Abstract
Subterranean ecosystems are among the most fragile and threatened worldwide. Among organisms living in the subterranean domain, source populations restricted to subterranean habitats are called troglobites, generally distinguished by sets of morphological, physiological, and ecological specializations. The singularities at both systemic (high dark and phylogenetic diversities) and species levels greatly contribute to regional and global biodiversity. However, good descriptive and interpretative knowledge about this diversity, which is important as a basis for effective conservation policies, is lacking especially for tropical areas. We describe and characterize Brazilian karst areas recognized as spots of high diversity of troglobites, highlighting particularly important cave systems. We considered not only taxonomic richness but also indicators of phylogenetic (e.g., presence of relictual taxa) and genetic diversities, the latter based on degree of specialization of individual species, i.e., accumulation of autapomorphies. For this, we used available literature and our own data, both published and unpublished. Only identifications validated by a taxonomist were considered, while all data based on parataxonomy were disregarded. We propose hypotheses based on models of origin of troglobites aiming to explain the differences between karst areas.
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References
Ab’Saber NA (1981) Domínios morfoclimáticos atuais e quaternários na região dos cerrados. Craton Intracraton 14:1–39
Ab’Saber NA (2000) Spaces occupied by the expansion of dry climates in South America during the quaternary ice ages. Revista do Instituto Geológico 21:71–78
Arponen A (2012) Prioritizing species for conservation planning. Biodivers Conserv 21:875–893. doi:10.1007/s10531-012-0242-1
Auler AS (2009) Styles of hypogene cave development in ancient carbonate areas overlying non-permeable rocks in Brazil and the influence of competing mechanisms and later modifying processes. In: Klimchouk A, Ford D (eds) Hypogene speleogenesis and Karst Hydrogeology of Artesian Basins, 1st edn. Ukrainian Institute of Speleology and Karstology, Simferopol, pp 173–179
Auler AS, Farrant AR (1996) A brief introduction to karst and caves in Brazil. Proc Univ Bristol Spelaeol Soc 20:187–200
Auler AS, Piló LB, Smart PL, Wang X, Hoffmann D, Richards DA, Edwards RL, Neves WA, Cheng H (2006) U-series dating and taphonomy of Quaternary vertebrates from Brazilian caves. Palaeogeogr Palaeoclim Palaeoecol 240:508–522. doi:10.1016/j.palaeo.2006.03.002
Auler AS, Smart PL, Wang X, Piló LB, Edwards RL, Cheng H (2009) Cyclic sedimentation in Brazilian caves: mechanisms and palaeoenvironmental significance. Geomorphology 106:142–153. doi:10.1016/j.geomorph.2008.09.020
Ball GE, Shpeley D (2013) Western Hemisphere Zuphiini: descriptions of Coarazuphium whiteheadi, new species, and Zuphioides new genus, and classification of the genera (Coleoptera, Carabidae). ZooKeys 315:17–54. doi:10.3897/zookeys.315.5293
Baptista RLC, Giuponni APL (2002) A New troglomorphic Charinus from Brazil (Arachnida: Amblypygi: Charinidae). Reviata Ibérica de Aracnología 6:105–110
Barr TC (1968) Cave ecology and the evolution of troglobites. Evol Biol 2:35–102
Batalha MA (2011) The Brazilian Cerrado is not a biome. Biota Neotrop 11:21–24
Bichuette ME (1998) Distribuição e biologia de gastrópodes de água doce, gênero Potamolithus, no Vale do Alto Ribeira, São Paulo (Mollusca: Gastropoda: Hydrobiidae). Dissertation, Universidade de São Paulo
Bichuette ME, Rizzato PP (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 (Silurifomes: Trichomycteridae). Zootaxa 3480:48–66
Bichuette ME, Trajano E (2003a) Epigean and subterranean ichthyofauna from São Domingos karst area, Upper Tocantins river basin, Central Brazil. J Fish Biol 63:1100–1121. doi:10.1046/j.1095-8649.2003.00227.x
Bichuette ME, Trajano E (2003b) A population study of epigean and subterranean Potamolithus snails from southeast Brazil. Hydrobiologia 505:107–117. doi:10.1023/B:HYDR.0000007299.26220.b8
Bichuette ME, Trajano E (2004) Three new subterranean species of Ituglanis from Central Brazil (Siluriformes: Trichomycteridae). Ichthyol Explor Freshw 15:243–256
Bichuette ME, Trajano E (2005) A new cave species of Rhamdia (Siluriformes: Heptapteridae) from Serra do Ramalho, northeastern Brazil, with notes on ecology and behavior. Neotrop Ichthyol 3:587–595. doi:10.1590/S1679-62252005000400016
Bichuette ME, Trajano E (2006) Morphology and distribution of the cave knifefish Eigenmannia vicentespelaea Triques, 1996 (Gymnotiformes: Sternopygidae) from Central Brazil, with an expanded diagnosis and comments on subterranean evolution. Neotrop Ichthyol 4:99–105. doi:10.1590/S1679-62252006000100011
Bichuette ME, Trajano E (2015) Population density and habitat of an endangered cave fish Eigenmannia vicentespelaea Triques, 1996 (Ostariophysi: Gymnotiformes) from a karst area in central Brazil. Neotrop Ichthyol 13:113–122. doi:10.1590/1982-0224-20140095
Bichuette ME, Rizzato PP, Camargo AL, Brandi R, Senna-Horta L (2013) Um novo bagrinho troglóbio brasileiro. O Carste 25:58–59
Bichuette ME, Rantin B, Hingst-Zaher E, Trajano E (2015a) Geometric morphometrics throws light on evolution of the subterranean catfish Rhamdiopsis krugi (Teleostei: Siluriformes: Heptapteridae) in eastern Brazil. Biol J Linn Soc 114:136–151. doi:10.1111/bij.12405
Bichuette ME, Fonseca-Ferreira R, Gallão JE (2015b) Biota associada às cavernas em formações ferríferas. In: Ruchkys UA, Travassos LEP, Rasteiro MA, Faria LE (eds) Patrimônio Espeleológico em Rochas Ferruginosas - propostas para sua conservação no Quadrilátero Ferrífero, Minas Gerais, 1ed. Sociedade Brasileira de Espeleologia, Campinas, pp 174–191
Borghezan R (2013) Ecologia populacional e comportamento de peixes subterrâneos, Rhamdia sp. n. e Ancistrus sp. n. da área cárstica da Serra da Bodoquena, Mato Grosso do Sul (Siluriformes: Heptapteridae, Loricariidae). Dissertation, Universidade de São Paulo
Bortulus A (2008) Error cascades in the Biological sciences: the unwanted consequences of using bad taxonomy in ecology. Ambio 37:114–118
Campos-Filho IS, Araujo PB, Bichuette ME, Trajano E, Taiti S (2014) Terrestrial isopods (Crustacea: Isopoda: Oniscidea) from Brazilian caves. Zool J Linn Soc 172:360–425. doi:10.1111/zoj.12172
Campos-Filho IS, Bichuette ME, Taiti S (2016) Three new species of terrestrial isopods (Crustacea, Isopoda, Oniscidea) from Brazilian caves. Nauplius 24:1–19. doi:10.1590/2358-2936e2016001
Carnaval AC, Moritz C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest. J Biogeogr 35:1187–1201. doi:10.1111/j.1365-2699.2007.01870.x
Castro MC, Montefeltro FC, Langer MC (2014) The Quaternary vertebrate fauna of the limestone cave Gruta do Ioiô, northeastern Brazil. Quatern Int 352:164–175. doi:10.1016/j.quaint.2014.06.038
Chagas-Jr A, Bichuette ME (2015) A new species of Scolopocryptops Newport: a troglobitic scolopocryptopine centipede from a remarkable siliciclastic area of eastern Brazil (Scolopendromorpha, Scolopocryptopidae, Scolopocryptopinae). ZooKeys 487:97–110. doi:10.3897/zookeys.487.9262
Christiansen K (2005) Morphological adaptations. In: Culver DC, White WB (eds) Encyclopedia of caves, 1st edn. Elsevier, Amsterdam, pp 386–397
Cianciaruso MV, Silva IA, Batalha MA (2009) Phylogenetic and functional diversities: new approaches to community Ecology. Biota Neotrop 9:93–103
Cordeiro LM (2014) Distribuição, filogeografia e ecologia de bagres troglóbios do gênero Trichomycterus da área cárstica da Serra da Bodoquena, MS (Siluriformes: Trichomycteridae). PhD Thesis, Universidade de São Paulo
Cordeiro LM, Borghezan R, Trajano E (2013) Distribuição, riqueza e conservação dos peixes troglóbios da Serra da Bodoquena, MS (Teleostei: Siluriformes). Revista da Biologia 10:21–27. doi:10.7594/revbio.10.02.04
Cordeiro LM, Borghezan R, Trajano E (2014) Subterranean biodiversity in the Serra da Bodoquena karst area, Paraguay river basin, Mato Grosso do Sul, Southwestern Brazil. Biota Neotrop 14:1–28. doi:10.1590/1676-06032014011414
Cruz FW Jr, Burns SJ, Karmann I, Sharp WD, Vuille M, Cardoso AO, Ferrari JA, Dias PLS, Viana O Jr (2005) Insolation-friven changes in atmospheric circulation over the past 116,000 years in subtropical Brazil. Nature 434:63–66
Culver DC, Pipan T (2009) The biology of caves and other subterranean habitats. Oxford University Press, New York
Culver DC, Sket B (2000) Hotspots of Subterranean Biodiversity in Caves and Wells. J Cave Karst Stud 62:11–17
de Almeida FFM (1965) Geologia da Serra da Bodoquena (Mato Grosso), Brasil. Boletim da Divisão de Geologia e Mineralogia DNPM 219:1–96
Deharveng L (2005) Diversity patterns in the Tropics. In: Culver DC, White WB (eds) Encyclopedia of caves, 1st edn. Elsevier, Amsterdam, pp 166–170
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10
Felice V, Visconti MA, Trajano E (2008) Mechanisms of pigmentation loss in subterranean fishes. Neotrop Ichtyol 6:657–662
Fernandes CS, Bueno SLS, Bichuette ME (2013) Distribution of cave-dwelling Aegla spp. (Decapoda: Anomura: Aeglidae) from the Alto Ribeira karstic area in southeastern Brazil based on geomorphological evidence. J Crustac Biol 33:567–575. doi:10.1163/1937240X-00002159
Fernandes CS, Batalha MA, Bichuette ME (2016) Does the cave environment reduce functional diversity? PLoS One 11(3):e0151958. doi:10.1371/journal.pone.0151958
Gallão JE (2012) Estado de conservação e dados de distribuição da fauna troglóbia brasileira com propostas de áreas prioritárias para proteção. Dissertation, Universidade Federal de São Carlos
Gallão JE, Bichuette ME (2015) Taxonomic distinctness and conservation of a new high biodiversity subterranean area in Brazil. An Acad Bras Cienc 87:209–217. doi:10.1590/0001-3765201520140312
Giachino PM, Vailati D (2010) The Subterranean Environment. Hypogean life, concepts and collecting techniques. WBA Handbooks, Verona, p 132
Gibert J, Deharveng L (2002) Subterranean ecosystems: a truncated functional biodiversity. Bioscience 52:473–481
Gnaspini P, Trajano E (1994) Brazilian cave invertebrates, with a checklist of troglomorphic taxa. Revista Bras Entomol 38:549–584
Halenar LB, Rosenberger AL (2013) A closer look at the “Protopithecus” fossil assemblages: new genus and species from Bahia, Brazil. J Hum Evol 65:341–478. doi:10.1016/j.jhevol.2013.07.008
Hattori N (2012) Fauna Subterrânea da Gruna do Enfurnado. Monograph, Universidade Federal de São Carlos, Sudoeste da Bahia
Holsinger JR (1988) Troglobites: The evolution of cave-dwelling organisms. Am Sci 76:146–153
Koenemann S, Holsinger JR (1999) Megagidiella Azul, a new genus and species of cavernicolous amphipod crustacean (bogidiellidae) from Brazil, with remarks on its biogeographic and phylogenetic relationships. P Biol Soc Wash 112:572–580
Köeppen W (1948) Climatología. Fondo de cultura economica, Mexico
Krell FT (2004) Parataxonomy vs. taxonomy in biodiversity studies—pitfalls and applicability of ‘morphospecies’ sorting. Biodivers Conserv 13:795–812. doi:10.1023/B:BIOC.0000011727.53780.63
Majka CG, Bondrup-Nielsen S (2006) Parataxonomy: a test case using beetles. Anim Biodivers Conserv 29:149–156
Mattox GMT, Bichuette ME, 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 Neotrop 8:145–152. doi:10.1590/S1676-06032008000400014
Mauriès JP, Geoffroy JJ (2000) Nouvelle description, classification, répartition et variations morphologiques interpopulations dún diplopode troglobie du sud-est du Brésil (Diplopoda, Polydesmida, Chelodesmodae). Zoosystema 22:153–168
Mendes LF, Fox EGP, Solis DR, Bueno OC (2009) New Nicoletiidae (Zygentoma: Insecta) from Brazil living in fire-ant (Hymenoptera: Insecta) nests. Pap Avulsos Zool 49:467–475. doi:10.1590/S0031-10492009003400001
Messana G, Baratti M, Benvenuti D (2002) Pongycarcinia xiphidiourus n. gen. n. sp., a new Brazlian Calabozoidae (Crustacea Isopoda). Trop Zool 15:243–252. doi:10.1080/03946975.2002.10531178
Moracchioli N (2002) Estudo dos Spelaeogriphacea brasileiros, crustáceos Peracarida subterrâneos. Phd Thesis, Universidade de São Paulo
Myers N (1990) The biodiversity challenge: expanded hot-spots analysis. Environmentalist 10:243–256
Nimer E (1989) Climatologia do Brasil. Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro
Palmer AN (2007) Cave Geology. Cave Books, Ohio
Pärtel M, Szava-Kovats R, Zobel M (2011) Dark diversity: shedding light on absent species. Trends Ecol Evol 26:124–128. doi:10.1016/j.tree.2010.12.004
Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644. doi:10.5194/hess-11-1633-2007
Pérez A, Kury AB (2002) A new remarkable troglomorph gonyleptid from Brazil (Arachnida, Opiliones, Laniatores). Revista Ibérica de Aracnología 5:43–50
Pérez-Gonzáles A, Proud DN, Cecarelli SF, Cruz-López J, Oliveira do Monte BG, Bichuette ME (2016) A seletiva arca de Noé: Opiliones (Arthopoda: Arachnida) relictuais cavernícolas evidenciam a história geoclimática do planeta. In: XXXI Congresso Brasileiro de Zoologia, Cuiabá, p 755
Pinto-da-Rocha R, Fonseca-Ferreira R, Bichuette ME (2015) A new highly specialized cave harvestman from Brazil and the first blind species of the genus: Iandumoema smeagol sp. n. (Arachnida, Opiliones, Gonyleptidae). Zookeys 537:79–95. doi:10.3897/zookeys.537.6073
Reis RE, Trajano E, Hingst-Zaher E (2006) Shape variation in surface and cave populations of the armoured catfish Ancistrus (Siluriformes: Loricariidae) from the São Domingos karst area, Upper Tocantins River, Brazil. J Fish Biol 68:414–429. doi:10.1111/j.0022-1112.2006.00891.x
Rizzato PP, Bichuette ME (2014) Ituglanis boticario, a new troglomorphic catfish from Mambaí karst area, central Brazil (Teleostei: Siluriformes: Trichomycteridae). Zoologia 31:577–598. doi:10.1590/S1984-46702014000600006
Rizzato PP, Costa EP Jr, Trajano E, Bichuette ME (2011) Trichomycterus dali: a new highly troglomorphic catfish (Silurifomes: Trichomycteridae), from Serra da Bodoquena, Mato Grosso do Sul State, Central Brazil. Neotrop Ichthyol 9:477–491. doi:10.1590/S1679-62252011000300003
Schobbenhaus C, Campos DA, Derze GR, Asmus HE (1984) Mapa Geológico do Brasil e da Área Oceânica Adjacente. Ministério das Minas e Energia/DNPM, Rio de Janeiro
Sendra A, Garay P, Ortuño VM, Gilgado JD, Teruel S, Reboleira ASPS (2014) Hypogenic versus epigenic subterranean ecosystem: lessons from eastern Iberian Peninsula. Int J Speleol 43:253–264. doi:10.5038/1827-806X.43.3.2
Simone LRL (2012) A new genus and species of cavernicolous Pomatiopsidae (Mollusca, Caenogastropoda) in Bahia, Brazil. Pap Avulsos Zool 52:515–524. doi:10.1590/S0031-10492012022000001
Souza S, Morais AL, Bichuette ME, Leal-Zanchet A (2016) Two new species of freshwater flatworms (Platyhelminthes:Tricladida:Continenticola) from South American caves. Zootaxa 4092:107–121. doi:10.11646/zootaxa.4092.1.6
Souza-Silva M, Martins RP, Ferreira RL (2015) Cave conservation priority index to adopt a rapid protection strategy: a case study in Brazilian Atlantic rain forest. Environ Manag 55:279–295. doi:10.1007/s00267-014-0414-8
Stiassny MJL, de Pinna MCC (1994) Basal taxa and the role of cladistic patterns in the evaluation of conservation priorities: a view from freshwater. In: Forey PL, Humphries CJ, Vane-Wright RI (eds) Systematics and conservation evaluation. Systematics association special volume no. 50. Clarendon Press, Oxford, pp 235–249
Strinati P (1971) Researches biospeleólogiques en Amerique du Sud. Ann Spéleol 26:439–450
Trajano E (1992) Biodiversidad, Sistemática y Cavernas. Spelaion 3:11–17
Trajano E (1994) Evolution of tropical troglobites: applicability of the model of Quaternary climatic fluctuations. In: XI International Symposium of Biospeleology, Firenze, pp 14–15
Trajano E (1995) Evolution of tropical troglobites: applicability of the model of Quaternary climatic fluctuations. Mémoirs Biospéologie 22:203–209
Trajano E (1997) Threatened fishes of the World: Pimelodella kronei (Ribeiro, 1907). Environ Biol Fish 49:332
Trajano E (2000) Cave faunas in the Atlantic tropical rain forest: composition, ecology and conservation. Biotrop 32:882–893
Trajano E (2001) Mapping subterranean biodiversity in Brazilian karst areas. In: Culver DC, Deharveng L, Gibert J, Sasowsky I (eds) Mapping subterranean biodiversity. Publ, Karst Waters Institute Spec, pp 67–70
Trajano E (2007) Sistema Areias—100 anos de estudos. Redespeleo Brasil, São Paulo
Trajano E (2012) Ecological classification of subterranean organisms. In: White WB, Culver DC (eds) Encyclopedia of Caves, 2nd edn. Elsevier, Amsterdam, pp 275–277
Trajano E, Bichuette ME (2010) Diversity of Brazilian subterranean invertebrates, with a list of troglomorphic taxa. Subterr Biol 7:1–16
Trajano E, Bockmann FA (2000) Ecology and behaviour of a new cave catfish of the genus Taunayia from northeastern Brazil (Siluriformes, Heptapterinae). Ichthyol Explor Freshw 11:207–216
Trajano E, Britski HA (1992) Pimelodella kronei (Ribeiro, 1907) e seu sinônimo Caecorhamdella brasiliensis Borodin, 1927: morfologia externa, taxonomia e evolução (Teleostomi, Siluriformes). Bol Zool 12:53–89
Trajano E, Moracchioli N (2002) Bodoquena karst area, southwest Brazil: a hotspot of biodiversity for aquatic troglobites. In: XVIth International Symposium of Biospeleology, Verona, pp 84–84
Wang X, Auler AS, Edwards RL, Cheng H, Cristalli PS, Richards DA, Smart PL, Shen CC (2004) Wet periods in northeastern Brazil over the past 210 kyr linked to distantclimate anomalies. Nature 432:740–743
Wilson EO (1992) The diversity of life. Penguin, London
Acknowledgments
We are deeply grateful to the numerous colleagues, biologists, speleologists and field guides that helped us in the field and with laboratory work throughout the last decades. Without their valuable cooperation, it would be impossible to gather the large body of knowledge constituting the basis for the present paper. We are also indebted to Rosely Rodrigues, Mary Andriani and Editage by revision of the English style; to Diego Monteiro von Schimonsky for maps confection; to Adriano Gambarini, Danté Fenolio and Pedro Pereira Rizzato for photographs of Plate 1.The Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP and the Conselho Nacional de Desenvolvimento científico e Tecnológico—CNPq supported us through grants and fellowships. To Instituto de Chico Mendes de Conservação da Biodiversidade - ICMBIO for collection permits.
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Trajano, E., Gallão, J.E. & Bichuette, M.E. Spots of high diversity of troglobites in Brazil: the challenge of measuring subterranean diversity. Biodivers Conserv 25, 1805–1828 (2016). https://doi.org/10.1007/s10531-016-1151-5
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DOI: https://doi.org/10.1007/s10531-016-1151-5