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Back from the deaf: integrative taxonomy revalidates an earless and mute species, Hylodes grandoculis van Lidth de Jeude, 1904, and confirms a new species of Pristimantis Jiménez de la Espada, 1870 (Anura: Strabomantidae) from the Eastern Guiana Shield

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Abstract

Many anuran species remain to be formally named and described in Amazonia, notably in the Guiana Shield, and particularly in megadiverse groups such as Pristimantis. Several species in the Guiana Shield region have been confused with Pristimantis marmoratus and P. ockendeni. Hylodes grandoculis, a taxon previously placed in the synonymy of P. marmoratus, may be available for one of these species. To disentangle this confusing situation, we examined the external morphology and osteology (via µ-CT scans) of the holotype of H. grandoculis, the holotype of Pristimantis marmoratus, and of recently collected material for which we also analyzed molecular, acoustic, and morphological variation. We concluded that some populations from Suriname and northern Pará, Brazil, are distinct from P. marmoratus and correspond to Pristimantis grandoculis. Other populations, from French Guiana, are closely related to P. grandoculis but their status remains ambiguous. Finally, some populations, from French Guiana and Amapá, Brazil, are conspicuously distinct from both P. marmoratus and P. grandoculis and are described herein as P. crepitaculus sp. nov. A third species, belonging to a “trans-amazon complex”, occurs in southern Suriname, Guyana, and Brazil and remains undescribed. Pristimantis grandoculis and related populations from French Guiana lack external tympanum, columella, pharyngeal ostia, vocal slits and do not vocalize. This represents a rare, perhaps unique, example of a deaf and mute species of frogs from the Amazonian lowlands.

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Availability of data and material

All new DNA sequences, call recordings, and µ-CT scans have been deposited in public repositories.

References

  • Albert, J. S., Val, P., & Hoorn, C. (2018). The changing course of the Amazon River in the Neogene: Center stage for Neotropical diversification. Neotropical Ichthyology, 16, e180033.

    Article  Google Scholar 

  • Anonymous. (1903). Guyanes, Brésil. In Annales de Géographie (t. 12, n°65, XII° Bibliographie Géographique Annuelle, 1902., pp. 288–292).

  • Ávila-Pires, T. C. S. D., Hoogmoed, M. S., & Rocha, W. A. D. (2010). Notes on the vertebrates of northern Pará, Brazil: A forgotten part of the Guianan Region, I. Herpetofauna. Boletim Do Museu Paraense Emílio Goeldi, 5, 13–11.

    Article  Google Scholar 

  • Barrio-Amorós, C. L., & Brewer-Cariás, C. (2008). Herpetological results of the 2002 expedition to Sarisariñama, a tepui in Venezuelan Guayana, with the description of five new species. Zootaxa, 1942, 1–68.

    Article  Google Scholar 

  • Bicudo, T. C., Sacek, V., de Almeida, R. P., Bates, J. M., & Ribas, C. C. (2019). Andean tectonics and mantle dynamics as a pervasive influence on Amazonian ecosystem. Scientific Reports, 9(1), 1–11.

    Article  CAS  Google Scholar 

  • Boistel, R., Aubin, T., Cloetens, P., Peyrin, F., Scotti, T., Herzog, P., Gerlach, J., Pollet, N., & Aubry, J. F. (2013). How minute sooglossid frogs hear without a middle ear. Proceedings of the National Academy of Sciences, 110(38), 15360–15364.

    Article  CAS  Google Scholar 

  • Boulenger, G. A. (1900). Batrachians. In E. R. Lankester (Ed.), Report on a collection made by Messrs. F. V. McConnell and J. J. Quelch at Mount Roraima in British Guiana. Transactions of the Linnean Society of London. 2nd series, Zoology, 8, 55–56.

  • Boulenger, G. A. (1912). Descriptions of new batrachians from the Andes of South America, preserved in the British Museum. Annals and Magazine of Natural History, Series, 8(10), 185–191.

    Article  Google Scholar 

  • Citadini, J. M., Brandt, R., Williams, C. R., & Gomes, F. R. (2018). Evolution of morphology and locomotor performance in anurans: Relationships with microhabitat diversification. Journal of Evolutionary Biology, 31, 371–381.

    Article  PubMed  CAS  Google Scholar 

  • Dewynter, M., Marty, C., Blanc, M., Gaucher, P., Vidal, N., Frétey, T., De Massary, J. C., & Fouquet, A. (2008). Liste des amphibiens et des reptiles de Guyane. Available online. Retrieved January 1, 2021, from http://www.chelidae.com/pdf/dewynter2008.pdf

  • Duellman, W. E., & Lehr, E. (2009). Terrestrial-breeding frogs (Strabomantidae) in Peru (p. 382). Nature und Tier Verlag.

    Google Scholar 

  • Elmer, K. R., & Cannatella, D. C. (2008). Three new species of leaflitter frogs from the upper Amazon forests: Cryptic diversity within Pristimantisockendeni”(Anura: Strabomantidae) in Ecuador. Zootaxa, 1784, 11–38.

    Article  Google Scholar 

  • Emerson, S. B. (1985). Skull shape in frogs: Correlations with diet. Herpetologica, 41, 177–188.

    Google Scholar 

  • Ernst, R., Rodel, M., & Arjoon, D. (2005). On the cutting edge-the anuran fauna of the Mabura Hill Forest Reserve, central Guyana. Salamandra, 41(4), 179–194.

    Google Scholar 

  • Ernst, R., Linsenmair, K. E., & Rödel, M. O. (2006). Diversity erosion beyond the species level: Dramatic loss of functional diversity after selective logging in two tropical amphibian communities. Biological Conservation, 133(2), 143–155.

    Article  Google Scholar 

  • Ernst, R., Linsenmair, K. E., Thomas, R., & Rödel, M. O. (2007). Amphibian communities in disturbed forests: Lessons from the Neo-and Afrotropics. In T. Tscharntke, C. Leuschner, M. Zeller, E. Guhardja, & A. Bidin (Eds.), Stability of Tropical Rainforest Margins (pp. 59–85). Springer.

    Chapter  Google Scholar 

  • Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39, 783–791.

    Article  PubMed  Google Scholar 

  • Ferrão, M., Colatreli, O., de Fraga, R., Kaefer, I. L., Moravec, J., & Lima, A. P. (2016). High species richness of Scinax treefrogs (Hylidae) in a threatened Amazonian landscape revealed by an integrative approach. PLoS ONE, 11, e0165679.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fouquet, A., Gilles, A., Vences, M., Marty, C., Blanc, M., & Gemmell, N. J. (2007). Underestimation of species richness in Neotropical frogs revealed by mtDNA analyses. PLoS ONE, 2(10), e1109. https://doi.org/10.1371/journal.pone.0001109

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fouquet, A., Noonan, B. P., Rodrigues, M. T., Pech, N., Gilles, A., & Gemmell, N. J. (2012). Multiple quaternary refugia in the eastern Guiana Shield revealed by comparative phylogeography of 12 frog species. Systematic Biology, 61, 461–489.

    Article  PubMed  Google Scholar 

  • Fouquet, A., Martinez, Q., Courtois, E. A., Dewynter, M., Pineau, K., Gaucher, P., Blanc, M., Marty, C., & Kok, P. J. R. (2013). A new species of the genus Pristimantis (Amphibia, Craugastoridae) associated with the moderately elevated massifs of French Guiana. Zootaxa, 3750, 569–586.

    Article  PubMed  Google Scholar 

  • Fouquet, A., Vacher, J.-P., Courtois, E. A., Villette, B., Reizine, H., Gaucher, P., Jairam, R., Ouboter, P., & Kok, P. J. R. (2018). On the brink of extinction: Two new species of Anomaloglossus from French Guiana and amended definition of Anomaloglossus degranvillei and A. surinamensis (Anura: Aromobatidae). Zootaxa, 4379, 001–023.

    Article  Google Scholar 

  • Fouquet, A., Vidal, N., & Dewynter, M. (2019). The amphibians of the Mitaraka massif, French Guiana. Zoosystema, 41, 359–374.

    Article  Google Scholar 

  • Fouquet A., Leblanc K., Framit M., Réjaud A., Rodrigues M. T., Castroviejo-Fisher S., Peloso P. L. V., Prates I., Manzi S., Suescun U., Baroni S., Moraes L. J. C. L., Recoder R., de Souza S. M., Dal Vecchio F., Camacho A., Guellere J. M., Rojas-Runjaic F. J. M., Gagliardi-Urrutia G., de Carvalho V. T., Gordo M., Menin M., Kok P. J. R, Hrbek T., Werneck F. P., Crawford A. J., Ron S. R., Mueses-Cisneros J. J., Rojas Zamora R. R., Pavan D., Simões P. I., Ernst R., & Fabre A. C. (2021a). Species diversity and biogeography of an ancient frog clade from the Guiana Shield (Anura: Microhylidae: Adelastes, Otophryne, Synapturanus) exhibiting spectacular phenotypic diversification. Biological Journal of the Linnean Society, 132(2), 233–256.

  • Fouquet, A., Marinho, P., Réjaud, A., de Carvalho, T., Caminer, M. A., Jansen, M., Rainha, R., Rodrigues, M. T., Werneck, F., Lima, A., Hrbek, T., Giaretta, A., Venegas, P. J., Chávez, G., & Ron, S. (2021b). Systematics and biogeography of the Boana albopunctata species group, with the description of two new species from Amazonia. Systematics & Biodiversity, 19, 375–399.

    Article  Google Scholar 

  • Frost, D. R. (1985). Amphibian Species of the World. Lawrence, Kansas, U.S.A. Association of Systematics Collections and Allen Press.

    Google Scholar 

  • Frost, D. R. (2021). Amphibian species of the world: An online reference. Version 6.1 (01/01/2021). Electronic Database accessible at https://amphibiansoftheworld.amnh.org/index.php, retrieved January 1, 2021. American Museum of Natural History, New York, USA. https://doi.org/10.5531/db.vz.0001

  • Gonzalez-Voyer, A., Padial, J. M., Castroviejo-Fisher, S., De la Riva, I., & Vilà, C. (2011). Correlates of species richness in the largest Neotropical amphibian radiation. Journal of Evolutionary Biology, 24, 931–942.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gehara, M., Crawford, A. J., Orrico, V. G., Rodríguez, A., Lötters, S., Fouquet, A., Barrientos, L. S., Brusquetti, F., De la Riva, I., Ernst, R., Urrutia, G. G., Glaw, F., Guayasamin, J. M., Hölting, M., Jansen, M., Kok, P. J. R., Kwet, A., Lingnau, R., Lyra, M., … Köhler, J. (2014). High levels of diversity uncovered in a widespread nominal taxon: Continental phylogeography of the Neotropical tree frog Dendropsophus minutus. PLoS ONE, 9(9), e103958.

    Article  PubMed  PubMed Central  Google Scholar 

  • Goutte, S., Mason, M. J., Christensen-Dalsgaard, J., Montealegre-Z, F., Chivers, B. D., Sarria-S, F. A., Antoniazzi, M. M., Jared, C., Sato, L. A., & Toledo, L. F. (2017). Evidence of auditory insensitivity to vocalization frequencies in two frogs. Scientific Reports, 7(1), 1–9.

    Article  CAS  Google Scholar 

  • Guayasamin, J. M., & Funk, W. C. (2009). The amphibian community at Yanayacu Biological Station, Ecuador, with a comparison of vertical microhabitat use among Pristimantis species and the description of a new species of the Pristimantis myersi group. Zootaxa, 2220, 41–66.

    Article  Google Scholar 

  • Hedges, S. B., Duellman, W. E., & Heinicke, M. P. (2008). New World direct-developing frogs (Anura: Terrarana): Molecular phylogeny, classification, biogeography, and conservation. Zootaxa, 1737, 1–182.

    Article  Google Scholar 

  • Hoorn, C., Bogotá-A, G. R., Romero-Baez, M., Lammertsma, E. I., Flantua, S. G. A., Dantas, E. L., Dino, R., & do Carmo, D. A., & Chemale, Jr. F. (2017). The Amazon at sea: Onset and stages of the Amazon River from a marine record, with special reference to Neogene plant turnover in the drainage basin. Global and Planetary Change, 153, 51–65.

    Article  Google Scholar 

  • IUCN. (2020). The IUCN Red List of Threatened Species. Version 2020–2. Retrieved July 9, 2020, from https://www.iucnredlist.org

  • Jairam, R. (2019). Checklist of the amphibians and reptiles of the Lely Mountains, eastern Suriname. Amphibian & Reptile Conservation, 13(2), 160–171.

    Google Scholar 

  • Jaramillo, A. F., De La Riva, I., Guayasamin, J. M., Chaparro, J. C., Gagliardi-Urrutia, G., Gutiérrez, R. C., Brcko, I., Vilà, C., & Castroviejo-Fisher, S. (2020). Vastly underestimated species richness of Amazonian salamanders (Plethodontidae: Bolitoglossa) and implications about plethodontid diversification. Molecular Phylogenetics and Evolution, 149, 106841.

    Article  PubMed  Google Scholar 

  • Jaslow, A. P., Hetherington, T. E., & Lombard, R. E. (1988). Structure and function of the amphibian middle ear. In B. Fritzsch, W. Walkowiak, & M. J. Ryan (Eds.), The evolution of the amphibian auditory system (pp. 69–91). University of Michigan, Wiley.

  • Jiménez de la Espada, M. (1870). Fauna neotropicalis species quaedam nondum cognitae. Jornal De Sciências, Mathemáticas, Physicas e Naturaes, Lisboa, 3, 57–65.

    Google Scholar 

  • Katoh, K., Rozewicki, J., & Yamada, K. D. (2017). MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinformatics, 20, 1160–1166.

    Article  Google Scholar 

  • Kirschner, J. A., & Hoorn, C. (2019). The onset of grasses in the Amazon drainage basin, evidence from the fossil record. Frontiers of Biogeography, 12, e44827.

    Google Scholar 

  • Köhler, J., Jansen, M., Rodríguez, A., Kok, P. J. R., Toledo, L. F., Emmrich, M., Glaw, F., Haddad, C. F. B., Rödel, M.-O., & Vences, M. (2017). The use of bioacoustics in anuran taxonomy: Theory, terminology, methods and recommendations for best practice. Zootaxa, 4251, 1–124.

    Article  PubMed  Google Scholar 

  • Kok, P. J. R. (2013). Two new charismatic Pristimantis species (Anura: Craugastoridae) from the tepuis of the “Lost World”(Pantepui region, South America). European Journal of Taxonomy, 60, 1–24.

    Google Scholar 

  • Kok, P. J. R., & Barrio-Amorós, C. L. (2013). On the taxonomic validity of Pristimantis tepuiensis (Schlüter & Rödder, 2007) and P. stegolepis (Schlüter & Rödder, 2007), with remarks on the type series of P. guaiquinimensis (Schlüter & Rödder, 2007). Zootaxa, 3694(1), 75–80.

  • Kok, P. J. R., Dezfoulian, R., Means, D. B., Fouquet, A., & Barrio-Amorós, C. L. (2018). Amended diagnosis and new description of Pristimantis marmoratus (Boulenger, 1900) (Amphibia: Craugastoridae), with description of its advertisement call and notes on its breeding ecology and phylogenetic relationships. European Journal of Taxonomy, 397, 1–30.

    Google Scholar 

  • Kok, P. J. R., Russo, V. G., Ratz, S., Means, D. B., MacCulloch, R. D., Lathrop, A., Aubret, F., & Bossuyt, F. (2017). Evolution in the South American “Lost World”: Insights from multilocus phylogeography of stefanias (Anura, Hemiphractidae, Stefania). Journal of Biogeography, 44, 170–181.

    Article  Google Scholar 

  • Latrubesse, E. M., Cozzuol, M., da Silva-Caminha, S. A., Rigsby, C. A., Absy, M. L., & Jaramillo, C. (2010). The Late Miocene paleogeography of the Amazon Basin and the evolution of the Amazon River system. Earth-Science Reviews, 99(3–4), 99–124.

    Article  CAS  Google Scholar 

  • Lê, S., Josse, J., & Husson, F. (2008). FactoMineR: An R package for multivariate analysis. Journal of Statistical Software, 25, 1–18.

    Article  Google Scholar 

  • Lescure, J., & Marty, C. (2000). Atlas des amphibiens de Guyane. Collection Patrimoines Naturels.

  • Lima, A. P., Magnuson, W. E., Menin, M., Erdtmann, L. K., Rodrigues, D. J., Keller, C., & Hödl, W. (2006). Guia de sapos da Reserva Adolpho Ducke, Amazônia Central. Áttema Design Editorial, Manaus.

  • Lösel, P. D., van de Kamp, T., Jayme, A., Ershov, A., Faragó, T., Pichler, O., Tan Jerome, N., Aadepu, N., Bremer, S., Chilingaryan, S. A., & Heethoff, M. (2020). Introducing Biomedisa as an open-source online platform for biomedical image segmentation. Nature Communications, 11(1), 1–14.

  • Lynch, J. D., & Duellman, W. E. (1997). Frogs of the genus Eleutherodactylus (Leptodactylidae) in western Ecuador: Systematic, ecology, and biogeography. University of Kansas.

    Book  Google Scholar 

  • Magnusson, W. E. (2016). The fish and the frogs. Open Science Publishers.

  • Marty, C., & Gaucher, P. (1999). Sound guide to the tailless amphibians of French Guiana. CEBA.

  • Means, D. B., & Savage, J. M. (2007). Three new malodorous rainfrogs of the genus Pristimantis (Anura: Brachycephalidae) from the Wokomung Massif in west-central Guyana, South America. Zootaxa, 1658, 39–55.

    Article  Google Scholar 

  • Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, (pp. 1–8). New Orleans, LA.

  • Miyamoto, M. M. (1982). Vertical habitat use by Eleutherodactylus frogs (Leptodactylidae) at two Costa Rican localities. Biotropica, 14, 141–144.

    Article  Google Scholar 

  • Myers, C. W., & Donnelly, M. A. (1996). A new herpetofauna from Cerro Yaví, Venezuela: first results of the Robert G. Goelet American Museum-Terramar Expedition to the northwestern tepuis. American Museum novitates, (3172), 1–56.

  • Myers, C. W., & Donnelly, M. A. (1997). A tepui herpetofauna on a granitic mountain (Tamacuari) in the borderland between Venezuela and Brazil: report from the Phipps Tapirapecó Expedition. American Museum novitates, (3213), 1–71.

  • Myers, C. W., & Donnelly, M. A. (2001). Herpetofauna of the Yutajé-Corocoro massif, Venezuela: Second report from the Robert G. Goelet American Museum-Terramar expedition to the Northwestern tepuis. Bulletin of the American Museum of Natural History, 261, 1–85.

    Article  Google Scholar 

  • Ouboter, P. E., & Jairam, R. (2012) Amphibians of Suriname. Brill, Leiden, 376 pp.

  • Padial, J. M., Grant, T., & Frost, D. R. (2014). Molecular systematics of terraranas (Anura: Brachycephaloidea) with an assessment of the effects of alignment and optimality criteria. Zootaxa, 3825(1), 1–132.

    Article  PubMed  Google Scholar 

  • Pereyra, M. O., Womack, M. C., Barrionuevo, J. S., Blotto, B. L., Baldo, D., Targino, M., et al. (2016). The complex evolutionary history of the tympanic middle ear in frogs and toads (Anura). Scientific Reports, 6(1), 1–9.

    Article  Google Scholar 

  • Pough, F. H., & Magnusson, W. E. (1992). Morphology, physiology, and foraging behaviour, (pp. 398–410). In: Feder, M. E., & Burggren, W. W. (Eds.), Environmental Physiology of the Amphibians. University Chicago Press. Chicago and London.

  • R Core Team. (2016). R: A language and environment for statistical computing. Vienna, Austria. Available at: https://www.R-project.org/. Retrieved January 1, 2021.

  • Réjaud, A., Rodrigues, M. T., Crawford, A. J., Castroviejo-Fisher, S., Jaramillo, A. F., Chaparro, J. C., Glaw, F., Gagliardi-Urrutia, G., Moravec, J., De la Riva, I. J., Perez, P., Lima, A. P., Werneck, F. P., Hrbek, T., Ron, S. R., Ernst, R., Kok, P. J. R., Driskell, A., Chave, J., & Fouquet, A. (2020). Historical biogeography identifies a possible role of the Pebas system in the diversification of the Amazonian rocket frogs (Aromobatidae: Allobates). Journal of Biogeography, 47(11), 2472–2482.

    Article  Google Scholar 

  • Rivero, J. A. (1968). A new species of Eleutherodactylus (Amphibia, Salientia) from the Guayana Region, Edo. Bolívar. Venezuela. Breviora, 306, 1–10.

    Google Scholar 

  • Salducci, M. D., Marty, C., Fouquet, A., & Gilles, A. (2005). Phylogenetic relationships and biodiversity in hylids (Anura: Hylidae) from French Guiana. Comptes Rendus Biologies, 328, 1009–1024.

    Article  PubMed  CAS  Google Scholar 

  • Schlüter, A., & Rödder, D. (2007). Three new frogs of the genus Eleutherodactylus (Amphibia, Leptodactylidae) from Guaiquinima table mountain, Bolívar. Venezuela. Herpetotropicos, 3(2), 88–99.

    Google Scholar 

  • Silva, S. M., Peterson, A. T., Carneiro, L., Burlamaqui, T. C. T., Ribas, C. C., Sousa-Neves, T., Miranda, L. S., Fernandes, A. M., d'Horta, F. M., Araújo-Silva, L. E., & Batista, R. (2019). A dynamic continental moisture gradient drove Amazonian bird diversification. Science Advances, 5(7), eaat5752.

  • Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Strauss, R. E. (1985). Evolutionary allometry and variation in body form in the South American catfish genus Corydoras (Callichthyidae). Systematic Biology, 34, 381–396.

    Article  Google Scholar 

  • Toledo, L. F., Martins, I. A., Bruschi, D. P., Passos, M. A., Alexandre, C., & Haddad, C. F. B. (2015). The anuran calling repertoire in the light of social context. Acta Ethologica, 18(2), 87–99.

    Article  Google Scholar 

  • Trevisan, C. C., Batalha-Filho, H., Garda, A. A., Menezes, L., Dias, I. R., Sole, M., Canedo, C., Junca, F. A., & Napoli, M. F. (2020). Cryptic diversity and ancient diversification in the northern Atlantic Forest Pristimantis (Amphibia, Anura, Craugastoridae). Molecular Phylogenetics and Evolution, 148, 106811.

    Article  PubMed  Google Scholar 

  • Vacher, J.-P., Kok, P. J. R., Rodrigues, M. T., Dias Lima, J., Lorenzini, A., Martinez, Q., Fallet, M., Courtois, E. A., Blanc, M., Gaucher, P., Dewynter, M., Jairam, R., Ouboter, P., Thébaud, C., & Fouquet, A. (2017). Cryptic diversity in Amazonian frogs: Integrative taxonomy of the genus Anomaloglossus (Amphibia: Anura: Aromobatidae) reveals a unique case of diversification within the Guiana Shield. Molecular Phylogenetics and Evolution, 112, 158–173.

    Article  PubMed  Google Scholar 

  • Vacher, J.-P., Chave, J., Ficetola, F. G., Sommeria-Klein, G., Tao, S., Thébaud, C., Blanc, M., Camacho, A., Cassimiro, J., Colston, T. J., Dewynter, M., Ernst, R., Gaucher, P., Gomes, J. O., Jairam, R., Kok, P. J. R., Lima, J. D., Martinez, Q., Marty, C., … Fouquet, A. (2020). Large scale DNA-based survey of frogs in Amazonia suggests a vast underestimation of species richness and endemism. Journal of Biogeography, 47, 1781–1791.

    Article  Google Scholar 

  • van Lidth de Jeude, T. W. (1904). Reptiles and batrachians from Surinam. Notes from the Leyden Museum, 25, 83–94.

    Google Scholar 

  • Vences, M., & Wake, D. B. (2007). Speciation, species boundaries and phylogeography of amphibians. Amphibian Biology, 7, 2613–2671.

    Google Scholar 

  • Vieites, D. R., Wollenberg, K. C., Andreone, F., Köhler, J., Glaw, F., & Vences, M. (2009). Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences, 106(20), 8267–8272.

    Article  CAS  Google Scholar 

  • von May, R., Lehr, E., & Rabosky, D. L. (2018). Evolutionary radiation of earless frogs in the Andes: Molecular phylogenetics and habitat shifts in high-elevation terrestrial breeding frogs. PeerJ, 6, e4313. https://doi.org/10.7717/peerj.4313

    Article  Google Scholar 

  • Zug, G. R. (1972). Anuran locomotion: Structure and function. I. Preliminary observations on relation between jumping and osteometrics of appendicular and postaxial skeleton. Copeia, 1972, 613–624.

    Article  Google Scholar 

Download references

Acknowledgements

We thank Ate Alma-Cohen and Esther Dondorp from the Leiden Naturalis Biodiversity Center (National Research Institute for Biodiversity, The Netherlands), and Mark Wilkinson from the Natural History Museum (UK) who provided the µ-CT scans of the holotype of Hylodes grandoculis and the holotype of Pristimantis marmoratus, respectively. Renaud Lebrun and Quentin Martinez (ISEM) helped with data acquisition with the µ-CT facilities of the MRI platform member of the National Infrastructure France-BioImaging (supported by the French National Research Agency (ANR-10-INBS-04, «Investments for the future»), the Labex CEMEB (ANR-10-LABX-0004), and NUMEV (ANR-10-LABX-0020)). We also thank E. Courtois, L. Brandão, M. Dewynter, N. Vidal, J. Devillechabrole, J.-P. Vacher, P. Nunes, B. Villette, S. Cally, D. Baêta, P. Ouboter, V. Kadosoe, M. Blanc, J. Dias Lima, P. Gaucher, M.T. Rodrigues, and V. Rufray who helped to collect some of the specimens and tissue samples used in this work. Permission to conduct biodiversity research in Guyana was provided by the Environmental Protection Agency of Guyana under research permit number 180609 BR 112, and fieldwork was made possible through the Forestry Department of the Guyana Forestry Commission (GFC-PRDD), particularly R. Thomas. Collection permits for Brazil were provided by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio).

Funding

This study benefited from an “Investissement d’Avenir” grant managed by the Agence Nationale de la Recherche (CEBA, rANR-10-LABX-25–01). PP and ATM were supported by fellowships from Conselho Nacional de Desenvolvimento Científico e Tecnológico (302501/2019–3 and 300822/2021–9 to PP; 142153/2019–2 to ATM). PP was also supported by an award from the Maxwell/Hanrahan Foundation. The work of RE was funded by the German Academic Exchange Service (DAAD) and Deutsche Forschungsgemeinschaft (DFG; ER 589/2–1). The work of PJRK was funded by the Fonds voor Wetenschappelijk Onderzoek (FWO12A7614N and FWO12A7617N).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Antoine Fouquet.

Ethics declarations

Ethics approval

Experiments have been conducted in accordance with relevant national legislation on the use of animals for research.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Appendices

Appendix 1 Molecular data

12S access

16S access

Genus

Species

Voucher

Voucher2

Locality

Country

lat

lon

NA

JQ742162

Pristimantis

abakapa

 

VUB3749

Abakapa-tepui

Venezuela

5.1892

 − 62.2944

NA

JQ742163

Pristimantis

abakapa

 

VUB3750

Angasima-tepui

Venezuela

5.0431

 − 62.0808

NA

JQ742151

Pristimantis

aureoventris

 

VUB3741

Roraima-tepui

Guyana

5.2500

 − 60.7167

NA

JQ742152

Pristimantis

aureoventris

 

VUB3748

Wei-Assipu-tepui

Guyana

5.2175

 − 60.7058

NA

JQ742153

Pristimantis

aureoventris

 

VUB3742

Wei-Assipu-tepui

Guyana

5.2175

 − 60.7058

NA

JQ742154

Pristimantis

aureoventris

 

VUB3747

Wei-Assipu-tepui

Guyana

5.2175

 − 60.7058

NA

JQ742155

Pristimantis

aureoventris

 

VUB3744

Wei-Assipu-tepui

Guyana

5.2175

 − 60.7058

NA

JQ742156

Pristimantis

aureoventris

 

VUB3745

Wei-Assipu-tepui

Guyana

5.2175

 − 60.7058

NA

JQ742157

Pristimantis

aureoventris

 

VUB3746

Wei-Assipu-tepui

Guyana

5.2175

 − 60.7058

NA

JQ742158

Pristimantis

aureoventris

 

VUB3743

Wei-Assipu-tepui

Guyana

5.2175

 − 60.7058

NA

JQ742159

Pristimantis

aureoventris

 

VUB3499

Wei-Assipu-tepui

Guyana

5.2175

 − 60.7058

NA

KDQF01000101

Pristimantis

espedeus

AF0265

 

Nouragues

French Guiana

4.0917

 − 52.7000

NA

KDQF01000107

Pristimantis

espedeus

AF0277

R116

Nouragues

French Guiana

4.0917

 − 52.7000

NA

KDQF01000108

Pristimantis

espedeus

AF0278

R117

Nouragues

French Guiana

4.0917

 − 52.7000

NA

KDQF01000150

Pristimantis

espedeus

AF0576

 

Itoupe

French Guiana

3.0250

 − 53.0800

NA

KDQF01000422

Pristimantis

espedeus

AF1156

R118

Trinité

French Guiana

4.6025

 − 53.4143

NA

KDQF01000423

Pristimantis

espedeus

AF1157

 

Trinité

French Guiana

4.6025

 − 53.4143

NA

KDQF01000439

Pristimantis

espedeus

AF1190

R119

Trinité

French Guiana

4.6025

 − 53.4143

NA

KDQF01000446

Pristimantis

espedeus

AF1203

R120

Trinité

French Guiana

4.6025

 − 53.4143

NA

KDQF01000452

Pristimantis

espedeus

AF1219

 

Trinité

French Guiana

4.6025

 − 53.4143

NA

KDQF01000570

Pristimantis

espedeus

AF1520

R121

Grande Montagne Tortue

French Guiana

4.2927

 − 52.3495

NA

KDQF01000571

Pristimantis

espedeus

AF1521

R122

Grande Montagne Tortue

French Guiana

4.2927

 − 52.3495

NA

KDQF01000572

Pristimantis

espedeus

AF1522

R123

Grande Montagne Tortue

French Guiana

4.29273

 − 52.3495

NA

KDQF01000952

Pristimantis

espedeus

AF2430

 

Nassau

Suriname

4.8041

 − 54.5555

NA

KDQF01000953

Pristimantis

espedeus

AF2431

 

Nassau

Suriname

4.8041

 − 54.5555

NA

KDQF01000955

Pristimantis

espedeus

AF2433

 

Nassau

Suriname

4.8041

 − 54.5555

NA

KDQF01001020

Pristimantis

espedeus

AF2616

 

Atachi Bakka

French Guiana

3.5444

 − 53.9128

NA

KDQF01001025

Pristimantis

espedeus

AF2629

 

Atachi Bakka

French Guiana

3. 5444

 − 53.9128

NA

KDQF01001028

Pristimantis

espedeus

AF2632

 

Atachi Bakka

French Guiana

3. 5444

 − 53.9128

NA

KDQF01001048

Pristimantis

espedeus

AF2670

 

Alikéné

French Guiana

3.2156

 − 52.3980

NA

KDQF01001057

Pristimantis

espedeus

AF2684

 

Alikéné

French Guiana

3.2156

 − 52.3980

NA

KDQF01001058

Pristimantis

espedeus

AF2685

 

Alikéné

French Guiana

3.2156

 − 52.3980

NA

KDQF01001061

Pristimantis

espedeus

AF2690

 

Alikéné

French Guiana

3.2157

 − 52.3973

NA

KDQF01001062

Pristimantis

espedeus

AF2694

 

Alikéné

French Guiana

3.2157

 − 52.3973

NA

KDQF01001063

Pristimantis

espedeus

AF2695

 

Alikéné

French Guiana

3.2157

 − 52.3973

NA

KDQF01001529

Pristimantis

espedeus

AG268

 

Lucifer

French Guiana

4.7774

 − 53.9475

NA

KDQF01001653

Pristimantis

espedeus

AG507

 

Saul

French Guiana

3.7193

 − 53.4128

NA

KDQF01001654

Pristimantis

espedeus

AG508

R124

Saul

French Guiana

3.7193

 − 53.4128

NA

KDQF01002024

Pristimantis

espedeus

BPN2908

 

RAP Basecamp 1

Suriname

2.5269

 − 55.7700

JN690706

JN691314

Pristimantis

espedeus

CM395

 

Lucifer

French Guiana

4.7774

 − 53.9475

NA

KDQF01003878

Pristimantis

espedeus

PG477

R131

Kotika

French Guiana

3.9333

 − 54.1972

NA

ON113943

Pristimantis

espedeus

PG524

R132

Pic Coudreau de l'Est

French Guiana

3.3005

 − 52.9493

NA

KDQF01004301

Pristimantis

espedeus

ST300

 

Parna Tumucumaque

AP

0.9091

 − 53.2285

NA

KDQF01004302

Pristimantis

espedeus

ST301

 

Parna Tumucumaque

AP

0.9091

 − 53.2285

NA

ON113944

Pristimantis

espedeus

ST315

 

Parna Tumucumaque

AP

0.9091

 − 53.2285

NA

ON113939

Pristimantis

imthurni

PK3671

 

Ptari-tepui

Venezuela

5.7639

 − 61.8112

NA

KDQF01000063

Pristimantis

inguinalis

AF0157

 

Brownsberg

Suriname

4.9365

 − 55.1948

NA

KDQF01000248

Pristimantis

inguinalis

AF0803

 

Kaw

French Guiana

4.5507

 − 52.1610

NA

KDQF01000253

Pristimantis

inguinalis

AF0813

 

Savane Virginie

French Guiana

4.1959

 − 52.1490

NA

KDQF01000256

Pristimantis

inguinalis

AF0820

 

Chutes Voltaire

French Guiana

5.0312

 − 54.0878

NA

KDQF01000295

Pristimantis

inguinalis

AF0883

 

Nouragues

French Guiana

4.0850

 − 52.6810

NA

KDQF01000514

Pristimantis

inguinalis

AF1386

 

Aratai

French Guiana

3.9909

 − 52.5902

NA

KDQF01000523

Pristimantis

inguinalis

AF1415

 

Savane Virginie

French Guiana

4.1959

 − 52.1490

NA

KDQF01000556

Pristimantis

inguinalis

AF1498

 

Nouragues

French Guiana

4.0848

 − 52.6806

NA

ON113918

Pristimantis

inguinalis

AF1503

 

Grande Montagne Tortue

French Guiana

4.2927

 − 52.3496

NA

KDQF01000609

Pristimantis

inguinalis

AF1626

 

Saul

French Guiana

3.5732

 − 53.1985

NA

KDQF01000814

Pristimantis

inguinalis

AF2054

 

Sipaliwini

Suriname

2.1751

 − 56.0832

NA

KDQF01000937

Pristimantis

inguinalis

AF2398

 

Nassau

Suriname

4.8170

 − 54.6037

NA

KDQF01000954

Pristimantis

inguinalis

AF2432

 

Nassau

Suriname

4.8041

 − 54.5555

NA

KDQF01001019

Pristimantis

inguinalis

AF2613

 

Atachi Bakka

French Guiana

3.5520

 − 53.9509

NA

KDQF01001043

Pristimantis

inguinalis

AF2659

 

Alikéné

French Guiana

3.2091

 − 52.4020

NA

KDQF01001121

Pristimantis

inguinalis

AF2858

 

Mitaraka

French Guiana

2.2358

 − 54.4493

NA

KDQF01001229

Pristimantis

inguinalis

AF3083

 

Mitan G

French Guiana

2.6284

 − 52.5540

NA

KDQF01001402

Pristimantis

inguinalis

AF3404

 

Bakhuis

Suriname

4.6837

 − 56.7721

NA

KDQF01001416

Pristimantis

inguinalis

AF3432

 

Bakhuis

Suriname

4.6837

 − 56.7721

NA

ON113921

Pristimantis

inguinalis

AF3531

 

Itoupe

French Guiana

3.0230

 − 53.0955

NA

ON113922

Pristimantis

inguinalis

AF3772

 

Voltzberg

Suriname

4.6817

 − 56.1857

NA

ON113923

Pristimantis

inguinalis

AF4777

 

Galbao

French Guiana

4.4880

 − 52.0445

NA

ON113925

Pristimantis

inguinalis

AF5402

 

Camp Savane Roche Dachine

French Guiana

3.4696

 − 53.2300

NA

ON113928

Pristimantis

inguinalis

AF5448

 

Trois-Saut

French Guiana

2.1969

 − 52.9017

NA

ON113929

Pristimantis

inguinalis

AF5524

 

Haute Courcibo

French Guiana

4.4723

 − 53.2459

NA

KDQF01001509

Pristimantis

inguinalis

AG102

 

Kaw

French Guiana

4.5710

 − 52.2206

NA

KDQF01001519

Pristimantis

inguinalis

AG225

 

Trinité

French Guiana

4.6709

 − 53.2843

JN690710

JN691317

Pristimantis

inguinalis

AG229

 

Trinité

French Guiana

4.6709

 − 53.2843

NA

KDQF01001538

Pristimantis

inguinalis

AG291

 

Trinité

French Guiana

4.6025

 − 53.4143

NA

KDQF01001595

Pristimantis

inguinalis

AG424

 

Atachi Bakka

French Guiana

3.6553

 − 53.8440

NA

KDQF01001643

Pristimantis

inguinalis

AG491

 

Saul

French Guiana

3.7193

 − 53.4128

NA

KDQF01001691

Pristimantis

inguinalis

AM015

 

Inini Tolenga

French Guiana

3.6632

 − 53.9283

NA

KDQF01002875

Pristimantis

inguinalis

 

MPEG30059

Serra do Acari. N ESEC Grão Pará

PA

1.2854

 − 58.6959

NA

KDQF01002876

Pristimantis

inguinalis

 

MPEG30060

Serra do Acari. N ESEC Grão Pará

PA

1.2854

 − 58.6959

NA

KDQF01003609

Pristimantis

inguinalis

 

MTR24299

Oiapoque

AP

3.8794

 − 51.7710

NA

KDQF01003778

Pristimantis

inguinalis

 

NZCS51

Brownsberg

Suriname

4.9365

 − 55.194826

NA

KDQF01004105

Pristimantis

inguinalis

QM0406

 

Montagne de fer

French Guiana

5.4074

 − 53.5548

NA

KDQF01004107

Pristimantis

inguinalis

QM0426

 

Montagne de fer

French Guiana

5.4074

 − 53.5548

NA

ON113942

Pristimantis

inguinalis

QM1074

 

Gaa_Kaba

French Guiana

4.4509

 − 54.4117

NA

JQ742170

Pristimantis

inguinalis

 

VUB3626

Cacao Mountain

French Guiana

4.5667

 − 52.4667

EU186739

EU186721

Pristimantis

jamescameroni

SBH268110

 

Bolivar, Aprada-tepui

Venezuela

5.4243

 − 62.4208

NA

ON113932

Pristimantis

jamescameroni

 

IRSNB4163

Bolivar, Aprada-tepui

Venezuela

5.4243

 − 62.4208

NA

JQ742169

Pristimantis

jester

 

VUB3493

Maringma-tepui

Guyana

5.21524

 − 60.5834

NA

MF037223

Pristimantis

marmoratus

CPI10703

 

Mt. Wokomung

Guyana

5.1175

 − 59.8225

EU186734

EU186716

Pristimantis

marmoratus

 

ROM43302

Mt. Wokomung

Guyana

5.1175

 − 59.8225

EU186741

EU186723

Pristimantis

marmoratus

 

KU181015

km 127, El Dorado-Santa Elena de Uairen Rd

Venezuela

5.8983

 − 61.4428

NA

JQ742166

Pristimantis

marmoratus

 

VUB3485

Kaieteur NP

Guyana

5.2686

 − 59.7686

NA

JQ742167

Pristimantis

marmoratus

 

VUB3491

Maringma-tepui

Guyana

5.2152

 − 60.5834

NA

KDQF01002108

Pristimantis

marmoratus

BPN3814

 

Bay Camp

Guyana

5.0112

 − 59.63930

NA

KDQF01002109

Pristimantis

marmoratus

BPN3815

 

Bay Camp

Guyana

5.0112

 − 59.6393

NA

KDQF01002110

Pristimantis

marmoratus

BPN3816

 

Bay Camp

Guyana

5.0112

 − 59.6393

NA

JQ742164

Pristimantis

pulvinatus

 

VUB3751

Iwokrama

Guyana

4.6714

 − 58.6850

NA

JQ742165

Pristimantis

pulvinatus

 

VUB3674

La Escalera

Venezuela

5.9158

 − 61.4347

NA

KDQF01004007

Pristimantis

pulvinatus

PK3509

 

Iwokrama

Guyana

4.6720

 − 58.6840

EU186692

EU186692

Pristimantis

saltissimus

 

ROM43913

Mt. Ayanganna

Guyana

5.3996

 − 59.9505

EU186693

EU186693

Pristimantis

saltissimus

 

ROM43310

Mt. Wokomung

Guyana

5.1175

 − 59.8225

NA

JQ742168

Pristimantis

saltissimus

 

VUB3490

Maringma-tepui

Guyana

5.2152

 − 60.5834

JN690708

JN691315

Pristimantis

crepitaculus

AF0021

 

Saul

French Guiana

3.6256

 − 53.2072

NA

KR811102

Pristimantis

crepitaculus

AF0563

 

Savane Virginie

French Guiana

4.1959

 − 52.1490

NA

KR811105

Pristimantis

crepitaculus

AF0757

 

St Georges

French Guiana

3.8112

 − 51.8896

NA

KDQF01000316

Pristimantis

crepitaculus

AF0910

MNHN-RA-2020.0093

Pic Coudreau du Sud

French Guiana

2.2534

 − 54.3534

NA

KDQF01000366

Pristimantis

crepitaculus

AF1014

 

Saul

French Guiana

3.6359

 − 53.2726

NA

KDQF01000382

Pristimantis

crepitaculus

AF1046

 

Saul

French Guiana

3.6112

 − 53.2886

NA

ON113933

Pristimantis

crepitaculus

AF1387

MNHN-RA-2020.0094

Aratai

French Guiana

3.9909

 − 52.5902

NA

ON113934

Pristimantis

crepitaculus

AF1388

MNHN-RA-2020.0095

Aratai

French Guiana

3.9909

 − 52.5902

NA

ON113935

Pristimantis

crepitaculus

AF1598

MNHN-RA-2020.0097

Nouragues

French Guiana

4.0848

 − 52.6806

NA

KDQF01000601

Pristimantis

crepitaculus

AF1607

MNHN-RA-2020.0100

Saul

French Guiana

3.5732

 − 53.1985

NA

KDQF01000749

Pristimantis

crepitaculus

AF1921

MNHN-RA-2020.0101

Flat de la Waki

French Guiana

3.0840

 − 53.4107

NA

KDQF01000754

Pristimantis

crepitaculus

AF1941

 

Flat de la Waki

French Guiana

3.0836

 − 53.4121

NA

KDQF01001103

Pristimantis

crepitaculus

AF2786

MNHN-RA-2020.0102

Mitaraka

French Guiana

2.2358

 − 54.4493

NA

ON113936

Pristimantis

crepitaculus

AF2799

MNHN-RA-2020.0103

Mitaraka

French Guiana

2.2358

 − 54.4493

NA

KDQF01001186

Pristimantis

crepitaculus

AF3002

 

Mémora D

AP

3.3129

 − 52.1804

NA

KDQF01001205

Pristimantis

crepitaculus

AF3047

 

Mitan G

French Guiana

2.6284

 − 52.5540

NA

KDQF01001276

Pristimantis

crepitaculus

AF3161

MNHN-RA-2020.0108

Mitan D

AP

2.6276

 − 52.5419

NA

KDQF01001437

Pristimantis

crepitaculus

AF3539

MNHN-RA-2020.0092

Itoupe

French Guiana

3.0230

 − 53.0955

NA

ON113924

Pristimantis

crepitaculus

AF5399

 

Camp Saut Richard

French Guiana

3.47363

 − 53.2086

NA

ON113927

Pristimantis

crepitaculus

AF5440

 

Trois-Saut

French Guiana

2.1969

 − 52.9017

JN690707

EU201063

Pristimantis

crepitaculus

AG_BM110

 

Kaw3

French Guiana

4.5481

 − 52.1519

NA

KDQF01001542

Pristimantis

crepitaculus

AG321

 

Kaw

French Guiana

4.5161

 − 52.1005

NA

KDQF01001568

Pristimantis

crepitaculus

AG378

 

Montagne Maripa

French Guiana

4.4088

 − 52.34301

NA

KDQF01001645

Pristimantis

crepitaculus

AG494

 

Saul

French Guiana

3.7193

 − 53.4128

NA

KDQF01001886

Pristimantis

crepitaculus

BOAM048

 

Borne 4

French Guiana

2.3709

 − 53.7728

NA

KDQF01002129

Pristimantis

crepitaculus

CAAM15

 

Montagne Cacao

French Guiana

2.3491

 − 53.2160

NA

EU201062

Pristimantis

crepitaculus

CM077

 

Trois-Sauts

French Guiana

2.2480

 − 52.8746

NA

KDQF01002243

Pristimantis

crepitaculus

CM171

 

Trijonction

French Guiana

2.3333

 − 54.6000

NA

KDQF01002504

Pristimantis

crepitaculus

FL04

 

Plote PPBIO

AP

0.9793

 − 51.6149

NA

KDQF01002521

Pristimantis

crepitaculus

FTA128

 

Rio Vila Nova

AP

0.4493

 − 52.0221

NA

KDQF01002528

Pristimantis

crepitaculus

FTA165

 

Rio Amapá Grande

AP

2.1271

 − 51.1913

NA

KDQF01002543

Pristimantis

crepitaculus

FTA239

 

Rio Amapá Grande

AP

2.1271

 − 51.1913

NA

ON113931

Pristimantis

crepitaculus

FTA96

 

Rio Vila Nova

AP

0.4493

 − 52.0221

NA

KDQF01003282

Pristimantis

crepitaculus

MTR13884

 

Lourenço

AP

2.32361

 − 51.6453

NA

KDQF01003293

Pristimantis

crepitaculus

MTR13930

 

Lourenço

AP

2.32361

 − 51.6453

NA

KR811104

Pristimantis

crepitaculus

MTR24285

 

Lourenço

AP

2.3216

 − 51.6109

NA

KR811103

Pristimantis

crepitaculus

MTR24300

 

Oiapoque

AP

3.8794

 − 51.7710

NA

KDQF01003952

Pristimantis

crepitaculus

PG748

 

St Georges

French Guiana

3.8061

 − 51.8934

NA

KDQF01004462

Pristimantis

crepitaculus

WAAM011

 

Flat de la Waki

French Guiana

3.18341

 − 53.4775

NA

KDQF01003322

Pristimantis

sp. Neblina 1

MTR15532

 

São Gabriel da Cachoeira

AM

0.7195

 − 66.0878

NA

KDQF01003323

Pristimantis

sp. Neblina 1

MTR15534

 

São Gabriel da Cachoeira

AM

0.7195

 − 66.0878

NA

KDQF01003325

Pristimantis

sp. Neblina 2

MTR15536

 

São Gabriel da Cachoeira

AM

0.7195

 − 66.0878

NA

KDQF01000102

Pristimantis

sp. “Guianas” East

AF0266

 

Nouragues

French Guiana

4.0917

 − 52.7000

NA

KDQF01000103

Pristimantis

sp. “Guianas” East

AF0268

 

Nouragues

French Guiana

4.0917

 − 52.7000

NA

KDQF01000104

Pristimantis

sp. “Guianas” East

AF0272

 

Nouragues

French Guiana

4.0917

 − 52.700

NA

KDQF01000354

Pristimantis

sp. “Guianas” East

AF0978

 

Saul

French Guiana

3.6359

 − 53.2726

NA

ON113917

Pristimantis

sp. “Guianas” East

AF1360

 

Grande Montagne Tortue

French Guiana

4.2927

 − 52.3496

NA

KDQF01000558

Pristimantis

sp. “Guianas” East

AF1505

 

Grande Montagne Tortue

French Guiana

4.2927

 − 52.3496

NA

KDQF01001024

Pristimantis

sp. “Guianas” East

AF2625

 

Atachi Bakka

French Guiana

3.5444

 − 53.9128

NA

ON113919

Pristimantis

sp. “Guianas” East

AF2626

 

Atachi Bakka

French Guiana

3.5444

 − 53.9128

NA

ON113920

Pristimantis

sp. “Guianas” East

AF2818

 

Mitaraka

French Guiana

2.2358

 − 54.4493

NA

ON113926

Pristimantis

sp. “Guianas” East

AF5414

 

Savane Roche Dachine

French Guiana

3.4696

 − 53.2298

NA

ON113930

Pristimantis

sp. “Guianas” East

AF5525

 

Haute Courcibo

French Guiana

4.4723

 − 53.2459

NA

KDQF01001850

Pristimantis

sp. “Guianas” East

BOAM001

 

Borne 4

French Guiana

2.3709

 − 53.7728

NA

KDQF01001860

Pristimantis

sp. “Guianas” East

BOAM012

 

Borne 4

French Guiana

2.3709

 − 53.7728

NA

KDQF01002249

Pristimantis

sp. “Guianas” East

CM184

 

Trijonction

French Guiana

2.3333

 − 54.6000

JN690709

JN691316

Pristimantis

sp. “Guianas” East

CM317

 

CisameG

French Guiana

4.1833

 − 52.3667

NA

ON113940

Pristimantis

sp. “Guianas” East

QM0423

 

Montagne de fer

French Guiana

5.4074

 − 53.5548

NA

ON113941

Pristimantis

sp. “Guianas” East

QM1073

 

Gaa Kaba

French Guiana

4.4520

 − 54.4193

ON117803

KDQF01004305

Pristimantis

sp. “Guianas” East

ST310

 

Parna Tumucumaque

AP

0.9091

 − 53.2285

NA

KDQF01004306

Pristimantis

sp. “Guianas” East

ST311

 

Parna Tumucumaque

AP

0.9091

 − 53.2285

NA

ON113937

Pristimantis

grandoculis

UFRJA024

NZCS A1211

Lelygebergte

Suriname

4.4158

 − 54.6498

NA

ON113938

Pristimantis

grandoculis

UFRJA023

NZCS A1210

Lelygebergte

Suriname

4.4158

 − 54.6498

NA

KDQF01002880

Pristimantis

grandoculis

 

MPEG30085

Serra do Acari

PA

1.2854

 − 58.6959

NA

KDQF01002881

Pristimantis

grandoculis

 

MPEG30088

Serra do Acari

PA

1.2854

 − 58.6959

NA

KDQF01003777

Pristimantis

grandoculis

 

NZCS50

Brownsberg

Suriname

4.9366

 − 55.1948

NA

KDQF01003795

Pristimantis

grandoculis

 

NZCS A1019

Tafelberg

Suriname

3.8049

 − 56.1539

NA

KDQF01003796

Pristimantis

grandoculis

 

NZCS A1212

Tafelberg

Suriname

3.8049

 − 56.1539

NA

KDQF01001388

Pristimantis

grandoculis

AF3365

 

Bakhuis

Suriname

4.6562

 − 56.7865

NA

KDQF01001400

Pristimantis

grandoculis

AF3402

 

Bakhuis

Suriname

4.6837

 − 56.7721

NA

KDQF01001403

Pristimantis

grandoculis

AF3408

 

Bakhuis

Suriname

4.6837

 − 56.7721

NA

KDQF01001417

Pristimantis

grandoculis

AF3435

MNHN-RA-2020.0118

Bakhuis

Suriname

4.6837

 − 56.7721

EU186676

EU186676

Pristimantis

sp. Ayangana

 

ROM40164

Mt. Ayanganna

Guyana

5.3995

 − 59.9505

ON117804

KDQF01004221

Pristimantis

cf. ockendeni

 

SMNS11989

Mabura Hill forest reserve

Guyana

5.1553

 − 58.6997

ON117805

KDQF01004222

Pristimantis

cf. ockendeni

 

SMNS11990

Mabura Hill forest reserve

Guyana

5.1553

 − 58.6997

ON117806

KDQF01004223

Pristimantis

cf. ockendeni

 

SMNS11994

Mabura Hill forest reserve

Guyana

5.1553

 − 58.6997

ON117807

KDQF01000865

Pristimantis

cf. ockendeni

AF2155

 

Sipaliwini

Suriname

2.02682

 − 56.1256

NA

KDQF01003210

Pristimantis

cf. ockendeni

MTR12690

 

Igarapé Açu, Rio Abacaxis

AM

 − 4.3442

 − 58.6350

NA

KDQF01001829

Pristimantis

cf. ockendeni

BM153

 

UHE Belo Monte, Vitória do Xingu, Rio Xingu

PA

 − 2.9506

 − 51.9366

NA

KDQF01004256

Pristimantis

cf. ockendeni

SMS155

 

Campo Catuquira

AM

 − 4.9136

 − 61.1092

NA

KDQF01004257

Pristimantis

cf. ockendeni

SMS156

 

Campo Catuquira

AM

 − 4.9136

 − 61.1092

NA

KDQF01002705

Pristimantis

cf. ockendeni

JOG847

 

MINA PALITO

PA

 − 6.3173

 − 55.7986

NA

KDQF01003224

Pristimantis

cf. ockendeni

MTR12855

 

São Sebastião, Rio Abacaxis

AM

 − 4.3089

 − 58.6364

NA

KDQF01000889

Pristimantis

cf. ockendeni

AF2257

 

Sipaliwini

Suriname

2.0244

 − 56.1251

NA

KDQF01002605

Pristimantis

cf. ockendeni

H2773

 

UHE Jirau

RO

 − 9.4459

 − 64.8247

NA

JQ742160

Pristimantis

yuruaniensis

 

VUB3717

Yuruani-tepui

Venezuela

5.3139

 − 60.8639

NA

JQ742161

Pristimantis

yuruaniensis

 

VUB3720

Yuruani-tepui

Venezuela

5.3139

 − 60.8639

Appendix 2 Specimens examined and types

Genus

Species

Museum

Field N

Sex

Type

Locality

Country

Lat

Lon

Collector

Date

Acoustic

Pristimantis

crepitaculus

MNHN-RA-2020.0093

AF0910

F

Paratype

Pic Coudreau du Sud

French Guiana

2.2534

 − 54.3534

M. Blanc

01_02_2013

 

Pristimantis

crepitaculus

MNHN-RA-2020.0104

AF2815

F

Paratype

Mitaraka

French Guiana

2.2358

 − 54.4493

A. Fouquet − M. Dewynter − N. Vidal

28_02_2015

 

Pristimantis

crepitaculus

MNHN-RA-2020.0105

AF2816

F

Paratype

Mitaraka

French Guiana

2.2358

 − 54.4493

A. Fouquet − M. Dewynter − N. Vidal

28_02_2015

 

Pristimantis

crepitaculus

MNHN-RA-2020.0094

AF1387

M

Paratype

Aratai

French Guiana

3.9909

 − 52.5902

A. Fouquet − J. Devillechabrolle

16_12_2013

 

Pristimantis

crepitaculus

MNHN-RA-2020.0095

AF1388

M

Paratype

Aratai

French Guiana

3.9909

 − 52.5902

A. Fouquet − J. Devillechabrolle

16_12_2013

 

Pristimantis

crepitaculus

MNHN-RA-2020.0096

AF1597

M

Paratype

Nouragues

French Guiana

4.0848

 − 52.6806

E. Courtois

09_02_2014

 

Pristimantis

crepitaculus

MNHN-RA-2020.0097

AF1598

M

Paratype

Nouragues

French Guiana

4.08489

 − 52.6806

E. Courtois

09_02_2014

 

Pristimantis

crepitaculus

MNHN-RA-2020.0098

AF1599

M

Paratype

Nouragues

French Guiana

4.08489

 − 52.6806

E. Courtois

09_02_2014

 

Pristimantis

crepitaculus

MNHN-RA-2020.0099

AF1606

M

Paratype

Saul

French Guiana

3.5732

 − 53.1985

A. Fouquet − E. Courtois − J.P. Vacher

20_02_2014

MNHN-SO-2022-559

Pristimantis

crepitaculus

MNHN-RA-2020.0100

AF1607

M

Paratype

Saul

French Guiana

3.5732

 − 53.1985

A. Fouquet − E. Courtois − J.P. Vacher

20_02_2014

 

Pristimantis

crepitaculus

MNHN-RA-2020.0101

AF1921

M

Paratype

Flat de la Waki

French Guiana

3.0840

 − 53.4107

J.P. Vacher

07_04_2014

 

Pristimantis

crepitaculus

MNHN-RA-2020.0102

AF2786

M

Holotype

Mitaraka

French Guiana

2.2358

 − 54.4493

A. Fouquet − M. Dewynter − N. Vidal

26_02_2015

MNHN-SO-2019–23

Pristimantis

crepitaculus

MNHN-RA-2020.0103

AF2799

M

Paratype

Mitaraka

French Guiana

2.2358

 − 54.4493

A. Fouquet − M. Dewynter − N. Vidal

27_02_2015

 

Pristimantis

crepitaculus

MNHN-RA-2020.0106

AF2860

M

Paratype

Mitaraka

French Guiana

2.2358

 − 54.4493

A. Fouquet − M. Dewynter − N. Vidal

04_03_2015

 

Pristimantis

crepitaculus

MNHN-RA-2020.0107

AF3054

M

Paratype

Mitan G

French Guiana

2.6284

 − 52.5540

A. Fouquet − P. Nunes

20_03_2015

 

Pristimantis

crepitaculus

MNHN-RA-2020.0108

AF3161

M

Paratype

Mitan D

AP

2.6276

 − 52.5419

A. Fouquet − P. Nunes

23_03_2015

 

Pristimantis

crepitaculus

MNHN-RA-2020.0109

AF3530

M

Paratype

Itoupe

French Guiana

3.0230

 − 53.0955

A Fouquet − E Courtois − B Villette − M Dewynter

06_01_2016

MNHN-SO-2022-561

Pristimantis

crepitaculus

MNHN-RA-2020.0092

AF3539

M

Paratype

Itoupe

French Guiana

3.0230

 − 53.0955

A Fouquet − E Courtois − B Villette − M Dewynter

06_01_2016

MNHN-SO-2022-560

Pristimantis

crepitaculus

MNHN-RA-2020.0110

AF3548

M

Paratype

Itoupe

French Guiana

3.02218

 − 53.1105

A Fouquet − E Courtois − B Villette − M Dewynter

06_01_2016

 

Pristimantis

crepitaculus

MNHN-RA-2020.0111

AF3664

M

Paratype

Itoupe

French Guiana

3.0256

 − 53.0525

A Fouquet − E Courtois − B Villette − M Dewynter

11_01_2016

 

Pristimantis

crepitaculus

MNHN-RA-2020.0112

AF3687

M

Paratype

Itoupe

French Guiana

3.0230

 − 53.0955

A Fouquet − E Courtois − B Villette − M Dewynter

14_01_2016

 

Pristimantis

grandoculis

MNHN-RA-2020.0118

AF3435

M

 

Bakhuis

Suriname

4.7246

 − 56.7638

A. Fouquet − S. Cally − R. Jairam

30_04_2015

 

Pristimantis

grandoculis

RMNH 4467

 

M

Holotype

Coppenname

Suriname

     

Pristimantis

grandoculis

NZCSA1212

 

M

 

Tafleberg

Suriname

3.8049

 − 56.1539

P. Ouboter − V. Kadosoe

  

Pristimantis

crepitaculus

MPEG 41,819

PLVP 289

M

Paratype

Oiapoque

Brazil

3.79889

 − 51.87993

P. Peloso − L. Brandão

04_12_2015

 

Pristimantis

crepitaculus

MPEG 41,820

PLVP 290

M

Paratype

Oiapoque

Brazil

3.79889

 − 51.87993

P. Peloso − L. Brandão

05_12_2015

 

Pristimantis

crepitaculus

MPEG 41,821

PLVP 301

M

Paratype

Oiapoque

Brazil

3.79889

 − 51.87993

P. Peloso − L. Brandão

05_12_2015

 

Pristimantis

crepitaculus

MPEG 41,822

PLVP 352

M

Paratype

Oiapoque

Brazil

3.79889

 − 51.87993

P. Peloso − L. Brandão

06_12_2015

MNHN-SO-2022-562

Pristimantis

crepitaculus

MPEG 41,823

PLVP 353

M

Paratype

Oiapoque

Brazil

3.79889

 − 51.87993

P. Peloso − L. Brandão

06_12_2015

MNHN-SO-2022-563

Pristimantis

crepitaculus

MPEG 41,824

PLVP 354

M

Paratype

Oiapoque

Brazil

3.79889

 − 51.87993

P. Peloso − L. Brandão

06_12_2015

 

Pristimantis

crepitaculus

MPEG 41,825

PLVP 355

F

Paratype

Oiapoque

Brazil

3.79889

 − 51.87993

P. Peloso − L. Brandão

06_12_2015

 

Pristimantis

grandoculis

NZCS A1210

UFRJA023

M

 

Lely Mountain

Suriname

4.2667

 − 54.7333

R. Jairam – D. Baeta

  

Pristimantis

grandoculis

NZCS A1211

UFRJA024

M

 

Lely Mountain

Suriname

4.2667

 − 54.7333

R. Jairam – D. Baeta

  

Pristimantis

cf. ockendeni

MNHN-RA-2020.0113

AF2155

F

 

Sipaliwini

Suriname

2.0268

 − 56.1256

A. Fouquet − J.P. Vacher

23_04_2014

 

Pristimantis

cf. ockendeni

MNHN-RA-2020.0114

AF2258

F

 

Sipaliwini

Suriname

2.0244

 − 56.1251

A. Fouquet − J.P. Vacher

27_04_2014

 

Pristimantis

cf. ockendeni

MTD47769

 

F

 

Mabura Hill forest reserve

Guyana

5.1553

 − 58.6997

R Ernst

18 08 2010

 

Pristimantis

cf. ockendeni

SMNS11990

 

F

 

Mabura Hill forest reserve

Guyana

5.1553

 − 58.6997

R Ernst

25 04 2003

 

Pristimantis

cf. ockendeni

SMNS11991

 

F

 

Mabura Hill forest reserve

Guyana

5.1553

 − 58.6997

R Ernst

25 04 2003

 

Pristimantis

cf. ockendeni

SMNS11995

 

F

 

Mabura Hill forest reserve

Guyana

5.15538

 − 58.6997

R Ernst

01 06 2004

 

Pristimantis

cf. ockendeni

MNHN-RA-2020.0115

AF2255

M

 

Sipaliwini

Suriname

2.0244

 − 56.12518

A. Fouquet − J.P. Vacher

27_04_2014

MNHN-SO-2021-XXX

Pristimantis

cf. ockendeni

MNHN-RA-2020.0116

AF2256

M

 

Sipaliwini

Suriname

2.02449

 − 56.1251

A. Fouquet − J.P. Vacher

27_04_2014

 

Pristimantis

cf. ockendeni

MNHN-RA-2020.0117

AF2289

M

 

Sipaliwini

Suriname

2.0334

 − 56.1318

A. Fouquet − J.P. Vacher

30_04_2014

MNHN-SO-2021-XXX

Pristimantis

cf. ockendeni

MTD47770

 

M

 

Mabura Hill forest reserve

Guyana

5.1553

 − 58.6997

R Ernst

18 08 2010

 

Pristimantis

cf. ockendeni

SMNS11987

 

M

 

Mabura Hill forest reserve

Guyana

5.1553

 − 58.6997

R Ernst

18 11 2002

 

Pristimantis

cf. ockendeni

SMNS11989

 

M

 

Mabura Hill forest reserve

Guyana

5.1553

 − 58.6997

R Ernst

17 04 2003

 

Pristimantis

cf. ockendeni

SMNS11993

 

M

 

Mabura Hill forest reserve

Guyana

5.1553

 − 58.6997

R Ernst

26 03 2004

 

Pristimantis

cf. ockendeni

SMNS11994

 

M

 

Mabura Hill forest reserve

Guyana

5.1553

 − 58.6997

R Ernst

01 06 2004

 

Appendix 3 Call recordings list

Pristimantis crepitaculus

  • PLPDR 126 (MPEG 41822), Paratype, Oiapoque – Amapá, Brazil MNHN-SO-2022-562

  • PLPDR 128 (MPEG 41823), Paratype, Oiapoque – Amapá, Brazil MNHN-SO-2022-563

  • track59 Marty and Gaucher (NA), Kaw montain − French Guiana

  • 160106_0692 (AF3530), Itoupé − French Guiana MNHN-SO-2022-561

  • 160106_0693(AF3539), Holotype, Itoupé − French Guiana MNHN-SO-2022-560

  • LS110010 (AF1606), Saul Limonade − French Guiana MNHN-SO-2022-559

Appendix 4

Mean pairwise p distance

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Fouquet, A., Peloso, P., Jairam, R. et al. Back from the deaf: integrative taxonomy revalidates an earless and mute species, Hylodes grandoculis van Lidth de Jeude, 1904, and confirms a new species of Pristimantis Jiménez de la Espada, 1870 (Anura: Strabomantidae) from the Eastern Guiana Shield. Org Divers Evol 22, 1065–1098 (2022). https://doi.org/10.1007/s13127-022-00564-w

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