Amphibians of caves in Serra do Ramalho karst area, a remarkable region of subterranean fauna in Brazil

Authors

  • Ariadne F. Sabbag
  • Jonas E. Gallão
  • Délio Baêta
  • Célio F. B. Haddad
  • Maria E. Bichuette

Keywords:

Anurans, Cerrado-Caatinga, Limestone caves, Refugia, Bahia state

Abstract

Serra do Ramalho karst area is part of the Bambuí group, the largest geomorphological unit of Brazil. It is in southwestern state of Bahia, and extends over the municipalities of Carinhanha, Feira da Mata, Coribe, and Serra do Ramalho. We inspected 34 caves of Serra do Ramalho karst area, actively looking for amphibians. We were able to find amphibians in 12 caves. We sequenced some of the specimens found for the barcode mitochondrial 16S to confirm identifications. We found 13 species of amphibians, all anurans: Rhinella granulosa, Rhinella mirandaribeiroi, Oreobates remotus, Boana crepitans, Scinax sp. 26, Scinax x-signatus, Leptodactylus macrosternum, L. troglodytes, L. vastus, Physalaemus cicada, P. cuvieri, P. albifrons, and Odontophrynus carvalhoi. As far as it is possible to say, these amphibians are using the cave to daily and seasonal retreat, where they can possibly protect themselves from the drought and heat of Caatinga during the day.

References

Andrade, M.C.M.d.; Costa, J.C.R. & Eterovick, P.C. 2021. Fidelity in the use of iron caves by Bokermannohyla martinsi (Anura: Hylidae): a step further in unveiling the importance of Brazilian caves for the herpetofauna. Salamandra 57: 502-512.

Araujo-Vieira, K.; Lourenço, A.C.C.; Lacerda, J.V.A.; Lyra, M.L.; Blotto, B.L.; Ron, S.R.; Baldo, D.; Pereyra, M.O.; Suárez- Mayorga, Á.M.; Baêta, D.; Ferreira, R.B.; Barrio-Amorós, C.L.; Borteiro, C.; Brandão, R.A.; Brasileiro, C.A.; Donnelly, M.A.; Dubeux, M.J.M.; Köhler, J.; Kolenc, F.; Fortes Leite, F.S.; Maciel, N.M.; Nunes, I.; Orrico, V.G.D.; Peloso, P.; Pezzuti, T.L.; Reichle, S.; Rojas-Runjaic, F.J.M.; Da Silva, H.R.; Sturaro, M.J.; Langone, J.A.; Garcia, P.C.A.; Rodrigues, M.T.; Frost, D.R.; Wheeler, W.C.; Grant, T.; Pombal, J.P.; Haddad, C.F.B. & Faivovich, J. 2023. Treefrog diversity in the Neotropics: phylogenetic relationships of Scinaxini (Anura: Hylidae: Hylinae). South American Journal of Herpetology 27: 1-145.

Araujo-Vieira, K.; Pombal Jr, J.P.; Caramaschi, U.; Novaes-e- Fagundes, G.; Orrico, V.G.D. & Faivovich, J. 2020. A neotype for Hyla x-signata Spix, 1824 (Amphibia, Anura, Hylidae). Papéis Avulsos de Zoologia 60: e20206056. Assis, L.d.; von Schimonsky, D.M. & Bichuette, M.E. 2021. The first troglobitic Pseudochthonius Balzan, 1892 (Pseudoscorpiones, Chthoniidae) from the karst area of Serra do Ramalho, Brazil: a threatened species. Subterranean Biology 40: 109-128.

Assis, L.d.; von Schimonsky, D.M.; Gallão, J.E. & Bichuette, M.E. 2023. Contribution to the knowledge of Brazilian troglobitic Pseudoscorpiones (Arachnida): description of Pseudochthonius lubueno sp. nov. (Chthoniidae) from Serra do Ramalho karst area, state of Bahia, Brazil. Zoologia 40: e22048.

Auler, A.S. 2002. Karst areas in Brazil and the potential for major caves - an overview. Boletín de la Sociedad Venezolana de Espeleología 36: 29-35.

Auler, A.S. & Piló, L.B. 2015. Lagoa Santa Karst: cradle of Brazilian cave studies. In: Vieira, B.C.; Salgado, A.A.R. & Santos, L.J.C. (eds.), Landscapes and Landforms of Brazil. Springer Science and Business Media Dordrecht.

Baptista, R.L.C. & Giupponi, A.P.d.L. 2002. A new troglomorphic Charinus from Brazil (Arachnida: Amblypygi: Charinidae). Revista Ibérica de Aracnología 6: 105-110.

Barcelos, L.A.; Almeida-Silva, D.; Santos, C.M.D. & Verdade, V.K. 2020. Description of a new species of fossil Ceratophrys (Anura: Ceratophryidae) from Versalles Cave, São Paulo, Brazil. Journal of Vertebrate Paleontology 40: e1811293.

Barcelos, L.A. & Verdade, V.K. 2022. A new fossil of Ceratophrys Wied-Neuwied (Ceratophryidae: Anura) from Southeastern Brazil. Zootaxa 5094: 495-500.

Beck, H.E.; Zimmermann, N.E.; McVicar, T.R.; Vergopolan, N.; Berg, A. & Wood, E.F. 2018. Present and future Koppen- Geiger climate classification maps at 1-km resolution. Scientific Data 5: 180214.

Bertani, R.; von Schimonsky, D.M.; Gallao, J.E. & Bichuette, M.E. 2018. Four new troglophilic species of Loxosceles Heinecken & Lowe, 1832: contributions to the knowledge of recluse spiders from Brazilian caves (Araneae, Sicariidae). Zookeys 806: 47-72.

Bichuette, M.E. & Rizzato, P.P. 2012. A new species of cave catfish from Brazil, Trichomycterus rubbioli sp.n., from Serra do Ramalho karstic area, São Francisco River basin, Bahia state (Siluriformes: Trichomycteridae). Zootaxa 3480: 48-66.

Bichuette, M.E.; Sperandei, V.d.F.; Bertolini, D.L.V.B.V.; Simão, P.X.A. & Sabbag, A.F. 2022. Frogs of seven granitic caves on Santa Catarina Island, Florianópolis municipality, Santa Catarina state, southern Brazil. Herpetology Notes 15: 353-359.

Bichuette, M.E. & Trajano, E. 2005. A new cave species of Rhamdia (Siluriformes: Heptapteridae) from Serra do Ramalho, northeastern Brazil, with notes on ecology and behavior. Neotropical Ichthyology 3: 587-595.

Bokermann, W.C.A. 1966. Lista anotada das localidades tipo de anfíbios brasileiros. Serviço de Documentação - RUSP. São Paulo.

Brescovit, A.D.; Gallão, J.E. & Cizauskas, I. 2023. A new species of Pinelema Wang & Li, 2012, a relictual telemid spider inhabiting caves in Brazil (Araneae, Telemidae). Zootaxa 5383: 352-364.

Campos-Filho, I.S.; Bichuette, M.E. & Taiti, S. 2016. Three new species of terrestrial isopods (Crustacea, Isopoda, Oniscidea) from Brazilian caves. Nauplius 24: e2016001.

Campos-Filho, I.S.; Gallo, J.S.; Gallão, J.E.; Torres, D.F.; Carpio- Diaz, Y.M.; Lopez-Orozco, C.M.; Borja-Arrieta, R.; Taiti, S. & Bichuette, M.E. 2022a. Expanding the knowledge on the diversity of the cavernicolous Styloniscidae Vandel, 1952 (Oniscidea, Synocheta) from Brazil, with descriptions of two new species from the semiarid karst regions. Zookeys 1101: 35-55.

Campos-Filho, I.S.; Gallo, J.S.; Gallão, J.E.; Torres, D.F.; Horta, L.; Carpio-Díaz, Y.M.; López-Orozco, C.M.; Borja-Arrieta, R.; Aguiar, J.O. & Bichuette, M.E. 2022b. Unique and fragile diversity emerges from Brazilian caves - two new amphibious species of Xangoniscus Campos-Filho, Araujo & Taiti, 2014 (Oniscidea, Styloniscidae) from Serra do Ramalho karst area, state of Bahia, Brazil. Subterranean Biology 42: 1-22.

Canedo, C.; Targino, M.; Leite, F.S.F. & Haddad, C.F.B. 2012. A new species of Ischnocnema (Anura) from the São Francisco basin karst region, Brazil. Herpetologica 68: 393-400.

Cardoso, G.M.; Bastos-Pereira, R. & Ferreira, R.L. 2022. A new species of Chaimowiczia from the karstic Serra do Ramalho plateau, Brazil (Oniscidea, Synocheta, Styloniscidae). Subterranean Biology 42: 139-149.

Cardoso, G.M.; Bastos-Pereira, R. & Ferreira, R.L. 2023. Cave-dwellers Diploexochus (Isopoda, Armadillidae): new species and new records of the genus from Brazil. Nauplius 31: e2023008.

Cordeiro, I.R.S.; Bichuette, M.E. & Moreira, F.F.F. 2023. A new species of Spelaeometra Polhemus & Ferreira, 2018 (Hemiptera: Heteroptera: Hydrometridae) from a hotspot of troglobites in Brazil, Serra do Ramalho karst area. Animals 13: 3199.

Dessen, E.M.B.; Eston, V.R.; Silva, M.S.; Temperini-Beck, M.T. & Trajano, E. 1980. Levantamento preliminar da fauna de cavernas de algumas regiões do Brasil. Ciência e Cultura 32: 714-725.

Dotmatics. 2023. Geneious Prime. Versão 2023.2.1.

Fernandes, C.S.; Campos-Filho, I.S.; Araujo, P.B. & Bichuette, M.E. 2019. Synopsis of terrestrial isopods (Crustacea: Isopoda: Oniscidea) from Brazilian caves, with emphasis on new records from north, midwest, northeast and southeast regions. Journal of Natural History 53: 1095-1129.

Ferreira, R.L.; Souza-Silva, M. & Zampaulo, R.d.A. 2022. A vida subterrânea no carste de Pains: biodiversidade, ameaças e conservação de fauna em uma notável paisagem cárstica tropical. In: Piló, L.B.Cruz, J.B. (eds.), A região cárstica de Pains. ICMBio. Brasília

Frost, D.R. 2025. Amphibian Species of the World: an Online Reference. Version 6.2. Avaiable at: https://amphibiansoftheworld.amnh.org/index.php. Access in: April 4th, 2025.

Gallão, J.E. & Bichuette, M.E. 2018. Brazilian obligatory subterranean fauna and threats to the hypogean environment. Zookeys 1-23.

Gouveia, S.F.; Rocha, P.A.d.; Mikalauskas, J.S. & Silveira, V.V.-B. 2009. Rhinella jimi (cururu toad) and Leptodactylus vastus (Northeastern pepper frog). Predation on bats. Herpetological Review 40: 210.

Haddad, C.F.B.; Toledo, L.F.; Prado, C.P.A.; Loebmann, D.; Gasparini, J.L. & Sazima, I. 2013. Guia dos Anfíbios da Mata Atlântica - Diversidade e Biologia. Anolis Books. São Paulo.

Hillman, S.S.; Withers, P.C.; Drewes, R.C. & Hillyard, S.D. 2009. Ecological and environmental physiology of amphibians. Oxford University Press Inc. New York.

Jared, C.; Mailho‐Fontana, P.L.; Mendelson, J. & Antoniazzi, M.M. 2019. Life history of frogs of the Brazilian semi‐arid (Caatinga), with emphasis in aestivation. Acta Zoologica 101: 302-310.

Lamas, C.J.E.; Mendes, L.L.; Falaschi, R.L. & Evenhuis, N.L. 2023. A second new species of Tamanduamyia Rafael and Limeira-de-Oliveira (Diptera, Mythicomyiidae, Mythicomyiinae) from Brazil, with discussion of the possible first cave dwelling record of a micro-bee fly. Neotropical Entomology 52: 560-570.

Lima, A.M.X.; Araujo, C.d.O. & Verdade, V.K. 2012. Cycloramphus eleutherodactylus (alto button frog): calling among rocks and caves. Natural History Notes 39-42.

Linares, A.M. & Mello, H.E.S.d. 2011. Physalaemus cicada Bokermann, 1966 (Anura: Leiuperidae): Distribution extension with new south limit and geographic distribution map. Check List 7: 859-861.

Lisboa, B.S. & Haddad, C.F.B. 2009. Amphiba, Anura, Leiuperidae, Physalaemus cicada Bokermann, 1966: Distribution extension and geographic distribution map. Check List 5: 699-701.

Lyra, M.L.; Haddad, C.F.B. & de Azeredo-Espin, A.M.L. 2017. Meeting the challenge of DNA barcoding Neotropical amphibians: polymerase chain reaction optimization and new COI primers. Molecular Ecology Resources 17: 966-980.

Magalhães, F.d.M.; Lyra, M.L.; Carvalho, T.R.d.; Baldo, D.; Brusquetti, F.; Burella, P.; Colli, G.R.; Gehara, M.C.; Giaretta, A.A.; Haddad, C.F.B.; Langone, J.A.; López, J.A.; Napoli, M.F.; Santana, D.J.; de Sá, R.O. & Garda, A.A. 2020. Taxonomic review of South American butter frogs: phylogeny, geography patterns, and species delimitation in the Leptodactylus latrans species group (Anura: Leptodactylidae). Herpetological Monographs 34: 131-177.

Matavelli, R.; Campos, A.M.; Feio, R.N. & Ferreira, R.L. 2015. Occurrence of anurans in Brazilian caves. Acta Carsologica 44: 107-120.

Mattox, G.M.T.; Bichuette, M.E.; Secutti, S. & Trajano, E. 2008. Surface and subterranean ichthyofauna in the Serra do Ramalho karst area, northeastern Brazil, with updated lists of Brazilian troglobitic and troglophilic fishes. Biota Neotropica 8: 145-152.

Motta, A.P.; Lyra, M.; Gazoni, T.; Parise-Maltempi, P.P. & Haddad, C.F.B. 2020. New distribution records of Oreobates antrum Vaz-Silva, Maciel, Andrade, and Amaro, 2018, a cave-associated species from the Seasonally Dry Tropical Forest in the Brazilian Cerrado (Anura: Brachycephalidae: Craugastoridae). Herpetology Notes 13: 561-563.

Narvaes, P. & Rodrigues, M.T. 2009. Taxonomic revision of Rhinella granulosa species group (Amphibia, Anura, Bufonidae), with a description of a new species. Arquivos de Zoologia 40: 1-73.

Navas, C.A.; Antoniazzi, M.M. & Jared, C. 2004. A preliminary assessment of anuran physiological and morphological adaptation to the Caatinga, a Brazilian semi-arid environment. International Congress Series 1275: 298-305.

NCBI; Camacho, C.; Madden, T.; Tao, T.; Agarwala, R. & Morgulis, A. 2019. BLAST Command Line Applications User Manual. National Center for Biotechnology Information. Bethesda, MD.

Nunes-de-Almeida, C.H.L.; Haddad, C.F.B. & Toledo, L.F. 2021. A revised classification of the amphibian reproductive modes. Salamandra 57: 413-427.

Oliveira, L.A.d.; Hoyos-Benjumea, D.; Zepon, T.; Bichuette, M.E. & Vieira, L. 2023. New records of ground beetles genera (Coleoptera: Carabidae: Scaritinae: Clivinini) from Brazilian caves. EntomoBrasilis 16: 1-11.

Orrico, V.G.D.; Nunes, I.; Mattedi, C.; Fouquet, A.; Lemos, A.W.; Rivera-Correa, M.; Lyra, M.L.; Loebmann, D.; Pimenta, B.V.S.; Caramaschi, U.; Rodrigues, M.T. & Haddad, C.F.B. 2017. Integrative taxonomy supports the existence of two distinct species within Hypsiboas crepitans (Anura: Hylidae). Salamandra 53: 99-113.

Palmeira, C.N.S.; Gonçalves, U. & Paz, V.N. 2011. Physalaemus albifrons Spix, 1824 (Anura: Leiuperidae): Distribution and geographic extension. Check List 7: 839-840.

Palumbi, S.; Martin, A.; Romano, S.; McMillan, W.O.; Stice, L. & Grabowski, G. 2002. The simple fool’s guide to PCR. University of Hawaii. Honolulu, Hawaii.

Pansonato, A.; Motta, A.; Cacciali, P.; Haddad, C.F.B.; Strüssmann, C. & Jansen, M. 2020. On the identity of species of Oreobates (Anura: Craugastoridae) from Central South America, with the description of a new species from Bolivia. Journal of Herpetology 54: 393-412.

Pellegrini, T.G.; Bichuette, M.E. & Vieira, L. 2022. Coarazuphium bambui (Carabidae: Zuphiini), a new cave-dwelling beetle from the threatened region of Serra do Ramalho, Brazil. Zootaxa 5129: 557-568.

Pereyra, M.O.; Baldo, D.; Blotto, B.L.; Iglesias, P.P.; Thomé, M.T.C.; Haddad, C.F.B.; Barrio-Amorós, C.; Ibáñez, R. & Faivovich, J. 2016. Phylogenetic relationships of toads of the Rhinella granulosa group (Anura: Bufonidae): a molecular perspective with comments on hybridization and introgression. Cladistics 32: 36-53.

Pinto-da-Rocha, R. 1995. Sinopse da fauna cavernícola do Brasil (1907-1994). Papéis Avulsos de Zoologia 39: 61-173.

Racovitza, E.G. 1907. Essai sur les problèmes biospéologiques. Archives de Zoologie Experimentale et Génerale 6: 371-488.

Rubbioli, E.; Auler, A.; Menin, D. & Brandi, R. 2019. Cavernas. Atlas do Brasil subterrâneo. Instituto Chico Mendes de Conservação da Biodiversidade. Brasília, Brasil.

Salvador, R.B. & Bichuette, M.E. 2024. Idiopyrgus Pilsbry, 1911 (Gastropoda, Tomichiidae): a relict genus radiating into subterranean environments. Zoosystematics and Evolution 100: 1543-1556.

Salvador, R.B.; Santos Silva, F. & Bichuette, M.E. 2023. Taxonomic study on a collection of terrestrial and freshwater gastropods from caves in Bahia state, Brazil, with the description of a new species. Folia Malacologica 31: 48-60.

Santos, D.L.; Andrade, S.P.; Rocha, C.F.; Maciel, N.M.; Caramaschi, U. & Vaz-Silva, W. 2017. Redescription of the tadpole of Odontophrynus carvalhoi Savage and Cei, 1965 (Anura, Odontophrynidae) with comments on the geographical distribution of the species. Zootaxa 4323: 419-422.

Santos, T.d.; Marques de Souza, A.; Bondezan, F.L. & Eterovick, P.C. 2022. Going underground: what the natural history traits of cave users can tell us about cave use propensity. Journal of Herpetology 56: 153-163.

Schiner, J.R. 1854. Fauna der Adelsberger-, Lueger- und Magdalen-Grotte.Verhandlungen der Zoologisch-Botanischen Gesellschaft 3: 1-40.

Simone, L.R.L. 2012. A new genus and species of cavernicolous Pomatiopsidae (Mollusca, Caenogastropoda) in Bahia, Brazil. Papéis Avulsos de Zoologia 52: 515-524.

Simone, L.R.L. 2013. Habeas, a new genus of Diplommatinidae from central Bahia, Brazil (Caenogastropodae), with description of three new species. Journal of Conchology 41: 519-525.

Sperandei, V.d.F.; Alvarenga, D.d.A.; Araújo, M.S.d. & Pereira, C.C. 2023. Are caves true habitats for anurans or more a favorable rocky environment? A discussion of habitat occupation by frogs in Neotropical caves. Neotropical Biology and Conservation 18: 131-137.

Sperandei, V.d.F.; Vaz-Silva, W. & Leonardo Tejerina-Garro, F. 2024. Characterization of anuran fauna inside caves in Brazil. Biota Neotropica 24: e20241657.

Teixeira Jr., M.; Amaro, R.C.; Recoder, R.S.; Sena, M.A.d. & Rodrigues, M.T. 2012. A relict new species of Oreobates (Anura, Strabomantidae) from the seasonally dry tropical forests of Minas Gerais, Brazil, and its implication to the biogeography of the genus and that of South American dry forests. Zootaxa 3158: 37-52.

Thomé, M.T.C.; Carstens, B.C.; Rodrigues, M.T.; Alexandrino, J. & Haddad, C.F.B. 2021. Genomic data from the Brazilian sibilator frog reveal contrasting pleistocene dynamics and regionalism in two South American dry biomes. Journal of Biogeography 48: 1112-1123.

Trajano, E. 1987. Fauna cavernícola brasileira: composição e caracterização preliminar. Revista Brasileira de Zoologia 3: 533-561.

Trajano, E. 2012. Ecological classification of subterranean organisms. In: White, W.B.Culver, D.C. (eds.), Encyclopedia of Caves. Elsevier Academic Press. Amsterdan

Trajano, E. & Bichuette, M.E. 2006. Biologia subterrânea: introdução. Redespeleo Brasil. São Paulo.

Trajano, E. & Bichuette, M.E. 2010a. Diversity of Brazilian subterranean invertebrates, with a list of troglomorphic taxa. Subterranean Biology 7: 1-16.

Trajano, E. & Bichuette, M.E. 2010b. Relevance of caves: why environmental studies have been inadequate. Espeleo-Tema 21: 105-112.

Trajano, E. & Gnaspini-Netto, P. 1991. Composição da fauna cavernícola brasileira, com uma análise preliminar da distribuição dos taxons. Revista Brasileira de Zoologia 7: 383-407.

Trajano, E.; Secutti, S. & Bichuette, M.E. 2009. Natural history and population data of fishes in caves of the Serra do Ramalho karst area, Middle São Francisco basin, northeastern Brazil. Biota Neotropica 9: 129-133.

Vaz-Silva, W.; Maciel, N.M.; de Andrade, S.P. & Amaro, R.C. 2018. A new cryptic species of Oreobates (Anura: Craugastoridae) from the seasonally dry tropical forest of central Brazil. Zootaxa 4441: 89-108.

Downloads

Published

2025-09-04

How to Cite

F. Sabbag, A. ., Gallão, J. E. ., Baêta, D. ., Haddad, C. F. B. ., & Bichuette, M. E. . (2025). Amphibians of caves in Serra do Ramalho karst area, a remarkable region of subterranean fauna in Brazil. Cuadernos De Herpetología, 1(1). Retrieved from https://cuadernosdeherpetologia.com/index.php/CdH/article/view/317

Issue

Section

Notas