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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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.
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.
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.
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.
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.
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.
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.
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.
Elmer, K. R., & Cannatella, D. C. (2008). Three new species of leaflitter frogs from the upper Amazon forests: Cryptic diversity within Pristimantis “ockendeni”(Anura: Strabomantidae) in Ecuador. Zootaxa, 1784, 11–38.
Emerson, S. B. (1985). Skull shape in frogs: Correlations with diet. Herpetologica, 41, 177–188.
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.
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.
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.
Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39, 783–791.
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.
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
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.
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.
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.
Fouquet, A., Vidal, N., & Dewynter, M. (2019). The amphibians of the Mitaraka massif, French Guiana. Zoosystema, 41, 359–374.
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.
Frost, D. R. (1985). Amphibian Species of the World. Lawrence, Kansas, U.S.A. Association of Systematics Collections and Allen Press.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Katoh, K., Rozewicki, J., & Yamada, K. D. (2017). MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinformatics, 20, 1160–1166.
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.
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.
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.
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.
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.
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.
Lê, S., Josse, J., & Husson, F. (2008). FactoMineR: An R package for multivariate analysis. Journal of Statistical Software, 25, 1–18.
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.
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.
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.
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.
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.
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.
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.
Rivero, J. A. (1968). A new species of Eleutherodactylus (Amphibia, Salientia) from the Guayana Region, Edo. Bolívar. Venezuela. Breviora, 306, 1–10.
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.
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.
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.
Strauss, R. E. (1985). Evolutionary allometry and variation in body form in the South American catfish genus Corydoras (Callichthyidae). Systematic Biology, 34, 381–396.
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.
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.
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.
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.
van Lidth de Jeude, T. W. (1904). Reptiles and batrachians from Surinam. Notes from the Leyden Museum, 25, 83–94.
Vences, M., & Wake, D. B. (2007). Speciation, species boundaries and phylogeography of amphibians. Amphibian Biology, 7, 2613–2671.
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.
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
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.
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).
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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
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PLPDR 126 (MPEG 41822), Paratype, Oiapoque – Amapá, Brazil MNHN-SO-2022-562
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PLPDR 128 (MPEG 41823), Paratype, Oiapoque – Amapá, Brazil MNHN-SO-2022-563
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track59 Marty and Gaucher (NA), Kaw montain − French Guiana
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160106_0692 (AF3530), Itoupé − French Guiana MNHN-SO-2022-561
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160106_0693(AF3539), Holotype, Itoupé − French Guiana MNHN-SO-2022-560
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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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DOI: https://doi.org/10.1007/s13127-022-00564-w