A COMPREHENSIVE ANALYSIS OF REPTILE DIVERSITY IN MADIDI NATIONAL PARK AND NATURAL INTEGRATED MANAGEMENT AREA, ONE OF THE WORLD’S MOST BIOLOGICALLY DIVERSE PROTECTED AREAS

James Aparicio; Mauricio Ocampo; Nuria Bernal-Hoverud; Enrique Domic; Robert B. Wallace

doi:10.22201/fc.25942158e.2025.2.1115

Authors

James Aparicio
Mauricio Ocampo Red de Investigadores en Herpetología - Bolivia
Nuria Bernal-Hoverud
Enrique Domic
Robert B. Wallace

DOI:

https://doi.org/10.22201/fc.25942158e.2025.2.1115

Keywords:

Amazonian reptiles, dark diversity, ecoregions, herpetofauna, species turnover

Abstract

The Amazon is the world's largest tropical rainforest, hosting a myriad of plants, fungi and animals, and encompassing a wide diversity of ecoregions. Bolivia has allocated 17 % of its territory to national protected areas, among which Madidi National Park and Natural Integrated Management Area boasts the largest representation of ecoregions in the country. However, despite its significance, knowledge of Madidi's herpetofauna remains limited. This study presents the most comprehensive survey of reptile diversity in and around Madidi, combining an extensive literature review with three years of fieldwork. We computed alpha, beta, gamma, and dark diversity indices to comprehend the composition of reptile species across the ecoregions represented within the protected area. We registered 110 reptile species within the park, with the Sub-Andean Amazon Forest ecoregion displaying the highest diversity. The diversity indices applied indicate the potential for discovering additional species in the area, and as expected for a mountainous area, there is a high turnover of species between ecoregions, each of them exhibiting a distinctive species composition. We recommend continuous monitoring in an area with such high reptile diversity, particularly considering the impacts that climate change will have on these species’ assemblages over time.

References

Aliaga-Rossel, E., C. Cortez & S. Reichle. 2020. Reptiles y mamíferos acuáticos y semi acuáticos de las áreas protegidas nacionales de Bolivia. Ministerio de Medio Ambiente y Agua, La Paz, Bolivia.

Antonelli, A., A. Zizka, F.A. Carvalho, R. Scharn, C.D. Bacon, D. Silvestro & F.L. Condamine. 2018. Amazonia is the primary source of Neotropical biodiversity. Proceedings of the National Academy of Sciences 115:6034-6039.

Ascenso, A.C., J.C.L. Costa & A.L.C. Prudente. 2019. Taxonomic revision of the Erythrolamprus reginae species group, with description of a new species from Guiana Shield (Serpentes: Xenodontinae). Zootaxa 4586:65-97.

Avila-Pires, T.C.S. 1995. Lizards of Brazilian Amazonia (Reptilia: Squamata). Zoologische Verhandelingen 299:1-706.

Balaguera-Reina, S.A. & A. Velasco. 2019. Caiman crocodilus, in: IUCN Red List of threatened species. Versión 2024.1. http://www.iucnredlist.org [Consultado en julio 2024].

Bass, M.S., M. Finer, C.N. Jenkins, H. Kreft, D.F. Cisneros-Heredia, S.F. McCracken, N. C. A. Pitman, P. H. English, K. Swing, G. Villa, A. Di Fiore, C. C. Voigt & T.H. Kunz. 2010. Global Conservation Significance of Ecuador’s Yasuní National Park. Plos One 5:e8767.

Brazaitis, P., G.H. Rebêlo & C. Yamashita. 1998. The distribution of Caiman crocodilus crocodilus and Caiman yacare populations in Brazil. Amphibia Reptilia 19:193-201.

Catenazzi, A., E. Lehr & R. Von May. 2013. The amphibians and reptiles of Manu National Park and its buffer zone, Amazon basin and eastern slopes of the Andes, Peru. Biota Neotropica 13:1-15.

Chávez, G., A. Catenazzi & P.J. Venegas. 2017. A new species of arboreal microteiid lizard of the genus Euspondylus (Gymnophtalmidae: Cercosaurinae) from the Andean slopes of central Peru with comments on Peruvian Euspondylus. Zootaxa 4350:301-316.

Chazot, N., D.L. De-Silva, K.R. Willmott, A.V.L. Freitas, G. Lamas, J. Mallet, C.E. Giraldo, S. Uribe & M. Elias. 2018. Contrasting patterns of Andean diversification among three diverse clades of Neotropical clearwing butterflies. Ecology and Evolution 8:3965-3982.

Cortez, C. & R. Tejada. 2002. Diagnóstico de herpetofauna del Parque Nacional y Área Natural de Manejo Integrado Madidi. Wildlife Conservation Society, La Paz, Bolivia.

Das, I. 2016. Rapid assessments of reptile diversity, Pp. 241-253. En C.K. Dodd Jr. (Ed.), Reptile Ecology and Conservation a Handbook of Techniques. Oxford University Press, Oxford, UK.

Doan, T.M. & T.A. Castoe. 2005. Phylogenetic taxonomy of the Cercosaurini (Squamata: Gymnophthalmidae), with new genera for species of Neusticurus and Proctoporus. Zoological Journal of the Linnean Society 143:405-416.

Dodd Jr., C.K. 2016. Reptile Ecology and Conservation: A Handbook of Techniques. Oxford, UK.

Domic, E., C. Cortez, D. Embert, J. Aparicio, S. Reichle, I. de la Riva & J.M. Padial. 2012. Los reptiles y anfibios de Madidi. Pp. 96-111. En E. Salinas & R.B. Wallace (Eds.), Conocimientos Científicos y Prioridades de Investigación en el Parque Nacional y Área Natural de Manejo Integrado Madidi. Servicio Nacional de Áreas Protegidas, La Paz, Bolivia.

Emmons, L.H. 1991. Observations on the Herpetofauna. En T. A. Parker Ill & B. Bailey (Eds.), A biological Assessment of the Alto Madidi Region and Adjacent Areas of Northwest Bolivia. Conservación Internacional, Washington D.C., USA

Escobar, S., A.J. Helmstetter, S. Jarvie, R. Montúfar, H. Balslev & T.L.P. Couvreur. 2021. Pleistocene climatic fluctuations promoted alternative evolutionary histories in Phytelephas aequatorialis, an endemic palm from western Ecuador. Journal of Biogeography 48:1023-1037.

Esquerré, D., I.G. Brennan, R.A. Catullo, F. Torres-Pérez & J.S. Keogh. 2019. How mountains shape biodiversity: The role of the Andes in biogeography, diversiﬁcation, and reproductive biology in South America’s most species-rich lizard radiation (Squamata: Liolaemidae). Evolution 73:214-230.

Garzón-Orduña, I.J., J.E. Benetti-Longhini & A.V.Z. Brower. 2015. Competing paradigms of Amazonian diversification and the Pleistocene refugium hypothesis. Journal of Biogeography 42:1357-1360.

GBIF.org (2014), GBIF Global Biodiversity Information Facility. https://www.gbif.org [Consulted on Januari 2014].

Gomes, de C.A.L., de B.M. Ribeiro & F.D. Silva. 2013. Biogeography of the lizard genus Tropidurus Wied Neuwied, 1825 (Squamata: Tropiduridae): distribution, endemism, and area relationships in South America. Plos One 8:e59736.

Haffer, J. 1969. Speciation in Amazonian Forest Birds. Science 165:131-137.

Harvey, M.B., E.J. Aparicio & A.L. Gonzales. 2003. Revision of venomous snakes of Bolivia: Part 1. The coralsnakes (Elapidae: Micrurus). Annals of Carnegie Museum 72:1-52.

Harvey, M.B., E.J. Aparicio & A.L. Gonzales. 2005. Revision of the venomous snakes of Bolivia. II: The pitvipers (Serpentes: Viperidae). Annals of Carnegie Museum 74:1-37.

Holland, M.M., P.G. Risser & R. Naiman. 1991. Ecotones: the role of landscape boundaries in the management and restoration of changing environments. Chapman & Hall, New York, USA.

Hoorn, C., F.P. Wesselingh, H. ter Steege, M.A. Bermudez, A. Mora, J. Sevink, I. Sanmartín, A. Sanchez-Meseguer, C. L. Anderson, J. P. Figueiredo, C. Jaramillo, D. Riff, F. R. Negri, H. Hooghiemstra, J. Lundberg, T. Stadler, T. Särkinen & A. Antonelli. 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330:927-931.

Hoorn, C., V. Mosbrugger, A. Mulch & A. Antonelli. 2013. Biodiversity from mountain building. Nature Geoscience 6:154.

Ibisch, P.L., S.G. Beck, G.B. & A. Carretero. 2003. Ecoregiones y ecosistemas. Pp. 47-88. En: P.L. Ibisch & G. Mérida (Eds.), Biodiversidad: La Riqueza de Bolivia. Estado de Conocimiento y Conservación. Ministerio de Desarrollo Sostenible. Editorial FAN, Santa Cruz de la Sierra, Bolivia.

Identidad Madidi & SERNAP. 2017. Informe Científico 2015. Relevamientos de biodiversidad en el Parque Nacional y Área Natural de Manejo Integrado Madidi. Wildlife Conservation Society, La Paz, Bolivia.

Identidad Madidi & SERNAP. 2019. Informe de la expedición científica Identidad Madidi 2016. Relevamientos de biodiversidad en el Parque Nacional y Área Natural de Manejo Integrado Madidi. Wildlife Conservation Society, La Paz, Bolivia.

Identidad Madidi. 2020. Informe de la expedición científica Identidad Madidi 2017. Relevamientos de biodiversidad en el Parque Nacional y Área Natural de Manejo Integrado Madidi. Wildlife Conservation Society, La Paz, Bolivia.

Köhler, G. & E. Lehr. 2004. Comments on Euspondylus and Proctoporus (Squamata: Gymnophthalmidae) from Peru, with the description of three new species and a key to the peruvian species. Herpetologica 60:501-518.

Kok, P.J.R. 2010. A new species of Chironius Fitzinger, 1826 (Squamata: Colubridae) from the Pantepui region, northeastern South America. Zootaxa 2611:31–44.

Leary, S., W. Underwood, R. Anthony, S. Carter, T. Grandin, C. Greenacre, S. Gwaltney-Brant, M.A. McCrackin, R. Meyer, D. Miller, J. Shearer, T. Turner & R. Yanong. 2020. AVMA Guidelines for the Euthanasia of Animals: 2020 Edition. American Veterinary Medical Association, Schaumburg, Illinois, USA.

Lehr, E., J. Moravec, A. Whitworth, J. Villacampa, J.C. Cusi & R. von May. 2018. New distribution records for Euspondylus excelsum Chávez, Catenazzi & Venegas, 2017 (Reptilia, Gymnophthalmidae, Cercosaurinae) in Peru. Check List 14:1141-1149.

Lewis, R.J., R. Szava-Kovats & M. Pärtel. 2016. Estimating dark diversity and species pools: an empirical assessment of two methods. Methods in Ecology and Evolution 7:104-113.

Lewis, R.J., F. de Bello, J.A. Bennett, P. Fibich, G.E. Finerty, L. Götzenberger, I. Hiiesalu, L. Kasari, J. Leps, M. Májeková, O. Mudrák, K. Riibak, A. Ronk, T. Rychtecká, A. Vitová & M. Pärtel. 2017. Applying the dark diversity concept to nature conservation. Conservation Biology 31:40-47.

MacQuarrie, K., A. Bärtschi & R. Mittermeier. 2001. Donde los Andes encuentran al Amazonas. Bahuaja-Sonene y Madidi, parques nacionales de Perú y Bolivia. Jordi Blassi, Barcelona.

Malkmus, R., U. Manthey, G. Vogel, P. Hoffmann & J. Kosuch. 2002. Amphibians and Reptiles of Mount Kinabalu (North Borneo). Gantner Verlag, Ruggell, Liechtenstein.

Montambault, J.R. 2002. Informes de las Evaluaciones Biológicas de Pampas del Heath, Perú, Alto Madidi, Bolivia, y Pando, Bolivia. Conservation International, Washington D. C., USA.

Ocampo, M., D. Pincheira-Donoso, F. Sayol & R.S. Rios. 2022. Evolutionary transitions in diet infuence the exceptional diversifcation of a lizard adaptive radiation. BMC Ecology and Evolution 22:74.

Ocampo, M., J.E. Aparicio, N. Bernal Hoverud, E. Domic & R.B. Wallace. 2024. Amphibian diversity in Madidi National Park and Natural Integrated Management Area, Bolivia, one of the most diverse parks in South America. Herpetology Notes 17:371-389.

Pérez-Bejar, M.E. 1997. Una evaluación preliminar de los anfibios y reptiles de las Pampas del Heath (Provinvia Iturralde, Departamento La Paz). Ecología en Bolivia 30:43-54.

Prates, I., M. Trefaut-Rodrigues, P.R. Melo-Sampaio & A.C. Carnaval. 2015. Phylogenetic relationships of Amazonian anole lizards (Dactyloa): Taxonomic implications, new insights about phenotypic evolution and the timing of diversification. Molecular Phylogenetics and Evolution 82:258-268.

Quinteros-Muñoz, O., P. Gómez-Murillo, T. Camacho-Badani, R. Aguayo, R. Carpio-Real, E. Pérez, B. Marca, L. Gonzales & O. Torres-Carvajal. 2024. A new species of Sipo Sanke, Chironius (Serpentes: Colubridae), from the Yungas of Bolivia. Amphibian & Reptile Conservation 18:58-67.

R Core Team. 2022. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

Remsen, J.V. & T.A. Parker. 1995. Bolivia has the opportunity to create the planet's richest park for terrestrial biota. Bird Conservation International 5:181-199.

Rocha, D.G. da & I.L. Kaefer. 2019. What has become of the refugia hypothesis to explain biological diversity in Amazonia? Ecology and Evolution 9:4302-4309.

Roque, N., B. Gross, A.L. Rodriguez-Cordero, S.A. Balaguera-Reina & L.D. Densmore III. 2024. First confirmed record of Spectacled Caiman, Caiman crocodilus Linnaeus 1758, in the Department of Pando, Bolivia. Reptiles & Amphibians 31:e21738.

Rueda-Almonacid, J.V., J.L. Carr, R.A. Mittermeier, J.V. Rodríguez-Mahecha, R.B. Mast, R.C. Vogt, A.G.J. Rhodin, J. de la Ossa -Velásquez, J.N. Rueda & C. Goettsch-Mittermeier. 2007. Las tortugas y los cocodrilianos de los países andinos del trópico. Conservación Internacional, Bogotá, Colombia.

Salinas, E. & R.B. Wallace. 2012. Conocimientos científicos y prioridades de investigación en el Parque Nacional y Área Natural de Manejo Integrado Madidi. Servicio Nacional de Áreas Protegidas, La Paz, Bolivia.

Seminara, G. 2006. Meanders. Journal of Fluid Mechanics 554:271-297.

Simmons, J.E. 2002. Herpetological collecting and collections management. Revised edition. Society for the Study of Amphibians and Reptiles, Salt Lake, Utah, USA.

Sobral-Souza, T., L. Lautenschlager, T.Q. Morcatty, C. Bello, D. Hansen & M. Galetti. 2017. Rewilding defaunated Atlantic Forests with tortoises to restore lost seed dispersal functions. Perspectives in Ecology and Conservation 15:300-307.

Sonne, J. & C. Rahbek. 2024. Idiosyncratic patterns of local species richness and turnover define global biodiversity hotspots. Proceedings of the National Academy of Sciences 121:e2313106121.

Tavares, A.S., T.Q. Morcatty, J. Zuanon & W.E. Magnusson. 2019. Influence of body size, topography, food availability and tree-fall gaps on space use by yellow-footed tortoises (Chelonoidis denticulatus) in Central Amazonia. Plos One 14:e0211869.

Torres-Carvajal, O. 2007. A taxonomic revision of south american Stenocercus (Squamata: Iguania) lizards. Herpetological Monographs 21:76-178.

Uetz, P., P. Freed, R. Aguilar, F. Reyes, J. Kudera & J. Hošek. 2024. The Reptile Database. http://www.reptile-database.org [Consulted on March 2024].

Umbrello, L.S., H. Newton, A.M. Baker, K.J. Travouillon & M. Westerman. 2024. Vicariant speciation resulting from biogeographic barriers in the Australian tropics: The case of the red-cheeked dunnart (Sminthopsis virginiae). Ecology and Evolution 14:e70215.

Wallace, R., A. Ramírez, E. Salinas & L. Painter. 2017. Inspirando a la población urbana mediante información científica e imágenes de biodiversidad - Identidad Madidi. Ecología en Bolivia 52:1-6.