponge-guest species richness, a few sponge species, such as Ircinia strobilina (Lamarck, 1816), Callyspongia (Cladochalina) aculeata (Linnaeus, 1759), and 1. felix (Duchassaing % Michelotti, 1864), concentrate 187 associated guest fauna (Dardeau, 1981; Carrera-Parra + Vargas-Hernández, 1997, Pérez-Botello, 2019), more than half of the associated species recorded, while 33 sponge species only interact with 51 spp., hosting between one to three spp. (for an exhaustive list of sponge-associated species diversity review Pérez-Botello e Simóes (2021) and visit the website https://marinespeciesinteractions.org/?p=2302). These host-guest species interactions array generates a complex network where sponges act both as hosts and connectors within the network, emerging the question of what functional characteristics regulate the contribution that each sponge species has to the structure of the host-guest interactions network within the NWTA coral reefs? Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 == 13/23 30 | P a g e PeerJ In the present study, we evaluated three traits that could regulate the structure of the interactions network. First, the sponge-accumulated geographic area, or the habitat availability to be colonized, could regulate the contribution that each sponge species has to the structure of the network. In addition to the widely recognized ecological species-area pattern described by the Island Biogeography Theory (MacArthur e Wilson, 1963; Cornell + Lawton, 1992; Lawton, 1999; Losos et al., 2009), Galiana et al. (2018) proposed a relationship between geographic area and the probability of establishing a species interaction. We tested the hypotheses that there is a positive correlation between the sponge-accumulated geographic area and the network structural importance of each sponge species (Moulatlet, Dáttilo + Villalobos, 2023). The second tested trait is how habitat heterogeneity, measured as the functional sponge morphology, promotes the establishment of guest species. For example, sponges with large volumes could host a certain types of guest organisms than sponges with smaller volumes and more tightly packed shapes (Koukouras et al., 1996; Hooper e van Soest, 2002a; Maldonado et al., 2016; Pérez-Botello, 2019). For this reason, we also tested the hypotheses that there is a plausible suitable functional morphological group that promotes the establishment of sponge-guest interactions. Lastly, we tested if the sponges” taxonomy bias could affect the importance of each taxon in the interaction network structure. In other guest-host interaction models, particularly mutualism between sea anemones and crustaceans of the Caribbean Sea, it has been demonstrated a pairwise taxonomic relationship between anemones and shrimps (Mascaró et al., 2012; McKeon e O'Donnell, 2015; Kou et al, 2015; Pérez-Botello, Mascaró e Simóes, 2021), such as Bartholomea annulata (Le Sueur, 1817) and Condylactis gigantea (Weinland, 1860), two sea anemones of the Actiniaria order that concentrate the major diversity of anemone-shrimps as Alpheus armatus Rathbun, 1901, Ancylomenes pedersoni (Chace, 1958), Thor amboinensis (De Man, 1888) and Periclimenes yucatanicus (Ives, 1891) (Silbiger e Childress, 2008; McCammon, Sikkel +- Nemeth, 2010; McCammon e Brooks, 2014). Therefore, there may be a pattern in which sponge orders with a higher associated species richness are essential to maintain the structure of the host-guest interaction network on reef sponges. Ecological networks can be visualized as a series of interconnected nodes and edges; these nodes represent different species within the ecosystem, and the edges represent the relationships and interactions between them (Ramírez-Flores et al., 2015; Cantor et al., 2018; Dehling, 2018; Martínez-Falcón, Martínez-Adriano e Dáttilo, 2019). These fixed representations of ecological processes help to identify keystone species that maintain and connect the network and predict changes in ecological communities, providing a comprehensive understanding of the dynamics of biological interactions (Bastolla et al, 2009; Cantor et al., 2018). Applying a network analysis to infer functional roles has been previously employed in other ecological systems, such as seed dispersal (Vidal et al., 2014), insect-plant mutualistic networks (Bastolla et al., 2009), vertebrate scavenging (Sebastián- González et al., 2021), and plant-pollinator—protective ant—seed disperser multi-interaction networks (Dáttilo et al., 2016). In this stady we perform a large-scale community-level network analysis on sponge-associated fauna, offering a valuable insight into the ecological importance of coral Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 | 14/23 ==> 0-7 31 | P a g e PeerJ reef sponges host-guest interactions. We aim to evaluate the structural importance of each sponge species and identify the keystone functions that maintain the organization of sponges host-guest interaction networks across NWTA coral reefs. MATERIALS AND METHODS Database We employed a bibliographic Database containing 101 host sponges species that inhabit the NWTA coral reefs, which were classified into 12 orders of class Demospongiae (Pérez- Botello e> Simóes, 2021; https://zenodo.org/record/3333023). In order to ensure the highest possible taxonomic resolution, the original database was filtered to include only sponge taxonomic entities at species level. The dataset analyzed in this meta-analysis comprised 65 scientific publications, yielding a total of 745 host-guest interactions between sponges and their associated fauna within the NWTA coral reefs (Dataset S1). We employed the Marine Ecoregions of the World (MEOW) to systematically organize the host-guest interactions dataset in a cohesive manner (Spalding et al., 2007). The analyzed ecoregions were Bahamian, Bermuda, Eastern Caribbean, Floridian, Greater Antilles, Northern Gulf of Mexico, Southern Caribbean, Southern Gulf of Mexico, Southwestern Caribbean and Western Caribbean. The number of interactions, locations and publications records per ecoregion varied, with Bahamian recording 46 interactions across 28 locations and 14 publications, Bermuda recording eight interactions across one location and one publications, Eastern Caribbean recording 55 interactions across 17 locations and six publications, Floridian recording 46 interactions across 22 locations and 14 publications, Greater Antilles recording 66 interactions across 23 locations and eight publications, Southern Caribbean recording 106 interactions across 14 locations and 10 publications, Northern Gulf of Mexico recording 131 interactions across seven locations and nine publications, Southwestern Caribbean recording 77 interactions across 19 locations and 146 publications, Southern Gulf of Mexico recording 317 interactions across 19 locations and 10 publications, and Western Caribbean recording 110 interactions across 15 locations and 18 publications. A total of 76 sponge species were recorded hosting 268 sponge-associated fauna (Fig. 1). To assess publication bias and measure the effect that could have in terms of replication we relate the number of publications by ecoregion (observed publication sample sizes) with the publications total number in the dataset (expected publication sample size) (Egger et al., 1997, Thompson, Smith ++ Sharp, 1997; Thompson e Sharp, 1999). With this citation proportion, we estimate the publication heterogeneity and evaluate the discrepancy between the observed and expected publication effort across ecoregions. The meta-bias analysis demonstrated that each ecoregion exhibited homogeneity in publications proportion Pp estimator = Maximum-likelihood, p-value = 0.99), and no statistically significant publication bias was found between regions (bias method = Thompson, p-value = 0.28) (Fig. S1) indicating that the replication of the study across the different regions is reliable. We evaluated the publication bias using the functions 'metaprop” and “metabias” from the package “meta” in R (Schwarzer, Carpenter e Riicker, 2015; Balduzzi, Rúcker e Schwarzer, 2019). Pérez-Botello et al. (2023), PeerJ, DOI 10.7717/peerj.16381 5/23 32 | P a g e PeerJ Figure 1 Regionalized map of sponge host-guest interactions in the Northwestern Tropical Atlantic coral reefs. The ecoregions are based on the Marine Ecoregions of the World classification (Spalding et al., 2007). Each region is labeled with the number of articles that provide information (1) and the number of recorded interactions (i). The sizes of each circle represent the number of citations that has each record. The colors of the circles represent the particular regionalization, gray for the Bahamian, light green for Bermuda, Blue for the Eastern Caribbean, light yellow for Floridian, dark yellow for the Grater Antilles, orange for the Northern Gulf of Mexico, sapphire for the Southeastern Caribbean, brown for the Southeastern Gulf of Mexico, light blue for the Southwestern Caribbean and dark green for the Western Caribbean. To interactively explore this map, visit the website https://marinespeciesinteractions.org/? p=2302. Full-size Ea] DOI: 10.7717/peerj.16381/fig-1 Interactive figures are available on Marine Species Interactions web site (https:// marinespeciesinteractions.org/?p=2271) and the working datasets, are available on Zenodo (https://doi.org/10.5281/zenodo.7549399). Characterizing the structure of sponge-assosiated fauna network To analyze the sponge host-guest interactions, we employed a complex network approach (Dáttilo +: Rico-Gray, 2018). The relationships (links) between different species are represented as interconnected nodes. Because the information on sponge-guest relationships used in this study came from different publication records employing several sampling methodologies and criteria for accounting interaction frequency, we used a qualitative network (Bellotti, 2014) in which a value of one represented the presence of an interaction between a sponge and one guest species, and O indicated the absence of a recorded interaction. This approach allowed us to analyze the contribution to network organization and species” importance without the influence of changing sampling methods and, therefore, ensuring that all species report the same type of biological information (Bellotti, 2014; Dáttilo et al., 2016). Pérez-Botello et al. (2023), PeerJ, DOI 10.7717/peerj.16381 A A 33 | P a g e PeerJ We begin by characterizing the contribution to network organization by using two structural properties frequently reported in species interaction networks: nestedness and modularity. In nested networks, species engaged in few interactions (i.e., potentially specialists) are connected to a subset of species engaged in many interactions (i.e., potentially generalists), while modularity describes a pattern where there are subgroups of species of one lower level (e.g., sponges) that interact strongly with a subgroup of species of another higher level (e.g., guests). Nestedness was estimated using the Nestedness Metric based on Overlap and Decreasing Fill (NODEF; Almeida-Neto, Frensel + Ulrich, 2012), a nestedness descriptor that varies from zero (not nested) to 100 (perfectly nested). We estimated the Modularity (Q) using the QuanBiMo algorithm, which repeatedly divides a network into modules (we set to 107 swaps) and re-calculates modularity until reaching an optimal Q value, which ranges from zero (no more links within modules than expected by chance) to one (maximum possible modularity). Then, we generated 1,000 random matrices to test the significance of nestedness and modularity according to a null model, in which the number of interactions and the number of links (and hence connectance) keep constant. We calculated nestedness and modularity using the function network level” from the package *bipartite” in R (Dormann, Gruber e Frind, 2008). Network structural contribution We considered seven complementary species-level descriptors to measure the species” contribution to network organization: species degree, betweenness, closeness, Katz centrality, among-module connectivity (ci), standardized within-module degree (zi), and contribution to nestedness (cni). We chose these descriptors because they provide complementary biological information on the contribution to network structure and, therefore, are expected to be more robust than on a single measure (Vidal et al., 2014; Corro et al., 2022). Degree centrality is the number of interactions established by a species (Borrett, 2012). Betweenness centrality calculates the fraction of the smallest number of links between any two species in a network that pass-through a given species. Closeness centrality is a measure of the average of the geodesic distances (shortest path lengths) from a focal species to all other species in the network. Biologically, a species with high closeness centrality is considered to be centrally located and has quick access to resources effectively throughout the network. Katz centrality calculates the number of immediate neighbors and the direct and indirect paths of a species to other species in the network (Katz, 1953). Among-module connectivity (ci) describes how evenly distributed are the interactions of a given species across modules (Olesen et al., 2007). Standardized within-module degree (zi) calculates of the extent to which each species is connected to the other species in its module within the network (Olesen et al., 2007). Contribution to nestedness (cni) is the degree to which the interaction of species increases or decreases the network's overall nestedness (Saavedra et al, 2011). Because all these descriptors were highly correlated (Fig. S2) we used a principal component ordination (PCO) to reduce the seven-dimensional space to a single generalized index summarizing species” contribution to network organization as often used in specialized literature. The first principal component (PCO1) accounted for 99.8% of the variability, indicating complementarity among the seven descriptors, where Pérez-Botello et al. (2023), PeerJ, DOI 10.7717/peerj.16381 7/23 34 | P a g e PeerJ Figure 2 Illustrations of sponge's functional morphologies. Dark yellow for Crust-like, light blue for Massive, pink for Cup-like and orange for Erec. For more information on the morphological standar- dization used, please refer to Schónberg (2021). Full-size Ka] DOI: 10.7717/peerj.16381/fig-2 species with higher PCO1 scores exhibit many interactions, are connected to other species by multiple direct and indirect pathways, and represent a higher contribution to network organization. Since the values obtained from PCO1 are both positive and negative and the magnitude of change exceeds the tens between the minimum and maximum value, we changed the starting point of the values to zero, and we did a square root transformation of PCO1 (PCO1'”). Sponge functional traits Information on two functional traits that may influence a sponges' ability to host a greater or lesser number of species was compiled: (1) The accumulated geographic area of host sponges and (2) host sponges” functional morphology. The accumulated geographic area of sponges was determined using records from the Global Biodiversity Information Facility (GBIF, 2021), the interaction records of Pérez-Botello + Simóes (2021) (Dataset S2), and the Caribbean and Gulf of Mexico coral reefs shapefile from the Allen Coral Atlas (Allen Coral Atlas, 2022). A circular buffer area of 10 m? was calculated for each sponge record, and the area was cropped with the reefs' shapefile. The results in square kilometers (km?) were used as colonizable sponges' areas. Sponges functional morphology (Cust-like, Massive, Cup-like, and Erect; Fig. 2) were classified with the Schónberg (2021) morphological standardization (Dataset $3), and with the original descriptions of each sponge species when is available or with a species taxonomy update. Statistical analysis To analyze the sponge contribution to the network concerning their geographic accumulated area, we used a generalized linear model (GLM: family = Poisson). This analysis provides a quantitative evaluation of the hypotheses that the sponges” organization contribution to the interaction network is positively related by the accumulated geographic area of sponges. The sponges that provide a large geographical colonizable area potentially had greater structural importance than those sponge species with a restricted distribution (Dataset S4), Pérez-Botello et al. (2023), PeerJ, DOI 10.7717/peerj.16381 8/23 35 | P a g e PeerJ At the same time, we conducted an analysis of variance (ANOVA) to compare the different morphologies and test the hypotheses that sponges functional morphology improve the sponge contribution to the interaction network organization, ¡.e., some sponges morphologies are more suitable for hosting more guests than other morphologies (Dataset 54). We also evaluated the potential for sponges” taxonomy bias in the network organization's importance. To do so, we grouped the different sponge species by order and conducted another ANOVA to compare the taxonomic groups (Dataset $4). RESULTS Network-level properties The analysis of nonrandom patterns in the sponge-host interaction network of NWTA coral reefs demonstrated a statistically significant occurrence of nestedness and modularity in the organization of ecological network (NODF = 15.03 and M = 0.51, respectively. Both p-values < 0.001). A nested network exhibits a hierarchical organization of species interactions, specialist species engaged in few interactions are connected to a subset of generalist species with more interactions. Additionally, modularity describes a pattern where there are subgroups of guest species that interact more frequently with a group of host species. The presence of both nestedness and modularity network suggests a complex and dynamic structure within the sponge associated community, with host sponge species like Ircinia strobilina (PCO1*? = 23.785; linked guest spp. 78) 1. felix (PCO1*” = 19.030; 46 guest spp.), Callyspongia aculeata (PCO1*” = 18.121; 63 guest spp.), and C. fallax Duchassaing $ Michelotti, 1864 (PCO1*” = 16.389; 29 guest spp.) acting like species connectors and maintaining the network's structure. At the same time this pattern exhibits a high diversity of low connected species, for example, Spongia (Spongia) obliqua Duchassaing $: Michelotti, 1864 (PCO1?” = 0.037; 1 guest sp.), Verongula rigida (Esper, 1794) (PCO1?? = 0.088; 1 guest sp.), and Cribrochalina vasculum (Lamarck, 1814) (PCO1*” = 1.004; 2 guest spp.). Despite their limited interactions, these low connected sponge species contribute to the overall sponge host diversity within the network (Fig. 3). The observed pattern highlights the remarkable dominance of interactions by a specific subset of sponge species within the ecological network. It is remarkable that a small number of sponge species play a crucial role in maintaining the organizational structure of the network through a high number of interactions, while a larger proportion of sponge species exhibit minimal associations with other species. In the same way, this pattern of a limited number of highly connected species making a significant contribution to the organization of the interaction network is constant regardless of the functional sponge morphology. Trait-level properties The sponge accumulated geographic area exhibited a positive relationship with the contribution of each sponge to the network organization (Intercept = 1.178, z value = 13.206, p-value < 0.001). Our findings reveal that as the sponge cumulative area increases, so does the contribution of sponges to network organization (Fig. 4). Widely distributed sponges such as Ircinia strobilina, I. felix or Callyspongia aculeata are essential Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 9/23 36 | P a g e PeerJ LT aA MS SO WN a S a b u o d S d d s Y tay X y Y ne Y 5 MAA »e ds Lz mm. 7 or s SY “dds 91 “9ÓS > Figure 3 Sponge host-guest interaction network for the Northwestern Tropical Atlantic coral reefs. The left side of the network represents the sponge-associated fauna, dark blue denotes Arthropods, red Annelids, green Vertebrates, golden Mollusks, pink Echinoderms and light-yellow Cnidarians. The left side of the network represents the host-sponges. The sponges are classified according to its functional morphology (Schónberg, 2021), pink for Cup-like, light blue for Massive, orange for Erect, and dark yellow for Crust-like. 'lo interactively explore the network, visit the website https:// marinespeciesinteractions.org/?p=2333. Full-size Ra] DOI: 10.7717/peerj.16381/fig-3 species with a significant structural contribution to the network and a higher accumulated area. In contrast, sponges with focal distributions or sponges with only reported in unique sites such as Cliona vermifera Hancock, 1867, Aplysina bathyphila Maldonado « Young, 1998 Niphates erecta Duchassaing £ Michelotti, 1864 and Ircinia ramosa (Keller, 1889) had a lower contribution to the network organization. In the same way sponges functional morphology also influenced the magnitude to which it contributed to the structure of the guest-host interaction network (ANOVA: FE) 731 = 5.389; p-value < 0.002; Fig. 5). Sponges with Cup-like (mean + s.e.: 8.348 + 5.886) and Massive morphologies (7.844 + 5.962) had a significant superior contribution to network organization than Erect (4.153 + 2.625), and Crust-like (8.348 + 1.746) morphologies. Finally, there were no significant differences in the contribution of sponge orders to the network organization (ANOVA: F) 941 = 0.587; p- value < 0.832; Fig. 6). DISCUSSION Our results provide evidence that supports the relationships between network organization, accumulated geographic area, and functional morphology in the interactions between sponge hosts and their associated guest species. The relationship between accumulated geographic area and network organization was already supported by the existing interactions theory (Galiana et al., 2018; Dallas + Jordano, 2021), however this Pérez-Botello et al. (2023), PeerJ, DOI 10.7717/peerj.16381 (AA 110/23 37 | P a g e PeerJ Co nt ri bu ti on to Ne tw or k Or ga ni za ti on 25 Functional Morphology O) Cup-ike (O) Massive O =. 0) Crustuik NS] o > a > o o o 5 » > e. do” ee s * e 0] e o + e 0 o» a 0 1000 2000 3000 Accumulated Geographic Area (km') Figure 4 Relationship between sponge contribution to network organization and sponges accumulated geographic area. General lineal model between sponge contribution to network organi- zation and sponges accumulated geographic area (Intercept = 1.178, z value = 13.206, p-value < 0.001). The sponges are classified according to its functional morphology (Schónberg, 2021), pink for Cup-like, light blue for Massive, orange for Erect, and dark yellow for Crust-like. Full-size L4] DOI: 10.7717/peerj.16381/fig-4 Co nt ri bu ti on to N e t w o r k O r g a n i z a t i o n 25 mw o => a A [e] a E ma Cup-like Massive Erect Crust-like Sponge Functional Morphology Figure 5 Sponge contribution to network organization according to sponge functional morphology. Crust-like and Massive morphologies are the statistically different groups (ANOVA: F>73, = 5.389; p-value < 0.002). The sponges are classified according to its functional morphology, pink for Cup-like, light blue for Massive, orange for Erect, and dark yellow for Crust-like. Full-size la] DOI: 10.7717/peerj.16381/fig-5 Pérez-Botello et al. (2023), PeerJ, DOI 10.7717/peerj.16381 ¡IS 11/23 38 | P a g e PeerJ 25, 20 ? | ñ e Co nt ri bu ti on to N e t w o r k O r g a n i z a t i o n al Dictyoceratida Haplosclerida Axinellida Verongiida Agelasida Poecilosclerida Suberitida Clionaida Teractinellida Bimenida Dendroceratida Scopalinida Sponge Order Figure 6 Sponge contribution to network organization according to sponge order. No statical dif- ferences between sponge orders (ANOVA: F 94, = 0.587; p-value < 0.832) are founded. "he boxplot interquartile black line provides the mean value. Upper and lower whiskers extend to visual represent all data distribution. Full-size Ra] DOI: 10.7717/peerj.16381/fig-6 result improves further theoretical development in coral reef interactions ecology. In contrast, although there are numerous studies of the actual fauna that use sponges as microhabitats (Bell, 2008; Maldonado et al., 2016; Pérez-Botello ++ Simóes, 2021), there has been not clarify the sponge morphological features that make them a suitable environment. The positive relationship between sponges” contribution to network organization and its accumulated geographic area has a significant ecological implication. Our results indicate that as the accumulated geographic area increases so does the possibility to interact with a wide diverse guest species. For example, Ircinia strobilina, 1. felix or Callyspongia aculeata are sponges with a wide distribution, also are generalist sponges in terms of hosted gest species. Isolated, each one of these three sponges can host up to 46 guest species of the five registered Phyla, like Arthropoda: Synalpheus townsendi Coutiére, 1909, S. fritzmuelleri Coutiére, 1909 and Colomastix heardi LeCroy, 1995; Annelida: Haplosyllis spongicola (Grube, 1855) and Loimia medusa (Savigny, 1822); Chordata: Elacatinus xanthiprora (Bóhlke Robins, 1968); Mollusca: Isognomon bicolor (C. B. Adams, 1845); Echinodermata: Ophiothrix (Ophiothrix) oerstedit Littken, 1856; Cnidaria: Umimayanthus parasiticus (Duchassaing de Fonbressin £ Michelotti, 1860); and together these sponge concentrates 187 guest species of the 745 recorded host guest-interactions (25% of the recorded interactions). According to this relationship sponges with less geographic accumulated area like, Aplysina bathyphila, Niphates erecta and I. ramosa had a lower Pérez-Botello et al. (2023), PeerJ, DOI 10.7717/peerj.16381 (AAA 112/23 39 | P a g e PeerJ contribution to the network organization, interacting with fewer guest species and showing a tendency to associate with guests like, S. townsendi and H. spongicola that are capable of colonizing a diverse array of sponge species. This relationship creates the situation where a sponge host already present in the network can increase the probability of interacting with a potential guest species if this sponge increases their geographical distribution, leading to a cascade effect between sponges” availability and potential guest diversity in tropical Atlantic coral reefs. However, it is important to note that there is a group of sponges with a low accumulated area and few occurrence records, but their geographical distribution covers both the Caribbean and the Gulf of Mexico reefs. For example, Agelas dispar Duchassaing « Michelotti, 1864, Aplysina lacunosa (Lamarck, 1814), Ircinia campana (Lamarck, 1814) and Dragmacidon lunaecharta (Ridley « Dendy, 1886). This feature could indicate that these sponge species are difficult to detect or identify to species level in the field or that they have low abundances in the different reef systems they inhabit. A variable that could be explored in the future is the paired-wise distance between records of sponges of the same species and analyzing if the sum of these distances is related to the structural importance of each sponge species. In the same way, sponges provide a complex living space for a large number of species from many taxa (Renard et al, 2013; Pérez-Botello ++ Simóes, 2021). Most sponge associated fauna live inside the sponge whether using the canals, oscula, or pores of the sponges (Westinga e> Hoetjes, 1981; Koukouras et al., 1996; Hultgren + Duffy, 2010). This fact generates that the interactions between sponges host and their guest species can be influenced by a particular sponges morphological features. Our results indicate that certain sponge functional morphotypes have an effect on the organization of the host-guest interaction networks. Specifically, we found that Cup-like and Massive functional morphologies, frequently are more important in the network organization than Erect and Crust-like functional morphotypes. Cup-like sponges have concave upper surface and can efficiently separate their in- and exhalant openings (Renard et al., 2013; Schónberg, 2021). This functional morphology commonly has a roughly cylindrical (tubes and barrels) or inverted-cone symmetry (cups) with a larger internal volume and wide tube oscula (entrance) and, if multiple Cup-like structures aggregates in a group of a single individual sponge, the sponge heterogeneity enhances (Schónberg, 2021). In addition, massive sponges are very roughly as wide as high; in many cases, this functional morphology has a unified body mass comprised of fused subunits, resulting in the formation of interconnected small cavities and microcompartments (Schónberg, 2021) Also, massive sponges are characterized by its remarkable robustness, making them capable of providing a stable habitat compared to other functional morphologies (Bell «+ Barnes, 2000; Schónberg, 2021). In contrast with these two volumetric and tridimensional complex functional morphologies Crust-like shapes combine encrusting and creeping sponges, resulting in a low-profile body shape that extends parallel to the substrate; this morpho have a larger surface area compared to their height, and lack three-dimensional or vertical structures (Schónberg, 2021). On the other hand, erect sponges have a small attachment area and are positioned away from the substrate, they exhibit a predominantly vertical orientation, minimizing their horizontal surface areas (Schónberg, 2021). Their vertical Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 13/23 40 | P a g e PeerJ orientation and small attachment area make them susceptible to fragmentation, detachment, and removal by strong flow, waves, or storm surges (Wulff_ 1995; Schónberg, 2021). This process could generate an unstable and dynamic habitat, despite the high sponge survival rate after fragmentation (Wulff, 1985, 1995, 1997, 2006). Additionally, the abundance and species richness of sponge associated fauna could be regulated by three main morphological features. Firstly, sponges total volume. The number of sponges-inhabiting taxa is logarithmically related to sponge volume; larger sponges provide more substrate and resources for the colonization of different species, resulting in higher sponge-associated diversity (Westinga «> Hoetjes, 1981). Secondly, the internal volume and diameter of the sponge's canals. The shape and size of the sponge inner canals can physically limit the size of organisms that can inhabit the sponge's interior; sponges with narrow canals provide suitable refuge for smaller organisms, while larger organisms are constrained by the reduced size and volume of the canals (Koukouras et al., 1996; Hultgren + Duffy, 2010). Lastly, the morphological heterogeneity of the sponge, including number of tubes, sponge surface, sponge total volume and sponge area, creates a complex and heterogeneous habitat that facilitate the colonization of different guest species (Pérez- Botello, 2019). As a result, it is the combination of these morphological features that makes Cup-Like and Massive sponges more significant in network organization and have a more diverse community of associated guests compared to Crust and Erect sponges. In parallel, at sponge species level, it is very likely that the physical restrictions of each sponge species are promoting or limiting the diversity of the host-guest interactions. For example, volumetric and complex sponges like Callyspongia aculeata, C. fallax and Ap. fistularis, can establish a host-guest interaction with both small guest like Leucothoe spinicarpa (Abildgaard, 1789), Colomastix irciniae LeCroy, 1995 or Ophiactis quinqueradia Ljungman, 1872, that usually lives associated to the sponge surface and pores (Carrera-Parra + Vargas-Hernández, 1997; Crowe + Thomas, 2002; Winfield + Ortiz, 2010) and larger guest like Synalpheus hemphilli Coutiére, 1909, S. townsendi or Pagurus brevidactylus (Stimpson, 1859) typically founded in the sponges canals (Christoffersen, 1979; Dardeau, 1981, 1984; Carrera-Parra + Vargas-Hernández, 1997, Ugalde García, 2014). In contrast restricted and spaceless morphologies, like the encrusting sponges Petrosia (Petrosia) weinbergi van Soest, 1980 or Cliona celata Grant, 1826 could mechanically limited the size range of potential guest species inhabiting the internal sponge cavities. Furthermore, sponge morphology and guest behavior could regulate the diversity of observed interactions. Sponges with more complex, convoluted tube systems, such as C. aculeata and Aiolochroia crassa (Hyatt, 1875), tend to host more guest species than massive sponges with interconnected channels. For example, sponge species such as Hyattella intestinalis (Lamarck, 1814) are colonized only by Synalpheus species. These Crustaceans are extremely territorial, and some have a eusocial behavior like S. regalis defending the host sponge against other organisms (Duffy, 1996; Duffy + Macdonald, 1999; Duffy, Morrison ++ Macdonald, 2002). Probably the territorial behavior of certain guest species pushing another potential guest out of the sponge. The effect of this behavior Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 14/23 41 | P a g e PeerJ could be reduced in sponge species with a system of tubes that allow different degrees of segmentation of the internal sponge volume. Finally, the taxonomic bias analysis revealed a no significant impact in the organization of the sponge host-guest interaction network. This result suggests that, at least at the sponges” order level, the relationship between sponges” order and host-guest network organization is primarily regulated by the sponge-accumulated geographic area and the functional sponge morphology and, to a minor degree, by evolationary processes. This pattern implies that the sponges host-guest interactions depend not only on sponge taxonomic classification but also on the functional roles and specific adaptations each sponge-host and associated-gest species develops. While this analysis revealed no statistically significant relationship at sponges” order level, it remains plausible that certain guest species may exhibit specific associations with particular sponges. For instance, the annelid H. aplysinicola Lattig £ Martin, 2011 was observed to exclusively interact with sponges belonging to the Aplysina genera, being a specialized host-guest interaction. CONCLUSIONS One of the main findings of our study is the positive relationship between accumulated geographic area and network organization. These results provide valuable information to the theory of ecological interaction networks in a marine environment. This research further enhances our understanding of how geographical distribution influences the diversity and complexity of host-guest interactions. We further demonstrate that as the accumulated geographic area of sponge hosts increases, so does the potential for interactions with a wide range of guest species. This effect highlights the significance of sponge availability in promoting guest diversity in Tropical Atlantic coral reefs. Also, our study demonstrates the crucial role of sponge functional morphologies in the organization of host-guest interaction networks. Cup-like and Massive morphologies exhibit greater importance in network organization compared to Crust-like and Erect morphotypes. Cup-like sponges, with their volumetric canals, and the potential to generate three-dimensional complexity, provide diverse living spaces. Massive sponges, characterized by their robust structures and interconnected small cavities, offer a stable habitat for guest species colonization. In contrast, Crust-like with their low-profile body shapes and erect sponges with vertical orientations, implies space limitations and potential instability due to fragmentation and detachment. Importantly, our research demonstrates that taxonomic classification has not significantly influenced the organization of host-guest interaction networks. Instead, the ecological patterns observed in these networks are primarily shaped by accumulated geographic area, and functional morphology. This highlights the need to consider the functional traits and characteristics of sponge hosts and their associated guest species in ecological studies. Finally with this research, we generate a comprehensive understanding of the regional structure generated in the network of host-guest interactions of reef sponges. Being able to detect emerging patterns and keystone species within that network. Sponges such as Ircinia strobilina, L felix, Callyspongia aculeata, and C. fallax were crucial in maintaining the Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 15/23 42 | P a g e PeerJ network organization. The potential extinction of one or several of these species, or even a slight decrease in their presence within NWTA coral reefs, could trigger cascading losses in abundance and diversity of their associated fauna. ACKNOWLEDGEMENTS We gratefully acknowledges the Biological Science Program, UNAM (Posgrado en Ciencias de la Biológicas, Facultad de Ciencias, Universidad Nacional Autónoma de México; PCB-FC-UNAM). We thank Diana Ugalde (DU), an expert in sponge taxonomy, for her input on the morphological classification of the recorded sponges in this study. Also, to the entire Biodiversidad Marina de Yucatán (BDMY) team by the constant exchange of ideas which generates a fertile land for scientific creativity and innovation. Finally, we gratefully acknowledge the IABO Hub for hosting this article. ADDITIONAL INFORMATION AND DECLARATIONS Funding This work was financed by grants to Nuno Simóes by the Harte Research Institute, the Harte Charitable Foundation, CONABIO-NE018, CONACyTCB-2012-01-177293 and PAPIT 1V300123. This Project and Antar M Pérez-Botello was supported by the Unidad Multidisciplinaria de Docencia e Investigación—Sisal, Facultad de Ciencias, Universidad Nacional Autonomy de México (UMDI Sisal-FC-UNAM), and by CONACyT doctoral fellowship 2019-000037-02NACEF through the PCB-FC-UNAM. There was no additional external funding received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Grant Disclosures The following grant information was disclosed by the authors: Harte Research Institute. Harte Charitable Foundation: CONABIO-NE018, CONACyTCB-2012-01-177293 and PAPIT 1V 300123. Unidad Multidisciplinaria de Docencia e Investigación —Sisal. Facultad de Ciencias. Universidad Nacional Autonomy de México (UMDI Sisal-FC-UNAM). CONACyT: 2019-000037-02NACF. Competing Interests The authors declare that they have no competing interests. Author Contributions e Antar Mijail Pérez-Botello conceived and designed the experiments, analyzed the data, prepared figures and/or tables, authored or reviewed drafts of the article, and approved the final draft. e Wesley Dáttilo conceived and designed the experiments, analyzed the data, authored or reviewed drafts of the article, and approved the final draft. Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 16/23 43 | P a g e PeerJ e Nuno Simóes conceived and designed the experiments, authored or reviewed drafts of the article, and approved the final draft. Data Availability The following information was supplied regarding data availability: The data is available at Zenodo: Antar Mijail Pérez-Botello, Wesley Dattilo, £ Nuno Simóes. (2023). Geographic range size and species morphology determines the organization of sponge host-guest interaction networks across tropical coral reefs (Raw data) (3.0) [Data set]. Zenodo. https://doi.org/10.5281/zenodo.8171115. Supplemental Information Supplemental information for this article can be found online at http://dx.doi.org/10.7717/ peerj.1638 1*supplemental information. REFERENCES Allen Coral Atlas. 2022. Imagery, maps and monitoring of the world's tropical coral reefs. Zenodo DOI 10.5281/zenodo.3833242. Almeida-Neto M, Frensel DMB, Ulrich W. 2012. Rethinking the relationship between nestedness and beta diversity: a comment on Baselga (2010). Global Ecology and Biogeography 21(7):772-777 DOI 10.1111/5.1466-8238.2011.00709.x. Baeza JA. 2015. Crustaceans as symbionts: an overview of their diversity, host use and life styles. In: Thiel M, Les W, eds. Lifestyles and Feeding Biology: The Natural History of the Crustacea. New York, USA: Oxford University Press, 163-189. Bagousse-Pinguet Y le, Soliveres S, Gross N, Torices R, Berdugo M, Maestre FT. 2019. Phylogenetic, functional, and taxonomic richness have both positive and negative effects on ecosystem multifunctionality. Proceedings of the National Academy of Sciences of the United States of America 116(17):8419-8424 DOI 10.1073/pnas.1815727116. Balduzzi S, Riicker G, Schwarzer G. 2019. How to perform a meta-analysis with R: a practical tutorial. Evidence Based Mental Health 22(4):153-160 DOI 10.1136/ebmental-2019-300117, Bastolla U, Fortuna MA, Pascual-García A, Ferrera A, Luque B, Bascompte J. 2009. The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458(7241):1018-1020 DOI 10.1038/nature07950. Bauer RT. 2004. Remarkable shrimps: adaptations and natural history of the Carideans. Oklahoma, EE.UU: Oklahoma University Press. Beauchard O, Veríssimo H, Queirós AM, Herman PMJ. 2017. The use of multiple biological traits in marine community ecology and its potential in ecological indicator development. Ecological Indicators 76(417-441):81-96 DOI 10.1016/;.ecolind.2017.01.011. Bedini R, Canali MG, Bedini A. 2003. Use of camouflaging materials in some brachyuran crabs of the Mediterranean infralittoral zone. Cahiers de Biologie Marine 44:375-383. Bell JJ. 2008. The functional roles of marine sponges. Estuarine, Coastal and Shelf Science 79(3):341-353 DOI 10.1016/j.ecss.2008.05.002. Bell JJ, Barnes DKA. 2000. The influences of bathymetry and flow regime upon the morphology of sublittoral sponge communities. Journal of the Marine Biological Association of the United Kingdom 80(4):707-718 DOI 10.1017/50025315400002538. Bell JJ, Davy SK, Jones T, Taylor MW, Webster NS. 2013. Could some coral reefs become sponge reefs as our climate changes? Global Change Biology 19(9):2613-2624 DOI 10.1111/gcb.12212. Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 | 17/23 44 | P a g e PeerJ Bellotti E. 2014. Qualitative networks. London: Routledge. Borrett SR. 2012. Throughflow centrality is a global indicator of the functional importance of species in ecosystems. Ecological Indicators 32(1-2):182-196 DOI 10.1016/j.ecolind.2013.03.014. Brusca RC, Moore W, Shuster S. 2018. Two basal metazoan phyla: porifera and placozoa. In: Brusca R, Moore W, Shuster S, eds. Invertebrates. Sunderland, Massachusetss: Sinauer Associates, Inc, 216-255. Cantor M, Longo GO, Fontoura L, Quimbayo JP, Floeter SR, Bender MG. 2018. Interaction networks in tropical reefs. In: Dáttilo W, Rico-Gray V, eds. Ecological Networks in the Tropics an Integrative Overview of Species Interactions from Some of the Most Species-Rich Habitats on Earth. Cham: Springer International Publishing. Carrera-Parra LF, Vargas-Hernández JM. 1997. Comunidad críptica de esponjas del arrecife de isla de enmedio, veracruz, México. Revista de Biologia Tropical 44-45:311-321 DOI 10.15517/rbt.v4413.22055. Chen J-Y. 2012. Evolutionary scenario of the early history of the animal kingdom: evidence from precambrian (ediacaran) weng'an and early cambrian maotianshan biotas, China. In: Talent JA, ed. Earth and Life. Springer Science+Business Media, 239-379. Christoffersen ML. 1979. Campagne de la calypso au large des cótes atlantiques de Pamerique du sud (1961-1962). i. decapod crustacea: alpheoida. Annales de Institut Océanographique 55:297-377. Cornell H v, Lawton JH. 1992. Species interactions, local and regional processes, and limits to the richness of ecological communities: a theoretical perspective. The Journal of Animal Ecology 61(1):1 DOI 10.2307/5503. Corro EJ, Villalobos F, Lira-Noriega A, Guevara R, Dáttilo W. 2022. Current climate and latitude shape the structure of bat-fruit interaction networks throughout the Neotropical region. Ecoscience 29(3):179-189 DOI 10.1080/11956860.2021.2007644, Costello MJ, Claus S, Dekeyzer S, Vandepitte L, Tuama É, Lear D, Tyler-Walters H. 2015. Biological and ecological traits of marine species. Peer] 2015(8):1-29 DOI 10.7717/peerj.1201. Crowe SE, Thomas JD. 2002. Modern approaches to the study of crustacea. Boston, MA: Springer Us. Cruz Ferrer MI. 2014. Distribución y Abundancia de Ircinia strobilina e Ircinia fistularis (Demospongiae: Irciniidae) y su fauna asociada en el arrecife Tuxpan, Veracruz. Tesis 1:54. Dáttilo W, Lara-Rodríguez N, Jordano P, Guimaráes PR, Thompson JN, Marquis RJ, Medeiros LP, Ortiz-Pulido R, Marcos-García MA, Rico-Gray V. 2016. Unravelling darwin's entangled bank: architecture and robustness of mutualistic networks with multiple interaction types. Proceedings of the Royal Society B: Biological Sciences 283(1843):20161564 DOI 10.1098/rspb.2016.1564. Dáttilo W, Rico-Gray V. 2018. Ecological networks in the tropics an integrative overview of species interactions from some of the most species-rich habitats on earth. Cham, Switzerland: Springer International Publishing. Dallas TA, Jordano P. 2021. Species-area and network-area relationships in host-helminth interactions. Proceedings of the Royal Society B: Biological Sciences 288(1947):20203143 DOI 10.1098/rspb.2020.3143. Dardeau MR. 1981. Caridea: general collections and observations. In: Rose N, ed. Northern Gulf of Mexico Topographic Features Study. Final Report to the U.S. Department of Interior, Bureau of Land Management. College Station: Texas A € M, 86-115. Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 | 18/23 45 | P a g e PeerJ Dardeau MR. 1984. Synalpheus shrimps (Crustacea: Decapoda: Alpheidae). 1. The gambarelloides group, with a description of a new species. Memoirs of the Hourglass Cruises 7:1-125. Dehling DM. 2018. The structure of ecological networks. In: Dáttilo W, Rico-Gray V, eds. Ecological Networks in the Tropics An Integrative Overview of Species Interactions from Some of the Most Species-Rich Habitats on Earth. Cham: Springer International Publishing. Dembowska WS. 1926. Study on the habits ofthe crab dromia vulgaris M.E. The Biological Bulletin 50(2):163-178 DOI 10.2307/1536681. Diaz MC, Rúitlzer K. 2001. Sponges: an essential component of Caribbean coral reefs. Bulletin of Marine Science 69:535-546. Dormann CF, Gruber B, Friind J. 2008. Introducing the bipartite package: analysing ecological networks. R News 8(2):8-11. Duffy JE. 1992. Host use patterns and demography in a guild of tropical sponge-dwelling shrimps. Marine Ecology Progress Series 90:127-138 DOI 10.3354/meps090127. Duffy JE. 1996. Synalpheus regalis, new species, a sponge-Dwelling shrimp from the Belize Barrier reef, with comments on host specificity in Synalpheus. Journal of Crustacean Biology 16(3):564-573 DOI 10.2307/1548748. Duffy JE, Macdonald KS. 1999. Colony structure of the social snapping shrimp synalpheus filidigitus in belize. Journal of Crustacean Biology 19(2):283 DOI 10.2307/1549235. Duffy JE, Morrison CL, Macdonald KS. 2002. Colony defense and behavioral differentiation in the eusocial shrimp Synalpheus regalis. Behavioral Ecology and Sociobiology 51(5):488-495 DOI 10.1007/500265-002-0455-5. Egger M, Smith GD, Schneider M, Minder C. 1997. Bias in meta-analysis detected by a simple, graphical test. BM] 315(7109):629-634 DOI 10.1136/bmj.315.7109.629. Gagic V, Bartomeus I, Jonsson T, Taylor A, Winqvist C, Fischer C, Slade EM, Steffan- Dewenter IL, Emmerson M, Potts SG, Tscharntke T, Weisser W, Bommarco R. 2015. Functional identity and diversity of animals predict ecosystem functioning better than species-based indices. Proceedings of the Royal Society B: Biological Sciences 282(1801):20142620 DOI 10.1098/rspb.2014.2620. Galiana N, Lurgi M, Claramunt-López B, Fortin MJ, Leroux S, Cazelles K, Gravel D, Montoya JM. 2018. The spatial scaling of species interaction networks. Nature Ecology and Evolution 2(5):782-790 DOI 10.1038/541559-018-0517-3. Gaiizére P, O'Connor L, Botella C, Poggiato G, Múnkemiiller T, Pollock LJ, Brose U, Maiorano L, Harfoot M, Thuiller W. 2022. The diversity of biotic interactions complements functional and phylogenetic facets of biodiversity. Current Biology 32(9):2093-2100.e3 DOI 10.1016/j.cub.2022.03.009. GBIF. 2021. The global biodiversity information facility, what is GBIE? Available at hítps://www. gbif.org/ (accessed 21 September 2022). González-Rivero M, Yakob L, Mumby PJ. 2011. The role of sponge competition on coral reef alternative steady states. Ecological Modelling 222(11):1847-1853 DOI 10.1016/j.ecolmodel.2011.03.020. Hagedorn M, Carter V, Zuchowicz N, Phillips M, Penfield C, Shamenek B, Vallen E a, Kleinhans FW, Peterson K, White M, Yancey PH. 2015. Trehalose is a chemical attractant in the establishment of coral symbiosis. PLOS ONE 10(1):e0117087 DOI 10.1371/journal.pone.0117087. Harada K, Hayashi N, Kagaya K. 2020. Individual behavioral type captured by a Bayesian model comparison of cap making by sponge crabs. Peer] 8(1856):e9036 DOI 10.7717/peerj.9036. Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 | 19/23 46 | P a g e PeerJ Hooper JNA, van Soest RWM. 2002a. Systema porifera a guide to the classification of sponges. In: Hooper JNA, van Soest RWM, Willenz P, eds. Systema Porifera. New York: Kluwer Academic/lPlenum, 1-8. Hooper JNA, van Soest RWM. 2002b. Systema porifera a guide to the classification of sponges. New York, Boston, Dordrecht, London, Moscow: Kluwer Academic/lPlenum. Hultgren KM, Duffy JE. 2010. Sponge host characteristics shape the community structure of their shrimp associates. Marine Ecology Progress Series 407:1-12 DOI 10.3354/meps08609. Katz L. 1953. A new status index derived from sociometric analysis. Psychometrika 18(1):39-43 DOI 10.1007/BF02289026. Knowlton N. 2001. The future of coral reefs. Proceedings of the National Academy of Sciences of the United States of America 98(10):5419-5425 DOI 10.1073/pnas.091092998. Kou Q, Li XZ, Chan TY, Chu KH. 2015. Divergent evolutionary pathways and host shifts among the commensal pontoniine shrimps: a preliminary analysis based on selected Indo-Pacific species. Organisms Diversity and Evolution 15(2):369-377 DOI 10.1007/513127-014-0198-y. Koukouras A, Russo A, Voultsiadou-Koukoura E, Arvanitidis C, Stefanidou D. 1996. Macrofauna associated with sponge species of different morphology. Marine Ecology 17(4):569-582 DOI 10.1111/5.1439-0485.1996.tb00418.x. Lawton JH. 1999. Are there general laws in ecology? Oíkos 84(2):177-192 DOI 10.2307/3546712. Losos JB, Ricklefs RE, MacArthur RH, Wilson EO, Losos JB, Ricklefs RE. 2009. The theory of island biogeography revisited. Nueva Jersey, Reino Unido: Princeton University Press. MacArthur RH, Wilson EO. 1963. An equilibrium theory of insular zoogeography. International Journal of Evolution 17(4):373-387 DO1 10.2307/2407089. Maldonado M, Aguilar R, Bannister RJ, James J, Conway KW, Dayton PK, Cristina D, Gutt J, Kelly M, Kenchington ELR, Leys SP, Shirley A, Tendal OS, Rapp HT, Klaus R, Young CM. 2016. Sponge grounds as key marine habitats: a synthetic review of types, structure, functional roles, and conservation concerns. In: Rossi S, Barmanti L, Gori A, Orejas C, eds. Marine Animal Forests the Ecology of Benthic Biodiversity Hotspots. Switzerland: Springer International Publishing, 1-39. Martínez-Falcón AP, Martínez-Adriano CA, Dáttilo W. 2019. Redes complejas como herramientas para estudiar la diversidad de las interacciones ecológicas, La biodiversidad en un mundo cambiante: fundamentos teóricos y metodológicos para su estudio. In: Moreno C, ed. La Biodiversidad En Un Mundo Cambiante: Fundamentos Teóricos Y Metodológicos Para Su Estudio. Ciudad de México: Universidad Autónoma del Estado de Hidalgo/Libermex, 265-283. Mascaró M, Rodríguez-Pestaña L, Chiappa-Carrara X, Simoes N. 2012. Host selection by the cleaner shrimp ancylomenes pedersoni: do anemone host species, prior experience or the presence of conspecific shrimp matter? Journal of Experimental Marine Biology and Ecology 413(71):87-93 DOI 10.1016/j.jembe.2011.11.026. McCammon AM, Brooks WR. 2014. Protection of host anemones by snapping shrimps: a case for symbiotic mutualism? Symbiosis 63(2):71-78 DOI 10.1007/513199-014-0289-8. McCammon AM, Sikkel PC, Nemeth D. 2010. Effects of three Caribbean cleaner shrimps on ectoparasitic monogeneans in a semi-natural environment. Coral Reefs 29(2):419-426 DOI 10.1007/500338-009-0583-8. McGill BJ, Enquist BJ, Weiher E, Westoby M. 2006. Rebuilding community ecology from functional traits. Trends in Ecology and Evolution 21(4):178-185 DOI 10.1016/.tree.2006.02.002. McKeon CS, O”Donnell JL. 2015. Variation in partner benefits in a shrimp-sea anemone symbiosis. Peer] 3(4661):e1409 DOI 10.7717/peerj.1409. Pérez-Botello et al. (2023), PeerJ, DOI 10.7717/peerj.16381 120/23 47 | P a g e PeerJ McLay CL. 1983. Dispersal and use of sponges and ascidians as camouflage by Cryptodromia hilgendorf (Brachyura: Dromiacea). Marine Biology 76(1):17-32 DOI 10.1007/BF00393051. Moulatlet GM, Dáttilo W, Villalobos F. 2023. Species-level drivers of avian centrality within seed- dispersal networks across different levels of organisation. Journal of Animal Ecology 92:2126-2137 DOI 10.1111/1365-2656.13986. Ocean Biodiversity Information System (OBIS). 2020. Intergovernmental Oceanographic Commission of UNESCO. Available at www.iobis.org (accessed 7 July 2020). Olesen JM, Bascompte J, Dupont YL, Jordano P. 2007. The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America 104(50):19891-19896 DOI 10.1073/pnas.0706375104. Overstreet RM, Lotz JM. 2016. Host-symbiont relationships: understanding the change from guest to pest. In: Christon J, Hurst, eds. The Rasputin E ect: When Commensals and Symbionts Become Parasitic. Cincinnati, Ohaio, USA: Springer, 27-64. Pawlik JR. 2011. The chemical ecology of sponges on Caribbean reefs: natural products shape natural systems. BioScience 61(11):888-898 DOI 10.1525/bi0.2011.61.11.8. Pawlik JR, Loh T-LL, McMurray SE, Finelli CM. 2013. Sponge communities on Caribbean coral reefs are structured by factors that are top-down, not bottom-up. PLOS ONE 8(5):e62573 DOI 10.1371/journal.pone.0062573. Pérez-Botello AM. 2019. Cambios de diversidad de fauna asociados a Callyspongia vaginalis, en arrecifes coralinos del Banco de Campeche. Master”s Thesis, Universidad Nacional Autonoma de Mexico, Mexico City, Mexico. Pérez-Botello AM, Mascaró M, Simóes N. 2021. The importance of home cleaning: sediment transport by alpheid shrimps provides a competitive advantage to their host anemones. Frontiers in Marine Science 8:1-14 DOI 10.3389/fmars.2021.677024. Pérez-Botello AM, Simóes N. 2021. Sponge-dwelling fauna: a review of known species from the Northwest Tropical Atlantic coral reefs. Biodiversity Data Journal 9(e63372):1-18 DOI 10.3897/BDJ.9.e63372. Pimiento C, Leprieur F, Silvestro D, Lefcheck JS, Albouy C, Rasher DB, Davis M, Svenning JC, Griffin JN. 2020. Functional diversity of marine megafauna in the Anthropocene. Science Advances 6(16):20161435 DOI 10.1126/sciadv.aay7650. Poff NLR, Olden JD, Vieira NKM, Finn DS, Simmons MP, Kondratieff BC. 2006. Functional trait niches of North American lotic insects: traits-based ecological applications in light of phylogenetic relationships. Journal of the North American Benthological Society 25(4):730-755 DOI 10.1899/0887-3593(2006)025[0730:FTNONA]2.0.CO;2. Ramírez-Flores VA, Villanueva-Gutiérrez R, Roubik DW, Vergara CH, Lara-Rodríguez N, Dáttilo W, Bonet Ferrer ME, Rico-Gray V. 2015. Topological structure of plant-bee networks in four Mexican environments. Sociobiology 62:56-64 DOI 10.13102/sociobiology.vé62i1. Renard E, Gazave E, Fierro-Constain L, Schenkelaars Q, Ereskovsky A, Vacelet J, Borchiellini C. 2013. Porifera (Sponges): recent knowledge and new perspectives. In: Encyclopedia of Life Sciences. Hoboken: Wiley DOI 10.1002/9780470015902.40029283. Rossi S, Barmanti L, Gori A, Orejas C. 2017. Marine animal forests the ecology of benthic biodiversity hotspots. Cham, Switzerland: Springer Nature. Riitlzer K. 2004. Sponges on coral reefs: a community shaped by competitive cooperation. Bollettino dei Musei e Degli Istituti Biologici dell'Universita di Genova 68:85-148. Saavedra S, Stouffer DB, Uzzi B, Bascompte J. 2011. Strong contributors to network persistence are the most vulnerable to extinction. Nature 478(7368):233-235 DOI 10.1038/nature10433., Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 121/23 48 | P a g e PeerJ Schmitz 0J, Buchkowski RW, Burghardt KT, Donihue CM. 2015. Functional traits and trait-mediated interactions. connecting community-level interactions with ecosystem functioning. Advances in Ecological Research 52:319-343 DOI 10.1016/bs.aecr.2015.01.003. Schwarzer G, Carpenter JR, Riicker G. 2015. Meta-A nalysis with R. Cham: Springer International Publishing. Schónberg CHL. 2021. No taxonomy needed: sponge functional morphologies inform about environmental conditions. Ecological Indicators 129:107806 DOI 10.1016/j.ecolind.2021.107806. Sebastián-González E, Morales-Reyes Z, Botella F, Naves-Alegre L, Pérez-García JM, Mateo- Tomás P, Olea PP, Moleón M, Barbosa JM, Hiraldo F, Arrondo E, Donázar JA, Cortés- Avizanda A, Selva N, Lambertucci SA, Bhattacharjee A, Brewer AL, Abernethy EF, Turner KL, Beasley JC, DeVault TL, Gerke HC, Rhodes OE, Ordiz A, Wikenros C, Zimmermann B, Wabakken P, Wilmers CC, Smith JA, Kendall CJ, Ogada D, Erehner E, Allen ML, Wittmer HU, Butler JRA, du Toit JT, Margalida A, Oliva-Vidal P, Wilson D, Jerina K, Krofel M, Kostecke R, Inger R, Per E, Ayhan Y, Sanci M, Yilmazer Ú, Inagaki A, Koike S, Samson A, Perrig PL, Spencer EE, Newsome TM, Heurich M, Anadón JD, Buechley ER, Gutiérrez-Cánovas C, Elbroch LM, Sánchez-Zapata JA. 2021. Functional traits driving species role in the structure of terrestrial vertebrate scavenger networks. Ecology 102(12):432 DOI 10.1002/ecy.3519. Silbiger NJ, Childress MJ. 2008. Interspecific variation in anemone shrimp distribution and host selection in the florida keys (USA): implications for marine conservation. Bulletin of Marine Science 83:329-345. Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J. 2007. Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57(7):573-583 DOI 10.1641/B570707. Thiel M. 1999. Host-use and population demographics of the ascidian-dwelling amphipod Leucothoe spinicarpa: indication for extended parental care and advanced social behaviour. Journal of Natural History 33(2):193-206 DOI 10.1080/002229399300371. Thiel M, Baeza JA. 2001. Factors affecting the social behaviour of crustaceans living symbiotically with other marine invertebrates: a modelling approach. Symbiosis 30(2):163-190. Thompson SG, Sharp SJ. 1999. Explaining heterogeneity in meta-analysis: a comparison of methods. Statistics in Medicine 18:2693-2708 DOI 10.1002/(155N)1097-0258. Thompson SG, Smith TC, Sharp SJ. 1997. Investigating underlying risk as a source of heterogeneity in meta-analysis. Statistics in Medicine 16:2741-2758 DOI 10.1002/(1885N)1097-0258. Ugalde García DM. 2014. Aspectos ecológicos de los camarones Carídeos asociados a espojas de la costa sureste del Golfo de México. Mexico: Universidad Nacional Autónoma de México. Vidal MM, Hasui E, Pizo MA, Tamashiro JY, Silva WR, Guimaráes PR. 2014. Frugivores at higher risk of extinction are the key elements of a mutualistic network. Ecology 95(12):3440-3447 DOI 10,1890/13-1584.1. Watson RA, Pollack JB. 1999. How symbiosis can guide evolution. Advances in Artificial Life 1674:29-38 DOI 10.1007/3-540-48304-7. Weiher E. 2011. A primer of trait and funcitional diversity. In: Magurran AE, McGill BJ, eds. Biological Diversity: Frontiers in Measurement and Assessment. Oxford, EEUU: Oxford University Press, 175-193. Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 122/23 49 | P a g e PeerJ Westinga E, Hoetjes PC. 1981. The intraponge fauna of spheciospongia vesparia (Porifera, Demospongiae) at Curacao and Bonaire. Marine Biology 62(2-3):139-150 DOI 10.1007/BF00388176. Winfield I, Ortiz M. 2010. Colomastigids (Amphipoda: Gammaridea: Colomastigidae) from the veracruz coral reef system, Sw Gulf of Mexico, with a description of two new species associated with sponges. Scientia Marina 74(4):773-782 DOI 10.3989/scimar.2010.74n4773. Wulff JL. 1985. Dispersal and survival of fragments of coral reef sponges. Proceedings of the Fifth International Coral Reef Congress, Tahiti 5:119-124. Wulff JL. 1995. Effects of a hurricane on survival and orientation of large erect coral reef sponges. Coral Reefs 14(1):55-61 DOI 10.1007/BF00304073. Wulff JL. 1997. Mutualism among species of coral reef sponges. Ecological Society of America 78(1):146-159 DOI 10.1890/0012-9658(1997)078[0146:MASOCR]2.0.CO;2. Wulff JL. 2006. Ecological interactions of marine sponges. Canadian Journal of Zoology 84(2):146-166 DOI 10.1139/z06-019. Wulff JL. 2016. Sponge contributions to the geology and biology of reefs: past, present, and future. In: Hubbard D, Rogers C, Lipps J, Stanley Jr G, eds. Coral Reefs at the Crossroads. Coral Reefs of the World. Vol. 6. Dordrecht: Springer DOI 10.1007/978-94-017-7567-0_5. Pérez-Botello et al. (2023), PeerJ, DO! 10.7717/peerj.16381 123/23 50 | P a g e 51 | P a g e Artículo 3: (en revisión) A multi-scale analysis of α-diversity and β-diversity spatial variability on living islands Revista: Coral Reefs/ Marine Ecology Progress Series/ Marine Ecology Autores: Antar Mijail Pérez-Botello; Edlin Guerra-Castro; Carlos Enrique Paz Rios; Gabriel Cervantes Campero; María del Refugio Muciño Reyes; Yoalli Quetzalli Hernández Diaz; Nuno Simões Estado: en revisión Año: 2023 DOI: Resumen Las esponjas pueden ser especies clave en la estructura comunitaria de los arrecifes de coral tropicales. De agosto de 2016 a septiembre de 2019 se muestrearon ocho sistemas arrecifales a lo largo de los límites oceánicos de la Plataforma Continental de Yucatán en el Golfo de México. El objetivo de esta investigación fue analizar la diversidad α y β de la comunidad asociada a la esponja tubular Callyspongia aculeata (como modelo experimental) a lo largo de tres escalas espaciales: ecosistema, hábitat y microhábitat. Nuestros resultados revelaron patrones complementarios entre la diversidad α y β en diferentes escalas espaciales. A nivel del ecosistema, la diversidad-α de la comunidad asociada a C. aculeata no mostró correlaciones significativas con atributos del arrecife, como el perfil del arrecife, el sistema de arrecifes, la cobertura de coral y la posición longitudinal del arrecife. Además, no se encontraron diferencias sustanciales entre la diversidad-α ecosistémica y los puntos de muestreo, la distancia entre esponjas y la profundidad de las esponjas (escala hábitat). Sin embargo, a nivel de microhábitat, existe una relación positiva entre la diversidad α de los huéspedes de las esponjas y la complejidad de las esponjas, lo que sugiere que el aumento de la complejidad estructural de las esponjas incrementa la posibilidad de albergar una mayor riqueza de especies. De manera complementaria al analizar la diversidad β, el recambio de especies entre los ocho sistemas arrecifales de la Plataforma Continental de Yucatán fue el factor principal que explica la mayor diversidad β a nivel ecosistémico. Los factores locales regularon los cambios a nivel del habita, sin embargo, ni la profundidad de las esponjas y ni la distancia entre esponjas fueron significativas. A nivel de microhábitat, la complejidad de las esponjas fue el principal impulsor del reemplazo de especies entre las esponjas muestreadas en sitios de arrecifes específicos. Nuestros resultados demuestran que la comunidad de especies huéspedes es un factor regulado por la escala espacial de análisis. Por ende, los patrones observados en fauna asociada a C. aculeata está condicionada por la dispersión de las especies huéspedes y la heterogeneidad ambiental en términos espaciales. 52 | P a g e Sponge dwelling fauna: A multi-scale analysis of α and β diversity spatial variability on living islands Antar Mijail Pérez-Botello1,2, Edlin Guerra-Castro3, Gabriel Cervantes Campero2, Yoalli Quetzalli Hernández Diaz2, María del Refugio Muciño Reyes1,2, Carlos E. Paz-Ríos5, Nuno Simões2,6,7 1. Posgrado en Ciencias Biológicas, Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM). Puerto de Abrigo s/n, C.P. 97356, Sisal, Yucatán, México. 2. Unidad Multidisciplinaria de Docencia e Investigación - Sisal, Yucatán. Facultad de Ciencias, (UNAM). Puerto de Abrigo s/n, C.P. 97356, Sisal, Yucatán, México 3. Escuela Nacional de Estudios Superiores (ENES-Mérida). Universidad Nacional Autónoma de México, Mérida, Yucatán, C.P. 97357 5. Instituto de Ecología, Pesquerías y Oceanografía del Golfo de México, Universidad Autónoma de Campeche (EPOMEX-UAC), Campus VI, 24029 San Francisco de Campeche, Campeche, México 6. Laboratorio Nacional de Resiliencia Costera (LANRESC, CONACYT), Puerto de Abrigo s/n, C.P. 97356, Sisal, Yucatán, México 7. International Chair for Coastal and Marine Studies in Mexico, Harte Research Institute for Gulf of Mexico Studies, Texas A&M University, Corpus Christi, TX 78412, USA Corresponding author: Nuno Simões ns@ciencias.unam.mx; Antar Mijail Pérez-Botello antarmijail@comunidad.unam.mx Keywords: 53 | P a g e Abstract This research aimed to analyze α and β species diversity of fauna dwelling in the sponge Callyspongia aculeata at three nesting spatial scales: ecosystem, habitat, and micro-habitat. Macroinvertebrates dwelling in sponges were collected by intermittent sampling from August 2016 to September 2019 across eight reef systems along the oceanic boundaries of the Yucatán Continental Shelf in the Gulf of Mexico. Findings revealed a complementary pattern between α- and β-diversity across scales. At ecosystem level, α-diversity of the sponge- dwelling fauna showed no significant correlations with reef profile, reef system, coral coverage, or geographical longitude. At habitat level, no significant differences in α-diversity were found between sample point, inter-sponge distances, or sponge depths. However, at the individual level, α-diversity of the guest fauna was positively related to heterogeneity of sponge morphology; hence, variability in sponge morphology enhances species richness. Regarding β-diversity at the ecosystem scale, variability among reef systems within the Yucatán Continental Shelf was the primary factor that explained the observed changes in the guest fauna, primarily due to a non-directional species variation between reef systems. At the habitat scale, β-diversity was significantly influenced by site identity but not by sponge depth or inter-sponge distances; some of the changes appear to have been regulated by habitat factors yet unrecognised. At the micro-habitat scale, sponge morphological variability was the main driver of species variability and species turnover among sampled sponges at specific reef sites. In conclusion, the α- and β-diversity patterns of these sponge-dwelling fauna depend on the spatial scale, influenced by ecosystem features, the dispersal capability of the sponge-dwelling species, and habitat/micro-habitat heterogeneity. 54 | P a g e Introduction Species diversity has two main components, α- and β-diversity, and these are strongly related to the spatial extent analyzed (Karkarey et al., 2022): α-diversity characterizes the abundance and number of species or traits within communities, describing a static condition; β-diversity characterizes the variation in number of species or species composition between communities across spatial units, thereby describing a dynamic condition (Karkarey et al., 2022). The influence of ecological processes on species diversity must be better understood if management and conservation measures are to be effective (Karkarey et al., 2022; Levin, 1992; Socolar et al., 2016; Zintzen et al., 2017). In marine environments, α-diversity tends to increase with increasing area and heterogeneity of the habitat (Gray, 2001; Jordán-Dahlgren, 2002); however, β-diversity analysis suggests that this relationship is less clear when species replacement at various spatial scales is incorporated (Qian and Ricklefs 2007; Soininen et al. 2007; Anderson et al. 2013), particularly in modular organisms, such as corals and sponges, that harbor guest fauna. Sponges contribute to coral reef ecosystems through multiple functions including water filtration, primary production, and participation in nutrient cycles (Bell, 2008) They can support diverse marine life forms including complex invertebrates, supplying their in-dwelling fauna with an ongoing stream of water with dissolved and particulate matter, including phytoplankton, organic and inorganic debris, and even sponge tissue (Corredor et al., 1988; García-Hernández et al., 2019; Pawlik, 1983). These conditions generate a microcosmos with well-defined boundaries (Uriz et al., 1992) that can be thought of as a ‘living island’ (Villamizar & Laughlin, 1991), several levels of interactions between the sponge host and the guest community take place simultaneously, frequently related with the aquiferous system of the sponge and its morphological variability (García-Hernández et al., 2019; Koukouras et al., 1996). Hence, reef sponges can be thought of as ecosystem engineers (Jones et al., 1994; Maldonado et al., 2016; Reyes-Bonilla & Jordán-Dahlgren, 2017). The present study analyzes at three spatially nested scales the α- and β-diversity of macroinvertebrates dwelling in the coral-reef sponge, Callyspongia (Cladochalina) aculeata (Linnaeus, 1759), from coral reefs. Across its geographical distribution from the Bahamas to 55 | P a g e Trinidad and Tobago, this sponge could host at least 65 animal species (Pérez-Botello and Simões 2021). Its distinct tubular or elongate-tubular morphology, with a clearly demarcated boundary between its internal and external spaces, facilitates quantitative studies of its guest fauna. The aims of our study were: (1) to analyze α- and β-diversity of sponge-dwelling fauna across three spatial scales, and (2) to partition the variation of β-diversity across these spatial scales by determining the differences in taxonomic composition between communities of sponge- dwelling fauna. The hypothesis was that the α-diversity and β-diversity measures of sponge- dwelling fauna are shaped by the contrasts between coral reefs, between local habitats within coral reefs, and between micro-habitats within each host sponge. Materials and methods STUDY AREA AND BIOLOGICAL MODEL The Yucatán Continental Shelf is a heterogeneous and dynamic marine region at the eastern border of the Southern Gulf of Mexico ecoregion (Paz-Ríos et al., 2021; Spalding et al., 2007; Wilkinson et al., 2009). It is a broad platform characterized by carbonate substrates, with a shift to terrigenous sediments on its western part (Paz-Ríos et al., 2021; Tunnell et al., 2007). The main coral reef ecosystems are remotes and are on the outer shelf, at 130 to 200 km from the mainland (Tunnell et al., 2007); there, the Loop Current separates from the Gulf of Mexico and the Caribbean Sea, connecting water masses between the Atlantic and the Gulf's interior, and generates an upwelling at Cape Catoche, at the southeastern Gulf of Mexico (Sanvicente-Añorve et al. 2014, 2018a; Lara-Hernández et al. 2019). This dynamic creates seasonal cyclonic and anticyclonic eddies over the inner shelf (Sanvicente-Añorve et al. 2018a). The connectivity patterns in this region have seasonal variations and differ between the western part and the northeastern edge of the shelf (Sanvicente-Añorve et al. 2014). On the western shelf, connectivity flows northward from March to August and southward from September to February and maintains an almost unidirectional connectivity through the influence of the cyclonic eddies in the Campeche Bay (Sanvicente-Añorve et al. 2014). In contrast, the northeastern edge maintains a northeastern connection throughout October to December (Fernández et al. 2013; Sanvicente-Añorve et al. 2014). 56 | P a g e Sponges (Callyspongia aculeata) and their guest fauna were collected intermittently between August 2016 and September 2019 from the main coral reef ecosystems on the outer shelf (Figure 1), namely Cayo Arcas, Cayo Arenas, Triangulos, Obispos, Banco Nuevo, Banco Pera, Alacranes reef, and Bajos del Norte (Supplementary 1). BIOLOGICAL SURVEY We employed a sampling framework structured across three distinct spatial scales, which were nested hierarchically: a) ecosystem (i.e. the reef systems sampled on the Yucatán Continental Shelf), b) habitat (i.e. the selected reef system sampling site), and c) micro- habitat (i.e. the sampled sponge). The 146 sponges collected in the shallow reef subtidal zone (<25 m depth) came from the reef systems as follows: Cayo Arcas 28 sponges, Cayo Arenas 15, Triangulos 26, Obispos 17, Cayo Nuevo 8, Banco Pera 7, Arrecife Alacranes 26, Bajos del Norte 19. Each individual sponge was regarded as a discrete unit of observation (sample). In the field, we compiled a preliminary overview of the morphospecies of the sponge-dwelling macroinvertebrates. These were subsequently identified in the laboratory to the lowest possible taxonomic level with the assistance of appropriate regional specialists and then checked against the World Register of Marine Species (WoRMS) Taxon Match Tool (WoRMS Editorial Board, 2023) (Supplementary 2). The collected sponges have been deposited at the Unidad Multidisciplinaria de Docencia e Investigación – Sisal (UMDI-Sisal), and the associated fauna is held at the Colección de Crustáceos de Yucatán (YUC-CC) and the Colección Regional de Equinodermos de la Península de Yucatán (COREPY). These collections are held at the UMDI-Sisal facilities of the Mexican National University (UNAM). Field collections were approved by the Mexican Department of Agriculture and Fisheries (SAGARPA), with permit numbers PPF/DGOPA-093/16 for sponges (Porifera: Demospongiae), PPF/DGOPA-066/16 for crustaceans (Arthropoda: Crustacea) and PPF/DGOPA-082/19 for echinoderms (Echinodermata). 57 | P a g e SAMPLE SIZE An appropriate sampling effort was determined by using the ‘SSP’ library (Guerra-Castro et al., 2021) in R-project software. It compared the values of dissimilarity-based multivariate standard error (MultSE) obtained when data matrices were simulated to mimic the communities found in an in-field pilot survey. The pilot survey, in August 2016 at seven sites in Cayo Arcas reef, selected 26 sponges. The simulation revealed an optimal reduction of standard error between 7 and 11 sites per ecosystem, and an optimal sample effort per ecosystem of 7 to 10 sponges (Supplementary 3). SAMPLE DATA DISPERSION As we had an unbalanced survey and to ensure the reliability of our dataset, the homogeneity of multivariate dispersions across these eight reef systems was evaluated by PERMDISP analysis (Anderson, 2006) using PRIMER v7 (Clarke & Gorley, 2015). There were no significant differences (pseudo-F= 1.22; P = 0.45), suggesting that our dataset is comparable for subsequent analyses. SPATIAL SOURCES OF VARIATION Spatial data were compiled from databases, from measurements in situ, and from laboratory analyses. Ecosystem scale. We quantified differences in α-diversity and β-diversity of the fauna dwelling in C. aculeata in terms of reef system, coral coverage area, reef profile, and longitudinal position. For α-diversity, we tested the relationship of species-with coral cover and the longitudinal gradient. We expect on one hand a positive correlation between the species richness in sponge-dwelling fauna and the coral coverage area (MacArthur and Wilson 1963; Losos et al. 2009), and on the other hand, a higher species richness in sponge-dwelling fauna at the eastern reef systems, as suggested for YCS coral reef species (Jordán-Dahlgren 2002; OBIS 2020). Regarding theFor β-diversity, we tested the null hypothesis that the sponge- dwelling fauna would be the same regardless of reef system identity, coral coverage area based on the coralline shape layer (Allen Coral Atlas 2022), reef profile classified into platform, atoll, or submerged keys (Jordán-Dahlgren & Rodríguez-Martínez, 2003), and geographical longitude. 58 | P a g e Habitat scale. Effects on α-diversity and β-diversity were quantified according to sample identity, inter-sponge distance, and depth of the host sponge. Inter-sponge distance was derived from the inverse of the sponge density at that site, as estimated from underwater video transects (UVTs): a 50 m line was laid out at each site and a diver positioned the camera perpendicular to the line to obtain a frame 0.6 m wide; this covered ~30m2 per transect (Aronson et al., 1994; Garza Pérez et al., 2010; Ninio et al., 2003). A total Of the 54 transects, Cayo Arcas had 12, Cayo Arenas 11, Triangulos 9, Obispos 8, Cayo Nuevo 2, Banco Pera 2, Alacranes 8, and Bajos del Norte 2. Each was parallel to the coastline to minimize changes in depth along the transect. Sponge depth was recorded on a dive computer at the time of sampling. Micro-habitat scale. We quantified effects of sponge morphology on α-diversity and β-diversity of the guest fauna. The characteristics used were covered area, surround volume, sponge volume, sponge surface area, and number of tubes. We tested whether the morphological variability of sponges (as an indicator of micro-habitat heterogeneity) regulates small-scale variability in the guest community. With the concept of a sponge as a living island, we predicted that a more homogeneous sponge would host a faunal community with lower α- diversity and lower β-diversity. To generate a three-dimensional model for each sponge, its height and width were measured and its tubes counted. Then the sponge was placed on a rotating motor that produced a 360° photographic imaging, and thence a digital record of each sponge. Each photographic dataset of 200 images was processed with 3DF Zephyr software (https://www.3dflow.net) to generate a 3D sponge model, which was scaled according to the height and width measurements. This allowed the use of Autodesk 3ds Max (https://www.autodesk.mx/) to calculate the area of substratum covered, the volume surrounding the sponge, sponge volume itself, and sponge surface area (Figure 2). Measurements in different numeric scales (cm2 and cm3) were normalized. Then to reduce the multi-dimensional profile of a sponge to a synthetic heterogeneity index incorporating the individual variability of five characteristics, we performed a principal components ordination (PCO) to represent by means of the first principal component (PCO1) a heterogeneity index; this accounted for 89.7% of the morphological variability (Supplementary 4). Since the values obtained from PCO1 are both positive and negative, we changed the point of origin to zero. 59 | P a g e DIFFERENCES IN SPECIES RICHNESS AND SPECIES COMPOSITION For α-diversity of the sponge-dwelling fauna a Mixed Lineal Model compared across the ecosystem, habitat, and micro-habitat scales, nesting the sample point in the reef system and nesting the reef system in the reef profile; we used as covariables the ‘sample point longitude’, ‘reef coverage area’, ‘sponge depth’, ‘sponge density at the sample point’ and ‘sponge morphological variability’. All α-diversity analyses used the ‘lme4’ library (Bates et al., 2015) in R-project software. For β-diversity, we generated a pairwise dissimilarity resemblances matrix using a Bray-Curtis geometrical space among sampled sponges. This matrix led to a linear model based on permutational multivariate analysis of variance (PERMANOVA, Anderson 2017), nesting the ‘sampled reef’ (random factor) in the ‘reef profile’ (fixed factor), then the ‘sample point’ (random factor) in the ‘sampled reef’ and using as covariables the ‘sample point longitude’, ‘reef coverage area’, ‘sponge depth’, ‘sponge density at the sample point’ and ‘sponge morphological variability’. We used a Type I (sequential) sum of squares and 9999 permutations. Also, we tested changes on β-diversity by factor levels of source of variations and quantified the proportion of variance by source of variation, measured with the square root of the coefficient of variation (Anderson, 2001, 2017; Anderson et al., 2011). All β- diversity analyses used PRIMER v7 software (Clarke & Gorley, 2015). To analyze the differences in β-diversity across the three spatial scales, a metric Multi- Dimensional Scaling (mMDS) used the Bray-Curtis similarity index for each spatial scale: among sponges, among centroids of the different sample sites, and among centroids of the different reef systems. Results VARIATION IN α-DIVERSITY AND β-DIVERSITY ACROSS SPATIAL SCALES Spatial variation in α-diversity (within-sample diversity) of sponge-dwelling macrofauna across ecosystem, habitat, and micro-habitat scales showed a notable homogeneity within each spatial scale (Table 1). At the ecosystem scale (figure 3), there was no significant association between α-diversity and reef profile (LRT = 0.0187; p = 0.89134), reef identity (LRT = 3.3229; p = 0.06832), coral-reef coverage area (t-value = -1.095; p = 0.353), or reef longitudinal 60 | P a g e location (t-value = 1.102; p = 0.337). Likewise, at the habitat scale (figure 4), there was no significant association between α-diversity and sample identity (LRT = 0.1713; p = 0.67892), inter-sponge distance (t-value = 1.269; p = 0.212), or sponge depth (t-value = -0.057; p = 0.955). At the micro-habitat scale (figure 5), there was a positive relationship between α- diversity of the guest fauna and the morphological variability of the sponge (t-value = 5.456; p < 0.01); this supported the expectation that a higher morphological variability in sponges would result in a higher α-diversity of associated species. On the other hand, β-diversity of the guest communities showed a different trend (table 2). At the ecosystem scale (figure 3) β-diversity (between-reef diversity) was influenced by variation among the reef systems (pseudo-F = 1.873; p = 0.028), rather than by reef profile (pseudo-F = 0.693; p = 0.831), longitudinal gradient (pseudo-F = 1.364; p = 0.215), or species-area relationship (pseudo-F = 0.614; p = 0.920). At the habitat scale (figure 4) there were differences between sampled communities (pseudo-F = 1.410; p < 0.001), but these showed no relationship to depth (pseudo-F = 1.163; p = 0.353) or inter-sponge distances (pseudo-F = 0.810; p = 0.662), suggesting that there are other, unmeasured variables that could contribute to these differences. At the micro-habitat scale (figure 5), the β-diversity of sponge-dwelling fauna increased with increasing heterogeneity of the sponge host (pseudo-F = 3.000; p < 0.006). GUEST SPECIES COMPOSITION AND SPATIAL SOURCES OF VARIATION Found here in the tubular sponge Callyspongia aculeata were 76 macroinvertebrate species representing Arthropoda (64 species), Echinodermata (11), and Cnidaria (1). Within Arthropoda, the subphylum Crustacea was dominant, although confined to Malacostraca, except for a non-identified morpho-species that was assigned to Pycnogonida. Within Echinodermata, specimens represented one class (Ophiuroidea) and two orders (Amphilepidida and Ophiacantida). Within the Cnidaria, the one species found belonged to the Parazoanthidae (Anthozoa). The factors that best explained the observed patterns of the β-diversity of sponge dwelling fauna differed between spatial scales (table 2). At the ecosystem scale, ～38.87% of the variability was explained by 4 components, the most important being the reef system which explained 15.94% of total variation. At the habitat scale, ～19.80% of total variation was 61 | P a g e explained by 3 local components, with sample point explaining 14.64%. At the micro-habitat scale, 5.10% of the total was explained by variation in sponge morphology. Only 36.24% of the total variation reflected intrinsic differences among the components of the sponge- dwelling communities (residual variation). Discussion While acknowledging dissimilarities in sponge-guest community assemblages between different spatial scales, our principal findings exhibited a complementary pattern between α- diversity and β-diversity. Specifically, ecosystemic variation in α-diversity and β-diversity was driven primarily by a difference in species composition between reef systems. At the habitat scale, the diversity indices differed between different parts of a reef but this was not attributable to differences in depth or in the in-between sponge distances. At the micro-habitat scale, both species richness (α-diversity) and variance in species composition (β-diversity) increased with increasing structural heterogeneity of the host sponges. ECOSYSTEM-SCALE COMPONENTS OF SPECIES DIVERSITY Patterns differed between α- and β-diversity. Species richness of the macroinvertebrates dwelling in Callyspongia aculeata was not influenced by the area of the ecosystem. Nor did it reflect the longitudinal geographic gradient along this study area; hence, these macroinvertebrates did not follow the pattern of reductions in species richness predicted for coral reef species along the path from the Caribbean Sea to the Gulf of Mexico (Jordán- Dahlgren, 2002). Each reef system appeared to maintain a similar number of species irrespective of size of reef or geographical position. However, the ecosystem-scale β-diversity index showed a clear reef-to-reef variability in composition of these sponge-dwelling communities. In other marine models, at ecosystem scales, a high β-diversity is expected when connectivity between environmental systems is low (Valanko, 2012). The process of emigration will persist, but the immigration of neighboring dominant species will be prioritized over less-dominant species (Matias et al., 2012; Mouquet & Loreau, 2003; Valanko, 2012). At the oceanographic level, over the entire Yucatán Continental Shelf the primary connection pathway occurs in the confluence zone between neritic and oceanic waters on the outer part of the shelf (Sanvicente-Añorve et al., 2014). Coral reefs of the northeastern shelf (Bajos del Norte and Alacranes) have a robust 62 | P a g e interconnectivity influenced by atmospheric systems and their associated wind and current changes (Sanvicente-Añorve et al., 2014, 2018), and this could lead to higher self-recruitment in these reefs (Sanvicente-Añorve et al., 2014). These currents generate a sporadic connectivity between these shelf reef systems (Jordán-Dahlgren, 2002). For benthic organisms, the planktonic larval stage is often the primary, and sometimes exclusive, method of dispersal, with critical implications for species colonization in new regions (Turon et al., 2000; Sanvicente-Añorve et al., 2018). Dispersion capability involves two crucial elements: larval energy supply and settlement strategies (Turon et al. 2000; Kendall et al. 2013); these determine the duration of the pelagic larval stage. Ultimately, planktonic larvae die if they fail to find a habitat suitable for settlement (Bonhomme and Planes 2000; Zapata and Herrón 2002; Lester and Ruttenberg 2005; Shanks 2009; Kendall et al. 2013; Sanvicente-Añorve et al. 2018a). We would expect those species with a longer pelagic larval stage to have an extensive distribution over the shelf, whereas those with a short larval phase or lacking planktonic larvae would be limited to self-recruitment within a single reef system. For instance, the primary community of macroinvertebrates dwelling in C. aculeata sponges across all reef systems in this study included Synalpheus hemphilli, S. fritzmuelleri, Lysmata pederseni, Ophiothrix lineata, Ophiactis savignyi, Leucothoe kensleyi, L. ashleyae, and Colomastix tridentata. Of these, S. hemphilli larvae can survive for up to 90 days (Knowlton, 1973), and Lysmata pederseni larvae for 18−160 days and with the capacity to delay settlement through a final molt (Rhyne et al., 2009; Anger, 2001). The dual reproductive strategy of O. savignyi (Hendler et al., 1995) contributes to its extensive distribution across the shelf. In contrast, larvae of smaller ophiuroids such as Ophiactis quinqueradia may have a briefer pelagic phase and limited dispersal within specific sponge hosts (Mladenov and Emson 1988; Hendler et al. 1995). Amphipods have no larval stage, and this limits their dispersal capacity, although certain species such as L. kensleyi, L. ashleyae, and C. tridentata have a wider distribution, apparently by rafting on sponge fragments (DeBiasse et al., 2016). Most amphipod species were limited to one, two, or three reef systems, with specific distributions noted (e.g., Ericthonius brasiliensis in Bajos del Norte, Obispos, and Cayo Arenas). Some organisms, such as O. angulata, Periclimenes sandyi, and Umimayanthus parasiticus, have a wider habitat range, not relying exclusively on sponges, and are found across various depths and substrates, including diverse sponge species (Hernández-Díaz et al., 2023; Pérez-Botello & Simões, 2021a; Santana et al., 2017; Ugalde 63 | P a g e García, 2014), and this contributes to their widespread distribution among the coral reef systems on the Yucatán Continental Shelf. This study underscores the significance of the relationship between ecosystem processes such as marine currents and biological processes such as the pelagic larval phase of sponge-dwelling species. Only those species capable of synchronizing their reproduction and dispersal with the sporadic reef interconnectivity will have the opportunity to migrate to other reefs. In contrast, organisms unable to achieve synchronization, or having a brief pelagic larval phase, or lacking a larval phase, will be constrained in their distribution. It is possible that reef-to-reef species homogeneity and species variation are regulated through i) the temporal connectivity of the coral reefs on this shelf and ii) the reproductive and dispersal strategies shown by the sponge-dwelling species themselves. This would result in dissimilarity among the sponge-dwelling communities on the shelf (higher ecosystem β-diversity) but maintaining stable the α-diversity of the individual communities. HABITAT-SCALE COMPONENTS OF SPECIES DIVERSITY Although depth and density of sponges contributed 19.70% of the overall variation, neither of these factors was statistically significant. The sampling point itself was a significant influence on species turnover, but there appear to be other, as yet unquantified local variables contributing to an increase of β-diversity. For instance, repetitive attempts to colonize could lead to a cumulative effect of founder and initial colonizer events. Dispersibility tends to decrease after establishment on a new island (i.e., a new sponge), and the distance between sponges may be an impediment, so dispersion from the island may be outweighed by the recurrence of colonization events; these are likely to drive further differentiation among communities within an “sponge archipelago” (Roscher et al., 2014; R. J. Whittaker & Fernández-Palacios, 2007). Depth can influence both species richness and taxonomic turnover to a degree that depends on the scale of analysis, whether tens, hundreds or thousands of meters (Anderson et al., 2013; Price et al., 1999). In our study, the sampled depth range extended from 1 to 25 m, revealing no distinct pattern in α- or β-diversity; this suggests that the macroinvertebrates associated with C. aculeata show a comparable likelihood of colonizing sponges in both shallow and deeper environments. 64 | P a g e The assessment here of sponge density may have oversimplified the true distance between the sponges within the reef, as each sampling site yields a unique sponge density value, from which we assume that sponges will be in closer proximity. It would be more precise to measure the in-field distance between the sampled sponges themselves, to test the effect of this separation between islands on the species diversity of their faunal communities. This could lead to a more realistic model of the diversity dynamics of the reef. Consequently, we propose that future research should measure distances between sampled sponges in situ, and if possible, also measure the first colonization effect and the implication that this could have in terms of the repeated founding events that could be happening at this spatial scale. MICRO-HABITAT-SCALE COMPONENTS OF SPECIES DIVERSITY The results suggested that species richness and species turnover in the guest community were higher in a sponge with a more heterogeneous morphology. In a reef ecosystem, an individual sponge could be considered as a micro-habitat patch available for colonization. At this spatial scale, the sponge-dwelling fauna of a reef can be conceptualized as an assembly of distinct focal communities, where each community corresponds to the fauna found on an individual sponge. Then, the assemblage of sponge-dwelling fauna over the reef can be characterized as a metacommunity, where several species interact across different sponges (Leibold et al., 2004). This perspective can be applied to the relationship between the patterns of diversity variation and the degree of heterogeneity of the sponge morphology. These patterns of diversity can be comprehended within the framework of the 'species-sorting' concept (Leibold et al., 2004), which identifies individual patches, such as distinct sponges in our context, as heterogeneous entities with diverse ecological factors. Consequently, the outcomes of species interactions depend upon specific factors of the environmental gradient that promote a species colonization-extinction dynamic (Leibold et al., 2004). Hence, the degree of heterogeneity in sponge morphology both within and between sponges could be regulating changes in the sponge-dwelling fauna by the change in the colonization-extinction rate of the guest species. This suggests that the greater the heterogeneity of the sponge, the higher the probability that it be colonized by a greater number of species and, in turn, that the more heterogeneous sponges promote the replacement of species within other sponges. Conversely, in smaller and simpler sponges there would be a higher probability that a guest individual would be expelled or unable to settle because of the limited colonizable space, and this would lead to a higher death rate and a lower rate of new colonizers. 65 | P a g e SPATIAL SCALES PARTITIONING ACROSS THE SPONGE-GUEST COMMUNITY Analysis of community composition within a multi-scale space offers the ability to comprehensively detect and measure the differential contribution of each component of variation in the species turnover system (Anderson, 2017; Legendre et al., 2005). The notable β-diversity in the present study was primarily (38.26%) attributable to a regional-scale community turnover, signifying a pattern of species replacement across the reef systems of the Yucatán Continental Shelf, with a lower contribution of local-scale or individual-scale turnover in the community composition. This implies that, initially, it is essential to have a stock of species within each reef system (regional factors) capable of colonizing each sponge present in a given reef site (local factors). Finally, it is the heterogeneity of each host sponge (individual factors) that regulates whether a new species can successfully colonize it. This implies that successfully colonization by these sponge-dwelling communities depends on a stock of their species within each reef system, capable of colonizing each sponge present in a given reef site, and with host sponges of sufficient morphological heterogeneity. These results demonstrate that the environmental heterogeneity provided by an individual sponge influences the number of species it can host (individual α-diversity) and also the number of those species in relation to the number of species in communities dwelling in other sponges (individual β-diversity). Hence, the morphology of sponges is one of the key factors regulating the small-scale processes occurring in the associated fauna of reef sponges. When combined with the behavior exhibited by each guest species, and the availability of guest larvae, the result is the community present in each host sponge. In conclusion, the patterns of sponge-associated β-diversity are a function of scale, which, in turn, reflects the ecosystem features, the dispersal capability of the sponge dwellers and the heterogeneity of the habitat/micro-habitat. Hence, a comprehensive analysis of coral reef species diversity across a broad multi-scale spatial spectrum will facilitate a deeper understanding of how sponges and their associated biota will respond to dynamic impacts and shifting environmental conditions. 66 | P a g e Acknowledgements We gratefully acknowledge the following: Secretaría de Marina-Armada de México (SEMAR), Ciudad del Carmen; Manuel Victoria and the crew of the Caribbean Kraken for logistical support during our field work; Diana Ugalde and Oscar Bocardo for help with first field identification of sponges; Julio Duarte for help with laboratory identification of shrimp species; and the entire Biodiversidad Marina de Yucatán team for their stimulating exchange of ideas. Funding This work was financed by grants to NS by the Harte Research Institute, the Harte Charitable Foundation, CONABIO-NE018, CONACyTCB-2012-01-177293 and PAPIIT IV300123. The Project and AP-B were supported by the Unidad Multidisciplinaria de Docencia e Investigación—Sisal, Facultad de Ciencias, Universidad Nacional Autonomy de México, and by CONACyT doctoral fellowship 2019-000037-02NACF. There was no additional external funding received for this study. 67 | P a g e Reference List Anderson, M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26(1), 32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x Anderson, M. J. (2006). Distance-based tests for homogeneity of multivariate dispersions. Biometrics, 62(1), 245–253. https://doi.org/10.1111/j.1541-0420.2005.00440.x Anderson, M. J. (2017). Permutational Multivariate Analysis of Variance (PERMANOVA). Wiley StatsRef: Statistics Reference Online, 1–15. https://doi.org/10.1002/9781118445112.stat07841 Anderson, M. J., Crist, T. O., Chase, J. M., Vellend, M., Inouye, B. D., Freestone, A. L., Sanders, N. J., Cornell, H. V., Comita, L. S., Davies, K. F., Harrison, S. P., Kraft, N. J. B., Stegen, J. C., & Swenson, N. G. (2011). Navigating the multiple meanings of β diversity: A roadmap for the practicing ecologist. Ecology Letters, 14(1), 19–28. https://doi.org/10.1111/j.1461-0248.2010.01552.x Anderson, M. J., Tolimieri, N., & Millar, R. B. (2013). Beta Diversity of Demersal Fish Assemblages in the North-Eastern Pacific: Interactions of Latitude and Depth. PLoS ONE, 8(3). https://doi.org/10.1371/journal.pone.0057918 Aronson, R. B., Edmunds, P. J., Precht, W. F., Swanson, D. W., & Levitan, D. R. (1994). Large-scale, long-term monitoring of Caribbean coral reefs: simple, quick, inexpensive techniques. Atoll Research Bulletin, 415–425(421), 1–19. https://doi.org/10.5479/si.00775630.421.1 Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software, 67(1). https://doi.org/10.18637/jss.v067.i01 Bell, J. J. (2008). The functional roles of marine sponges. Estuarine, Coastal and Shelf Science, 79(3), 341–353. https://doi.org/10.1016/j.ecss.2008.05.002 Chase, J. M., & Leibold, M. A. (2003). Ecological Niches: Linking Classical and Contemporary Approaches (J. N. Thompson, Ed.; Vol. 13). University of Chicago Press. https://doi.org/10.1023/B:BIOC.0000029366.24837.fc Clarke, K., & Gorley, R. (2015). PRIMER v7: User Manual/Tutorial. PRIMER-E (p. 296). Plymouth. Corredor, J. E., Wilkinson, C. R., Vicente, V. P., Morell, J. M., & Otero, E. (1988). Nitrate release by Caribbean reef sponges. Limnology and Oceanography, 33(1), 114–120. https://doi.org/10.4319/lo.1988.33.1.0114 DeBiasse, M. B., Richards, V. P., Shivji, M. S., & Hellberg, M. E. (2016). Shared phylogeographical breaks in a Caribbean coral reef sponge and its invertebrate commensals. Journal of Biogeography, 43(11), 2136–2146. https://doi.org/10.1111/jbi.12785 García-Hernández, J. E., Hammerman, N. M., Cruz-Motta, J. J., & Schizas, N. V. (2019). Associated organisms inhabiting the calcareous sponge Clathrina lutea in La Parguera, Puerto Rico. Caribbean Journal of Science, 49(2–3), 239. https://doi.org/10.18475/cjos.v49i2.a12 Garza Pérez, J. R., Mata Lara, M., García Guzmán, S., & Schirp García, E. A. (2010). Reporte de Caracterización y Evaluación de Estado de condición Arrecifal. Akumal, Q. Roo. 2010. 46. Gray, J. S. (2001). Marine diversity: the paradigms in patterns of species richness examined. Scientia Marina, 65(2), 41–56. 68 | P a g e Guerra-Castro, E. J., Cajas, J. C., Simões, N., Cruz-Motta, J. J., & Mascaró, M. (2021). SSP: an R package to estimate sampling effort in studies of ecological communities. Ecography, 1–13. https://doi.org/10.1111/ecog.05284 Hendler, G., Miller, J. E., Pawson, D. L., & Kier, P. M. (1995). Class Ophiuroidea. In Gordon Hendler, John E. Miller, David L. Pawson, & Porter M. Kier (Eds.), Sea Stars, Sea Urchins, and Allies: Echinoderms of Florida and the Caribbean (pp. 89–196). Smithsonian Institution. Hernández-Díaz, Y. Q., Solis, F., Beltrán-López, R. G., Benítez, H. A., Díaz-Jaimes, P., & Paulay, G. (2023). Integrative species delimitation in the common ophiuroid Ophiothrix angulata (Echinodermata: Ophiuroidea): insights from COI, ITS2, arm coloration, and geometric morphometrics. PeerJ, 11, e15655. https://doi.org/10.7717/peerj.15655 Jones, C. G., Lawton, J. H., & Shachak, M. (1994). Organisms as Ecosystem Engineers. Oikos, 69(3), 373. https://doi.org/10.2307/3545850 Jordán-Dahlgren, E. (2002). Gorgonian distribution patterns in coral reef environments of the Gulf of Mexico: evidence of sporadic ecological connectivity? Coral Reefs, 21, 205–215. https://doi.org/10.1007/s00338-002-0226-9 Jordán-Dahlgren, E., & Rodríguez-Martínez, R. E. (2003). The Atlantic Coral Reefs of México. Latin American Coral Reefs, 131–158. https://doi.org/10.1016/B978-044451388-5/50007- 2 Karkarey, R., Arthur, R., Nash, K. L., Pratchett, M. S., Sankaran, M., & Graham, N. A. J. (2022). Spatial decoupling of α and β diversity suggest different management needs for coral reef fish along an extensive mid-oceanic ridge. Global Ecology and Conservation, 36. https://doi.org/10.1016/j.gecco.2022.e02110 Knowlton, R. E. (1973). Larval development of the snapping shrimp alpheus heterochaelis say, reared in the laboratory. Journal of Natural History, 7(3), 273–306. https://doi.org/10.1080/00222937300770231 Koukouras, A., Russo, A., Voultsiadou-Koukoura, E., Arvanitidis, C., & Stefanidou, D. (1996). Macrofauna Associated With Sponge Species of Different Morphology. Marine Ecology, 17(4), 569–582. https://doi.org/10.1111/j.1439-0485.1996.tb00418.x Legendre, P., Borcard, D., & Peres-Neto, P. R. (2005). Analyzing beta diversity: Partitioning the spatial variation of community composition data. Ecological Monographs, 75(4), 435– 450. Leibold, M. A., Holyoak, M., Mouquet, N., Amarasekare, P., Chase, J. M., Hoopes, M. F., Holt, R. D., Shurin, J. B., Law, R., Tilman, D., Loreau, M., & Gonzalez, A. (2004). The metacommunity concept: A framework for multi-scale community ecology. In Ecology Letters (Vol. 7, Issue 7, pp. 601–613). https://doi.org/10.1111/j.1461-0248.2004.00608.x Levin, S. A. (1992). The problem of pattern and scale in ecology. Ecology. https://doi.org/10.2307/1941447 Maldonado, M., Aguilar, R., Bannister, R. J., James, J., Conway, K. W., Dayton, P. K., Cristina, D., Gutt, J., Kelly, M., Kenchington, E. L. R., Leys, S. P., Shirley, A., Tendal, O. S., Rapp, H. T., Klaus, R., & Young, C. M. (2016). Sponge Grounds as Key Marine Habitats: A Synthetic Review of Types, Structure, Functional Roles, and Conservation Concerns. In S. Rossi, L. Barmanti, A. Gori, & C. Orejas (Eds.), Marine Animal Forests The Ecology of Benthic Biodiversity Hotspots (pp. 1–39). Springer International Publishing. https://doi.org/10.1007/978-3-319-17001-5 Matias, M. G., Mouquet, N., & Chase, J. M. (2012). Dispersal stochasticity mediates species richness in source-sink metacommunities. Oikos, 122(3), 395–402. https://doi.org/10.1111/j.1600-0706.2012.20479.x 69 | P a g e Mouquet, N., & Loreau, M. (2003). Community Patterns in Source-Sink Metacommunities. American Naturalist, 162(5), 544–557. https://doi.org/10.1086/378857 Ninio, R., Delean, S., Osborne, K., & Sweatman, H. (2003). Estimating cover of benthic organisms from underwater video images: variability associated with multiple observers. Marine Ecology Progress Series, 265, 107–116. https://doi.org/10.3354/meps265107 OBIS. (2020). Intergovernmental Oceanographic Commission of UNESCO. Ocean Biodiversity Information System. www.iobis.org Pawlik, J. R. (1983). A Sponge‐Eating Worm from Bermuda: Branchiosyllis oculata (Polychaeta, Syllidae). Marine Ecology, 4(1), 65–79. https://doi.org/10.1111/j.1439- 0485.1983.tb00288.x Paz-Ríos, C. E., Pech, D., Carrera-Parra, L. F., & Simões, N. (2021). Biodiversity and biogeographic affinity of benthic amphipods from the Yucatan Shelf: an analysis across the warm Northwest Atlantic ecoregions. Systematics and Biodiversity, 19(8), 928–939. https://doi.org/10.1080/14772000.2021.1947920 Pérez-Botello, A. M., & Simões, N. (2021). Sponge-dwelling fauna: a review of known species from the Northwest Tropical Atlantic coral reefs. Biodiversity Data Journal, 9: e63372, 1– 18. https://doi.org/10.3897/BDJ.9.e63372 Price, A. R. G., Keeling, M. J., & O’callaghan, C. J. (1999). Ocean-scale patterns of “biodiversity” of Atlantic asteroids determined from taxonomic distinctness and other measures. In Biological Journal of the Linnean Society (Vol. 66). http://www.idealibrary.comon Reyes-Bonilla, H., & Jordán-Dahlgren, E. (2017). Caribbean Coral Reefs: Past, Present, an Insights into the Future. In S. Rossi, L. Bramanti, A. Gori, & C. Orejas (Eds.), Marine Animal Forests The Ecology of Benthic Biodiversity Hotspots (pp. 31–72). Springer Nature. https://doi.org/10.1007/978-3-319-17001-5_2-1 Roscher, C., Gerighausen, U., Schmid, B., & Schulze, E. D. (2014). Plant diversity and community history shift colonization success from early- to mid-successional species. Journal of Plant Ecology, 8(3), 231–241. https://doi.org/10.1093/jpe/rtu011 Santana, A., Manso, C. L. C., Almeida, A. C. S., & Alves, O. F. S. (2017). Redescription and designation of a neotype for Ophiothrix angulata (Say, 1825) (Echinodermata: Ophiuroidea: Ophiotrichidae). Zootaxa, 4344(2), 291–307. https://doi.org/10.11646/zootaxa.4344.2.5 Sanvicente-Añorve, L., Zavala-Hidalgo, J., Allende-Arandía, E., & Hermoso-Salazar, M. (2018). Larval dispersal in three coral reef decapod species: Influence of larval duration on the metapopulation structure. PLoS ONE, 13(3). https://doi.org/10.1371/journal.pone.0193457 Sanvicente-Añorve, L., Zavala-Hidalgo, J., Allende-Arandía, M. E., & Hermoso-Salazar, M. (2014). Connectivity patterns among coral reef systems in the southern Gulf of Mexico. Marine Ecology Progress Series, 498, 27–41. https://doi.org/10.3354/meps10631 Socolar, J. B., Gilroy, J. J., Kunin, W. E., & Edwards, D. P. (2016). How Should Beta-Diversity Inform Biodiversity Conservation? In Trends in Ecology and Evolution (Vol. 31, Issue 1, pp. 67–80). Elsevier Ltd. https://doi.org/10.1016/j.tree.2015.11.005 Spalding, M. D., Fox, H. E., Allen, G. R., Davidson, N., Ferdala, Z. A., Finlayson, M., Halpern, B. S., Jorge, M. A., Lombana, A. L., Lourise, S. A., Martin, K. D., McManus, E., Molar, J., Recchia, C. A., Robertson, J., Ferdaña, Z. A., Finlayson, M., Halpern, B. S., Jorge, M. A., … Robertson, J. (2007). Marine Ecoregions of the World: A Bioregionalization of Coastal and Shelf Areas. BioScience, 57(07), 573. https://doi.org/10.1641/B570707 Tunnell, J. W., Chávez, E. A., & Withers, K. (2007). Arrecifes coralinos del sur del Golfo de México. In Texas A&M University Press, College Station, Harte Research Institute. 70 | P a g e Ugalde García, D. M. (2014). Aspectos ecológicos de los camarones Carídeos asociados a espojas de la costa sureste del Golfo de México. Universidad Nacional Autónoma de México. Uriz, M.-J., Rosell, D., & Maldonado, M. (1992). Parasitism, commensalism or mutualism? The case of Scyphozoa (Coronatae) and horny sponges. In MARINE ECOLOGY PROGRESS SERIES Mar. Ecol. Prog. Ser (Vol. 81). Valanko, S. (2012). Dispersal and metacommunity dynamics in a soft-sediment benthic system - how well is the seafloor connected? [Ph.D.]. Abo Akademia University: Finland. Villamizar, E., & Laughlin, R. A. (1991). Fauna Associated with the Sponges Aplysina archeri and Aplysina lacunosa in a Coral Reef of the Archipiélago de Los Roques, National Park, Venezuela. Fossil and Recent Sponges, 522–542. https://doi.org/10.1007/978-3-642- 75656-6_44 Whittaker, R. H. (1972). Evolution and measurement of species diversity. TAXON, 21(2–3), 213–251. https://doi.org/10.2307/1218190 Whittaker, R. J., & Fernández-Palacios, J. M. (2007). Island Biogeography Ecology, evolution, and conservation (R. J. Whittaker & J. M. Fernández-Palacios, Eds.; Second). Oxford University Press. Wilkinson, T. A. C., Wiken, E., Bezaury-Creel, J. E., Hourigan, T., Agardy, T., Herrmann, H., Janishevski, L., Madden, C., Morgan, L., & Padilla, M. (2009). Marine ecoregions of North America. Commission for Environmental Cooperation. WoRMS Editorial Board. (2023). World Register of Marine Species. Available from Http://Www.Marinespecies.Org at VLIZ. https://doi.org/https://doi.org/10.14284/170 Zintzen, V., Anderson, M. J., Roberts, C. D., Harvey, E. S., & Stewart, A. L. (2017). Effects of latitude and depth on the beta diversity of New Zealand fish communities. Scientific Reports, 7(1). https://doi.org/10.1038/s41598-017-08427-7 71 | P a g e Figures Figure 1. Sampling sites on the Yucatan Continental Shelf. Reef systems: A, Cayo Arcas; B, Obispos; C, Banco Nuevo; D, Banco Pera; E, Triangulos; F, Cayo Arcas; G, Alacranes; H, Bajos del Norte 72 | P a g e Figure 2. Digitalization of a sponge morphology. Sponge measurements: the length, width, and height of each sponge were measured, followed by capturing between 230 and 250 photographs from all perspectives of the sponge. Model generation: each photo was processed using 3DF Zephyr to generate a digital mesh of each sponge 73 | P a g e Figure 3. Ecosystem-scale α and β diversity. Left: relationship between α-diversity and habitat components; for letters identifying reef systems, see Fig.1. Right: metric MDS showing similarity among reef systems based on the sponge-dwelling fauna. Reef profile: light blue, atol; dark blue, platform; purple, submerged reef. 74 | P a g e Figure 4. Habitat-scale α and β diversity. Left: relationship between α-diversity and habitat components. Right: metric MDS showing site similarity based on the sponge-dwelling community at each sample point. The colors on both sides of the figure correspond to the reef system identity: purple Alacranes Reef, orange Bajos del Norte, yellow Banco Nuevo, green Banco Pera, ligth blue Cayo Arcas, ligth green Cayo Arenas, gray Obispos, and dark blue Triangulos. 75 | P a g e Figure 5. Micro-habitat scale α and β diversity. Left relationship between α-diversity and morphological variability of sponges. Right: mMDS showing similarity of guest communities among sponges. Reef systems: purple Alacranes Reef, orange Bajos del Norte, yellow Banco Nuevo, green Banco Pera, ligth blue Cayo Arcas, ligth green Cayo Arenas, gray Obispos, and dark blue Triangulos. 76 | P a g e Tables Table 1. Mixed Linear Model revealing the significance of both random effects (top) and fixed effects (bottom) as sources of variation in the α-diversity model. PERMANOVA Estimates of Components of Variation Source Df Ss MS Pseudo-F Plperm) perms % of variation Complexity 1 5564.1 5564.1 3.00 0.01 9931 5.10 Sponges density 1 3514.3 3514.3 0.81 0.66 9929 2.65 Depth 1 5989.5 5989.5 1.16 0.35 —9944 2.49 Reef Area 1 3070.0 3070.0 0.61 0.92 9935 6.49 Longitude 1 9730.5 9730.5 1.36 0.22 9921 5.55 Reef Profile 2 7083.1 3541.6 0.69 0.83 9924 10.89 Reef System(Reef Profile) 4 181240 — 4531.0 1.87 0.03 —9920 15.94 Sample Point(Reef System(Reef Profile)) 39 711810 1825.2 1.41 0.00 9746 14.65 Residuals 94 121600.0 1293.6 36.24 Total 144 2.46E+05 77 | P a g e Table 2. Sources of variation in sponge-dwelling macroinvertebrate communities, based on the β-diversity model, and percentage contribution of each component to the overall model. 78 | P a g e Supplementary Material Supplementary 3. Sampling effort model based on the Multivariate Standard Error. This simulation shows the optimal range of sample sites and sampled sponges per reef system PC 2 (6 .7 % of to ta l va ri at io n) un J in < > o a 1 un 1 Sponge morphology 60] Kyo Normalize Euclidean Distance O Sponge w O 5 0 50 PC1 (89.7% of total variation) 10 79 | P a g e Supplementary 4. Principal Component Ordination of sponge morphological variables. Yellow dot: sampled sponge. 80 | P a g e Discusión Las esponjas, al igual que otras especies bioconstructoras, son ingenieros ecosistémicos que generan complejidad ambiental y manteniendo gran parte de la biodiversidad asociada a los ecosistemas que habitan (Jones et al. 1994; Rossi et al. 2017). En esta tesis se ha demostrado que uno de los factores ecológicos que regulan la estructura de la red de interacciones huésped-hospedero es el área geográfica acumulada de las diferentes especies de esponjas. Este factor se puede interpretar como el hábitat disponible para ser colonizado por diferentes especies hospederas. En este sentido la diversidad de especies asociadas a cada esponja tiene un comportamiento similar al patrón ecológico de especies-área (MacArthur & Wilson, 1963; Macarthur & Wilson, 1967), siendo que a mayor área geográfica reportada para cada esponja mayor será la riqueza de especies huéspedes. A la par, la morfología funcional que desarrolla cada especie de esponja también es un factor fundamental en el arreglo de la red de interacciones. Las esponjas con formas funcionales más complejas serán especies seleccionadas por una mayor riqueza de especies hospederas en contraste con formas estructurales sencillas. Por último, estos resultados sugieren que en niveles taxonómicos inferiores no hay una relación taxonómica clara entre los organismos que colonizan esponjas y las esponjas mismas. Con estos análisis se demostró que, a nivel de Orden, las esponjas no presentan un patrón claro de asociaciones. No obstante, es importante resaltar que, si subimos un nivel taxonómico, la Clase Demospongiae fue dominante, siendo prácticamente la única Clase que presentó algún tipo de fauna asociada. De igual manera, con el análisis multiescalar de diversidad α y β fue posible evaluar cómo la fauna asociada a Callyspongia aculeata es regulada primero por los factores 81 | P a g e ecosistémicos del sistema arrecifal, después por las características del hábitat, y por último por las características del microhábitat que proporciona cada esponja. Con estos resultados se demostró que los patrones de diversidad α y diversidad β presentes en la Plataforma de Yucatán son complementarios. Específicamente, la diversidad de especies a nivel ecosistémico está siendo regulada por la variación comunitaria de la fauna asociada presente en los diferentes sistemas arrecifales. Similar a nivel del hábitat, la variación de la comunidad se da entre los distintos puntos de muestreo. Mientras que, a nivel del microhábitat, la variabilidad en la morfología de cada esponja regula la riqueza de especies presente, así como el recambio de especies asociadas a cada esponja. Estos resultados demuestran que, al menos para la fauna asociada a las esponjas en la Plataforma de Yucatán, existe una regulación descendente, lo que quiere decir que en primer lugar, es necesario tener un conjunto de especies dentro de cada sistema de arrecifes (factores ecosistémicos) que puedan colonizar cada esponja presente en un sitio de arrecife (factores del hábitat) y, en última instancia, es la heterogeneidad de cada esponja anfitriona (factores del microhábitat) la que regula si una nueva especie puede colonizarla. Similar a los resultados obtenidos en esta tesis se ha observado que la riqueza de fauna asociada a esponjas podría estar siendo regulada por condiciones del hábitat cómo el nivel de exposición al oleaje, la profundidad o el tipo de sustrato (Briceño-Vera et al., 2021). De igual manera, en otros estudios se ha demostrado que la variabilidad morfológica de las esponjas determina la diversidad de especies que se pueden asociar a una esponja. Por ejemplo, para Spheciospongia vesparium, la riqueza de especies huéspedes está correlacionada con el volumen total de la esponja, aumentando a medida que el volumen de la esponja aumenta (Westinga & Hoetjes, 1981; Hultgren & Duffy, 2010). En el caso de las esponjas Amorphinopsis atlántica, Haliclona implexiformisel y Neopetrosia exigua, además 82 | P a g e del volumen de la esponja, el diámetro promedio de los ósculos es un factor que influye en la riqueza de especies asociadas; un ósculo de menor tamaño implica una abertura más pequeña a la esponja, limitando así el tamaño máximo de los organismos que pueden colonizar cada esponja (Briceño-Vera et al., 2021; Beepat et al., 2015). Conclusiones Esta tesis proporciona una perspectiva integral de la importancia de las esponjas como especies clave en la estructura comunitaria de los arrecifes de coral tropicales. La recopilación y análisis de datos, así como la aplicación de herramientas de análisis de redes, han proporcionado un entendimiento profundo y novedoso sobre las interacciones huésped- hospedero que ocurren en los arrecifes de coral tropicales. Esta aproximación es fundamental para el manejo y la conservación de los arrecifes de coral, ya que las esponjas son organismos centrales en la estructura de la red lo cual significa que gracias a ellas se mantiene gran parte de la diversidad de especies de los arrecifes de coral. Los resultados de esta investigación ofrecen una base sólida para futuros estudios y esfuerzos de conservación que buscan preservar la biodiversidad y la salud de los ecosistemas marinos. Además, el análisis de redes reveló la complejidad y la especificidad que se tiene en la fauna asociada a esponjas, destacando la función clave de algunas especies de esponjas, pero sobre todo la importancia funcional de la morfología de los organismos hospederos en el mantenimiento de la comunidad asociada a las esponjas arrecifales. Con este trabajo se demostró la relación entre la escala espacial de observación y los componentes de diversidad de especies al momento de analizar la biodiversidad asociadas a esponjas arrecifales, teniendo patrones distintos y complementarios tanto para diversidad α como para diversidad β a nivel ecosistémico, a nivel de hábitat y a nivel de microhábitat. Por último, los datos generados en esta investigación representan una valiosa fuente de información actualizada sobre interacciones ecológicas huésped-hospedero en los arrecifes de coral del Atlántico Tropical 83 | P a g e Noroccidental, generando una nueva línea base de conocimiento, lo que facilita futuros análisis. 84 | P a g e Referencias bibliográficas Aerts, L. (1998). Sponge-coral interactions on Caribbean reefs. Marine Ecology Progress Series, 175, 241–249. http://dare.uva.nl/document/470044 Andermann, T., Antonelli, A., Barrett, R. L., & Silvestro, D. (2022). Estimating Alpha, Beta, and Gamma Diversity Through Deep Learning. Frontiers in Plant Science, 13. https://doi.org/10.3389/fpls.2022.839407 Anderson, M. J., & Santana-Garcon, J. (2015). Measures of precision for dissimilarity-based multivariate analysis of ecological communities. Ecology Letters. https://doi.org/10.1111/ele.12385 Anderson, M. J., Tolimieri, N., & Millar, R. B. (2013). Beta Diversity of Demersal Fish Assemblages in the North-Eastern Pacific: Interactions of Latitude and Depth. PLoS ONE, 8(3). https://doi.org/10.1371/journal.pone.0057918 Andresen, E., Arroyo-Rodríguez, V., & Escobar, F. (2018). Tropical Biodiversity: The Importance of Biotic Interactions for Its Origin, Maintenance, Function, and Conservation. En W. Dáttilo & V. Rico-Gray (Eds.), Ecological Networks in the Tropics An Integrative Overview of Species Interactions from Some of the Most Species-Rich Habitats on Earth. Springer International Publishing. https://doi.org/10.1007/978-3-319-68228-0 Ávila, E., Carballo, J. L., & Cruz-barraza, J. A. (2007). Symbiotic relationships between sponges and other organisms from the Sea of Cortes (Mexican Pacific coast): same problems, same solutions. Porifera Research: Biodiversity, Innovation and Sustainability, January, 147–156. Baselga, A., & Gómez-Rodríguez, C. (2019). Diversidad alfa, beta y gamma: ¿cómo medimos diferencias entre comunidades biológicas? Alpha, beta and gamma diversity: measuring differences in biological communities. Nova Acta Científica Compostelana (Bioloxía), 26, 39–45. Bedini, R., Canali, M. G., & Bedini, A. (2003). Use of camouflaging materials in some brachyuran crabs of the Mediterranean infralittoral zone. Cahiers de Biologie Marine, 44(4), 375–383. https://www.vliz.be/imisdocs/publications/289289.pdf Beepat, S. S., Appadoo, C., Marie, D. E. P., Paula, J. P. M., Çinar, M. E., & Sivakumar, K. (2015). Macrofauna Associated with the Sponge Neopetrosia exigua (Kirkpatrick, 1900) in Mauritius. Bell, J. J. (2008). The functional roles of marine sponges. Estuarine, Coastal and Shelf Science, 79(3), 341–353. https://doi.org/10.1016/j.ecss.2008.05.002 Bell, J. J., Davy, S. K., Jones, T., Taylor, M. W., & Webster, N. S. (2013). Could some coral reefs become sponge reefs as our climate changes? Global Change Biology, 19(9), 2613–2624. https://doi.org/10.1111/gcb.12212 85 | P a g e Briceño-Vera, A. E., Ávila, E., Rodríguez-Santiago, M. A., & Ruiz-Marín, A. (2021). Macrofaunal assemblages associated with two common seagrass‐dwelling demosponges (Amorphinopsis atlantica and Haliclona implexiformis) in a tropical estuarine system of the southern Gulf of Mexico. Helgoland Marine Research, 75(1). https://doi.org/10.1186/s10152-021-00546-z Chase, J. M., & Knight, T. M. (2013). Scale-dependent effect sizes of ecological drivers on biodiversity: Why standardised sampling is not enough. Ecology Letters. https://doi.org/10.1111/ele.12112 Chase, J. M., McGill, B. J., McGlinn, D. J., May, F., Blowes, S. A., Xiao, X., Knight, T. M., Purschke, O., & Gotelli, N. J. (2018). Embracing scale-dependence to achieve a deeper understanding of biodiversity and its change across communities. Ecology Letters, 1737– 1751. https://doi.org/10.1111/ele.13151 Cruz Ferrer, M. I. (2014). Distribución y Abundancia de Ircinia strobilina e Ircinia fistularis (Demospongiae: Irciniidae) y su fauna asociada en el arrecife Tuxpan, Veracruz. En Tesis (Vol. 1, p. 54). Universidad de Veracruz. Dáttilo, W., & Rico-Gray, V. (2018). Ecological Networks in the Tropics An Integrative Overview of Species Interactions from Some of the Most Species-Rich Habitats on Earth. En W. Dáttilo & V. Rico-Gray (Eds.), Ecological Networks in the Tropics. Springer International Publishing. https://doi.org/10.1007/978-3-319-68228-0 Dembowska, W. S. (1926). Study on the Habits of the Crab Dromia Vulgaris M.E. The Biological Bulletin, 50(2), 163–178. https://doi.org/10.2307/1536681 Diaz, M. C., & Rütlzer, K. (2001). Sponges: An essential component of Caribbean coral reefs. Bulletin of Marine Science, 69(2), 535–546. http://www.scopus.com/inward/record.url?eid=2-s2.0- 0035681585&partnerID=40&md5=06c39bf986cf0c184e882cd505ae8956 Ďuriš, Z., Horká, I., Juračka, P. J., Petrusek, A., & Sandford, F. (2011). These squatters are not innocent: The evidence of parasitism in Sponge-Inhabiting shrimps. PLoS ONE, 6(7). https://doi.org/10.1371/journal.pone.0021987 Feldman, M. W. (1970). An Introduction to Mathematical Ecology. Science, 169(3940), 43–44. https://doi.org/10.1126/science.169.3940.43-a Freilich, M. A., Wieters, E., Broitman, B. R., Marquet, P. A., & Navarrete, S. A. (2018). Species co-occurrence networks: Can they reveal trophic and non-trophic interactions in ecological communities? Ecology, 99(3), 690–699. https://doi.org/10.1002/ecy.2142 González-Rivero, M., Yakob, L., & Mumby, P. J. (2011). The role of sponge competition on coral reef alternative steady states. Ecological Modelling, 222(11), 1847–1853. https://doi.org/10.1016/j.ecolmodel.2011.03.020 Harada, K., Hayashi, N., & Kagaya, K. (2020). Individual behavioral type captured by a Bayesian model comparison of cap making by sponge crabs. PeerJ, 2020(3). https://doi.org/10.7717/peerj.9036 86 | P a g e He, F., & Legendre, P. (2002). Species diversity patterns derived from species-area models. En Ecology. https://doi.org/10.2307/3071933 Holt, R. D. (1992). Ecology at the Mesoscale: The Influence of Regional Processes on Local Communities. En R. E. Ricklefs & D. Schluer (Eds.), Species Diversity in Ecological Communities: A Historical and Geographical Perspective (pp. 77–89). The University of Chicago Press. Hultgren, K. M., & Duffy, J. E. (2010). Sponge host characteristics shape the community structure of their shrimp associates. Marine Ecology Progress Series, 407, 1–12. https://doi.org/10.3354/meps08609 Legendre, P., & Legendre, L. (2012). Numerical Ecology, Volume 24. En Developments in Environmental Modelling 20 (3th ed.). Elsevier. https://doi.org/10.1017/CBO9781107415324.004 MacArthur, R. H., & Wilson, E. O. (1963). An Equilibrium Theory of Insular Zoogeography. International Journal of Evolution, 17(4), 373–387. https://doi.org/10.2307/2407089 Macarthur, R. H., & Wilson, E. O. (1967). The Theory of Island Biogeography. Princeton University Press. http://www.jstor.org/stable/j.ctt19cc1t2 Maldonado, M., Aguilar, R., Bannister, R. J., Bell, J. J., Conway, K. W., Dayton, P. K., Díaz, C., Gutt, J., Kelly, M., Kenchington, E. L. R., Leys, S. P., Pomponi, S. A., Rapp, H. T., Rütlzer, K., Tendal, O. S., Vacelet, J., & Young, C. M. (2017). Sponge Graunds as Key Marine Habitats: A Synthetic Review of Types, Structure, Functional Roles, and Conservation Concerns. En S. Rossi, L. Bramanti, A. Gori, & C. Orejas (Eds.), Marine Animal Forests The Ecology of Benthic Biodiversity Hotspots (pp. 145–184). Springer Nature. https://doi.org/10.1007/978-3-319-17001-5 Maldonado, M., Aguilar, R., Bannister, R. J., James, J., Conway, K. W., Dayton, P. K., Cristina, D., Gutt, J., Kelly, M., Kenchington, E. L. R., Leys, S. P., Shirley, A., Tendal, O. S., Rapp, H. T., Klaus, R., & Young, C. M. (2016). Sponge Grounds as Key Marine Habitats: A Synthetic Review of Types, Structure, Functional Roles, and Conservation Concerns. En S. Rossi, L. Barmanti, A. Gori, & C. Orejas (Eds.), Marine Animal Forests The Ecology of Benthic Biodiversity Hotspots (pp. 1–39). Springer International Publishing. https://doi.org/10.1007/978-3-319-17001-5 Martínez-Falcón, A. P., Martínez-Adriano, C. A., & Dáttilo, W. (2019). Redes complejas como herramientas para estudiar la diversidad de las interacciones ecológicas. En C. Moreno (Ed.), La biodiversidad en un mundo cambiante: Fundamentos teóricos y metodológicos para su estudio (Número December, pp. 265–283). Universidad Autónoma del Estado de Hidalgo/Libermex. McGlinn, D. J., & Palmer, M. W. (2009). Modeling the sampling effect in the species-time-area relationship. Ecology. https://doi.org/10.1890/08-0377.1 McLay, C. L. (1983). Dispersal and use of sponges and ascidians as camouflage by Cryptodromia hilgendorfi (Brachyura: Dromiacea). Marine Biology, 76(1), 17–32. https://doi.org/10.1007/BF00393051 87 | P a g e Pawlik, J. R. (2011). The Chemical Ecology of Sponges on Caribbean Reefs: Natural Products Shape Natural Systems. BioScience, 61(11), 888–898. https://doi.org/10.1525/bio.2011.61.11.8 Pawlik, J. R., Loh, T.-L. L., McMurray, S. E., & Finelli, C. M. (2013). Sponge Communities on Caribbean Coral Reefs Are Structured by Factors That Are Top-Down, Not Bottom-Up. PLoS ONE, 8(5), e62573. https://doi.org/10.1371/journal.pone.0062573 Perea-Blázquez, A. (2011). Interactions between sponges and the water column: nutrient utilisation and feeding by New Zealand subtidal sponges [Ph.D.]. Victoria University of Wellington. Pérez-Botello, A. M., & Simões, N. (2021). Sponge-dwelling fauna: a review of known species from the Northwest Tropical Atlantic coral reefs. Biodiversity Data Journal, 9: e63372, 1– 18. https://doi.org/10.3897/BDJ.9.e63372 Pugh, B. E., & Field, R. (2022). Biodiversity: The role of interaction diversity. En Current Biology (Vol. 32, Número 9, pp. R423–R426). Cell Press. https://doi.org/10.1016/j.cub.2022.03.063 Robson, B. J., & Barmuta, L. A. (1998). The effect of two scales of habitat architecture on benthic grazing in a river. Freshwater Biology, 30, 207–220. https://doi.org/10.1046/j.1365-2427.1998.00271.x Rossi, S., Barmanti, L., Gori, A., & Orejas, C. (2017). Marine Animal Forests The Ecology of Benthic Biodiversity Hotspots. En S. Rossi, L. Barmanti, A. Gori, & C. Orejas (Eds.), Springer. Springer Nature. https://doi.org/10.1007/978-3-319-21012-4 Rütlzer, K. (2004). Sponges on coral reefs: a community shaped by competitive cooperation. Boll Mus Ist Biol Univ Genova, 68, 85–148. https://doi.org/https://repository.si.edu/handle/10088/163 Thiel, M., & Baeza, J. A. (2001). Factors affecting the social behaviour of crustaceans living symbiotically with other marine invertebrates: a modelling approach. Symbiosis, 30, 163– 190. Tuomisto, H. (2010). A diversity of beta diversities: Straightening up a concept gone awry. Part 1. Defining beta diversity as a function of alpha and gamma diversity. Ecography, 33(1), 2–22. https://doi.org/10.1111/j.1600-0587.2009.05880.x Turon, X., Codina, M., Tarjuelo, I., Uriz, M. J., & Becerro, M. A. (2000). Mass recruitment of Ophiothrix fragilis (Ophiuroidea) on sponges: Settlement patterns and post-settlement dynamics. Marine Ecology Progress Series, 200(November 2016), 201–212. https://doi.org/10.3354/meps200201 Tylianakis, J. M., Laliberté, E., Nielsen, A., & Bascompte, J. (2010). Conservation of species interaction networks. Biological Conservation, 143(10), 2270–2279. https://doi.org/10.1016/j.biocon.2009.12.004 88 | P a g e Underwood, A. J., Chapman, M. G., & Connell, S. D. (2000). Obsevation in ecology: you can’t make progress on process without understanding the patterns. Journal of Experimental Marine Biology and Ecology, 20(2000), 97–115. Watson, R. A., & Pollack, J. B. (1999). How symbiosis can guide evolution. Advances in Artificial Life, 1674, 29–38. https://doi.org/10.1007/3-540-48304-7_7 Webster, N. S., & Taylor, M. W. (2012). Marine sponges and their microbial symbionts: Love and other relationships. Environmental Microbiology, 14(2), 335–346. https://doi.org/10.1111/j.1462-2920.2011.02460.x Westinga, E., & Hoetjes, P. C. (1981). The Intraponge fauna of Spheciospongia vesparia (Porifera, Demospongiae) at Curacao and Bonaire. Mar Biol, 62, 139–150. Whittaker, R. H. (1972). Evolution and measurement of species diversity. TAXON, 21(2–3), 213–251. https://doi.org/10.2307/1218190 Whittaker, R. J., Willis, K. J., & Field, R. (2001). Scale and species richness: Towards a general, hierarchical theory of species diversity. Journal of Biogeography. https://doi.org/10.1046/j.1365-2699.2001.00563.x Wulff, J. L. (1997). Mutualism among species of coral reef sponges. Ecological Society of America, 78(1), 146–159. https://doi.org/10.2307/2265985 Wulff, J. L. (2006). Ecological interactions of marine sponges. Canadian Journal of Zoology, 84(2), 146–166. https://doi.org/10.1139/z06-019 89 | P a g e 1! 1! y Ethology Ecology € Evolution, 2020 a Taylor £, Francis https:doi.org/10.1080/03949370.2020.1755371 Vagos 6, Fsañci Coop (0 Check for updates. Effects of floral display and abiotic i on the foraging activity of bees on Kallstroemia pubescens (Zygophvyllaceae) Mario A. SanbovaL-MOLIMA (3 +, NaTHALIa A. FLÓREZ-GÓMEZ (E, ANTAR M. Pérez-BoTELLO (5, IsmaeL A. Hinososa-Díaz (6, Jessica M. REYES- Tovar (p” and RicARDO AYALa? instituto de Ecología A.C., Red de Ecología Funcional, Carretera Antigua a Coatepec 351, El Haya, Xalapa, Veracruz C.P. 91070, México “Research Group in Ecology and Evolutionary Biology, Department of Natural Sciences, Autonomonus University of the State of Mexico, Mexico, Carretera Toluca-Tlachaloya, km 18, Cerrillo Piedras Blancas, Toluca, Estado de México, C.P. 50200, México Instituto de Biología, Universidad Nacional Autónoma de México (UNAM). Tercer Circuito sín, Ciudad Universitaria, Copileo, Coyoacán, A.P. 70-153, Ciudad de México C.P. 04510, México “Posgrado en Ciencias Biológicas, Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM). Puerto de Abrigo sín, Sisal, Yucatán, C.P. 97356, México Instituto de Ecología, Universidad Nacional Autónoma de México (UNAM). Tercer Circuito sín, Ciudad Universitaria, Copilco, Coyoacán, A.P. 70-153, Ciudad de México C.P. 04510, México "Estación de Biología Chamela, Instituto de Biología, Universidad Nacional Autónoma de México (UNAM). Apartado Postal 21, San Patricio, Jalisco 48980, México Received 22 March 2019, accepted 6 April 2020 Foraging activity of bees depends on a combination of their biology, floral traits attractive for bees and environmental factors. We carried out this study to determine whether the variation of Moral aperture, Moral display and environ- mental factors throughout the day influence the foraging activity and composi- tion of bee visitors in Kallstroemiía pubesceris (G. Don) Dandy. This research was conducted at the Chamela Biological Station, UNAM, Jalisco, Mexico. During anthesis, we collected bees and recorded the foraging behavior hourly. We mea- sured hourly the environmental factors (temperature, relative humidity, and light intensity), Moral aperture, floral display and floral reward. Using generalized linear mixed-effects models we tested which of the factors have more influence on floral aperture and foraging activity. To determine the dissimilarity of the species composition between the hours sampled, we used a one-way analysis of "Corresponding author: Mario A. Sandoval-Molina, Research Group in Ecology and Evolutionary Biology, Department of Natural Sciences, Autonomous University of the State of Mexico, Mexico, Carretera Toluca-Tlachalova, km 18, Cerrillo Piedras Blancas, C.P. 50200 Toluca, Estado de México, México and Instituto de Ecología A.C., Red de Ecología Funcional, Carretera Antigua a Coatepec 351, El Hava, Xalapa C.F. 91070, Veracruz, México (E-mail: sandoval mé hotmail.com. 5 2020 Dipartimento dí Biologia, Universitá di Firenze, ltalia 90 | P a g e Apéndices Apéndice I. Artículos publicados adicionalmente durante el programa doctoral. Y trontiers in Marine Science ORIGINAL RESEARCH published: 28 May 2021 dor 10. 3389'tmarz. 2001 6770064 OPEN ACCESS This articio was a twnitiod to Manne Bialogy a section of fhe paumnal Frontors nm Manna Somnco Receivod: 07 March 2023 Accepted: 30 Aprí 2021 Published: 23 lAxy 2021 Citation: Péraz Lotnlo AM Mascaró 1 ano Sintes N (2021) The importanco Front. Mar. Sci. £.677024. on: 10. 338%/%mnars 2021.677024 The Importance of Home Cleaning: Sediment Transport by Alpheid Shrimps Provides a Competitive Advantage to Their Host Anemones Antar Mijail Pérez-Botello'”, Maite Mascaró*” and Nuno Simóoes*”** ' Posgrado en encías Silológicas, Faciitad de Cancias, Livweraidad Naciona! Autónoma de léxico (LAM), Sisal Musco, * Unidad Auticisapiinana de Docencia e Investigación, Faciítad de Ciencias. Linwensidad Macional Autánama de Miboco (UNWWA), Sisal, Musaco, * Laboratano Nacional de Fiesdencia Costera LANRESC, CONACYT), Sisal, Meco, ' International Chair for Coastal and Marne Stuches in Mesco, Harto Resaarch insttute for Guéf of Mevoco Studes, Texas A£M Universit; Collage Station, TX, Linitad States Bartholomea annulata is a facuítative host of the A. armatus species complex. In the Mexican Caribbean it is commonty found in cracks and crevices located where the vertical walls meet the sandy bottom or on large coral patches away from the sand. To protect themselves from predators, anemones often contract their hydraulic body into a cavernous den and extend the stinging tentacies toward the entrance. The high sediment dynamics of the region, however, result in a permanent risk of animal shelters to be obstructed by sand. By both analysing field data and conducting laboratory experiments with antificial shelters, the present study explored the den cleaning behaviour widely extended amongst alpheid shrimp, and íts role in the alpheid-anemone symbiotic interaction. Videorecordings showed that den cleaning was composed of three main behaviours: digging, tossing and tamping. lt commenced as soon as 7.2 + 10.5 mín after anemones were recognised by alpheids, and behaviours wera displayed systematically amongst all 12 replicates. Despite being completely burrowed in sand, Alpheus spp. were capable of finding the anemone and liberating the entrance of the artificial shelters in less than 2.5 h. in addition, manipulative experiments showed that anemones confronted with shelters that were obstructed with sediment had a 25% probability of fufty retracting when Aloheus spp. were absent, compared to a 75% probability when shrimps had cleaned the shelter's entry and internal passage. The analysis of field data indicated that the presence of alpheid shrimps as symbionts of B. annulata was 30% higher amongst anemones in close contact with sandy bottoms than when inhabiting crevices on the top or lateral walls of hard substrates, away from the sediment. Overall, our study concludes that den cleaning constítutes a quick and effective mechanism to assure the anemone's full retraction into their den, and by keeping the sediment away, alphelds provide the necessary conditions that serve both Fronters mn Marro Science | www. hrorfñoarzn.ceg 1 May 2021 | Voksmo 8 | Artio 677024 91 | P a g e rojects « Theteam Ourwork 5 AIN A A ar METRES IE ads 92 | P a g e Apéndice II. Generación y mantenimiento del sitio web Marine Species Interactions www.marinespeciesinteractions.org