UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO POSGRADO  EN  CIENCIAS  BIOLÓGICAS   CENTRO  DE  INVESTIGACIONES  EN  ECOSISTEMAS     Y   ESCUELA  NACIONAL  DE  ESTUDIOS  SUPERIORES  UNIDAD  MORELIA       GENÉTICA  DE  LA  CONSERVACIÓN,  PÉRDIDA  Y  CARACTERIZACIÓN  DEL   HABITAT  DE  LA  GUACAMAYA  VERDE  (Ara  militaris)  EN  MÉXICO     TESIS   QUE  PARA  OPTAR  POR  EL  GRADO  DE:   DOCTOR EN CIENCIAS   PRESENTA:   FRANCISCO  ALBERTO  RIVERA  ORTÍZ     TUTOR  PRINCIPAL  DE  TESIS:  DR.  ALBERTO  KEN  OYAMA  NAKAGAWA   ESCUELA  NACIONAL  DE  ESTUDIOS  SUPERIORES  UNIDAD  MORELIA  ,  UNAM   COMITÉ  TUTOR:  DRA.  MARÍA  DEL  CORO  ARIZMENDI  ARRIAGA   FACULTAD  DE  ESTUDIOS  SUPERIORES  IZTACALA,  UNAM   COMITÉ  TUTOR:  DR.  ENRIQUE  MARTÍNEZ  MEYER   INSTITUTO  DE  BIOLOGÍA,  UNAM           MÉXICO, D.F. 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COORDINACIÓN -.- RHDO E Ciencias Biológicas Dr. Isidro Ávila Martínez Director General de Administración Escolar, UNAM Presente Por medio de la presente me permito informar a usted que en la reunión ordinaria del Subcomité de (Ecología y Manejo Integral de Ecosistemas), del Posgrado en Ciencias Biológicas, celebrada el día 28 de octubre del 2013, se acordó poner a su consideración el siguiente jurado para el examen de DOCTOR EN CIENCIAS del alumno RIVERA ORTÍZ FRANCISCO ALBERTO con número de cuenta 97362416, con la tesis titulada: “Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde (Ara militaris) en México”, bajo la dirección del Dr. Alberto Ken Oyama Nakagawa. Presidente: Dra. Ella Gloria Vázquez Domínguez Vocal: Dra. Katherine Renton Secretario: Dra. Maria del Coro Arizmendi Arriaga Suplente: Dr. Mauricio Ricardo Quesada Avendaño Suplente: Dr. Adolfo Gerardo Navarro Siguenza Sin otro particular, quedo de usted. Atentamente “POR MI RAZA HABLARA EL ESPIRITU” Cd. Universitaria, D.F., a 9 de enero del 2014, Dra. María del Coro Arizmendi Arriaga Coordinadora del Programa c.c.p. Expediente del interesado Edif. de Posgrado P. B. (Costado Sur de la Torre Il de Humanidades) Ciudad Universitaria C.P. 04510 México, D.F. Tel. 5623-0173 Fax: 5623-0172 http://pcbiol.posgrado.unam.mx UN M POSG DOHO.A~' 0.05). The tree growth form prevailed in all the sites (Table 3). The vertical forest structure composed of 16 strata showed significant differences among the 8 sampled sites (X 2= 36.124, D. F.= 15, p< 0.001); the height strata varied from 0 to 28 m across the sites (Table 3). Trees and shrubs ranging from 2 to 10 m in height dominated the vertical forest stratification in the 8 sites; however, in the localities of El Mirador del Aguila and El Cielo, the tallest trees reached over 26 m (Fig. 2). The highest species richness was documented in El Tuito (63 species), followed by Papalutla (59 species) and Nuestra Señora del Mineral (46 species); the site with the lowest species richness was Santa María de Cocos (22 species) (Table 3). The sites with the highest plant diversity were Papalutla (H’ = 3.8) and El Tuito (H’ = 3.5), while Santa María de Cocos had the lowest diversity (H’= 2.2). The analysis of permutational variance indicated that the diversity of plant communities was not significantly different among the sampling sites (F7, 40= 0.83, p> 0.05) (Table 3). The tree coverage significantly differed among the sites (F 7, 38= 0.56, p< 0.001) (Table 3). The sites with the greatest tree coverage were Mirador del Águila (162.85 m2) and El Cielo (118.28 m2). In contrast, the lowest tree coverage was documented in Papalutla (39.26 m2) and Santa María de Cocos (50.73 m2). The tree growth form had the highest coverage values in all of the sampling sites. The areas with plant species with greater height and larger DBH were Mirador del Águila, El Cielo, and El Tuito (Table 3). We found significant differences in height (F7,38= 20.17, p< 0.001) and DBH (F7, 38= 5.63, p< 0.001) among the sites. The IVI values showed that plants sampled in all of the sites were highly variable (Appendix 1, supporting information). A total of 14 tree species (Brosimum alicastrum, Bursera simaruba, Ceiba aescutifolia, Ceiba pentandra, Cyrtocarpa procera, Guaiacum coulteri, Guazuma ulmifolia, Hura polyandra, Haematoxylon brassileto, Ipomea arborences, Lysiloma divaricata, Lysiloma microphylla, Plumeria rubra, and Taxodium mucronatum) had an IVI above 0.20 and were used for modeling their distribution in association with the modeling of the Military Macaw (see the corresponding section below). The plants that showed the highest values of IVI were Lysiloma divaricata, L. microphyla, Brosimum alicastrum, Hura polyandra, and Cyrtocarpa procera. Important plant species that were present in more than one site were: L. divaricata, B. alicastrum, H. polyandra, Taxodium mucronatum, Bursera simaruba, and Guazuma ulmifolia. With the results of structure and composition obtained, it was observed that plant species with highest IVIs are those that the Military Macaw uses for feeding and nesting (Appendix 1). Comparison of structure and floristic composition. In the vegetation structure, no significant differences were found comparing the cover height and DBH between sites with and without the Military Macaw [coverage (t (11)= 0.987, p> 0.05), height (t (12)= 1780, p> 0.05) and DBH (t (12)= 15, p> 0.05)], indicating that the forests were structurally similar. A comparison of Sorensen´s similarity index among the sites confirmed 2 clearly separated groups; one contained those sites with records of the presence of the Military Macaw, and a second group formed by sites without the bird (Fig. 3). Distribution models, land cover changes, and environmental overlap. All the models obtained presented predictions above the expected by random (X 2 test, all models: p< 0.01, D. F.= 1), Also, the potential distribution of the Military Macaw showed low levels of omission (i.e., the model was successful in predicting most of the primary source data), indicating a predictive power above 90%. Figure 4 shows the modeled distribution potential map of the Military Macaw and the most important plant species for feeding and nesting. We analyzed the potential distribution and species richness of the important plants associated with the Military Macaw under 4 scenarios of land use change for the country (Fig. 4). In the potential distribution map without land use, the sites located in the Pacific slope had greater availability Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   31   1206 Rivera-Ortíz et al.- Habitat of the Military Macaw of resources (plant richness) compared with sites in eastern Mexico (Fig. 4). The highest number of species (12 to 14 species) was found scattered from Nayarit to Oaxaca in forest fragments that occupied less than 7% of the potential range of the Military Macaw habitat (Fig. 5). The 4 species that the Military Macaw predominantly relies on for food resources occupied slightly more than 28% of the potential distribution (Fig. 5). Analyzing the changes in land use from those observed in the original map (without land use) in the 1976 scenario indicated that areas with 2 to 6 species have been the most affected by the change in land use, with a reduction of 32% to 48% of their original distribution. In the Series III and Series IV, it is shown that the areas with 4 and 6 species have had a decrease of 2% and 3% respectively with respect the Series II, showing a decrease of 50%- 51% of the potential distribution in comparison with the original distribution. This finding is in contrast to other areas that had 7 and 14 plant species, which were not significantly affected by land use changes, with only 10% Table 3. Habitat characteristics of Ara militaris in Mexico Locality LSD H´ S Coverage (m2 ha−1) Height (m) Density (Ind./ ha) DBH (cm) Trees Shrubs La Sierrita 1.78 3.1 36 68.44 ± 14.11 16.41 ± 4.93 107 70 7.35 ± 0.74 Nuestra Señora del Mineral 1.90 3.2 46 81.44 ± 10.46 17.10 ± 1.16 179 90 8.88 ± 0.63 Salazares 2.57 2.7 37 162.85 ± 22.83 27.23 ± 3.00 149 48 140.50±1.7 El Tuito 2.13 3.5 63 96.24 ± 16.21 18.79 ± 2.36 245 46 74.70± 0.38 Papalutla 1.52 3.8 59 39.26 ± 6.74 10.66 ± 2.30 90 41 4.52 ± 0.74 Santa María Tecomavaca 1.19 3.2 38 58.82 ± 14.93 13.82 ± 2.42 166 21 2.93 ± 0.20 El Cielo, Tamaulipas 2.43 2.8 35 118.28 ± 22.40 23.91 ± 3.95 199 69 123.10±1.1 Santa María de Cocos, Querétaro 1.54 2.2 22 50.73 ± 4.52 9.78 ± 1.25 218 39 5.62 ± 0.39 LSD= leaf strata diversity; H´= plant diversity; S= plant richness; DBH= diameter at breast height. General values of coverage, DBH and height are the averages of each sampling site ± standard deviation. Figure 2. Vertical structure of the habitat of Ara militaris in Sonora, Sinaloa, Guerrero, Oaxaca, Querétaro, Jalisco, Nayarit, and Tamaulipas. Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   32   Revista Mexicana de Biodiversidad 84: 1200-1215, 2013 DOI: 10.7550/rmb.34953 1207 of the original distribution reduced under the 4 scenarios (1976, 2000, 2005, 2010) (Figs. 4, 5). The potential distribution of Military Macaw in Mexico suggests the existence of 226 000 km2 of suitable climatic area without considering any impact caused by changing land use. When changes were considered, the estimated remaining area was 182 000 km2, a 21.12% reduction of the original area in the 1976 scenario. For Series II, the estimation was 160 000 km2 (28.82% reduction) and for Series III, the estimated remaining habitat was 158 000 km2 (30.23% reduction), similar to Series IV with an estimated potential distribution of 154 000 km2 (32%) (Fig. 4). This pattern showed a drastic decrease in the percentage of forest cover reaching up to 32% for the species. In 2011, the calculation of protected areas available for the Military Macaw in NPAs and IBAs only accounted for 5% and 15%, respectively, of 100% (154 000 km2) of the area distributed in 26 NPAs and 43 IBAs, along the Sierra Madre Occidental and 5 NPAs and 19 IBAs in the Sierra Madre Oriental. In the western zone, the potential area was in Sinaloa, Durango, and Guerrero, and did not include any NPAs. In the eastern zone, the NPAs and IBAs were well represented through the potential distribution of the Military Macaw. In the PCA, component 1 explained 37.8% and component 2 explained 25.8% of the total variance of 19 environmental variables and altitude; PCA showed a single group (Fig. 6). In the discriminant analysis, the component LD1 explained 53.0 % and LD2 component explained 18.0 %; there was a clear overlap of environmental requirements of the Military Macaw with the 14 most important tree species associated to its distribution (Fig. 6). The projections of the environmental dimensions of Military Macaw and the 14 tree species are represented by ellipses in Figure 6. According to the Jacquard index, tree species distributions that showed the highest overlap with those of the Military Macaw were: Lysiloma microphylla (0.64), Lysiloma divaricata (0.53), Guaiacum coulteri (0.50), Ipomea arborences (0.50), Hura polyandra (0.46), Plumeria rubra (0.45), Guazuma ulmifolia (0.39), Haematoxylon brassileto (0.37), and Ceiba aescutifolia (.36). Species that showed lower overlap with Military Macaw were: Cyrtocarpa procera (0.27), Taxodium mucronatum (0.26), Ceiba pentandra (0.22), Bursera simaruba (0.16), and Brosimum alicastrum (0.14) Discussion Habitat characterization. The structural variables of the Military Macaw habitat indicated that the type of vegetation influenced the habitat selection. The Military Macaw is considered a canopy species (Íñigo-Elías, 1996; Loza, Figure 3. Cluster analyses using the Sorensen’s similarity values of sites with and without presence of Ara militaris. Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   33   1208 Rivera-Ortíz et al.- Habitat of the Military Macaw Figure 4. Models of potential geographical distribution of Ara militaris in Mexico. A, regardless of changing land use; B, scenario of changing land use of 1976; C, scenario of changing land use of year 2000 (Series II); D, scenario of changing land use of 2005 (Series III), and E, scenario of changing land use of 2010 (Series IV). Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   34   Revista Mexicana de Biodiversidad 84: 1200-1215, 2013 DOI: 10.7550/rmb.34953 1209 1997; Gómez, 2004) because it requires large canopy trees of deciduous and subdeciduous forests for feeding, breeding, and nesting behavior as well as protection against predators and thermal cover (Forshaw, 1989; Collar and Juniper, 1992; Collar, 1997; Loza, 1997; Íñigo-Elías, 1999; Salazar, 2001; Peterson et al., 2004; Rivera-Ortiz et al., 2008; Contreras-González et al., 2009). This species nests in trees of at least 15 m in height and the nests are 90 cm wide. In the nesting sites of El Mirador del Aguila, El Tuito, and El Cielo, the trees had the required structural characteristics for nesting (Collar, 1997; Loza 1997). The Military Macaw has the ability to shift its nesting sites to inaccessible sites such as steep cliffs in well-preserved areas: in La Sierrita, Papalutla, Santa María Tecomavaca, and Santa María de Cocos (Carreón, 1997; Gómez, 2004; Rivera-Ortiz et al., 2008). The suitability of habitats for the Military Macaw requires the presence of certain genera of trees, such as Brosimum, Cyrtocarpa, Celtis, Hura, Quercus, Bunchonsia, Lysiloma, and Bursera; plant species of these genera have been reported in the distribution of the Military Macaw in Mexico as important sources either for nesting or as food supply by different authors (Carreón, 1997; Loza, 1997; Gaucín, 2000 and Contreras-González et al., 2009). In populations of Colombia and Peru, species of Hura and Bursera are also reported as important trees for feeding (Flores and Sierra, 2004); these plant species contain a large amount of nutrients, such as lipids, carbohydrates, and proteins, that are important for egg laying and the development of chicks (Contreras-González et al., 2009) Comparing the vegetation structure and floristic composition in sites with and without presence of the Military Macaw, we found significant differences in the floristic composition but structural similarities. These findings indicate the reliance of the Military Macaw on specific floristic composition, commonly found in bird specialists (such as the Military Macaw). This pattern is due to the close relationship between the availability of food resources and reproductive effort (Saunders, 1977; Saunders, 1990; Collar and Juniper, 1992) with significant implications for the conservation of this species (Ruth et al., 2003). The information available to establish conservation strategies for the Military Macaw has been based mainly on the effects of illegal traffic and other biological and ecological aspects, such as abundance, demography, and reproduction (Carreón, 1997; Loza, 1997; Gaucin, 2000; Íñigo-Elías, 2000; Rivera-Ortíz et al., 2008; Contreras- Figure 5. Patterns of plant species richness associated with the hypothetical distribution of Ara militaris in Mexico. They represent the conditions of the original vegetation and its amendments considering vegetation cover assessments for 1976, 2000 (Series II), 2005 (Series III), and 2010 (Series IV). Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   35   1210 Rivera-Ortíz et al.- Habitat of the Military Macaw González et al., 2009). Feeding and reproductive habitat modification has not taken into account in the analysis of land-use changes (Jetz and Rahbek, 2002). The Military Macaw is not adequately protected in Mexico because only 5% of the potential distribution for the species is covered by the NPAs and 15% by IBAs. Of the 8 studied sites, 3 are located within a Biosphere Reserve (El Cielo, Santa María de Cocos, and Tecomavaca); one site is considered subject to ecological conservation (Cosalá), and la Sierrita Alamos is considered an area under the Protection of Flora and Fauna, while the other sites (El Tuito, Papalutla, and Salazares) are not protected ( November 18, 2010). We suggest that at least 30% of forests of the potential distribution should be protected to guarantee specific areas of nesting and feeding of the Figure 6. Environmental overlap. A, Pca of the 14 tree species and Ara militaris associated to 20 variables ecological (arrows) in the correlation circle; B, discriminant analysis of the 14 tree species and Ara militaris; C, ordination of the 19 environmental variables and altitude in 1st and 2nd LD axes. Ellipses (95% confidence) represent spatial overlap in the 14 tree species and Ara militaris. Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   36   Revista Mexicana de Biodiversidad 84: 1200-1215, 2013 DOI: 10.7550/rmb.34953 1211 Military Macaw. Distribution models, vegetation cover changes, and environmental overlap. Ecological niche modeling represents a conceptualization of the distribution of favorable environmental conditions in which a species could be found (Peterson, 2001). Our models indicate that Military Macaw and 14 arboreal plant species are found in areas with similar characteristics, at least in a coarse environmental space; this is reinforced by the high overlap environmental found in the discriminant analysis. The reciprocal prediction of environmentally based overlap could indicate few ecological differences between the Military Macaw and tree species. It is important to identify and preserve the habitats of endangered species with particular requirements such as the Military Macaw. We estimated a reduction of 32% in the potential distribution of the Military Macaw comparing 4 land-use change scenarios since 1976 to 2010. These changes were particularly dramatic when only 6 of the plant species that the Military Macaw relies on were present (Lysiloma microphylla, Lysiloma divaricata, Hura polyandra, Ceiba aescutifolia, Guaiacum coulteri, and Ipomea arborences). These findings indicated the potential negative impacts on the survival of the Military Macaw if reductions of available habitats occur as land-cover changes continue in the future (Peterson et al., 2006; Ríos- Muñoz and Navarro-Sigüenza, 2009; Contreras-Medina et al., 2010). This is supported by previous studies. Ríos- Muñoz and Navarro-Sigüenza (2009) reported a reduction of 28.5% in the available habitat of the Military Macaw by the year 2000. Marin-Togo et al. (2011) and Monterrubio- Rico et al. (2010) declared the Military Macaw locally extinct in the Mexican Pacific Coast (i.e., Michoacán, Guerrero, and Oaxaca states) and in coastal areas of more than 400 m in altitude, with a decrease of 16% of the distribution as of 2000. The land-cover change in tropical rain forests has caused the highest rates of deforestation in the country (Trejo and Dirzo, 2000), and as a consequence, Mexican parrots have suffered severe habitat declines. Specifically, a drastic decrease has been reported in habitat occupied by Ara macao (Scarlet Macaw) (86% reduction), Aratinga astec (Aztec Parakeet) (48%), and Pionus senilis (White- crowned Parrot) (49%) (Ríos-Muñoz and Navarro- Sigüenza et al., 2009; Marín-Togo et al., 2011). Renton and Salinas-Melgoza (2004) found that fragmentation and climatic variations of habitats in seasonally dry forests could adversely affect the reproductive success of Amazona finschi (Liliac-crowned Parrot). According to our results, the habitat of the Military Macaw in tropical dry forests has already been reduced drastically by almost 32%, endangering the viability of its populations. In addition, the illegal international trade of wild species has also seriously affected populations of the Military Macaw and this directly affects the loss of species distribution (Gaucín, 2000; Marín-Togo et al., 2011). Although models based on the intended habitat are very important to detect changes in the potential distribution of the Military Macaw in different scenarios, we must take into account the use of updated cartographic information of land-cover change and factors such as hunting and illegal capture to make better predictions for this species (Marin- Togo et al., 2011; Monterrubio-Rico et al., 2011). Conservation implications. The present study provides information regarding the type of vegetation and species composition that is critical for the preservation of the Military Macaw. Our findings suggest the importance of knowing the floristic composition of the habitat of endangered species and the impact of land-use variation over time on the potential distribution of those species as a tool to direct conservation efforts. It is worth noting that the use of ecological niche models and geographic data of land-use change are fundamental tools to be considered in the conservation efforts of the Military Macaw. Therefore, the protection of suitable habitats and the implementation of sustainable activities should be prioritized in conservation strategies for the Military Macaw. Habitat degradation and capture of the Military Macaw for illegal trade must be stopped and the size and number of natural protected areas must be increased. Acknowledgments F. A. Rivera-Ortíz and C. A. Ríos-Muñoz acknowledge Conacyt for doctoral scholarships for their studies in the Posgrado en Ciencias Biológicas of the Universidad Nacional Autónoma de México. 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Centro de 8   Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México (UNAM). 9   Antigua Carretera a Pátzcuaro No. 8701. Colonia Ex Hacienda de San José de La Huerta C.P. 10   58190. Morelia, Michoacán, México. 11   Email: frivera@cieco.unam.mx 12   13   2. Ramiro Aguilar. Instituto Multidisciplinario de Biología Vegetal, Universidad Nacional de 14   Córdoba (CONICET), CC 495, (5000) Córdoba, Argentina. 15   16   3. María del Coro Arizmendi. Facultad de Estudios Superiores Iztacala, Universidad Nacional 17   Autónoma de México (UNAM), Avenida de los Barrios No. 1, Colonia, Los Reyes Iztacala, 18   C. P. 54090. Tlalnepantla, Estado de México, México. 19   20   4. Ken Oyama. Escuela Nacional de Estudios Superiores (ENES) Unidad Morelia and Centro 21   de Investigaciones en Ecosistemas (UNAM). Antigua Carretera a Pátzcuaro No. 8701. 22   Colonia Ex Hacienda de San José de La Huerta C.P. 58190. Morelia, Michoacán, México. 23   24   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   43   Abstract. In the last two centuries, the development of human civilization has transformed 25   large natural areas into anthropogenic landscapes, making habitat fragmentation a pervasive 26   feature of modern landscapes. In vertebrate populations, habitat fragmentation may alter their 27   genetic diversity and structure due to limited gene flow and dispersion and reduced effective 28   population sizes, potentially leading to genetic drift in small habitat patches. We tested the 29   hypothesis that habitat fragmentation affects genetic diversity of tetrapod populations using a 30   meta-analysis. We also examined life history and ecological traits that may determine 31   differential susceptibility to genetic erosion in fragmented habitats. Our results showed that 32   habitat fragmentation reduces overall genetic diversity of tetrapod populations. Stronger 33   negative fragmentation effects were detected for amphibians, birds, and mammals. Within 34   each taxonomic group, species with large body size were more strongly affected by 35   fragmentation. The extent of habitat loss was also important; as expected, studied ecosystems 36   with extreme habitat loss showed stronger negative effects on genetic diversity irrespectively 37   of taxonomic groups. The information gathered in this review also highlights research bias 38   and gaps in the literature. The results found here should help to identify and determine the 39   probability of risk of extinction of wild populations to prioritize conservation efforts. 40   41   Key works: Amphibians, Birds, Conservation genetics, Habitat fragmentation, Genetic 42   variability, Mammalians, Reptiles, Tetrapods. 43   44   45   46   47   48   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   44   Resumen. En los últimos dos siglos, el desarrollo de la civilización humana ha transformado 49   grandes áreas naturales en paisajes antropogénicos, por lo que la fragmentación del hábitat en 50   un aspecto dominante de los paisajes modernos. En los vertebrados, la fragmentación del 51   hábitat puede afectar la diversidad y estructura genética de sus poblaciones, debido a 52   limitaciones en el flujo de genes y reducción del tamaño efectivo poblacional, lo que puede 53   llevar a procesos de deriva genética en pequeños parches de hábitat. Pusimos a prueba la 54   hipótesis de que la fragmentación del hábitat afecta a la diversidad genética de las poblaciones 55   de tetrápodos usando un meta-análisis. También examinamos rasgos ecológicos y de historia 56   de vida que pueden determinan susceptibilidad a la erosión genética en hábitats fragmentados. 57   Nuestros resultados muestran que la fragmentación del hábitat reduce la diversidad genética 58   global de las poblaciones de tetrápodos. Se detectaron fuertes efectos negativos de la 59   fragmentación para anfibios, aves y mamíferos. Dentro de cada grupo taxonómico, las 60   especies con un gran tamaño corporal fueron más fuertemente afectados por la fragmentación. 61   El grado de pérdida de hábitat también fue importante; como era de esperar, en estudios en los 62   ecosistemas con pérdida de hábitat extrema mostraron mayores efectos negativos sobre la 63   diversidad genética, independientemente de los grupos taxonómicos. La información recogida 64   en este estudio también pone de relieve sesgos y ausencias de investigación. Los resultados 65   encontrados sirven para identificar y determinar rasgos susceptibles de probabilidad de riesgo 66   de extinción de las poblaciones silvestres, lo permitirá generar criterios para priorizar los 67   esfuerzos de conservación. 68   69   Palabras claves: Anfibios, Aves, Conservación genética, Fragmentación del hábitat, 70   Variabilidad genética, Mamíferos, Reptiles, Tetrápodos. 71   72   73   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   45   Introduction 74   Human activities have changed natural habitats into anthropogenic landscapes, 75   resulting in a loss and fragmentation of originally continuous ecosystems. Such processes 76   impose important changes in the structure and distribution of natural communities, which 77   often results in the reduction of both the size and connectivity of plant and animal populations 78   surviving in fragmented habitats (Saunders et al., 1991; Fahrig, 2003; Alcaide et al., 2009). 79   Such rapid and drastic changes in land use across the globe represent the main driving forces 80   behind current biodiversity loss and will continue to do so throughout the present century 81   (Sala et al., 2000). Although not always properly acknowledged, genetic diversity represents 82   one of the three forms of biodiversity. The amount of genetic diversity is crucial in 83   determining the potential of animal populations to adapt and evolve in changing 84   environments. Thus, it is important to assess the effects of habitat fragmentation on tetrapod 85   population genetic diversity in order to help to develop tools and strategies for the 86   conservation of wild populations (Ouborg et al., 2006; Pertoldi et al., 2007). 87   After nearly three decades of research, considerable attention has been given to the 88   effects of habitat fragmentation on population abundance and distribution of different groups 89   of tetrapods (e.g. Stauffer & Best, 1980; Catan et al., 1994; Vickery et al., 1994; Kolozsvary 90   & Swilhart, 1999; Férnandez-Juricic, 2004). Within the last 15 years, however, there has 91   been a growing interest in assessing the genetic consequences of habitat fragmentation 92   (Triggs et al., 1989; Cunningham & Moritz, 1998; Lindsay et al., 2008; Meyer et al., 2008). 93   Changes in landscape configuration imposed by habitat fragmentation can affect the genetic 94   characteristics of tetrapod populations by limiting gene flow and dispersion, reducing the 95   effective population sizes and increasing the effects of genetic drift in small habitat patches 96   (Reed & Frankham, 2003; Caizergues et al., 2003). As a result, the distribution patterns of 97   genetic diversity within and among populations (i.e., genetic structure) can change drastically. 98   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   46   The immediate effects on genetic composition depend mainly on three factors: 1) the effective 99   size of remaining populations, 2) the pattern of genetic diversity of the original population 100   before fragmentation and 3) the rate of migration of individuals among patches (Bates, 2000; 101   Young et al., 1996; Meyer et al., 2008). 102   Current evidence shows that not all fragmentation scenarios result in genetic erosion 103   of vertebrate populations. Certain characteristics of species may confer differential 104   susceptibility to lose genetic diversity in fragmented habitats. For example, degree of vagility 105   of tetrapod species can be an important susceptibility trait. In this regard, amphibians and 106   reptiles would be more likely to lose genetic diversity due to their low vagility, high 107   philopatry and greater susceptibility to changes in the environment, compared to birds and 108   mammals that may be able to move across matrices of unsuitable habitat (Wind, 1996; Moore 109   et al., 2008; Dixo et al., 2009; Allentoft & O'Brien, 2009). Moreover, the size of mobile 110   organisms determines the spatial scale of their habitat requirements. Tetrapod species with 111   large body size require large foraging and reproductive areas and usually make use of 112   different habitat types (Gurrutxaga & Lozano, 2006), which can be strongly limited in the 113   remaining fragmented habitats. Thus, within the same taxonomic group, large-body species 114   would be more susceptible to lose reproductive and genetic connectivity, being more likely to 115   suffer genetic erosion compared to small-body species. 116   In addition to the potential susceptibility of particular life-history traits of species to 117   suffer rapid genetic erosion in fragmented landscapes, other external drivers such as the 118   degree of habitat loss and fragmentation can determine the magnitude of fragmentation effects 119   on genetic diversity of tetrapod populations. Because patch size tends to be correlated with 120   genetic diversity (Frankham, 1995), we might expect that studies evaluating genetic 121   consequences of fragmentation in tetrapod populations surviving in extremely fragmented 122   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   47   habitats will show stronger effects than studies selecting less extreme or more moderately 123   fragmented systems (Holmes et al., 2013). 124   In this work, we conducted a quantitative review to evaluate the overall effects of 125   habitat fragmentation on genetic diversity of vertebrate (tetrapod) populations by testing some 126   of predictions on conservation genetics paradigms. Specifically we aim (i) to determine the 127   overall magnitude and direction of habitat fragmentation effects on genetic variability of 128   tetrapod populations, (ii) whether the magnitude of fragmentation effects on genetic diversity 129   is driven by vagility of different taxonomic groups (amphibians, reptiles, birds and mammals) 130   and body size of species within the same taxonomic group, and (iii) whether the level of 131   habitat fragmentation also guides the magnitude on of the observed effects. 132   133   Methods 134   Literature search 135   We conducted a systematic literature search comprising the period 1989-2013 through 136   several databases such as Cambridge Scientific Abstracts, Science Citation Index, Searchable 137   Ornithological Research Archive and databases of Biological Abstracts, and major publishers 138   (Blackwell Science, Springer-Verlag and Elsevier) and scientific societies that group the most 139   relevant journals in ecology, biology and conservation genetics. For this review, we only used 140   the group of tetrapod vertebrates (amphibians, reptiles, birds, and mammals). We used a 141   combination of the following keywords for conducting the literature search: (fragment* or 142   “habitat loss”) and (“genetic diversity” or “inbreeding”) and (“vertebrate*” or “amphibian*” 143   or “reptile*” or “bird*” or “mammal*”). We obtained 462 studies that were examined to 144   determine whether they met the requirements for entry into the meta-analysis. 145   Because the process of habitat fragmentation produces habitat loss, reduces population 146   size, and increases isolation between populations, our review allowed the inclusion of studies 147   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   48   analyzing any of these measures of fragmentation. We later evaluate the relative effects of 148   each of these fragmentation parameters on genetic diversity. We only excluded articles that 149   analyzed correlations between population size and genetic variability with no explicit 150   mentions to the effects of habitat fragmentation. 151   The measures of genetic variability considered were: expected heterozygosity (He), 152   number of alleles (A) and inbreeding coefficient (FIS). In studies using dominant markers 153   (RAPDs and AFLPs) we used molecular variance or gene diversity as alternative measures. 154   These four genetic parameters were not necessarily evaluated altogether within the same 155   study, so the sample sizes for each of these genetic parameters in the meta-analyses were 156   different. In studies that did not provide the inbreeding coefficient, it was calculated using the 157   expected (He) and observed (Ho) heterozygosity (FIS = He - Ho / He). 158   For each vertebrate species studied, we collected information on body sizes and 159   classified them into discrete categories (large or small) to compare their relative effect of size 160   within each taxonomic group (i.e., large vs. small amphibians, etc.). All this information was 161   obtained from the original paper or from other publications on the same species, but not all 162   features of all species were available; therefore, the predictor variables in the meta-analyses 163   did not share the same sample size. Finally, because the studies differed in their extent of 164   fragmentation extreme values encompassed, we created two categories (moderate and extreme 165   habitat loss) to compare the magnitude of effect sizes. Following Winfree et al. (2009), we 166   categorized as ‘‘extreme habitat loss’’ to studies in which most fragmented site was < 5 Ha in 167   area, surrounded by < 5% natural habitat or was > 5km from the nearest natural habitat. 168   ‘‘Moderate habitat loss’’ refer to study systems where all these landscape parameters were 169   less extreme. 170   Some authors assessed habitat fragmentation effects on genetic parameters in more 171   than one species within the same paper and we included all these species in our meta-analysis. 172   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   49   Because the magnitude and sometimes the direction of genetic responses to habitat 173   fragmentation in each species within the same study were quite different, it is reasonable to 174   assume that the effects are independent for each species (Gurevitch & Hedges, 2001; Aguilar 175   et al., 2008). 176   177   Data analysis 178   We used a categorical meta-analysis approach to assess population genetic parameters 179   of tetrapods in two contrasting habitat conditions (fragmented vs. continuous forest), thus we 180   obtained the average and standard deviations of each of the genetic parameters (He, A, and 181   FIS) across tetrapod populations (n) in each of the two habitat conditions and these data were 182   taken from the text, tables or graphs. The magnitude of fragmentation effects on each genetic 183   parameter was quantified by calculating Hedge's d (Gurevitch & Hedges, 2001). The effect 184   size (d) can be interpreted as the difference between the genetic diversity of the vertebrate 185   groups in fragmented and continuous habitats measured in standard deviation units (Gurevitch 186   & Hedges, 2001). 187   We run separate meta-analyses for each of the different genetic parameters assessed in 188   each study. Negative values for the effect size (d) of He and A imply negative effects of 189   habitat fragmentation on these parameters, while positive values of d imply positive effects of 190   fragmentation. The interpretation of the direction of effect size for inbreeding coefficient (FIS) 191   is exactly the opposite; positive values of d imply negative effects of habitat fragmentation 192   (high inbreeding), while negative values of d indicate positive effects of fragmentation (low 193   inbreeding). 194   MetaWin software version 2.0 (Rosenberg et al., 2000) was used to run the analyses 195   and bootstrap resampling procedures as described in Adams et al. (1997) and to calculate 196   confidence intervals of effect sizes. The effects of habitat fragmentation were considered 197   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   50   significant if the 95% biased-corrected bootstrap confidence intervals (CI) of the effect size 198   (d) did not overlap zero (Rosenberg et al., 2000). Confidence intervals based on resampling 199   IC estimates are more conservative (Adams et al., 1997). The data were analyzed with 200   random effects model, assuming that differences between studies is due to sampling errors 201   and also to random variation (Raudenbush, 1994). The heterogeneity of effect sizes was 202   evaluated with Q statistics (Gurevitch & Hedges, 2001). Specifically, we examined the P 203   values associated with Qbetween statistics, which describe the variation in effect sizes attributed 204   to differences between the categorical predictors (e.g., life history and ecological traits). 205   Publication bias 206   Different methods were used to detect potential publication bias, first graphically 207   (funnel plots and weighted histograms), and secondly by weighted calculation of the failsafe 208   numbers (Rosenberg et al., 2000; Rosenberg, 2005). If the calculated failsafe number was 209   greater than 5n + 10, where n is the number of studies, then publication bias can be ignored 210   because the results are robust regardless of publication bias (Rosenberg, 2005). 211   212   Phylogenetic Meta-analysis 213   In any meta-analysis involving multiple species it is crucial to consider the 214   phylogenetic relationships among them, since more closely related species may share similar 215   response to the same factor (Rifkin et al., 2012). We used phyloMeta software version 1.3 to 216   conduct a phylogenetically independent meta-analysis (Lajeunesse, 2011). Before running the 217   analysis we constructed a phylogenetic tree for all tetrapod species included in this review 218   (Appendix S1) using cytochrome b sequences for each species, retrieved from the GenBank 219   database and aligned using the ClustalW algorithm (Thompson et al., 1994). We used 720 bp 220   to estimate the length of the tree branches covering all species included in this study using 221   PAUP 4 beta 10 (Swofford, 2003), which is based on a model of a nucleotide substitution 222   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   51   GTR + 1 + G (Meunier et al., 2011). Trees were obtained using ultrametric length branches, 223   adjusted to one (Sanderson, 2002) using R 2.9.2 (Paradist et al., 2004). Sub-trees were 224   obtained trough pruning of species for each class of tetrapods, these sub-trees were used 225   depending on the genetic parameter measured (Meunier et al., 2011). Some the tetrapod 226   species were evaluated by more than one author (see Appendix S2). For the phylogenetic 227   meta-analysis we pooled these multiple effect sizes per species using a traditional meta-228   analysis with a fixed effects model (Koricheva et al., 2013), so that we used one effect size 229   per species. 230   We used the AIC (model selection criteria) to compare model fit between the 231   conventional meta-analysis and the phylogenetic-independent meta-analysis (Lajeunesse, 232   2011). The model with the smallest AIC was selected as the best fitting the data (Hedges & 233   Olkin, 1985; Hedges, 1992). 234   235   Results 236   Conventional and Phylogenetic Meta-analyses 237   The conventional meta-analysis provided a significantly better-fit model than the 238   phylogenetically corrected meta-analysis (He: AIC = 296.23 vs. 335.21, A: AIC = 229.11 vs. 239   245.52 and FIS: AIC = 139.97 vs. 174.15), suggesting that the phylogenetic structure is not 240   influencing the variation among effects sizes and thus we only show the results from the 241   conventional meta-analyses. 242   Sample of studies 243   We obtained a total of 101 scientific publications that evaluated the effect of habitat 244   fragmentation on genetic diversity of tetrapod populations. These studies measured at least 245   one genetic parameter in 93 species of vertebrates, of which 15.4% were amphibians, 19.0% 246   reptiles, 33.6% birds and 32.0% mammals. Some species were studied more than once by 247   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   52   different authors, thus we obtained a total of 99 data points for the traditional meta-analysis 248   for the expected heterozygosity (He), 77 for the number of alleles (A), and 52 for the 249   inbreeding coefficient (FIS). Most of the studies used microsatellites (93%) as genetic markers 250   to assess the effect of habitat fragmentation on genetic variability, and the 7% of the 251   remaining studies with sequences. 252   The weighted histograms of He, A and FIS, showed unimodal distributions, with the 253   highest frequency around zero and the graph of effect size vs. sample size, showed a 254   symmetric funnel shape, indicating no publication bias in our sample (Figures not shown). 255   Similarly the fail-safe numbers calculated for each meta-analysis were always greater than 5n 256   + 10 (He 4668.8 > (5 * 99) + 10 = 505, A: 4103.1 > (5 * 77) + 10 = 395; FIS: 839.3 > (5 * 52) 257   + 10 = 260), reinforcing the robustness of these results. 258   Overall, the average weighted effect sizes of habitat fragmentation on He and A were 259   negative and significantly different from zero (Fig. 1). In contrast, habitat fragmentation had 260   no significant effect on FIS, but there was a slight trend of increased inbreeding in populations 261   living in fragmented conditions (Fig. 1). 262   When looking separately at each vertebrate group we found that fragmentation effects 263   on He were significantly negative for amphibians, mammals and birds, whereas for reptiles 264   overall mean effect was non-significant (Fig. 2). Overall effects on A were significantly 265   negative for all four taxonomic groups (Fig. 2). Fragmentation effects on inbreeding 266   coefficient (FIS) were consistently non-significant for all vertebrate groups (Fig. 2). 267   The evaluation of body size within each tetrapod group revealed that fragmentation 268   effects on He were significantly different for amphibians and birds (amphibians: Qbetween = 269   9.9873, p = 0.0015; birds: Qbetween = 2.8681, p = 0.0503; Fig. 3), with larger-sized species of 270   birds and amphibians showing significantly stronger mean effect sizes than their smaller-sized 271   counterparts on He. When analyzing A, all tetrapod groups showed significant differences 272   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   53   between small versus large sized species (amphibians: Qbetween = 12.2179 p = 0.00004; 273   reptiles: Qbetween = 4.2532, p = 0.0391; birds: Qbetween = 4.4264, p = 0.0353) with the exception 274   of mammals (Qbetween = 3.6570, p = 0.0558). The response patterns remain as before, with 275   significantly larger mean negative effect sizes in large-bodied species (Fig. 3). In particular 276   for amphibians and reptiles, only large-sized species showed significant negative effects in A, 277   while small-sized species show no significant fragmentation effects in A (Fig. 3). 278   We also detected that populations found in extremely fragmented habitats have 279   significantly stronger effects in A (Q between = 3.6983, p = 0.007). Although with a similar 280   trend, no significant differences were observed in He (Q between = 2.3649, p = 0.501) and FIS 281   (Q between = 0.2689, p = 0.634) (Fig. 4). 282   283   Discussion 284   In this study, we showed that habitat fragmentation reduces overall genetic diversity 285   of tetrapod populations. The four groups of tetrapods showed similar negative fragmentation 286   effects in allelic richness. Although a relatively fewer effect sizes were calculated for 287   amphibians and reptiles, we still detected lower genetic diversity in fragmented habitats. Such 288   decrease in allelic richness is likely to be the immediate result of sudden population 289   reductions due to habitat loss and fragmentation, generating genetic bottlenecks. The impact 290   of bottlenecks in genetic variation depends primarily on two factors: the effective size of the 291   population and the time during which the population is kept small. Drastic reduction in the 292   effective size of populations caused by habitat fragmentation reduces the genetic variation of 293   remaining populations and will also affect the genetic variation of the following generations 294   that remain in the fragments should gene flow is interrupted (Hoelzel, 1999). 295   We also observed negative fragmentation effects on the expected heterozygosity in 296   amphibians, birds and mammals but not in reptiles. Reduced expected heterozygosity in 297   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   54   fragmented populations can be the result of genetic drift. When populations remain small and 298   isolated for some generations, reductions in genetic variability occur by random elimination 299   of heterozygous genotypes, affecting the number and frequencies of alleles (Reed & 300   Frankham, 2003; Caizergues et al., 2003). 301   In contrast to the genetic diversity parameters, we did not observe significant changes 302   in the inbreeding coefficients in fragmented habitats. The vast majority of the studies included 303   here, the inbreeding coefficients were estimated on adults, not on progeny, thus, reflecting 304   mating patterns of long-lived adult individuals, which may precede fragmentation events. It 305   would be very interesting to determine inbreeding on progeny generated in fragmented 306   habitats, as new habitat configurations may be causing changes in mating patterns towards 307   increased biparental inbreeding (Aguilar et al., 2008). 308   We observed that amphibian populations surviving in fragmented conditions showed a 309   stronger decreased in genetic diversity, especially in expected heterozygosity. Because their 310   inherent high philopatry and low vagility, amphibian populations can be especially affected 311   by decreased connectivity in fragmented habitats, strongly limiting gene flow between 312   populations (Gibbs, 1998, Saunders et al., 1991; Couvet, 2002, Bowne & Bowers, 2004; 313   Allendorf & Luikart, 2007; Allentoft & O `Brien, 2010). Moreover, amphibians are 314   comparatively shorter-lived, thus individuals living in fragmented conditions expressed 315   stronger effects on expected heterozygosity than the rest of the tetrapods (Cushman 2006). 316   The loss of genetic diversity in amphibian populations has been little recognized as a potential 317   factor in the overall decline of their populations. Our results suggest that genetic erosion 318   imposed by habitat fragmentation can play an important role in the rate of species loss of 319   amphibians (e.g., Allentoft & O `Brien, 2010). 320   In reptiles, we only observed fragmentation effects in allelic richness. No significant 321   decrease in expected heterozygosity of fragmented reptile populations may be due to their 322   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   55   relative longer life spans, which imply that individuals surviving in fragmented conditions 323   may have been there before fragmentation occurred. Thus, genetic diversity measured as 324   expected heterozygosity in such adult populations would simply reflect the pre-fragmented 325   situation, because not enough time has yet elapsed to reveal genetic drift effects (Cunningham 326   & Moritz, 1998; Ciofi et al., 2002; Kuo & Janzen, 2004; Marsack & Swanson, 2009). 327   Another potential reason may be due to taxonomic bias of the studied species within reptiles. 328   Most of the species belong to the suborder saurians (lizards), which have higher mobility 329   compared to the suborder ophidians (snakes) that have been less well studied. 330   The observed negative effects of habitat fragmentation on the genetic diversity of 331   birds is surprising, given that this group is considered highly vagile and presumably able to 332   cross large areas of unsuitable habitat compared to the other tetrapod groups (Avise, 1996; 333   Busch et al., 2000; Crochet, 2000; Ehrich & Stenseth, 2001; Wang & Schreiber, 2001). Most 334   of the studies up to now have been conducted in bird species of the orders Passeriformes and 335   Galliformes. Within Passeriformes group there is high incidence of philopatric bird species 336   with restricted flight capacity and specific habitat requirements (Avise, 1996; Boone & 337   Rhodes, 1996, Kurtis et al., 1999). Therefore, for this particular taxonomic group, habitat 338   fragmentation may reduce gene flow between remnant populations increasing genetic drift 339   and genetic erosion (e.g., Bates, 2000; Segelbacher & Storch 2002; Brown et al., 2004; 340   Mercival et al., 2007; Lindsay et al., 2008; MacDougall-Shackleton et al., 2011).  341   Like amphibians and birds, mammals had lower genetic diversity in fragmented 342   environments. The majority of species studied are small philopatric mammals that are 343   particularly sensitive to environmental perturbations. Such biological characteristics make 344   them particularly vulnerable because isolated populations of small mammals are less capable 345   to disperse across the inhospitable matrix, restricting gene flow and increasing genetic drift, 346   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   56   thereby losing genetic variability (e.g., Telfer et al., 2003, White & Searle, 2007; Lada et al., 347   2008; Olivieri et al., 2008, Meyer et al., 2008; Pacioni et al., 2011). 348   According to our results, the genetic variability of species with large body size within 349   each tetrapod group was more strongly affected by habitat fragmentation. Body size is 350   positively related to the range of distribution, as larger species require more amount of habitat 351   for feeding and breeding. Also, large-sized species usually occur in low densities. Therefore, 352   larger spatial requirements together with lower population densities may make large-sized 353   species particularly susceptible to suffer genetic erosion in fragmented habitats (Bergl et al., 354   2008). In addition, bird and mammal species of large body size in particular have 355   reproductive traits such as low number of offspring per reproductive event and longer time to 356   reach sexual maturity, which can also increase genetic erosion susceptibility (Wooten & 357   Smith, 1985; Caro & Laurenson 1994; Caughley, 1994; Frankham, 1995; Jost & Brandl, 358   1997; Ewers & Didham, 2006; Prugh et al., 2008). 359   360   Conservation implications. The controversy about whether ecological and 361   demographic factors are more important than genetic factors for the decline and extinction of 362   populations or even species has been recently evaluated (Frankham et al., 2003, Spielman et 363   al. 2004). Most taxa are not driven to extinction before genetic factors have been negatively 364   affected (Spielman et al., 2004). Tetrapod species surviving in fragmented habitats are, 365   overall, likely to suffering genetic erosion, compared to populations living in continuous 366   forests. Therefore, it is crucial to detect susceptible tetrapod groups of species that may 367   experience lower evolutionary potential due to their ecological and life history traits. 368   Here we observed that habitat fragmentation reduces allelic richness of all tetrapod 369   groups evaluated, and also the genetic diversity expressed as expected heterozygosity of 370   amphibian, bird, and mammal populations. Moreover, large-bodied species living in highly 371   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   57   fragmented systems are particularly prone to suffer strong genetic erosion, regardless of their 372   taxonomic identity. The information gathered in this quantitative review should help to 373   identify and determine the probability of risk of extinction of wild populations to prioritize 374   conservation efforts (Amos & Balmford, 2001; Lowe et al., 2005; Aguilar et al., 2008). 375   Despite these unequivocal signs of fragmentation effects on genetic variability, there 376   is a clear gap in the literature of population genetics of tetrapods that prevents additional 377   generalizations. Most data come from adults, and their genetic makeup may differ from that 378   of their progeny that have been subjected to fragmentation conditions. 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Phylogenetic tree of tetrapods used to performing correction in phylogenetic in 689   phyloMeta, in format Newik and image. 690    691    692    693    694    695    696   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   70   Figure Legends 697   Figure 1. Overall weighted mean effect sizes and 95% bias-corrected confidence 698   intervals (CI) of habitat fragmentation on expected heterozygosity (He), number of alleles (A), 699   and inbreeding coefficient (FIS). Sample sizes for each meta-analysis are shown in 700   parenthesis; dotted line indicates Hedge's d = 0. 701   Figure 2. Weighted mean effect sizes and 95% bias-corrected CI of habitat 702   fragmentation effects on He, A, and FIS in different tetrapod groups (Amp = amphibians, Rep 703   = reptiles, Bir = birds, Mam = mammals). Sample sizes for each group are given in 704   parentheses; dotted line Indicates Hedge's d = 0. 705   Figure 3. Weighted mean effect sizes and 95% bias-corrected CI of habitat 706   fragmentation effects on He and A of tetrapod groups (Amp = amphibians, Rep = reptiles, Bir 707   = birds, Mam = mammals) with different body size (large and small). Sample sizes for each 708   group are given in parentheses; dotted line Indicates Hedge's d = 0. 709   Figure 4. Weighted mean effect sizes and 95% bias-corrected CI of habitat 710   fragmentation effects on He, A, and FIS of tetrapod populations subjected to different extent of 711   habitat fragmentation (extreme and moderate habitat loss). Sample sizes for each group are 712   given in parentheses; dotted line Indicates Hedge's d = 0. 713    714    715    716    717    718    719    720    721   He dg e' s d 0.57 0.57 Genetic parameters -1,5- He A (99) (77) Fis (32) Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   71   FIGURE 1. 722    723    724    725    726    727    728    729    730    731    732    733    734    735    736    737    738    739    740    741    742    743    744    745    746   He Amp Rep Bir Mam (17) Q0) (32) (30) Group vertebrate A Fis Amp Rep Bird Mam Amp Rep Bir Mam (17) (16) (4) (0) (9) (9) (12) (22) Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   72   FIGURE  2.  747    748    749    750    751    752    753    754    755    756    757    758    759    760    761    762    763    764    765    766    767    768    769    770    771   Body size Large Y 0 Small He dg e' s d H 4 — H — = H — = = 0: -D0 (90) (1915 (19 (15) (6) (6) (9)(8) (1) (8) (10)(16) Amp Rep Bir Mam Amp Rep Bir Man Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   73   FIGURE  3.  772    773    774    775    776    777    778    779    780    781    782    783    784    785    786    787    788    789    790    791    792    793    794    795    796   He dg e' s d Different extent of habitat fragmentation A A A A PP a - e e e e e e Ll Extreme habitat loss 0 Moderate habitat loss (23)(21) (15) (20) (9) (11) . A Fis Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   74   FIGURE  4.  797    798    799    800    801    802    803    804    805    806    807    808    809    810    811    812    813    814    815    816    817    818    819    820    821   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   75       7.0 Capítulo III Rivera-Ortíz, F. A., Arizmendi, M. C., Solórzano, S. and Oyama, K. Genetic structure of the Military Macaw (Ara militaris) in Mexico: implications for conservation Sera enviado a la revista Conservation Genetic Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   76   Conservation genetics of the Military Macaw 1   2   Genetic structure of the Military Macaw (Ara militaris) in Mexico: implications for 3   conservation. 4   5   6   Francisco A. Rivera-Ortíz1, María Del Coro Arizmendi2, Sofía Solórzano2 and Ken 7   Oyama3 8   9   1. Francisco A. Rivera-Ortíz (Corresponding author). Centro de Investigaciones en 10   Ecosistemas, Universidad Nacional Autónoma de México (UNAM). Antigua Carretera a 11   Pátzcuaro No. 8701.Colonia Ex Hacienda de San José de La Huerta C.P. 58190. Morelia, 12   Michoacán, México. 13   Email: frivera@cieco.unam.mx 14   Telephone: (55) 56-23-27-17 15   16   2. María del Coro Arizmendi and Sofía Solórzano. Facultad de Estudios Superiores Iztacala, 17   Universidad Nacional Autónoma de México (UNAM), Avenida de los Barrios No. 1, Colonia, 18   Los Reyes Iztacala, C. P. 54090. Tlalnepantla, Estado de México, México. 19   20   3. Ken Oyama. Escuela Nacional de Estudios Superiores Unidad Morelia y Centro de 21   Investigaciones en Ecosistemas (UNAM). Antigua Carretera a Pátzcuaro No. 8701.Colonia 22   Ex Hacienda de San José de La Huerta C.P. 58190. Morelia, Michoacán, México. 23   24   25   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   77   Abstract The loss and fragmentation of ecosystems have been identified as the main threats 26   to the survival of wild populations including the Military Macaw. Accordingly, these 27   processes are expected to have influenced the genetic diversity and structure of this species. 28   We used microsatellites as a molecular marker to determine levels of genetic variability and 29   gene flow in seven sites of nesting and feeding Military Macaws in Mexico. The results 30   suggest that, compared with other species of Psitttacidae, the Military Macaw has a 31   intermediate genetic diversity, and that individuals along the Gulf of Mexico are genetically 32   distinct from populations of the Military Macaw on the Pacific slope. This may be due to two 33   barriers: the Central Mexican Plateau and the Trans-Mexican Volcanic Belt. The intermediate 34   genetic diversity detected for the Military Macaw does not seem to represent a threat for 35   survival of this species, while habitat destruction and poaching are factors that adversely 36   affect their wild populations. One important factor that influences the genetic structure of the 37   Military Macaw seems to be the topography, as revealed by the barrier analysis. Given that 38   the genetic structure observed serves to protect different regions in order to maintain genetic 39   diversity in the Military Macaw, we posit that the creation of a system of natural corridors 40   between remnant populations of the species will ensure gene flow between Military Macaw 41   populations and thus, their survival in nature. 42   43   Keywords Aramilitaris, Genetic structure, Genetic variability, Military Macaw, Macaws, 44   Psittacidae. 45   46   47   48   49   50   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   78   Resumen La pérdida y la fragmentación de los ecosistemas han sido identificados como las 51   principales amenazas para la supervivencia de las poblaciones silvestres , incluyendo la 52   Guacamaya Verde. En consecuencia, se espera que estos procesos han influido en la 53   diversidad genética y la estructura de esta ave. Se utilizó microsatélites como marcadores 54   moleculares para determinar los niveles de variabilidad genética y el flujo genético en siete 55   sitios de anidación y alimentación de la Guacamaya Verde en México. Los resultados 56   sugieren que, en comparación con otras especies de psitácidos, la Guacamaya Verde tiene una 57   diversidad genética intermediaa y que los individuos de la vertiente del Golfo de México son 58   genéticamente distintos de las poblaciones de Guacamaya Verde de la vertiente del Pacífico, 59   debido a dos barreras: El Altiplano Mexicano y el Eje Neo-Volcánico Transversal. La 60   diversidad genética moderada detectada en la Guacamaya Verde no parece representar una 61   amenaza para la supervivencia de esta especie, mientras que la destrucción del hábitat y la 62   caza furtiva son los factores que afectan negativamente a sus poblaciones silvestres. Un factor 63   importante que influye en la estructura genética de la Guacamaya Verde parece ser la 64   topografía, según lo revelado por el análisis de barreras. Dado que la estructura genética 65   observada sirve para proteger a las diferentes regiones con el fin de mantener la diversidad 66   genética en la guacamaya verde, postulamos que la creación de un sistema de corredores 67   naturales entre las poblaciones remanentes de la especie para garantizar el flujo genético entre 68   las poblaciones de Guacamaya Verde, y por lo tanto su supervivencia en la naturaleza. 69   70   Palabras clave Ara militaris, Guacamaya Verde, Guacamaya, Psitácidos, Variabilidad 71   genética, Estructura genética. 72   73   74   75   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   79   Introduction 76   The loss and fragmentation of ecosystems have been identified as the main threats to 77   the survival of wild populations (Sutherland 2000; Solórzano et al. 2003). Moreover, the 78   ecological effects of these two processes on natural populations have been recognized as 79   devastating for their long-term persistence (Saunders et al. 1991; Fahrig 2003; Alcaide et al. 80   2009). 81   In conservation biology, conceptual and methodological contributions have been 82   proposed to standardize criteria focused on searching for patterns and processes at multiple 83   scales to minimize the loss of biodiversity at all levels (Simberloff1988). However, the 84   challenge remains to determine the conservation status of species, including detailed 85   knowledge of their biology, ecology and genetics (Fernández et al. 2003; Solórzano 2003; 86   Zizumbo 2005). 87   Conservation genetics aims to investigate genetic patterns and the evolutionary 88   processes of natural populations, with particular emphasis on endangered species. An 89   additional objective in conservation genetics is to identify potential and real threats that 90   endanger the survival of such taxa (Frankham2003; Solórzano 2003; Martínez-Cruz 2011), so 91   that appropriate actions and decisions can be taken for their management and protection 92   (Lande1999; Solórzano 2003). 93   The particular case of the Military Macaw (Ara militaris), an emblematic threatened 94   bird species, is a challenge in conservation genetics. This evasive species is widely distributed 95   in fragmented tropical dry forests along Mexico´s slopes, crossing down into Central America 96   and even into parts of South America. Some field studies have concluded that the global 97   population of this bird amounts to no more than 10, 000 individuals, which represents a clear 98   decrease in its population size and distribution (Collar et al. 1992; Snyder et al. 2000; 99   BirdLife International 2013). This species is listed in Appendix I of the Convention on 100   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   80   International Trade in Endangered Species of Fauna and Flora (CITES1998), and at the global 101   level it is considered vulnerable due to habitat destruction and illegal trade 102   (BirdLifeInternational 2013). In Mexico, the Military Macaw is considered an endangered 103   species according to the official standard [Norma Oficial Mexicana (SEMARNAT 2002)]. 104   In Mexico, the Military Macaw has been recorded along the Pacific slope, from the 105   northern state of Sonora through Chihuahua to southern Chiapas (Peterson and Chaliff1989; 106   Howell and Webb1995). In the northeast of Mexico, along the slope of the Gulf of Mexico, it 107   has been reported in the state of Tamaulipas, crossing into the central states of San Luis 108   Potosi and Queretaro. In central-south Mexico, the Military Macaw has been recorded in the 109   semiarid Tehuacán-Cuicatlán valley (Peterson and Chaliff 1989; Howell and Webb; 1995; 110   Iñigo-Elías1999; Arizmendi and Márquez2000; Iñigo-Elias 2001a; 2002b;  Rivera-­‐Ortíz  111   2007). 112   Currently, the Military Macaw lives in highly fragmented forests, in which few 113   individuals have been recorded (20 to 78 individuals in some sites) (Carreón 1997; Gaucín 114   2000; Rivera-Ortíz et al. 2008), which suggests that large populations have formed small 115   isolated colonies (Iñigo-Elias 1999) that exhibit an insular distribution pattern. In addition, 116   this bird species is found in most tropical deciduous and semi-deciduous forests, with 117   seasonal movements to Pine-Oak forests. 118   This habitat fragmentation is of conservation concern because of the potential genetic 119   consequences to the species (Triggs et al. 1989; Cunningham and Moritz 1998; Lindsay et al. 120   2008; Meyer et al. 2008; Solórzano et al. 2009). Changes in landscape configuration imposed 121   by habitat fragmentation can affect the genetic characteristics of populations by limiting gene 122   flow and dispersion, thus reducing the effective population sizes and increasing the effects of 123   genetic drift in small habitat patches (Reed and Frankham 2003; Caizergues et al. 2003). As a 124   result, the distribution patterns of genetic diversity within and among populations (i.e., genetic 125   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   81   structure) can change drastically. Thus, it is important that conservation programs of 126   vulnerable species include assessment of levels of intra-specific genetic diversity (Haig 1998). 127   In this context, should be directed conservation efforts to maintain genetically diverse 128   populations, therefore need to know the levels of diversity and gene flow to try to guarantee 129   the long-term survival of this bird. Currently, many contributions have been proposed to 130   distinguish at intraspecific level the namely conservation priorities (Loza 1997; Iñigo-Elias 131   1999; Gaucín 2000; Rubio et al. 2007; Rivera-Ortiz et al. 2013). Moritz (1994) proposed that 132   genetic differentiation and the maintenance of allelic richness should be the main criteria to 133   identify conservation priorities. In the present study we applied these genetic criteria in order 134   to contribute to the conservation of the Military Macaw. For this, population genetic analyses 135   were carried out across the entire distribution range of this species in Mexico. We expected 136   that the recent habitat loss and fragmentation documented for this species (Iñigo-Elías 1999; 137   2000; Ríos-Muñoz and Navarro-Sigüenza 2009; Rivera-Ortíz et al. 2013) have led to depleted 138   levels of genetic diversity but high genetic structure among populations. 139   To date, no information is available on the structure and genetic variation of the 140   Military Macaw, and our work is intended to fill this gap. Recently, habitat loss and 141   fragmentation were identified as the main threats to Military Macaw (Ríos-Muñoz and 142   Navarro-Sigüenza 2009; Rivera-Ortíz et al. 2003). Thus, it is expected that these processes 143   have influenced the genetic diversity and structure of this bird. 144   This study analyzes the structure and genetic variability of the Military Macaw using 145   microsatellites as molecular markers. To achieve this, we characterized levels of genetic 146   variability at seven locations along the distribution of Military Macaw in Mexico and 147   evaluated the level of genetic structure in these populations. 148   149   150   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   82   Material and methods 151   Area of Study. This study was conducted at seven sites in Mexico that represent the 152   largest populations reported for Military Macaw (Gaucín 2000; Gómez-Garduño 2004; Rubio 153   et al. 2007; Rivera-Ortíz et al. 2008; Jiménez-Arcos et al. 2012). Four of these sites are 154   located in the Pacific slope: La Sierrita, Sonora; Nuestra Señora del Mineral, Sinaloa; El 155   Mirador del Águila, Nayarit; El Tuito, Jalisco. Two other areas are found in the Gulf of 156   Mexico slope: El Cielo, Tamaulipas and Santa María de Cocos, Queretaro. One area is found 157   in central Mexico in Santa María Tecomavaca, Oaxaca (Fig. 1). 158   The Protected Natural Area of the Sierrita (26 ° 52 '48'' N, 108 ° 34' 12'' W) is located 159   in Alamos, Sonora, with a maximum number of 38-40 individuals (Ordonez and Flores 1995). 160   The Ecological Conservation Area of the Nuestra Señora del Mineral (24 ° 24 '44 "N, 106 ° 161   41 '22" W) is located in the municipality of Cosalá, Jalisco, with a number of individuals by 162   census of 25-40 individuals (Rubio et al. 2007). The Mirador del Águila, Nayarit (21 ° 30 '28 163   "N, 104 ° 55' 47" W) is located in Tepic, and has a maximum number of 50 individuals on 164   average (Rivera-Ortíz et al. 2013). The Tuito is located in Jalisco (20 ° 17 '35 "N, 105 ° 23' 165   6.4" W), with a number of individuals by census of 14-20 individuals (Palomera-Garcia et al. 166   1994; Rivera-Ortíz et al. 2013). The Biosphere Reserve El Cielo is located in Tamaulipas (23 167   ° 04 '22 "N, 99 ° 09 '24" W), with a number of individuals by census of of 35-40 individuals 168   (Arizmendi and Márquez 2000; Rivera-Ortíz et al. 2013). Santa Maria de Cocos is located in 169   the Biosphere Reserve of the Sierra Gorda, Querétaro (21 ° 18 '37 "N, 99 ° 40' 4" W), with a 170   maximum number of 70 individuals (Gaucin 2000). Santa María Tecomavaca is located in 171   the Biosphere Reserve Tehuacán-Cuicatlán, Puebla-Oaxaca (17 ° 51 '43 "N, 97 ° 02 '40" W), 172   with a maximum number of 76 individuals (Rivera-Ortiz et al. 2008) (Fig.1). 173   Sample Collection. A total of 86 feather samples were collected at seven sites during 174   the fieldwork carried out during 2010 to 2012, and each sample was considered an individual. 175   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   83   These feathers were collected at the base of the trees in sites of nesting, feeding and resting, 176   and in some cases they were obtained directly from nests (each nest represented an 177   individual). These feathers were considered from different individuals until genotyping 178   confirmed they were from the same individuals. 179   We collected feathers from five individuals in La Sierrita and 23 individuals at 180   Nuestra Señora del Mineral. Thirty-six feathers were collected in El Mirador del Águila, six 181   in Santa Maria Tecomavaca and El Tuito, while five were taken in Santa Maria de Cocos and 182   El Cielo. The sampled feathers were cleaned with 90% alcohol and maintained at the 183   environmental temperature in paper bags during their transportation to the laboratory. 184   DNA extraction and Genotyping. The total genomic DNA was extracted using the 185   standard digestion proteinase K/SDS, followed by chloroform:alcohol purification as 186   described by Leeton and Christidis (1993). 187   In total, nine polymorphic nuclear microsatellite loci were amplified, of these; six 188   were designated for Blue-and-yellow Macaw (Ara ararauna) (Caparroz et al. 2003), and three 189   for The Saint Vincent Amazon (Amazon guildinguii) (Russello et al. 2001; 2005) (Table 1). 190   The nine loci assayed were prepared in individual PCR reactions using the QIAGEN 191   Multiplex PCR kit (QIAGEN), with a final volume of 5 µL including master Mix (contains 192   HotStarTaq DNA Polymerase, Multiplex PCR buffer, 3 mM MgCl2, and dNTPs), primers (5 193   pmol / µL), distilled / deionized water, and template (total genomic DNA, 20-50 ng/µL). 194   The amplifications were carried out in a GeneAmp PCR System 2720 Thermal Cycler 195   (Applied Biosystems) using multiplex PCR protocol for amplification of microsatellite loci 196   (QIAGEN): 15 min at 95 ° C (initial stage activation), followed by 30 cycles of denaturation 197   at 94 ° C for 30 s, and followed by 90 s of alignment of the primers at specific temperatures 198   (Table 1), followed by an extension of 72 ° C for 30 min, and a final extension of 60 ° C for 199   30 min. The PCR products were mixed with formamide and Gene Scan LIZ-500 standard size 200   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   84   (Applied Biosystems) and denatured for 5 min at 95 ° C for their analysis by the sequencer 201   ABI PRISM 3100-Avant (Applied Biosystems) for detecting the primer and the internal 202   standard size. The analyses of the produced fragments and their final size were determined 203   using Gene Mapper 4.0 software (Applied Biosystems). We verified and corroborated the 204   assignment of the genotype of the eight loci by testing null alleles, small alleles domain 205   registration and stutters for each population using the software Micro-Checker (Oosterhout et 206   al. 2004). 207   Genetic diversity. We estimated the total number of alleles (NT) and effective number 208   of alleles (Nae) for loci, using the software Genalex 6.3 (Peakall and Smouse 2006). For each 209   population we estimated the average number of alleles (A) and private allelic richness (PA) by 210   rarefaction with ADZE 1.0 software (Szpiech et al. 2008) due to differences in sample size 211   among the seven populations of the Military Macaw studied. Furthermore, we estimated 212   observed heterozygosity (HO), expected heterozygosity (HE), and the inbreeding coefficient 213   (FIS) by locus and for each population. Also, we estimated the probability of significant 214   deviation from the equilibrium under Hardy-Weinberg (Nei, 1978) through the Markov chain 215   method with the following parameters: dememorizations1000, batches 50 and iterationss1000, 216   adjusted to a nominal level of 5% with Bonferroni correction, with GENETIX 4.05 software 217   (Belkhir et al. 2004). 218   Differentiation and Genetic structure patterns. The genetic differentiation of 219   populations paired was calculated by FST (Weir and Cockerham1984) according to the 220   infinites alleles model (IAM) with 10,000 permutations using the software 4.05 MSA 221   (Microsatellite Analyzer) (Dieringer and Schlötterer2003). The distribution of genetic 222   variation within and among populations was estimated among the predetermined groups of 223   populations (Pacific slope and slope of the Gulf of Mexico) by analysis of molecular variance 224   (AMOVA) in ARLEQUIN 3.0 (Excoffier et al. 2005), and the statistical significance of FST 225   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   85   and RST was tested with 10,000 permutations. The levels of gene flow between populations 226   were assessed using MIGRATE 3.0 (Beerli 2008), under the Brownian model of 227   microsatellite based on maximum likelihood, with variable theta (θ) assuming a constant 228   mutation rate. 229   To assign genetic structure patterns, we used a Bayesian method available in the 230   software STRUCTURE 2.3.1 (Pritchard et al. 2000; Falush et al. 2003). In this analysis, all 231   individuals are assigned probabilistically to values of predefined K populations, to identify 232   the optimal number of genetic groups (Evanno et al. 2005). The optimal number of genetic 233   groups (K) is determined by varying the value of K from 1 to 10 and of run the analysis 10 234   times value with of K, with order to determine the maximum value of the a posteriori 235   probability [lnP (D)]. The duration of the burn-in was 500,000 steps, followed by 106 236   interactions under the model admixture with correlated allele frequencies without any prior 237   information. We determined the most probable value of K using the maximum value of ΔK 238   according to Evannoo et al. (2005). To visualize the pattern of K along the Military Macaw 239   distribution, the proportion of admixture by population was plotted on a map. 240   To determine whether the pattern of admixture is associated with the geographic 241   location of the populations, we constructed a UPGMA tree with FST distance matrix using 242   SplitsTree version 4.11.3 (Huson and Bryant 2006) and edited version Dendroscope 2, 4 243   (Huson et al. 2007). To test isolation by distance gene flow model, we performed a Mantel-244   Haenszel test with AIS 1.0 software (Alleles in Space) with 100, 000 replicas (Miller 2005). 245   Finally, to determine the geographic location of the major genetic discontinuities 246   between populations, we used the maximum difference algorithm of Monmonier, with 247   BARRIER 2.2 software (Manni et al. 2004). This program creates a map of the geographical 248   coordinates of the locations sampled. The barriers are represented on the map by identifying 249   the maximum values in the distance matrix paired population genetics. A genetic distance 250   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   86   matrix based on the proportion of shared allele (Bowcock et al. 1994) values was calculated 251   with software 4.05 MSA (Microsatellite Analyzer) (Dieringer and Schlötterer 2003). 252   Results 253   Genetic diversity. According to the Micro-Checker analysis, the probability of the 254   presence of null alleles was significant for locus UnaCT41 in all populations, and inference of 255   null alleles was 85% with the participation of 86 individuals. Therefore, this locus was 256   eliminated from the genetic analyses. The remaining microsatellite loci showed no deviation 257   from Hardy-Weinberg equilibrium (p > 0.00833, adjusted nominal level 5% with Bonferroni 258   correction, pBC = 0.00833) (Table 1). For all the loci, 151 alleles were recorded; the loci with 259   less variability were UnaCT43, UnaCT74, UnaCT55 and AgGT19, with 12 to14 alleles, and 260   the loci with most variability were UnaCT21, UnaCT32, AgGT17 and AgGT32, with 20 to 29 261   alleles. All loci varied in size from 78-227 bp, and showed high levels of observed 262   heterozygosity, from 0.63 to 0.75 (Table 1). All populations showed no deviation from 263   Hardy-Weinberg equilibrium, resulting in non-significant f values (p > 0.00167, pBC = 264   0.0133), suggesting random mating within populations (Table 2). 265   The average number of alleles (A) was high for all populations with values of 16.10 266   (El Cielo) to 19.27 (El Mirador del Águila), while the private alleles (PA) ranged from 4.85 267   (Santa María Tecomavaca) to 8.51 (Santa María Tecomavaca). The expected heterozygosis 268   (HE) ranged from 0.76 (El Mirador del Águila) to 0.54 (Santa Maria de Cocos and El Cielo), 269   and the observed heterozygosis (HO) ranged from 0.69 (Heaven) to 0.51 (La Sierrita), whereas 270   in the inbreeding coefficient (FIS), the population of El Cielo showed an excess of 271   heterozygosis (-0.16) (Table 2). 272   Differentiation and Genetic structure patterns. The comparison of paired populations 273   showed little genetic differentiation (FST) among nearby populations (Table 3). The highest 274   differentiation was in populations of Santa María de Cocos and El Cielo with rest of the 275   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   87   populations (FST = 0.12 to 0.25, P <0.05); however, the lowest differentiation was between in 276   the populations of Mirador del Águila, La Sierrita (FST = 0.02, P> 0.05), Nuestra Señora del 277   Mineral (FST = 0.05, P> 0.05), and El Tuito (FST = 0.09, P> 0.05) (Table 3). 278   The AMOVA indicated that there was variation due to differences between groups 279   (Table 4). For the FST, 6.6% of the variation was due to genetic differences between groups, 280   and 93.4% to variation within the groups, similar to the RST, in which 53.9% of the variation 281   was due to genetic differences between groups, and 46% to variation within groups (Table 4). 282   Gene flow levels (M) among the seven populations are shown in Table 5. More gene flow 283   was detected between populations of Nuestra Señora del Mineral and El Mirador del Aguila 284   (1.39), slightly less between Santa Maria Tecomavaca and La Sierrita (1.36), followed by El 285   Tuito and Santa María Tecomavaca (1.22), and finally Santa Maria de Cocos and El Cielo 286   (1.24) (Table 5). 287   The ΔK statistic revealed K = 2 to be the optimum value for the number of genetic 288   clusters in the data (Fig. 2). The proportion of ancestry of each population and individuals in 289   these two genetic clusters, represented by the green and red colors, is represented in Figure 3. 290   The populations of La Sierrita, Nuestra Señora del Mineral, El Mirador del Águila, El Tuito 291   and Santa Maria Tecomavaca, all from the Pacific slope, have a higher proportion of the 292   green genotype (80%), in contrast to the populations of Santa María de Cocos and El Cielo 293   along the Gulf slope, that have a higher proportion of 99% of the red genotype (Fig. 3). 294   The analysis of genetic distances between populations confirmed that the ratio of the 295   admixtures are geographically structured (Fig. 4a). We found that 78% of individuals in the 296   populations on the Pacific slope have the green genotype (q ≥ 0.80); however, 97% of 297   individuals in the populations along the Gulf Mexico have the red genotype (q ≥ 0.90). The 298   Mantel-Haenszel test highlighted a correlation between genetic distance and geographic 299   distance (r = 0.1330, p = 0.005), indicating isolation by distance. 300   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   88   The maximum difference algorithm of Monmonier, applied to matrix linearized FST values, 301   placed six barriers, of which two barriers have major 95 - 100% support, whereas the other 302   four barriers have 10 - 20% support (Fig. 4b). The first barrier is located between the 303   populations of La Sierrita and Nuestra Señora del Mineral (15% support), the second barrier 304   is located between the populations of Nuestra Señora del Mineral and El Mirador del Águila 305   (15% support), and the third barrier is located between the populations of Mirador del Águila 306   and El Tuito with support of 20% (Fig 4). The fourth barrier separates the populations of the 307   Pacific slope from the population of the slope of the Gulf Mexico, with a support of 100% 308   (Fig 4). The fifth barrier is located between the population of Santa María de Cocos and El 309   Cielo (10% support; Fig 4). The sixth barrier separates the population of Santa María 310   Tecomavaca from the population of the slope of the Gulf Mexico, with a support of 95% 311   (Figure 4). This analysis was very consistent with the results obtained from the structure and 312   UPGMA tree based on genetic distances (Fig 5). 313   314   Discussion 315   The levels of heterozygosis we found in the Military Macaw (HE = 0.63) are relatively 316   moderate compared with other studies of macaws. Historically, the species of macaws that 317   have had low values for heterozygosis are Spix’s Macaw (Cyanopsitta spixii), Lears Macaw 318   (Anodorhynchus leari) and the Hyacinth Macaw (Anodorhynchus hyacinthinus) (Faria et al. 319   2008; Presti et al. 2011; Presti et al. 2013) with HE values from 0.36 to 0.51. By contrast, the 320   macaw species that have had high levels for heterozygosis are the Scarlet Macaw (Ara 321   macao) (Nader et al. 1999; Presti et al. 2011) and Blue-and-Yellow Macaw (Ara ararauna) 322   (Caparroz et al. 2003) with HE levels of 0.86 and 0.80, respectively. Although the Military 323   Macaw is a vulnerable species globally and is considered endangered by Mexican norms, this 324   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   89   species maintains moderate levels of genetic diversity in Mexico, despite anthropogenic 325   pressures on wild populations (Iñigo-Elias 1999; Rivera-Ortiz et al. 2008). 326   When we compared the values of genetic diversity among populations of the Military 327   Macaw, we observed that populations of the slope of the Gulf of Mexico have a lower genetic 328   diversity (HE = 0.54). This is likely due to isolation from the rest of the distribution of the 329   Military Macaw, which causes gene flow to be more restricted than in the Pacific slope 330   populations. However, these relatively high levels of heterozygosity may reflect still the 331   diversity contained in ancestral large populations. As the estimators are strongly affected by 332   historical factors they did not detect the effects of population size decreasing and genetic 333   isolation. 334   We did not find a pattern of genetic differentiation in populations of the Macaw 335   Military due to fragmentation and habitat loss, because the Military Macaw has a long life 336   expectancy (60 years captive individuals) (Iñigo-Elias 1999), and fragmentation in the 337   geographic distribution of this species is a recent event (less than 50 years), considering the 338   life cycle of this species. Possibly, some individuals that are still breeding may be older than 339   the first anthropic disturbances. Thus, the effects of these impacts may have not yet affected 340   the genetic structure and diversity of this species. Furthermore, with a long life expectancy, it 341   is possible that the current population of Military Macaw is composed mainly of old 342   individuals, and when these old individuals die, the populations will suffer a sudden, drastic 343   size reduction, which may cause a reduction in genetic variability (Leite et al. 2008). 344   An important result is that is found clear genetic differentiation due to the 345   biogeographic regions. In this way we found significant genetic differentiation in populations 346   of the slope of the Gulf of Mexico compared to populations of the Pacific slope. This suggests 347   that the two Military Macaw populations along the Gulf coast of Mexico are closely related, 348   whereas the populations along the Pacific coast of Mexico in La Sierrita, Nuestra Señora del 349   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   90   Mineral, El Mirador del Águila, El Tuito and Santa Maria Tecomavaca show a close 350   relationship among them. Specifically, these results indicate connectivity among these 351   populations of Military Macaws, that are able to fly long distances (Gaucín et al. 2000), and 352   this hypothesis is reinforced by the high values for gene flow between these populations. The 353   dispersion that occurs is not effective, because it is limited by the selective use of the habitat 354   and availability of forest resources, and for this reason the movements are determined by the 355   spatial-time patterns from fruiting (Collar 1997, Rivera-Ortiz et al. 2008; Contreras-González 356   et al. 2009; Rivera -Ortiz et al. 2013). Consequently, habitat fragmentation appears to be an 357   important factor in the distribution and choice of breeding sites of the populations of the 358   Military Macaw (Faria et al. 2008). 359   We predicted a strong genetic structure among the populations of the Pacific slope and 360   the slope on the Gulf of Mexico. This hypothesis is supported by the Bayesian analysis, which 361   shows a major compression of the structure within and between populations (see Figure 3), 362   meaning that the populations of the slope of the Gulf Mexico are different from the 363   populations of the Pacific slope, which is consistent with the geographical region. 364   This structural pattern of the Military Macaw is similar to the biogeographic patterns 365   found in other species of Mexican birds, such as the Ferruginous Pygmy Owl (Glaucidium 366   brasilianum) (Proudfoot et al. 2006) and Wild Turkey (Melagris gallopavo) (Mock et al. 367   2002) where the genetic differences are due to the presence of geographic barriers such as 368   mountain ranges (The Sierra Madre Oriental and The Sierra Madre Occidental) and the 369   Central Mexican Plateau (Mock et al. 2002, Proudfoot et. al. 2006). 370   The two genetic groups detected in this study have a geographic concordance (see 371   Figure 4), indicating that each slope can be considered a priority conservation unit, namely 372   Management Units (MUs) (Moritz, 1994a, 1994b). MUs are defined as a population or a 373   group of individuals with high allelic differences, regardless of the evolutionary history given 374   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   91   by these alleles; such is the case of the populations of Military Macaw. While it is true that 375   sample size is an important factor in conservation studies, the small sample size in some 376   populations of Military Macaw is not cause to dismiss the results, because endangered species 377   typically have small population sizes (Moritz 1994a, 1994b; Solórzano et al. 2009). 378   The moderate genetic variation seen in Military Macaws does not appear to pose 379   problems for current conservation efforts; rather, the high degree of specialization in their diet 380   and nesting sites, and low reproductive rates, appear to be the strongest threats arising from 381   human factors (loss of habitat and illegal hunting) (Iñigo-Elias et al. 1999; Rivera-Ortiz et al. 382   2008; Contreras-González et al. 2009; Ríos-Muñoz and Navarro-Sigüenza 2009; Rivera-Ortiz 383   et al. 2013). 384   Our results on the genetic structure of Military Macaw populations has implications 385   for conservation, since most of the sites we studied represent breeding populations, and 386   therefore need effective protection actions at the regional level to preserve the habitat of the 387   Military Macaw, and with it the genetic diversity of this bird. The biological conservation 388   criteria within species are not entirely sufficient for the whole taxon (e.g. Moritz 1994a; 389   Young 2001). Therefore, we propose that these two groups (Gulf of Mexico and Pacific 390   slope) be considered a reference for conservation programs of the Military Macaw in Mexico, 391   including maintenance of the genetic connectivity among different groups with its effects on 392   sustaining gene flow, in order to preserve the genetic diversity of the Military Macaw. 393   In this respect, it has been suggested that the habitats of the Military Macaw continue 394   to be evaluated (Rivera-Ortiz et al. 2013), and that from these data a system of natural 395   corridors be created between remnant populations of the Military Macaw, then incorporated 396   into national systems of protected areas. These measures can help to ensure the maintenance 397   of the species populations in nature. 398   399   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   92   Acknowledgements 400   F. A. Rivera-Ortiz is grateful to the Consejo Nacional de Ciencia y Tecnología (CONACYT) 401   for a doctoral scholarship to conduct studies in the Posgrado en Ciencias Biológicas at the 402   Universidad Nacional Autónoma de México (UNAM). Financial support was provided by 403   CONACYT projects 60270 (S. Solórzano) and DT006 (M. C.Arizmendi); well as by UNAM 404   by project PAPIIT_UNAM IN207305 (K. Oyama). Logistical support was provided by 405   project SDEI-PTID-02-UNAM of P. Davila. We thank the various authorities for the facilities 406   provided for the completion of fieldwork. C. Brown and Dr. M. Healy provided assistance 407   with Academic English grammar and vocabulary. A. L. Albarran-Lara assisted with statistical 408   analyses. V. Rocha and D. L. Aquino provided technical assistance in the laboratory. Many 409   colleagues participated in field research and data collection, and the authors are particularly 410   grateful for the dedication shown by V. Garcia, A. M. Contreras-González, E. Berrones, H. 411   Verdugo and Y. Rubio. 412   413   References 414   Arizmendi MC, Márquez L (2000) Áreas de importancia para la conservación de las aves en 415   México. México, D.F. 416   Alcaide M, Serrano D, Negro JJ, Tella JT, Laaksonen T (2009) Population fragmentation 417   leads to isolation by distance but not genetic impoverishment in the philopatric Lesser 418   Kestrel: a comparison with the widespread and sympatric Eurasian Kestrel. Heredity 419   102:190-198. 420   Belkhir K, Borsa P, Chikhi L, Raufaste N (2004). GENETIX 4.05, Logiciel Sous Windows 421   TM Pour la Génétique des Populations. 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Genetic diversity estimated by locus over the eight population of Military Macaw. 594   The total number of alleles (NT), the number effective of alleles (NAE), observed (HO) and 595   expected (HE) heterozygosity, the inbreeding coefficient (FIS). 596   597   598   599   600   601   602   603   604   605   606   607   608   609   610   611   Locus Sequence (5’-3’) ºT Allelic size range Genetic Diversity NT NAE HO HE FIS UnaCT21! CTTTCCCATACTTAGCCATA 58 153-277 29 4 0.48 0.63 0.23* UnaCT32! TCTTGCTTATTCTTCCCCAG 56 248-268 27 4 0.78 0.72 -0.09* UnaCT43! TCATCCTATCACCAGAAGG 60 184-216 14 3 0.68 0.70 0.01* UnaCT74! CTGGACTGCTGCTCTTAAA 58 138-190 15 3 0.57 0.63 0.08* UnaGT55! TCTGCCCTCTGTCTTATGCC 58 181-257 13 4 0.76 0.75 -0.01* AgGT17º CCTGGATGTGCTCTGTGAG 60 134-242 21 3 0.81 0.65 -0.25* AgGT19+ CCTGCCTCCCAAAAGAACT 60 167-189 12 2 0.66 0.64 -0.03* AgGT32+ ACCCAGCTTCAGGTTTGTA 60 78-120 20 4 0.56 0.65 0.12* Overall 151 28 0.66 0.67 0.005 !Caparroz et al. 2003, ºRussello et al. 2001, +Russello et al. 2005 *HWD, Bonferroni correction P > 0.05 Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   101   Table 2. Estimates of genetic diversity patterns of the Military Macaw. 612   613   614   615   616   617   618   619   620   621   622   623   624   625   626   627   628   629   Populations N A PA HE HO FIS La Sierrita 5 18.05 4.65 0.60 ± 0.04 0.51 ± 0.12 0.33 Ntra. Sra. Mineral 23 18.67 6.37 0.72 ± 0. 03 0.59 ± 0.08 0.19* El Mirador del Águila 36 19.27 6.11 0.76 ± 0.02 0.58 ± 0.06 0.25* El Tuito 6 18.06 4.95 0.60 ± 0.05 0.66 ± 0.08 0.06 Sta. Ma. Tecomavaca 6 17.98 4.85 0.61 ± 0.05 0.61 ± 0.08 0.09 Sta. Ma. Cocos 5 17.55 8.51 0.54 ± 0.07 0.48 ± 0.13 0.31* El Cielo 5 16.10 5.70 0.54 ± 0.10 0.69 ± 0.14 -0.14 Overall 17.95 5.87 0.62 ± 0.08 0.58 ± 0.07 0.15 The average values are given ± s. e. as the case. N = Sample size, A = allelic richness, PA = private alleles, HE = expected heterozygosis, HO = observed heterozygosis, and FIS = index inbreeding. *HWD, Bonferroni correction P > 0.05 Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   102   630   Table 3. Paired genetic differentiation (FST) among the seven populations the Military Macaw. 631   632   633   634   635   636   637   638   639   640   641   642   643   644   645   646   647   Populations Ntra. Sra. Mineral El Mirador del Águila El Tuito Sta. Ma. Tecomavaca Sta. Ma. Cocos El Cielo La Sierrita 0.083* 0.025ns 0.180* 0.140* 0.142* 0.253* Ntra. Sra. Mineral 0.056ns 0.094* 0.075* 0.166* 0.167* El Mirador del Águila 0.093ns 0.046ns 0.120* 0.169* El Tuito 0.125* 0.177* 0.118* Sta. Ma. Tecomavaca 0.184* 0.206* Sta. Ma. Cocos 0.075ns *P < 0.05, ns = non significant P < 0.05 Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   103   Table 4. Analysis of Molecular Variance (AMOVA), comparing genetic distance between and 648   within of the populations the Military Macaw. 649   650   651   652   653   654   655   656   657   658   659   660   661   662   Source of variation d. f. Sum of squares Variance components Percentage of variation F-statistic Among populations 6 38.91 0.19 6.61 FST = 0.066* Within populations 165 443.79 2.68 93.39 Total 171 482.70 2.87 Among populations 6 144673.37 1142.36 46.10 RST=0.46* Within populations 165 220414.19 1335.84 53.90 Total 171 365087.56 2478.20 *P=0.0001 Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   104   Table 4. Levels of gene flow between the seven populations the Military Macaw. 663   664   665   666   667   668   669   670   671   672   673   674   675   676   677   678   679   Populations +La Sierrita +Ntra. Sra. Mineral +El Mirador del Águila +El Tuito +Sta. Ma. Tecomavaca +Sta. Ma. Cocos +El Cielo La Sierrita - 1.01 1.11 1.35* 0.85 1.17 0.85 Ntra. Sra. Mineral 1.12 - 1.39* 1.07 1.25* 1.07 1.02 El Mirador del Águila 0.96 1.18 - 0.79** 1.02 0.89 0.77 El Tuito 0.86 0.98 1.14 - 0.65** 0.88 0.74 Sta. Ma. Tecomavaca 1.36* 0.82 0.71 1.22* - 0.89 090 Sta. Ma. Cocos 1.08 0.45** 0.89 1.32* 0.99 - 1.05 El Cielo 0.77 0.58** 0.93 1.09 0.73 1.24* - +Receiving population, * Populations with greater gene flow, ** Populations with lower gene flow Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   105   Figure Legends 680   Figure 1. Location of populations of the Military Macaw. 1 = La Sierrita, Sonora, 2 681   = Nuestra Señora del Mineral, Sinaloa, 3 = El Mirador del Águila, Nayarit, 4 = El Tuito, 682   Jalisco, 5= Santa Maria Tecomavaca, Oaxaca, 6 = Santa Maria de Cocos, Queretaro, 7 = El 683   Cielo, Tamaulipas. The gray shading represents the potential historic distribution of the 684   Military Macaw, taken from Rivera-Ortiz et al. 2003. 685   Figure 2. Estimated genetic groups (K) from the clustering analysis of 686   STRUCTURE. Statistical plot of ΔK with regarding to the genetic clusters K (1 to 10 687   Figure 3. Graphic of the genetic structure of K = 2. A vertical line represents each 688   individual with colored segments in proportion to their membership of a genetic group. 689   Black lines separate the different populations. 1 = La Sierrita, 2 = Nuestra Señora del 690   Mineral, 3 = El Mirador del Águila, 4 = El Tuito, 5 = Santa Maria Tecomavaca, 6 = Santa 691   Maria de Cocos and 7 = El Cielo. 692   Figure 4. A) Distribution of the Military Macaw populations in Mexico, indicating 693   the barriers between populations. B) Frequency distribution of genotypes obtained by 694   Bayesian analysis in populations related with barriers. The Roman numerals indicate the 695   number of barriers. 1 = La Sierrita, 2 = Nuestra Señora del Mineral, 3 = El Mirador del 696   Águila, 4 = El Tuito, 5 = Santa Maria Tecomavaca, 6 = Santa Maria de Cocos and 7 =El 697   Cielo. 698   Figure 5. UPGMA tree obtained with genetic distances between pairs of 699   populations (FST). The ratio of admixture of the group of populations is represented by 700   genotypes green and red color obtained from the results of K = 2 of Bayesian analysis. 701   702   703   704   11 ano 1 cd dl 1 PeDO ES UA 25 ”0 '0 'N 30 %0 '0 "N 2 0 0 ' 0 " N Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   106   705   FIGURE 1. 706   707   708   709   710   711   712   713   714   715   716   717   718   719   720   721   722   723   724   725   726   727   728   729   A K OQ = H N UY de s i n Q AK = [m(¡L"K]ys(L(K))] Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   107   730   FIGURE 2. 731   732   733   734   735   736   737   738   739   740   741   742   743   744   745   746   747   748   749   750   751   752   753   754   1.00 0.80 0.60 0.40 0.20 0.00 Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   108   755   FIGURE 3. 756   757   758   759   760   761   762   763   764   765   766   767   768   769   770   771   772   773   774   775   776   777   778   779   A) B) -90 -100 -110 Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   109   780   FIGURE 4. 781   782   783   784   785   786   787   788   789   790   791   792   793   794   795   796   797   798   799   800   801   802   803   804   La Sierrita Ntra. Sra. Mineral El Mirador del Águila Sta. Ma. Tecomavaca El Tuito Sta. Ma. Cocos El Cielo Pacific slope slope of the Gulf of Mexico Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   110   FIGURE 5. 805   806   807   808   809   810   811   812   813   814   815   816   817   818   819   820   Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   111   8.0 Discusión general Cada uno de los tres capítulos de la tesis nos permitió contestar preguntas especificas a diferentes niveles (ecología y genética) y que refieren al campo de la biología de la conservación. Este campo ha contribuido con propuestas conceptuales y metodológicas para minimizar la pérdida de la diversidad biológica que nos permita conocer el estatus de conservación en cada especie (Simberlloff, 1988). En la biología de la conservación se reconoce a los procesos de fragmentación y de pérdida de hábitat como las principales amenazas que han causado un declive poblacional y ha colocado en riesgo de extinción a varios taxa (Brower et al., 1990; Solórzano, 2003). En el Capítulo I mostramos la idoneidad de los hábitats para la Guacamaya Verde y cómo se ha perdido dicho hábitat por la fragmentación y pérdida del hábitat. Las variables estructurales del hábitat de esta especie indicaron que el tipo de vegetación influye en la selección del hábitat. La Guacamaya Verde se considera una especie de dosel (Iñigo-Elías, 1996; Loza, 1997; Gómez, 2004), ya que requiere árboles de gran tamaño con un dosel grande en bosques tropicales caudifolios y subcaducifolios para alimentación, reproducción y nidificación, así como la protección contra los depredadores (Forshaw, 1989; Collar y Juniper, 1992; Collar, 1997; Loza, 1997; Iñigo-Elías, 1999; Salazar, 2001; Peterson et al., 2004; Rivera - Ortiz et al, 2008; Contreras -González et al., 2009). La idoneidad de los hábitats de esta especie requiere la presencia de especies de ciertos géneros de árboles, como Brosimum, Cyrtocarpa, Celtis, Hura, Quercus, Bunchonsia, Lysiloma y Bursera, las cuales son importantes tanto para anidar o como suministro de alimentos (Carreón, 1997; Loza, 1997; . Gaucín, 2000 y Contreras-González et al., 2009). En las poblaciones de Colombia y Perú también se Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   112   reportan especies de Hura y Bursera como árboles importantes para la alimentación (Flores y Sierra, 2004). Estas plantas tienen gran cantidad de nutrientes, tales como lípidos, carbohidratos y proteínas que son importantes para la puesta de huevos y el desarrollo de los pollos (Contreras-González et al., 2009). Estos resultados fueron respaldados al comparar la estructura de la vegetación y composición florística en sitios con y sin presencia de la Guacamaya Verde, donde se encontraron diferencias significativas en la composición florística pero similitudes estructurales. Las especies florales con las que se observa una gran relación son: Brosimum alicastrum, Bursera simaruba, Ceiba aescutifolia, Ceiba pentandra, Cyrtocarpa procera, Guaiacum coulteri, Guazuma ulmifolia, Hura polyandra, Haematoxylon brassileto, Ipomea arborences, Lysiloma divaricata, Lysiloma microphylla, Plumeria rubra and Taxodium mucronatum. Estos hallazgos indican que la dependencia de la Guacamaya Verde en la composición florística específica, patrones que se encuentran comúnmente en las especies de aves especialistas debido a la estrecha relación entre la disponibilidad de recursos alimenticios y la actividad reproductiva (Saunders, 1977; Saunders, 1990; Collar y Juniper, 1992). Ello tiene implicaciones importantes para la conservación de esta especie (Ruth et al., 2003). Al realizar los modelos de cambio de cobertura vegetal sobre los modelos de distribución potencial de la Guacamaya Verde se observó que la Guacamaya Verde y las 14 especies de plantas arbóreas asociadas se encuentran en áreas con características similares, por lo menos en un espacio ambiental ordinario; esto se ve reforzado por las alta superposición ambiental encontrados en el análisis discriminante. En el presente estudio identificamos una reducción del 32% de la distribución potencial de la Guacamaya Verde comparando cuatro escenarios de Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   113   cambio de uso del suelo desde 1976 al 2010. Estos cambios fueron especialmente dramáticos en zonas donde se presenta la Guacamaya Verde asociada a seis especies de plantas (Lysiloma microphylla, Lysiloma divaricata, Hura polyandra, Ceiba aescutifolia, Guaiacum coulteri, Ipomea arborences). Estos hallazgos indican los posibles efectos negativos sobre la supervivencia de la especie si se continúan produciendo reducciones de hábitat disponibles en el futuro (Peterson et al., 2006; Ríos-Muñoz y Navarro-Sigüenza, 2009; Contreras- Medina et al., 2010). Lo anterior concuerda con lo reportado en otros estudios, por ejemplo Ríos-Muñoz y Navarro-Sigüenza (2009) reportaron una reducción del 28,5 % en el hábitat disponible de la guacamaya verde en el año 2000. Marin-Togo et al. (2011) y Monterrubio-Rico et al. (2010) declararon localmente extinta a la Guacamaya Verde en la costa del Pacífico mexicano (Michoacán, Guerrero y Oaxaca ) y en las zonas costeras de más de 400 m de altitud, con una disminución del 16 % de la distribución hasta el año 2000. En este capitulo presentamos información sobre el tipo de vegetación y la composición de especies que es fundamental para la conservación de la Guacamaya Verde. Nuestros resultados sugieren la importancia de conocer la composición florística del hábitat de especies en peligro de extinción y el impacto del cambio de uso de suelo y su variación a través del tiempo para los esfuerzos de conservación directas. Vale la pena señalar que el uso de modelos de nicho ecológico y datos geográficos del cambio de uso del suelo son herramientas fundamentales a tener en cuenta en los esfuerzos de conservación de la esta especie. En este sentido observamos que la fragmentación y perdida del hábitat de especies vulnerables aparte de tener consecuencias ecológicas, podría tener Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   114   consecuencias directas sobre la variabilidad genética debido al aislamiento geográfico que se genera entre las poblaciones. La diversidad genética es crucial para determinar el potencial de las poblaciones de animales de adaptarse y evolucionar en entornos cambiantes. Por lo tanto, es importante evaluar los efectos de la fragmentación del hábitat sobre la diversidad genética con el fin de contribuir al desarrollo de herramientas y estrategias para la conservación de las poblaciones silvestres (Ouborg et al., 2006; Pertoldi et al., 2007), por lo que en el Capitulo II se realizó una revisión sobre el efecto de la fragmentación sobre la variabilidad genética (A = riqueza alélica, HE = heterocigosis esperada y FIS = índice de endogamia) en tetrápodos (anfibios, reptiles, aves y mamíferos). Encontramos que la fragmentación del hábitat reduce la diversidad genética global de las poblaciones de tetrápodos. Los cuatro grupos de tetrápodos mostraron efectos de la fragmentación negativos similares en la riqueza alélica (A). La disminución en A es probable que sea el resultado inmediato de la repentina reducción poblacional debido a la pérdida y fragmentación del hábitat, generando cuellos de botella genéticos. El impacto de los cuellos de botella en la variación genética depende principalmente de dos factores: el tamaño efectivo de la población y el tiempo durante el cual la población se mantiene pequeña. Una drástica reducción en el tamaño efectivo de las poblaciones causada por la fragmentación del hábitat reduce la variación genética de las poblaciones restantes y también afectará a la variación genética de las siguientes generaciones que permanecen en los fragmentos debido a la interrupción del flujo de genes (Hoelzel ,1999). También en esta tesis observamos efectos negativos de la fragmentación del hábitat sobre la heterocigosis esperada (HE) en tres grupos de tetrápodos (anfibios, Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   115   aves y mamíferos); esta reducción en poblaciones fragmentadas pueden ser el resultado de deriva genética. Cuando las poblaciones siguen siendo pequeñas y aisladas por generaciones, la reducción de la variabilidad genética se producen por la eliminación al azar de los genotipos heterocigóticos, afectando el número y las frecuencias de los alelos (Reed y Frankham, 2003; Caizergues et al., 2003). En contraste con los parámetros de diversidad genética, no observamos cambios significativos en el índice de consanguinidad (FIS) en hábitats fragmentados. La gran mayoría de los estudios que evalúan FIS son con individuos adultos, por lo tanto , la ausencia de cambios en el FIS está reflejando por los patrones de apareamiento de los individuos adultos de vida larga, que pueden preceder a los eventos de fragmentación. Sería muy interesante determinar FIS en la progenie generada en nuevos hábitats fragmentados y como las configuraciones nuevas de hábitats pueden ser la causa de los cambios en los patrones de apareamiento hacia una mayor endogamia biparental (Aguilar et al., 2008). En este capitulo también se mostró que la variabilidad genética de especies con un tamaño corporal grande dentro de cada grupo de tetrápodos fue más fuertemente afectado por la fragmentación del hábitat. El tamaño del cuerpo se relaciona positivamente con el rango de distribución, es decir las especies más grandes requieren más cantidad de hábitat para la alimentación y reproducción. Además, las especies de gran tamaño suelen ocurrir en bajas densidades. Los requerimientos espaciales más grandes, junto con bajas densidades poblacionales pueden hacer que las especies de gran tamaño sean especialmente susceptibles de sufrir erosión genética en hábitats fragmentados (Bergl et al., 2008). Otro hallazgo es que el tiempo transcurrido en condiciones de fragmentación es crucial para determinar la reducción de la diversidad genética en las poblaciones Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   116   de los tetrápodos. Se observaron efectos negativos más fuertes sobre la diversidad genética (HE) en los estudios realizados en los sistemas que han sido fragmentados por más de 100 años. Estos resultados están de acuerdo con las expectativas teóricas, que predice la erosión genética más fuerte en las poblaciones sometidas a períodos más largos de tiempo en condiciones fragmentadas y aisladas. La deriva genética tendrá efectos más fuertes a medida que más generaciones pasan por tales condiciones, la fijación de alelos homocigotos a través de generaciones y la disminución de la variabilidad genética general (Lande, 1993; Foose, 1993; Mech y Hallett, 2001). A pesar de estas señales de los efectos de la fragmentación sobre la variabilidad genética, hay una clara diferencia en la literatura de la genética de poblaciones de tetrápodos que evita generalizaciones adicionales. La mayoría de los datos provienen de adultos, y su composición genética puede diferir de la de su progenie que se han sometido a las condiciones de fragmentación. Tal es el caso de los pocos estudios que examinaron el efecto de la fragmentación sobre las especies vágiles y los estudios escasos que examinaron la progenie establecida en hábitats fragmentados (Aguilar et al., 2008). Por lo tanto, hacemos un llamado a un incremento de los estudios que evalúan los efectos genéticos sobre la progenie de tetrápodos, lo que nos permitirá estimar el apareamiento y los patrones de flujo de genes en condiciones fragmentadas y evaluar cómo los cambios en los patrones de apareamiento pueden afectar la diversidad genética de las generaciones futuras de las poblaciones de tetrápodos. En el Capítulo III unimos los dos primeros capítulos para determinar si la diversidad y estructura genética de las poblaciones de la Guacamaya Verde en México son afectadas por la fragmentación y pérdida del hábitat. Uno de los Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   117   resultados es que no se encontró un patrón de diferenciación genética de las poblaciones de la Guacamaya Verde por la fragmentación y pérdida de hábitat, sin embargó se mostró diferenciación genética encontrada entre las poblaciones de la vertiente del Golfo de México y la del Pacífico asociada a las regiones biogeográficas (Figura 5). Se observó una fuerte separación de la vertiente del Pacífico respecto al Golfo de México, barrera que coincidió con el Altiplano mexicano, más específica,mente a la Meseta de Anáhuac, que tiene mayor a 2900 msnm y se extiende al sur colindando con el Eje Neo-Volcánico (Flores, 2005). Otra división que se observó es la que separa a las poblaciones en el Golfo de México con las poblaciones más meridionales de la vertiente del Pacífico (Santa María Tecomavaca), esta barrera coincide con el Eje Neo-Volcánico que alcanza alturas de más de 4000 msnm (Flores, 2005) . Estas barreras probablemente actúan como barreras físicas para el movimiento y la dispersión de la Guacamaya Verde. A diferencia de las poblaciones de la vertiente del Pacífico, que forma un grupo, en este caso la distribución de los bosques tropicales caducifolios y subcaducifolios podrían ser un corredor natural entre las poblaciones de la Guacamaya Verde. Este modelo de estructura de la población es muy similar a los patrones biogeográficos encontrados en otras especies de aves mexicanas con marcadores de ADN mitocondrial, como es el caso del búho pigmeo (Glaucidium brasilianum) (Proudfoot et al., 2006) y del pavo silvestre (Melagris gallopavo) (Mock et al., 2002), donde las diferencias genéticas se deben a la presencia de barreras geográficas como la Sierra Madre Oriental, la Sierra Madre Occidental y el Altiplano Mexicano ( Mock et al., 2002 , Proudfoot et al., 2006). Los dos grupos genéticos detectados en este estudio tienen una concordancia geográfica (véase la Figura 4), lo que indica que se podría considerar Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   118   como unidades prioritarias para la conservación, más específicamente como unidades de manejo (MU´s). Sin embargo, el tamaño pequeño de la muestra en algunas poblaciones debe tomarse en cuenta, ya que el tamaño de la muestra es un factor clave en la estudios de conservación, aunque las especies en peligro de extinción tienen pequeños tamaños poblacionales (Moritz, 19941, 19942; Solórzano et al., 2009). Por otra parte, los niveles de heterocigosis de la Guacamaya Verde (SE = 0.63) son relativamente moderados en comparación con otros estudios de guacamayos (e. g. Nader et al., 1999; Caparroz et al., 2003; Faria et al., 2008; Presti et al., 2011; Presti et al., 2013). Aunque la Guacamaya Verde es una especie vulnerable en todo el mundo y se considera en peligro de extinción por las Normas Mexicanas aun mantiene niveles moderados de diversidad genética a pesar de intensas presiones antropogénicas sobre los recursos naturales y la caza ilegal (Iñigo-Elías, 1999; Rivera-Ortiz et al., 2008). La variación genética moderada no parece plantear problemas actuales para la conservación de la Guacamaya Verde, por otra parte el alto grado de especialización en su dieta, en los sitios de anidación y tasas de reproducción bajas, parecen ser las amenazas más fuertes relacionados con los factores humanos (pérdida de hábitat y la caza ilegal) (Iñigo -Elías et al., 1999; Rivera-Ortiz et al., 2008, Contreras-González et al., 2009, Ríos- Muñoz y Navarro-Sigüenza, 2009; Rivera- Ortíz et al., en prensa). Los resultados sobre la estructura genética de las poblaciones de esta especie tiene implicaciones para la conservación ya que la mayoría de los sitios presentan poblaciones reproductoras, por lo tanto necesitan una protección eficaz en las regiones que habita, con el fin de preservar los niveles de diversidad genética a lo largo de su distribución. Los criterios biológicos de conservación dentro de las especies no son del todo satisfactorios para todos los Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   119   taxones (e.g. Moritz, 19941; Young, 2001). En este sentido, proponemos que estos dos grupos deben ser considerados como Mu´s y una referencia para los programas de conservación de la Guacamaya Verde en México, por lo tanto, los programas de conservación deben incluir el mantenimiento de la conectividad entre las diferentes poblaciones con la capacidad de mantener el flujo de genes, con el fin de preservar la diversidad genética de la Guacamaya Verde (Solórzano et al., 2009). Estas medidas pueden ayudar a garantizar el mantenimiento de las poblaciones de la especie en la naturaleza. Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   120   8.1 Recomendaciones de conservación para la Guacamaya Verde 1.- Protección de los hábitats adecuados y la realización de actividades sostenibles para la conservación de la Guacamaya Verde. 2.- Sugerimos que al menos el 30% de los bosques de la distribución potencial de la Guacamaya Verde debe ser protegido para garantizar áreas específicas de anidación y alimentación, por lo tanto se debe aumentar el tamaño y el número de áreas naturales protegidas en México. 3.- La estructura genética encontrada en las poblaciones de la Guacamaya Verde nos demuestra dos grupos (vertiente del Pacífico y vertiente del Golfo de México) que pueden ser considerados como unidades prioritarias para la conservación independientes por lo que se sugiere programas nacionales de protección y monitoreo específicos para cada grupo. 5.- Dentro de cada vertiente no se observo una diferenciación entre sus poblaciones lo que sugiere que las poblaciones de cada una de las vertientes existe flujo génico reciente, por lo que se recomienda proteger los bosques tropicales caducifolios y subcaducifolios para garantizar el flujo génico entre poblaciones. 6.- Se sugiere realizar el estudio de los patrones filogeográficos de las poblaciones de las Guacamaya Verde con el fin de localizar y enfatizar las unidades prioritarias de conservación. 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Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   135   10.0 APÉNDICES 10.1 Apéndice 1. Floristic composition and importance value (IVI), of the eight sites studied (A = La Sierrita, B = Nuestra Señora del Mineral, C = Mirador del Águila, D= El Tuito, E = Papalutla, F = Santa María Tecomavaca, G = El Cielo and H = Santa María Tecomavaca). Family Plants species Localites A B C D E F G H Anacardiaceae Rhus pachyrrhachis - - - - - - - 0.155 Mangifera indica - - - - - - 0.226 - Cyrtocarpa procera - - - - 0.228 0.407 - - Spondias purpurea - - - 0.133 0.028 - - - Spondias mombin - - - - 0.037 - - - Pseudosmodingium perniciosum - - - - 0.142 - - - Annonaceae Annona cherimola - 0.037 - 0.215 - - - - Annona globiflora - 0.005 - - - - - 0.021 Annona longiflora - - 0.009 - - - - - Apocynaceae Rauvolfia nitida 0.028 - - - - - - - Vallesia laciniata 0.165 - - - - - - - Stemmadenia palmeri - 0.176 - - - - - - Plumeria acutifolia - - - - - - 0.023 - Plumeria rubra - - - - 0.021 0.123 - - Araliaceae Dendropanax arboreus - - - - - - 0.011 - Callistephus chinensis - - - - - - 0.006 - Montanoa xanthifolia - - - - - - - 0.068 Pseudosmodingium multifolium - - - - - 0.014 - - Begoniaceae Begonia angustifolia - 0.006 - - - - - - Begonia monophylla - - - - 0.016 - - - Begonia palmeri - - - - 0.039 - - - Bixaceae Cochlospermum vitifolium - 0.007 - - - - - - Bombacaceae Ceiba acuminata 0.066 0.05 - - 0.106 - - - Ceiba parviflora - - - - - - - - Pseudobombax ellipticum - - - - 0.039 - - - Ceiba pentandra 0.483 - - 0.018 - 0.054 - - Ceiba aesculifolia - - - - - 0.286 - - Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   136   Ceiba grandiflora - - - 0.013 - - - - Croton sp. - - - 0.018 - - - - Boraginaceae Cordia parviflora 0.011 - - - - - - Tabebuia palmeri 0.251 0.053 0.062 0.095 - - - - Tabebuia rosea - - - 0.09 - - 0.012 - Tabebuia chrysantha - 0.083 0.004 0.102 - - - - Cordia alliodora - 0.057 - - - - - - Cordia sonorae - 0.005 - - - - - - Cordia morelosana - - - - 0.023 - - - Cordia boissieri - - - - - - - 0.051 Buddlejaceae Buddleja scordioides - - - - - - - 0.008 Burseraceae Bursea aloxylon - - - - 0.053 0.089 - - Bursera aptera - - - - - 0.18 - - Bursera arborea - - - 0.082 - - - - Bursera ariensis - - - - 0.12 - - - Bursera bicolor - - - - 0.039 - - - Bursera excelsa - 0.171 0.079 - - - - - Bursera grandifolia 0.011 - - - - - - - Bursera innopinata 0.068 0.016 - - - - - - Bursera laxiflora 0.008 - - - 0.014 - - - Bursera microphylla 0.265 0.008 - 0.006 - - - - Bursera morelensis - - - - 0.014 0.145 - - Bursera multifolia - - - - 0.015 - - - Bursera schlechtendali - - - - - 0.152 - - Bursera simaruba - 0.091 - 0.078 - - 0.261 0.219 Bursera xochipalensis - - - - 0.036 - - - Cactaceae Pachycereus pectenaboriginum 0.008 - - - - - - - Myrtillocactus geometrizans - - - - - 0.009 - - Neobuxbaumia tetezo - - - - - 0.016 - - Opuntia depressa - - - - - 0.029 - - Paquicerius hollianus - - - - - 0.019 - - Cappareaceae Capparis sp - 0.036 - - - - - - Capparis angustifolia - - - - 0.048 - - - Capparis incana - - - - - 0.094 - 0.146 Celastraceae Wimmeria concolor - - - - - - 0.087 - Clusiaceae Calophyllum brasiliense - - 0.097 - - - - - Compositaceae Senecio praecox - - - - 0.017 - - - Convolvulaceae Ipomea arborescens 0.122 0.158 - 0.091 0.065 0.089 - - Ipomea conzantii - - - - - 0.008 - - Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   137   Ipomea sp. - - - 0.013 - - - - Ipomea carnea - - - - 0.023 - - - Cuscuta sp. - - - - 0.03 - - - Euphorbiaceae Celaenodendron mexicanum - - - 0.009 - - - - Cnidoscolus multilobus - - - - - - 0.007 - Croton adspersus - - - - - - 0.009 - Croton flavescens - - - - 0.018 - - - Croton fragilis - 0.05 - - - - - - Croton niveus - - - - - - 0.098 - Croton sp. - 0.059 - - - - - - Croton sp. - - - - - - - 0.008 Croton sp. - - - 0.006 - - - - Euforbia pringlei - - - - - 0.028 - - Euforbia schlechtendali - - - - - 0.091 - - Euphorbia antisyphilitica - - - - - 0.038 - - Euphorbia colorata - - - - 0.013 - - - Euphorbia francoana - - - - 0.06 - - - Euphorbia graminea - - - 0.013 - - - - Euphorbia misera 0.116 - - - - - - - Euphorbia rossiana - - - - 0.018 - - - Hevea brasiliensis - - - 0.019 - - - - Hura polyandra - 0.106 0.573 0.357 - - - - Jatrofa elbae - - - - 0.026 - - - Jatropha cunneata 0.184 - - - - - - - Jatropha dioica - 0.015 - - - - - - Jatropha neopaucifolia - - - - - 0.126 - - Jatropha rzedowskii - - - - - 0.01 - - Jatropha sp. - - 0.015 - - - - Sapium pedicellatum - - 0.017 - - - - - Sebastiana bilocularis 0.122 - - - - - - - Sebastiana pavoniana - - - - - 0.056 - - Fabaceae Haematoxylon brassileto 0.021 0.223 - - - - - - Senna wislizeni - - - - - - 0.028 Senna obtusifolia - - - - - 0.191 - - Quercus tuitensis - - - 0.315 - - - - Quercus sp - - - 0.102 - - - - Quercus conspersa - - - - 0.012 - - - Quercus castanea - - - - 0.074 - - - Quercus sacame - - - - - - - 0.008 Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   138   Pithecellobium dulce - - - 0.035 - - - - Parkinsonia preacox - - - - - 0.28 - - Mimosa priga - - 0.004 - - - - - Mimosa laxiflora - - 0.002 - - - - - Erythrina herbacea - - - - - - 0.028 Desmodium asperum - 0.005 - - - - - - Conzattia sericea - 0.027 - - - - - - Caesalpinia cacalaco - - - 0.007 - - - - Flacourtiaceae Casearia dolichopylla - - 0.023 - - - - - Fouquieriaceae Foquieria leonilae - - - - 0.039 - - - Fouquieria formosa 0.048 - - - - 0.035 - - Hidrophylaceae Nama demiscum - - - - - - - - Wigondia urens - - - 0.005 - - - - Julianaceae Amphiterygium adstringens - - - 0.009 0.027 0.011 - - Lamiaceae Mentha piperita - - - 0.01 - - - - Lauraceae Nectandra sanguinea - - - - - - 0.03 - Nectandra salicifolia - - 0.009 - - - - - Malpighiaceae Bunchonsia sp. - - - 0.127 - - - - Bunchonsia canences - - - - 0.094 - - - Lasiocarpus salicifolius - - - - 0.054 - 0.026 - Malvaceae Malviscus arboreus - 0.007 - - - - - - Gaudichaudia mucronata - - - - - - - 0.007 Meliaceae Melia azadarach 0.047 - - - - - - Cedrela mexicana - - 0.016 - - - 0.017 - Cedrela occidentalis - - 0.012 - - - - - Cedrela odorata - - - - - - 0.292 - Swietenia humilis - 0.018 - - - - - - Swietenia macrophyla - - 0.029 0.025 - - - - Trichilia havanensis - - - - - - 0.006 - Mimosaceae Platymiscium lasiocarpum - - 0.034 - - - - - Pithecellobium mangense - 0.022 - - - - - - Pitecellubium dulce - 0.041 - - - - - - Pitecellobium mexicanun - - 0.031 - - - - - Piscidia piscipula - - - - - - 0.01 - Piscidia mollis - - - 0.011 - - - - Olneya tesota 0.047 - - - - - - - Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   139   Mimosa polyantha - - - - 0.15 - - - Mimosa mollis - - - - 0.127 - - - Mimosa luisiana - - - - - 0.183 - - Lysiloma watsoni 0.056 - - - - - - - Lysiloma tergemina - - - - 0.027 - - - Lysiloma microphylla - - - 0.008 - - - 0.123 Lysiloma divaricata 0.278 0.433 0.068 0.009 0.083 0.009 0.02 - Lysiloma acapulquensis - - - 0.008 0.02 - 0.016 - Leucaena leucocephala - - - - 0.048 - - - Esenbeckia marginata - - - - - - 0.009 - Erythrina occidentalis - 0.011 - - - - - - Enterolobium cyclocarpum - - 0.074 - - - 0.066 - Conzattia multiflora - - - - 0.012 - - - Chamaecrista flexuosa - - - - 0.044 - - - Cercidium preacox - - - - 0.032 - - - Cassia emarginata - - - 0.038 - - - - Calliandra grandiflora - - - - 0.036 - - - Caesalpinia platyloba 0.02 - - 0.056 - - - - Caesalpina emarginata 0.031 - - - - - - - Caesalpina celadenia 0.01 - - - - - - - Caesalpina pumila 0.092 - - - - - - - Acacia pennatula - 0.023 - - 0.026 - - 0.063 Acacia oligoacantha 0.008 - - - - - - - Acacia micrantha - - - - - - - 0.149 Acacia cymbispina 0.017 - 0.015 - - - - - Acacia coulteri - 0.019 - - - - - - Acacia cornigera - 0.033 0.004 0.008 - - - - Acacia cochiliacantha - 0.066 - - - 0.016 - - Acacia angustissima - - - - - - 0.008 - Acacia acatlensis - - - - 0.017 - - - Moraceae Ficus goldmanii 0.181 - - - - - - - Brosimum alicastrum 0.009 0.248 1.209 0.108 - - 0.609 - Chlorophora tinctoria - 0.018 - - - - - - Ficus benjamina - - - - 0.03 - - - Ficus cotinifolia - - - - - - 0.303 - Ficus mexicana - 0.031 - - - - - - Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   140   Ficus microchlamys - - - 0.018 - - - - Ficus sp - - 0.055 - - - - - Ficus sp - - - 0.061 - - 0.012 - Myrtaceae Eugenia capuli - - - - - - - - Nyctaginaceae Pisonia aculeata - - 0.004 - - - - - Oxalidaceae Oxalis angustifolia - - - - 0.07 - - - Oxalis latifolia - - - - 0.035 - - - Piperaceae Pipper arboreum - - - 0.005 - - - - Pipper rosei - - - 0.005 - - - - Poaceae Guadua amplexifolia - - - 0.018 - - - - Rhamnaceae Karwinskia humboldtiana 0.048 - - - - - - Zizyphus amole - 0.039 - 0.005 - 0.018 - 0.011 Karwiskia parafolia - 0.01 - - - - - - Ziziphus mexicana - - 0.019 - - - - - Rosaceas Licanea arborea - - 0.014 - - - - - Rubiaceae Randia echinocarpa 0.156 - 0.077 0.1 0.084 - - - Borreria verticillata - - - - 0.056 - - - Coutarea pterosperma - - 0.005 - - - - - Diodia teres - - 0.063 - - - - - Krugiodendron ferrum - - - - - - 0.193 0.009 Randia aculeata - - - - - - 0.007 - Ruscaceae Dracaena marginata - - - - - - 0.031 - Rutaceae Casimiroa pringlei - - - - - - 0.022 - Esenbeckia berlandieri - - - - - - 0.155 0.082 Zanthoxylum pringlei - - - - - - 0.107 - Zanythoxylum arborescens - - 0.003 - - - - - Salicaceae Salix bonplandiana - - 0.156 - - - - - Sapindaceae Sapindus lateriflorum - 0.039 - - - - - - Thouinidium decamdrum - 0.201 - - - - - - Sapindus saponaria - - - - - - 0.025 - Thouinidium decamdrum - - - 0.027 - - - - Sapotaceae Sideroxylon capiri 0.031 - - - - - - - Simaroubaceae Castela erecta - - - - - 0.038 - - Smilacaceae Smilax aspera 0.008 - - - - - - - Solanaceae Solanum americanum - - 0.002 - - - - - Solanum rostratum - - - - - 0.02 - - Solanum sp. - - - 0.01 - - - - Solanum - - - 0.005 - - - - Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   141   americanum Capsicum annum - - - 0.007 - - - - Sterculiacea Guazuma ulmifolia 0.013 0.038 0.064 0.067 - - 0.133 0.279 Melochia nodiflora - - - 0.02 - - - - Taxodiaceae Taxodium mucronatum - - 0.111 0.123 - - - - Theophrastaceae Jacquinia pungens 0.048 - - 0.025 - - - - Tiliaceae Luehea candida 0.096 0.036 0.029 - - - - - Turneraceae Turnera ulmifolia - - - - 0.029 0.052 - - Ulmaceae Celtis pallida 0.171 - - - - - - Celtis caudata - - - 0.005 0.183 - - 0.014 Celtis iguanaea - - - - 0.052 - - - Mirandaceltis monoica - - - - - - 0.179 - Urticaceae Parietaria debilis - 0.007 - - - - - - Urera baccifera - 0.016 0.015 - - - 0.007 - Urera coracasona - - - - - - - Verbenaceae Lantana camara - - - 0.007 - - - - Lippia pringlei 0.062 - - - - - - - Vitex mollis - - 0.027 - - - - - Verbena sp. - 0.089 - - - - - - Verbena sp. - - - 0.012 - - - - lippia graveolens - - - - - 0.017 - - Vitaceae Cissus sp. - - - 0.007 - - - - Zygophyllacae Guaiacum coulteri 0.241 0.008 - - - - - - Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   142   10.2 Apéndice 2. List of publications used for the realization of the meta-analysis. Publication Class Gender Species Kraaijeveld-Smit et al., 2005 Amphibians Alytes Alytes muletensis Spear & Storfer, 2010 Amphibians Ascaphus Ascaphus montanus Wahbe et al., 2005 Amphibians Ascaphus Ascaphus truei Hitchings & Beebee, 1998 Amphibians Bufo Bufo bufo Dubey et al., 2008 Amphibians Hyla Hyla arborea Luquet et al., 2011 Amphibians Hyla Hyla arborea Gibbs, 1998 Amphibians Plethodon Plethodon cinereus Jordan et al., 2009 Amphibians Plethodon Plethodon cinereus Noe ̈l et al., 2007 Amphibians Plethodon Plethodon cinereus Noël et al., 2010 Amphibians Plethodon Plethodon cinereus Arens et al., 2007 Amphibians Rana Rana arvalis Lesbarréres et al., 2006 Amphibians Rana Rana dalmatina Wilson et al., 2008 Amphibians Rana Rana pipiens Hitchings et al., 1997 Amphibians Rana Rana temporaria Johansson et al., 2005 Amphibians Rana Rana temporaria Measey et al., 2007 Amphibians Schoutedenella Schoutedenella xenodactyloides Björklund et al., 2010 Birds Parus Parus major Leite et al., 2008 Birds Amazona Amazona aestiva Albertani et al., 2000 Birds Amazona Amazona Ochrocephala Bush et al., 2011 Birds Centrocercus Centrocercus urophasianus Delaney et al., 2010 Birds Chamaea Chamaea fasciata Mercival et al., 2007 Birds Chiroxiphia Chiroxiphia caudata Croteau et al., 2007 Birds Chiroxiphia Chiroxiphia caudata Barnett et al., 2008 Birds Corapipo Corapipo altera/Manacus candei Lindsay et al., 2008 Birds Dendroica Dendroica chrysoparia Meyer et al., 2009 Birds Emberiza Emberiza schoeniclus Brown et al., 2004 Birds Eucometis Eucometis penicillata Bates, 2000 Birds Glyphorynchus Glyphorynchus spirurus Brown et al., 2004 Birds Gymnopithys Gymnopithys leucaspis Brown et al., 2004 Birds Henicorhina Henicorhina leucosticta Bates, 2000 Birds Hylophylax Hylophylax poecilonota Bates, 2000 Birds Hypocnemis Hypocnemis cantator Bech et al., 2009 Birds Lagopus Lagopus muta pyrenaica Bates, 2000 Birds Leptopogon Leptopogon amaurocephalus Leberg, 1991 Birds Meleagris Meleagris gallopavo MacDougall-Shackleton et al., 2011 Birds Melospiza Melospiza melodia Roques & Negro 2005 Birds Milvus Milvus milvus Bates, 2000 Birds Myrmeciza Myrmeciza hemimelaena Zhan et al., 2007 Birds Nipponia Nipponia nippon Miño & Lama, 2007 Birds Platalea Platalea ajaja Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   143   Galbusera et al., 2004 Birds Pogonocichla Pogonocichla stellata Triggs et al., 1989 Birds Strigops Strigops habroptilus Ping-Ping et al., 2004 Birds Syrmaticus Syrmaticus ellioti Caizergues et al., 2003 Birds Tetrao Tetrao tetrix Höglund et al., 2007 Birds Tetrao Tetrao tetrix Segelbacher et al., 2003 Birds Tetrao Tetrao urogallus Bellinger et al., 2003 Birds Tympanuchus Tympanuchus cupido Bouzat et al., 1998 Birds Tympanuchus Tympanuchus cupido Lucid & Cook, 2004 Mammals Peromyscus Peromyscus keeni He et al., 2007 Mammals Ailuropoda Ailuropoda melanoleuca García del Valle et al., 2005 Mammals Alouatta Alouatta pigra Lada et al., 2008 Mammals Antechinus Antechinus flavipes Telfer et al., 2003 Mammals Arvicola Arvicola terrestris Pacioni et al., 2011 Mammals Bettongia Bettongia penicillata ogilbyi Estes-Zumpf et al., 2010 Mammals Brachylagus Brachylagus idahoensis Meyer et al., 2009 Mammals Carillia Carollia perspicillata Tallmon et al., 2002 Mammals Clethrionomys Clethrionomys californicus Redeker et al., 2005 Mammals Cletherionomys Clethrionomys glareolus Banassezek et al., 2010 Mammals Cricetus Cricetus cricetus Magle et al., 2010 Mammals Cynomys Cynomys ludovicianus Aranguren-Méndez et al., 2001 Mammals Equus Equus asinus Bergl et al., 2008 Mammals Gorilla Gorilla gorilla Small et al., 2003 Mammals Martes Martes americana Olivieri et al., 2008 Mammals Microcebus Microcebus bongolBirdsnsis Olivieri et al., 2008 Mammals Microcebus Microcebus danfossi Olivieri et al., 2008 Mammals Microcebus Microcebus ravelobensis Campbell et al., 2009 Mammals Myotis Myotis macropus Haag et al., 2010 Mammals Panthera Panthera onca Taylor et al., 2007 Mammals Petauroides Petauroides volans/Pseudocheirus peregrinus Banks et al., 2005 Mammals Antechinus Antechinus agilis Goossens et al., 2005 Mammals Pongo Pongo pygmaeus Macqueen et al., 2008 Mammals Rattus Rattus fuscipes White & Searle, 2007 Mammals Sorex Sorex araneus Biedrzychka & Konopinski, 2008 Mammals Spermophilus Spermophilus suslicus Heller et al., 2010 Mammals Syncerus Syncerus caffer Meyer et al., 2009 Mammals Uroderma Uroderma bilobatum Proctor et al., 2005 Mammals Ursus Ursus arctos Ohnishi et al., 2007 Mammals Ursus Ursus thibetanus Rodriguez-Robles et al., 2008 Reptiles Anolis Anolis cooki Dutra et al., 2008 Reptiles Bothrops Bothrops moojeni Tzika et al., 2008 Reptiles Conolophus Conolophus pallidus Tzika et al., 2008 Reptiles Conolophus Conolophus subscrita Stow et al., 2001 Reptiles Egernia Egernia cunninghami Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   144   HOEHN et al., 2007 Reptiles Gehyra Gehyra variegata Cunningham & Moritz, 1998 Reptiles Gnypetoscincus Gnypetoscincus queenslandiae SUMNER et al., 2001 Reptiles Gnypetoscincus Gnypetoscincus queenslandiae Ennen et al., 2010 Reptiles Gopherus Gopherus Polyphemus Bennett et al., 2010 Reptiles Graptemys Graptemys geographica Marshall Jr et al., 2009 Reptiles Nerodia Nerodia erythrogaster Hoehn et al., 2007 Reptiles Oedura Oedura reticulata Berry et al., 2004 Reptiles Oligosoma Oligosoma grande Berry & Gleeson, 2005 Reptiles Oligosoma Oligosoma grande Delaney et al., 2010 Reptiles Plestiodon Plestiodon skiltonianus Cunningham et al., 2002 Reptiles Psammobates Psammobates geometricus Delaney et al., 2010 Reptiles Sceloporus Sceloporus occidentalis Moore et al., 2008 Reptiles Sphenodon Sphenodon punctatus Chih-Horng & Janzen, 2004 Reptiles Terrapene Terrapene ornata Munguia-Vega et al., 2009. Reptiles Urosaurus Urosaurus nigricaudus Delaney et al., 2010 Reptiles Uta Uta stansburiana Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   145   Apendice 3. Phylogenetic tree the tetrapods used to performing correction in phylogenetic in phyloMeta, in format Newik and image. (((((((Schoutedenella_xenodactyloides:4.0,Hyla_arborea:4.0):1.0,Bufo_bufo:5.0):1.0,( Ascaphus_truei:1.0,Ascaphus_montanus:1.0):5.0):1.0,(Rana_arvalis:1.0,Rana_dalm atina:1.0,Rana_pipiens:1.0,Rana_temporaria:1.0):6.0):3.0,Alytes_muletensis:10.0):1. 0,(Plethodon_cinereusa:9.0,Plethodon_cinereusb:9.0,Plethodon_cinereusc:9.0,Pleth odon_cinereusd:9.0):2.0):10.0,((((((((Platalea_ajaja:2.0,Nipponia_nippon:2.0):1.0,Milv us_milvus:3.0):12.0,(((Amazona_aestiva:1.0,Amazona_ochrocephala:1.0):4.0,(Hylop hylax_poecilonota:3.0,((Gymnopithus_leucaspis:1.0,Hypocnemis_cantator:1.0):1.0,M yrmecima_hemimelaena:2.0):1.0):2.0):8.0,(Strigops_habroptilus:12.0,((Leptopogon_ amauroce:2.0,Pogonocichla_stellata:2.0,Glyphorynchus_spirurus:2.0):9.0,(((Eucomet is_penicilata:4.0,(Henicornia_leucosticta:2.0,(Chiroxiphia_caudata.1:1.0,Chiroxiphia_ caudata.2:1.0):1.0,Dendroica_chrysoparia:2.0,Corapipo_altera:2.0):2.0,(Emberiza_sc hoeniclus:1.0,Melospiza_melodia:1.0):3.0):3.0,Chamaea_fasciata:7.0):1.0,Parus_maj or:8.0):3.0):1.0):1.0):2.0):1.0,(((Tetrao_urogallus:2.0,(Tetrao_tetrix.1:1.0,Tetrao_tetrix .2:1.0):1.0):1.0,Centrocercus_urophasianus:3.0,Syrmaticus_ellioti:3.0):2.0,(((Tympan uchus_cupido.1:1.0,Tympanuchus_cupido.2:1.0):2.0,Lagopus_muta:3.0):1.0,Meleagr is_gallopavo:4.0):1.0):11.0):1.0,Bothrops_moojeni:17.0):1.0,(Psammobates_geometr icus:4.0,(Terrapene_ornata:1.0,Gopherus_polyphemus:1.0):3.0,Graptemys_geograp hica:4.0):14.0):1.0,(Nerodia_erythrogaster:9.0,((((Sceloporus_occidentalis:1.0,Urosa urus_nigricaudus:1.0):1.0,Uta_stansburiana:2.0):1.0,Anolis_cooki:3.0):2.0,(((Spheno don_punctatus:2.0,(Oligosoma_grande.1:1.0,Oligosoma_grande.2:1.0,Egernia_cunni nghami:1.0):1.0,(Gnypetoscincus_queenslandiae:1.0,Plestiodon_skiltonianus:1.0):1. 0):1.0,(Gehyra_variegata:1.0,Oedura_reticulata:1.0):2.0):1.0,(Conolophus_pallidus:1. 0,Conolophus_subscrita:1.0):3.0):1.0):4.0):10.0):1.0,(((((Gorilla_gorilla:3.0,Pongo_py gmaeus_abelii:3.0):3.0,Alouatta_pigra:6.0):1.0,(Microcebus_bongolavensis:1.0,Micro cebus_danfossi:1.0):6.0):2.0,((Bettongia_penicillata:1.0,Antechinus_flavipes.1:1.0,An techinus_flavipes.2:1.0):7.0,(((((Cletherionomys_glareolus:1.0,Cletherionomys_califo rnicus:1.0):1.0,Peromyscus_keeni:2.0,(Petauroides_volans:1.0,Cricetus_cricetus:1.0) :1.0,Arvicola_terrestris:2.0):1.0,Rattus_fuscipes:3.0):3.0,Cynomys_ludovicianus:6.0): 1.0,Brachylagus_idahoensi:7.0,(Spermophilus_suslicus.1:1.0,Spermophilus_suslicus .2:1.0):6.0):1.0):1.0):7.0,((((Equus_asinus:10.0,(Panthera_onca:8.0,((Ailuropoda_mel Genética de la conservación, pérdida y caracterización del hábitat de la Guacamaya Verde en México Francisco Alberto Rivera-Ortíz   146   anoleuca:2.0,(Ursus_thibetanus:1.0,Ursus_arctos:1.0):1.0):4.0,Martes_americana:6. 0):2.0):2.0):1.0,Syncerus_caffer:11.0):1.0,((Carollia_perspicillata:2.0,Uroderma_bilob atum:2.0):4.0,Myotis_macropus:6.0):6.0):1.0,Sorex_araneus:13.0):3.0):4.0):1.0);