Abstract
The present work brings information on threats to the subterranean fishes in Brazil. Currently, at least 36 species are known, 22 of which are already formally described. Endemism is the rule for most of them. Regarding their conservation, these fishes are in general considered threatened: and most of the already formally described species are included in national lists of threatened fauna, and only four of them are included in the global list of the IUCN. Regarding habitats, Brazilian subterranean fishes occur in alluvial sediments (part of the hyporheic zone), shallow base-level streams, flooded caves, lakes in the water table, upper vadose tributaries, and epikarst aquifers. We detected 11 main threats, mainly related to agriculture, pasture, and hydroelectric plans, but unmanaged tourism and pollution are also significant threats. Two threats affect a high number of species (physical change of the habitat and food restriction). The river basins with the higher number of identified threats are the upper Tocantins (eight) followed by the upper Paraguaçu (six). Effective proposals to protect this neglected component of the Brazilian biodiversity are still scarce, such as monitoring projects and their function in the subterranean communities, besides education projects aiming to develop public awareness.
Keywords:
Conservation; Human impacts; IUCN; Subterranean fishes; Threats
Resumo
O presente trabalho traz informações sobre as ameaças aos peixes subterrâneos no Brasil. Atualmente, são conhecidas pelo menos 36 espécies, 22 das quais já foram formalmente descritas. O endemismo é a regra para a maioria destas espécies. Em relação à conservação, esses peixes são em geral considerados ameaçados: a maioria das espécies já descritas está incluída em listas regionais de fauna ameaçada e apenas quatro delas estão incluídas na lista global da IUCN. Em relação aos habitats, os peixes subterrâneos brasileiros ocorrem em sedimentos aluviais (parte da zona hiporreica), riachos de nível de base, cavernas inundadas, lagos no lençol freático, tributários vadosos superiores e aquíferos no epicarste. Detectamos onze ameaças principais, a maioria relacionada à agricultura, pecuária e projetos hidrelétricos, entretanto, turismo sem planos de manejo e poluição também representam ameaças significativas. Duas ameaças afetam um grande número de espécies: a mudança física do habitat e a restrição de alimento. As bacias hidrográficas com o maior número de ameaças identificadas são a do alto Tocantins (oito) seguida pela do alto Paraguaçu (seis). Propostas eficazes para proteger esse componente negligenciado da biodiversidade brasileira são ainda escassos, como os projetos de monitoramento e sua função nas comunidades subterrâneas, além de projetos relacionados à educação, visando a sensibilização do público.
Palavras-chave:
Ameaças; Conservação; Impactos Humanos; IUCN; Peixes subterrâneos
INTRODUCTION
The subterranean or hypogean environment comprises a series of interconnected subsurface spaces of variable dimensions, from interstices of a few millimeters to very large galleries and caves, formed in solid rock and filled with water or air (Juberthie, 2000aJuberthie C. The diversity of the karstic and pseudokarstic hypogean habitats in the world. In: Wilkens H, Culver D, Humphreys WF, editors. Ecosystems of the world Vol. 30 Subterranean Ecosystems. Amsterdam: Elsevier; 2000a. p.17–39.). When compared to surface or epigean habitats, subterranean habitats (including non-cave habitats) show particularities that, together, form a specific kind of selective regime, which may constrain potential colonizer organisms. Examples are the permanent absence of light in the deeper zones and, consequently, of primary producers, generally resulting in conditions of food scarcity and dependence of allochthonous input (originated in epigean habitats). Another characteristic is the tendency towards climatic stability as a consequence of the buffer effect of the surrounding rocks (Culver, Pipan, 2009Culver DC, Pipan T. The biology of caves and other subterranean habitats. Acta Carsologica. 2009; 38(2–3):309–11. https://doi.org/10.3986/ac.v38i2-3.168
https://doi.org/10.3986/ac.v38i2-3.168...
).
It is widely accepted that organisms with abilities to explore dark and food-scarce habitats are potential colonizers of subterranean environments (Poulson, White, 1969Poulson TL, White WB. The cave environment. Science. 1969; 3897(165):971–80.; Culver, Pipan, 2009Culver DC, Pipan T. The biology of caves and other subterranean habitats. Acta Carsologica. 2009; 38(2–3):309–11. https://doi.org/10.3986/ac.v38i2-3.168
https://doi.org/10.3986/ac.v38i2-3.168...
). Organisms that rely on sensory modalities other than vision, such as chemo- and mechanoreception, with a generalist and/or detritivorous diet, could be more successful in colonizing subterranean environments and establishing hypogean populations. Trajano, (2012)Trajano E. Ecological classification of subterranean organisms. In: White WB, Culver DC, editors. Encyclopedia of Caves. Amsterdam: Elsevier; 2012. p.275–77. proposed a classification of subterranean organisms based on the concept of sink-source populations. This classification defines as trogloxenes, organisms that have source populations in the epigean environment but use subterranean resources (e.g., bats); troglophiles, organisms that have source populations in both hypogean and epigean environments (e.g., several populations of fishes, spiders, and crickets); and troglobites, organisms that have source populations exclusively in the hypogean environment (e.g., several species of fishes, crustaceans, insects and others). In Brazil, troglobitic and troglophilic populations of fishes were already identified (e.g., Bichuette, Trajano, 2003Bichuette ME, Trajano E. Epigean and subterranean ichthyofauna from the São Domingos karst area, upper Tocantins River basin, Central Brazil. J Fish Biol. 2003; 63(5):1100–21. https://doi.org/10.1046/j.1095-8649.2003.00227.x
https://doi.org/10.1046/j.1095-8649.2003...
, 2021Bichuette ME, Trajano E. Monitoring Brazilian cavefish: Ecology and conservation of four threatened catfish of genusItuglanis (Siluriformes: Trichomycteridae) from Central Brazil. Diversity. 2021; 13(2):91. https://doi.org/10.3390/d13020091
https://doi.org/10.3390/d13020091...
; Trajano, Bichuette, 2010Trajano E, Bichuette ME. Subterranean fishes of Brazil. In: Trajano E, Bichuette ME, Kapoor BG, editors. Biology of Subterranean Fishes. Enfield: Science Publishers; 2010. p.331–56. ; Ratton et al., 2018Ratton P, Ferreira RL, Pompeu PS. Fish community of a small karstic Neotropical drainage and its relationship with the physical habitat. Mar Freshwater Res. 2018; 69(8):1312–20. https://doi.org/10.1071/MF17167
https://doi.org/10.1071/MF17167...
; Rabello, 2021Rabello GCR. Ictiofauna da região da Serra da Canastra, Minas Gerais: cavernas são filtros ambientais considerando-se riqueza, diversidade e comportamento alimentar? [Master Dissertation]. São Carlos: Universidade Federal de São Carlos; 2021. Available from: https://repositorio.ufscar.br/handle/ufscar/14060
https://repositorio.ufscar.br/handle/ufs...
); no trogloxen fishes are reported in Brazil.
It is a worldwide consensus that subterranean habitats, as well as their communities, are highly singular, fragile, and represent one of the most threatened environments in the world (Elliott, 2005Elliott WR. Protecting caves and cave life. In: Culver DC, White WB, editors. Encyclopedia of Caves Vol. 1. Amsterdam: Elsevier; 2005. p.458–67.; Culver, Pipan, 2019Culver DC, Pipan T. The biology of caves and other subterranean habitats. Oxford: Oxford University Press; 2019. Available from: https://doi.org/10.1093/oso/9780198820765.001.0001
https://doi.org/10.1093/oso/978019882076...
; Mammola et al., 2019Mammola S, Cardoso P, Culver DC, Deharveng L, Ferreira RL, Fisër C et al. Scientists’ warning on the conservation of subterranean ecosystems. Bioscience. 2019; 69(8):641–50. https://doi.org/10.1093/biosci/biz064
https://doi.org/10.1093/biosci/biz064...
). Troglobites, in particular, are intrinsically fragile and vulnerable to environmental changes, given their small populations with low resilience (Culver, Pipan, 2009Culver DC, Pipan T. The biology of caves and other subterranean habitats. Acta Carsologica. 2009; 38(2–3):309–11. https://doi.org/10.3986/ac.v38i2-3.168
https://doi.org/10.3986/ac.v38i2-3.168...
). All troglobitic species should be protected by law and included in at least the Vulnerable category (VU) of IUCN (International Union for Conservation of Nature), an idea that has been advocated by several authors (e.g., Juberthie, 2000bJuberthie C. Conservation of subterranean habitats and species. In: Wilkens W, Culver DC, Humphreys WF, editors. Ecosystems of the World Vol. 30 Subterranean Ecosystems. Amsterdam: Elsevier; 2000b. p.691–700.; Bichuette, Trajano, 2010Bichuette ME, Trajano E. Conservation of subterranean fishes. In: Trajano E, Bichuette ME, Kapoor BG, editors. Biology of subterranean fishes. Enfield: Science Publishers; 2010. p.65–80. https://doi.org/10.1201/EBK1578086702
https://doi.org/10.1201/EBK1578086702...
, 2021Bichuette ME, Trajano E. Monitoring Brazilian cavefish: Ecology and conservation of four threatened catfish of genusItuglanis (Siluriformes: Trichomycteridae) from Central Brazil. Diversity. 2021; 13(2):91. https://doi.org/10.3390/d13020091
https://doi.org/10.3390/d13020091...
; Fernandes et al., 2016Fernandes CS, Batalha MA, Bichuette ME. Does the cave environment reduce functional diversity? PLoS ONE. 2016; 11(3):e0151958. https://doi.org/10.1371/journal.pone.0151958
https://doi.org/10.1371/journal.pone.015...
; Trajano et al., 2016Trajano E, Gallão JE, Bichuette ME. Spots of high diversity of troglobites in Brazil: the challenge of measuring subterranean diversity. Biodivers Conserv. 2016; 25:1805–28. https://doi.org/10.1007/s10531-016-1151-5
https://doi.org/10.1007/s10531-016-1151-...
; Gallão, Bichuette, 2018Gallão JE, Bichuette ME. Brazilian obligatory subterranean fauna and threats to the hypogean environment. Zookeys. 2018; 746:1–23. https://doi.org/10.3897/zookeys.746.15140
https://doi.org/10.3897/zookeys.746.1514...
; Culver, Pipan, 2019Culver DC, Pipan T. The biology of caves and other subterranean habitats. Oxford: Oxford University Press; 2019. Available from: https://doi.org/10.1093/oso/9780198820765.001.0001
https://doi.org/10.1093/oso/978019882076...
; Mammola et al., 2019Mammola S, Cardoso P, Culver DC, Deharveng L, Ferreira RL, Fisër C et al. Scientists’ warning on the conservation of subterranean ecosystems. Bioscience. 2019; 69(8):641–50. https://doi.org/10.1093/biosci/biz064
https://doi.org/10.1093/biosci/biz064...
; Bichuette, 2021Bichuette ME. Ecologia de peixes de riachos de cavernas e outros habitat subterrâneos. Oecologia Australis. 2021; 25(2):620–41.https://doi.org/10.4257/oeco.2021.2502.24
https://doi.org/10.4257/oeco.2021.2502.2...
).
In Brazil, the intense exploration of mineral resources, agriculture and pasture activities, urban expansion, and pollution of aquifers have grown in the years following the publication of the Decree 6640 (Brasil, Brasil. 2008. Decreto no 6.640, de 7 de novembro de 2008. Dá nova redação aos arts. 1°, 2°, 3°, 4° e 5o e acrescenta os arts. 5-A e 5-B ao Decreto n° 99.556, de 1 de outubro de 1990, que dispõe sobre a proteção das cavidades naturais subterrâneas existentes no território nacional. Brasília, DF, 7 de novembro de 2008. Available from: http://www.planalto.gov.br/ccivil_03/_Ato2007-2010/2008/Decreto/D6640.htm
http://www.planalto.gov.br/ccivil_03/_At...
2008) that classifies caves by their levels of relevance (see Gallão, Bichuette, 2018Gallão JE, Bichuette ME. Brazilian obligatory subterranean fauna and threats to the hypogean environment. Zookeys. 2018; 746:1–23. https://doi.org/10.3897/zookeys.746.15140
https://doi.org/10.3897/zookeys.746.1514...
). Only those caves classified as of maximum relevance with basis on a list of attributes are considered prone to be effectively protected by the Brazilian legislation. This has led to the suppression, in some cases, of entire massifs, whether of limestone or other lithologies (e.g., sandstone, igneous, iron ore) and consequently to expressive losses of subterranean biodiversity (Gallão, Bichuette, 2012Gallão JE, Bichuette ME. The list of endangered fauna and impediments to inclusion of species - the example of Brazilian troglobitic fish. Nat Conserv. 2012; 10(1):83–87. https://doi.org/10.4322/natcon.2012.014
https://doi.org/10.4322/natcon.2012.014...
, 2018Gallão JE, Bichuette ME. Brazilian obligatory subterranean fauna and threats to the hypogean environment. Zookeys. 2018; 746:1–23. https://doi.org/10.3897/zookeys.746.15140
https://doi.org/10.3897/zookeys.746.1514...
). Attributes that classify a given cave as of maximum relevance, therefore assuring (in theory) its full protection according to the Decree, are: it harbors rare troglobitic species, includes unique ecological interactions, or is essential for the preservation of relict, endemic, or threatened troglobites – in this case, the species must be included in official lists (regional, national or global) of threatened fauna, an important attribute that denotes total protection to caves (Gallão, Bichuette, 2012Gallão JE, Bichuette ME. The list of endangered fauna and impediments to inclusion of species - the example of Brazilian troglobitic fish. Nat Conserv. 2012; 10(1):83–87. https://doi.org/10.4322/natcon.2012.014
https://doi.org/10.4322/natcon.2012.014...
).
Furthermore, it is a worldwide consensus that subterranean habitats are highly singular, and one of the most threatened in the world (Culver, Pipan, 2019Culver DC, Pipan T. The biology of caves and other subterranean habitats. Oxford: Oxford University Press; 2019. Available from: https://doi.org/10.1093/oso/9780198820765.001.0001
https://doi.org/10.1093/oso/978019882076...
). Unfortunately, other types of Brazilian subterranean habitats beyond caves, such as the hyporheic zone (defined as an active ecotone delimited superiorly by channel water and inferiorly by underground water, constituted by particles of the riverbed; Mugnai et al., 2015Mugnai R, Messana G, Di Lorenzo T. The hyporheic zone and its functions: revision and research status in Neotropical regions. Braz J Biol. 2015; 75(3):524–34. https://dx.doi.org/10.1590/1519-6984.15413
https://dx.doi.org/10.1590/1519-6984.154...
), MSS (Milieu Souterrain Superficiel, defined as the upper zone of the rock, forming a subterranean network of empty air-filled voids of rock fragments; Juberthie, 2000aJuberthie C. The diversity of the karstic and pseudokarstic hypogean habitats in the world. In: Wilkens H, Culver D, Humphreys WF, editors. Ecosystems of the world Vol. 30 Subterranean Ecosystems. Amsterdam: Elsevier; 2000a. p.17–39.), and even aquifers, are not considered in the Decree 6640.
The Brazilian subterranean ichthyofauna is remarkable due to its phylogenetic diversity, at both the family and genus levels, when compared to subterranean ichthyofaunas of other regions of the world. The countries with the higher number of troglobitic fish species are China (more than 79 species) and Brazil (36 species, see below) (Bichuette, 2021Bichuette ME. Ecologia de peixes de riachos de cavernas e outros habitat subterrâneos. Oecologia Australis. 2021; 25(2):620–41.https://doi.org/10.4257/oeco.2021.2502.24
https://doi.org/10.4257/oeco.2021.2502.2...
). However, the phylogenetic diversity in China, 10 genera in four families (Niemiller et al., 2019Niemiller ML, Bichuette ME, Chakrabarty P, Fenolio DB, Gluesenkamp AG, Soares D et al. Cavefishes. In: White WB, Culver DC, Pipan T, editors. Encyclopedia of Caves. Amsterdam: Elsevier; 2019. p.227–36.) is smaller when compared to Brazil, with 13 genera in seven families (see below). This is somehow expected given the fact that Brazil is a megadiverse country and houses a substantial part of the world’s freshwater ichthyofauna, which includes potential colonizers of subterranean habitats. The vast majority of the Brazilian troglobitic ichthyofauna belongs to the order Siluriformes (catfishes), mainly from the families Trichomycteridae and Heptapteridae (Trajano, Bichuette, 2010Trajano E, Bichuette ME. Subterranean fishes of Brazil. In: Trajano E, Bichuette ME, Kapoor BG, editors. Biology of Subterranean Fishes. Enfield: Science Publishers; 2010. p.331–56. ; Bichuette, 2021Bichuette ME. Ecologia de peixes de riachos de cavernas e outros habitat subterrâneos. Oecologia Australis. 2021; 25(2):620–41.https://doi.org/10.4257/oeco.2021.2502.24
https://doi.org/10.4257/oeco.2021.2502.2...
).
By considering also the several Brazilian fish species that have troglophilic populations, about 50 (Bichuette, Trajano, 2003Bichuette ME, Trajano E. Epigean and subterranean ichthyofauna from the São Domingos karst area, upper Tocantins River basin, Central Brazil. J Fish Biol. 2003; 63(5):1100–21. https://doi.org/10.1046/j.1095-8649.2003.00227.x
https://doi.org/10.1046/j.1095-8649.2003...
; Trajano, Bichuette, 2010Trajano E, Bichuette ME. Subterranean fishes of Brazil. In: Trajano E, Bichuette ME, Kapoor BG, editors. Biology of Subterranean Fishes. Enfield: Science Publishers; 2010. p.331–56. ; Bichuette, 2021Bichuette ME. Ecologia de peixes de riachos de cavernas e outros habitat subterrâneos. Oecologia Australis. 2021; 25(2):620–41.https://doi.org/10.4257/oeco.2021.2502.24
https://doi.org/10.4257/oeco.2021.2502.2...
), the urge to protect subterranean habitats that house these populations is evident. Considering this concerning scenario, we present herein updated data about the already identified threats to this particular ichthyofauna, with a discussion on existing and persisting gaps of distribution data.
MATERIAL AND METHODS
We evaluated the threats to the 36 subterranean species reported herein (see Tabs. 1–2). The undescribed species (14 from 36) are under study by specialists, and their status as new taxon is corroborated by morphological studies, with detection of diagnosis.
A descriptive analysis of threats was considered through search in data published in literature concerning the conservation of cavefishes, including the information of the original description of species: articles in journals, books, chapter books, thesis and dissertations, and proceedings of national and international meetings (e.g., Bichuette, 2008Bichuette ME. Eigenmannia vicentespelaea Triques, 1996. In: Machado ABM, Drummond GM, Paglia AP, editors. Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. Belo Horizonte: Ministério do Meio Ambiente e Fundação Biodiversitas; 2008. p.176–77.; Trajano, 2008aTrajano E. Pimelodella kronei (Ribeiro, 1907). In: Machado ABM, Drummond GM, Paglia AP, editors. Livro vermelho da fauna brasileira ameaçada de extinção. Belo Horizonte: Ministério do Meio Ambiente e Fundação Biodiversitas; 2008a. p.230–31.,bTrajano E. Trichomycterus itacarambiensis Trajano & de Pinna, 1996. In: Machado ABM, Drummond GM, Paglia AP, editors. Livro vermelho da fauna brasileira ameaçada de extinção. Belo Horizonte: Ministério do Meio Ambiente e Fundação Biodiversitas; 2008b. p.252–53.; Bichuette, Trajano, 2010Bichuette ME, Trajano E. Conservation of subterranean fishes. In: Trajano E, Bichuette ME, Kapoor BG, editors. Biology of subterranean fishes. Enfield: Science Publishers; 2010. p.65–80. https://doi.org/10.1201/EBK1578086702
https://doi.org/10.1201/EBK1578086702...
, 2015Bichuette ME, Trajano E. Population density and habitat of an endangered cave fish Eigenmannia vicentespelaea Triques, 1996 (Ostariophysi: Gymnotiformes) from a karst area in central Brazil. Neotrop Ichthyol. 2015; 13(1):113–22. https://doi.org/10.1590/1982-0224-20140095
https://doi.org/10.1590/1982-0224-201400...
, 2021Bichuette ME, Trajano E. Monitoring Brazilian cavefish: Ecology and conservation of four threatened catfish of genusItuglanis (Siluriformes: Trichomycteridae) from Central Brazil. Diversity. 2021; 13(2):91. https://doi.org/10.3390/d13020091
https://doi.org/10.3390/d13020091...
; Gallão, Bichuette, 2012Gallão JE, Bichuette ME. The list of endangered fauna and impediments to inclusion of species - the example of Brazilian troglobitic fish. Nat Conserv. 2012; 10(1):83–87. https://doi.org/10.4322/natcon.2012.014
https://doi.org/10.4322/natcon.2012.014...
, 2018Gallão JE, Bichuette ME. Brazilian obligatory subterranean fauna and threats to the hypogean environment. Zookeys. 2018; 746:1–23. https://doi.org/10.3897/zookeys.746.15140
https://doi.org/10.3897/zookeys.746.1514...
; Borghezan, 2013Borghezan R. 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). [Master Dissertation]. São Paulo: Universidade de São Paulo; 2013. Available from:https://teses.usp.br/teses/disponiveis/41/41133/tde-12062013-090146/fr.php
https://teses.usp.br/teses/disponiveis/4...
; ICMBio, 2018Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). Livro vermelho da fauna brasileira ameaçada de extinção: Volume VI - Peixes. In: Instituto Chico Mendes de Conservação da Biodiversidade, organizers. Livro vermelho da fauna brasileira ameaçada de extinção. Brasília: ICMBio/MMA; 2018.). In addition, we included personal observations collected during fieldwork in several regions of Brazil for the last 18 years.
These data are presented in detail in the maps of the known subterranean fish species occurring in Brazil, including the ones not yet described, tables, and graphs, considering the threats for each taxon. Maps were elaborated using the software Quantum GIS (QGIS, version 3.6.0, https://www.qgis.org/en/site), and shapefiles from MapBiomas (version 5.0, https://mapbiomas.org).
RESULTS
Brazil houses a rich subterranean ichthyofauna compared to China and Mexico, both megadiverse countries for subterranean fishes. We have reported 36 species so far, 22 of which have already been formally described (Tab. 1). Brazilian subterranean fishes are found in six basins (Figs. 1-2) and eight federated states (Tab. 1). Considering the occurrences, we observe several gaps of distribution, for example, the Amazon basin and the upper rio Paraguai (Fig. 1) and some regions with high richness and still high potential for troglobitic species, such as the northeastern region of Goiás, Central Brazil, and the southwestern and northern regions of Bahia (Figs. 1 and 3). The bias in collection explains these gaps since northeastern of Goiás was intensively prospected in search of cavefish in the last 15 years by our team. Endemism is the rule for most of them, with at least 20 species occurring in one single cave or cave system (i.e., one or more caves extending continuously between sinkholes and resurgences) or in non-cave habitats, such as hyporheic zone.
List of the currently known Brazilian subterranean fishes species occurring in Brazil, their basins of occurrence, type of habitats / number of localities (caves or non-cave habitats). * Undescribed species with references.
Map of Brazil showing the distribution of the subterranean fish species according to the basins included in the country’s territory.
Detailed maps showing the distribution of Brazilian subterranean fishes in different federated states, including vegetation and impacts nearby. AP, Amapá State; PA, Pará State; RO, Rondônia State; MS, Mato Grosso do Sul State; BA, Bahia State; SP, São Paulo State, MG, Minas Gerais State; GO, Goiás State. Outcrops, landscape areas with rocks and potentially cave occurrences.
In relation to habitats, the Brazilian subterranean fishes occur from alluvial sediments (which are part of the hyporheic zone) to shallow base-level streams, flooded caves, upper vadose tributaries, lakes in the water table, and the epikarst (Tab. 1; Fig. 4). The vadose tributaries are located in the unsaturated zone and extend from the top of the ground surface to the water table. Epikarst is the upper part of the vadose zone and is defined as the heterogeneous interface between unconsolidated material, (such as sediment and soil), and altered rock, partially saturated with water and capable of delaying or storing and locally rerouting vertical infiltration to the deeper, phreatic zone of the karst aquifer (Jones et al., 2004Jones W, Culver DC, Herman JS. Epikarst, Karst Waters Institute. Special Publication Vol. 9. Charles Town: Karst Waters Institute; 2004. 160p. ).
Most species occur in shallow base-level streams, but the occurrence of species in singular habitats is notable. One remarkable species, Ituglanis epikarsticus Bichuette & Trajano, 2004 (Fig. 5A) is so far the only subterranean fish species in the world known to occur in the epikarst (Culver, Pipan, 2009Culver DC, Pipan T. The biology of caves and other subterranean habitats. Acta Carsologica. 2009; 38(2–3):309–11. https://doi.org/10.3986/ac.v38i2-3.168
https://doi.org/10.3986/ac.v38i2-3.168...
; Bichuette, 2021Bichuette ME. Ecologia de peixes de riachos de cavernas e outros habitat subterrâneos. Oecologia Australis. 2021; 25(2):620–41.https://doi.org/10.4257/oeco.2021.2502.24
https://doi.org/10.4257/oeco.2021.2502.2...
), which emphasized the urge to effectively protect the cave of its occurrence, Lapa do São Mateus, a touristic cave of northeastern Goiás. Some cavefish habitats in Bahia state are fed by aquifers, highly impacted by lowering of the phreatic level, that is observed for two new Heptapteridae catfishes, highly specialized and under threat (e.g., Rhamdiopsis sp. “caatinga”, Fig. 5B). In the case of the subterranean catfish species of the genera Glaphyropoma de Pinna, 1992 and Copionodon de Pinna, 1992 (Trichomycteridae: Copionodontinae), the streams pass through sandstone caves associated with quartzites and conglomerates, representing the only record of troglobitic fishes in this type of lithology in Brazil (Bichuette et al., 2008Bichuette ME, de Pinna MCC, Trajano E. A new species of Glaphyropoma: the first subterranean copionodontine catfish and the first occurrence of opercular odontodes in the subfamily (Siluriformes, Trichomycteridae). Neotrop Ichthyol. 2008; 6(3):301–06. https://doi.org/10.1590/S1679-62252008000300002
https://doi.org/10.1590/S1679-6225200800...
). Most Brazilian subterranean fishes live in habitats accessible through caves, except for Stygichthys typhlops Brittan & Böhlke, 1965 (Fig. 5C) and species of Phreatobius Goeldi, 1905, which are always sampled in artificial wells of karst water outcrops (Moreira et al., 2010Moreira CR, Bichuette ME, Oyakawa OT, de Pinna MCC, Trajano E. Rediscovery and redescription of the unusual subterranean characiform Stygichthys typhlops, with notes on its life history. J Fish Biol. 2010; 76(7):1815–24. https://doi.org/10.1111/j.1095-8649.2010.02625.x
https://doi.org/10.1111/j.1095-8649.2010...
) or submerged litter banks in the hyporheic zone (Muriel-Cunha, Pinna, 2005Muriel-Cunha J, de Pinna M. New data on cistern catfish, Phreatobius cisternarum, from subterranean waters at the mouth of the Amazon River (Siluriformes, Incertae Sedis). Pap Avulsos Zool. 2005; 45(26):327–39.https://doi.org/10.1590/S0031-10492005002600001
https://doi.org/10.1590/S0031-1049200500...
; Ohara et al., 2016Ohara WM, Fonseca ML, Da Costa ID. Behaviour, feeding habits and ecology of the blind catfish Phreatobius sanguijuela (Ostariophysi: Siluriformes). J Fish Biol. 2016; 89(2):1295–301. https://doi.org/10.1111/jfb.13037
https://doi.org/10.1111/jfb.13037...
), respectively. Such fragile environments are rarely reported in the literature.
A.Ituglanisepikarsticus from the Lapa do São Mateus cave, São Domingos, Goiás State, live specimen, 28 mm SL; Photo: Adriano Gambarini. B. Rhamdiopsis sp. “caatinga”, live specimen, 59 mm SL; Photo: Jonas Eduardo Gallão. C. Stygichthys typhlops from the Jaíba region, Minas Gerais State, live specimen, 25 mm SL, specimen captured in July 2008; Photo: Adriano Gambarini. All specimens were photographed in an aquarium at Laboratório de Estudos Subterrâneos, Universidade Federal de São Carlos.
Sixteen subterranean fish species were evaluated in the most recent edition of the Brazilian Red List (ICMBio, 2018Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). Livro vermelho da fauna brasileira ameaçada de extinção: Volume VI - Peixes. In: Instituto Chico Mendes de Conservação da Biodiversidade, organizers. Livro vermelho da fauna brasileira ameaçada de extinção. Brasília: ICMBio/MMA; 2018.). Nine were classified as Vulnerable (VU), five as Endangered (EN), two as Critically Endangered (CR), one as Least Concern (LC), and one as Data Deficient (DD) (Tab. 2). Besides these 16 species, which are under re-evaluation in the Red List workshops, four additional species are under evaluation for the first time (Aspidoras mephisto Tencatt & Bichuette, 2017, Ituglanis boticario Rizzato & Bichuette, 2015, Phreatobius sanguijuela Fernandez, Saucedo, Carvajal-Vallejos & Schaefer, 2007, and Rhamdia enfurnada Bichuette & Trajano, 2005, Tab. 2). In the global Red List of IUCN, only four species are included, three classified as DD (Pimelodella kronei (Miranda Ribeiro, 1907), Phreatobius cisternarum Goeldi, 1905, and Stygichthys typhlops) and one as CR (Phreatobius sanguijuela).
In total, eleven threats were identified, related to at least 15 causes (Figs. 3 and 6; Tab. 2). The main threats to their areas of occurrence are consequences of human activities related to agriculture, pasture, and hydroelectrical plans (Fig. 6). These activities affect different subterranean aquatic habitats, from shallow base-level streams to vadose tributaries, epikarst, and aquifers (Fig. 2; Tab. 2). The main consequences are alterations in the water table (level/volume and pollution) and the physicochemical characteristics of the habitats (pH and alterations and siltation/destruction of microhabitats), causing fragmentation and chemical disturbance. In addition, mining activities can be extremely harmful to this particular ichthyofauna, since can alter the physical characteristics of the habitats. Unmanaged touristic activities also represent an important threat, since can, besides alter the physical habitat, introduce species and even diseases.
The threats that affect more species are the physical change of the habitat (21 species), followed by the food restriction (14 species). The physical change of habitat is the alteration of microhabitats, such as shelters and sites for reproduction (Tab. 2); the food restriction is related to the alterations in the landscape harboring the caves and other subterranean habitats, impacting the input of food for the fish species (Tab. 2).
The basin with more threats is the upper rio Tocantins (eight) followed by upper rio Paraguaçu (six), being the four remaining river basins with two or three threats per each (Fig. 7).
Sixteen taxa (including described and undescribed ones) occur in caves inside Conservation Units (National/State Parks or Environmental Protection Areas/APA) or their boundaries, with minimal legal protection (Tab. 2).
Brazilian subterranean fishes: threats, possible causes, IUCN categories, and occurrence in Conservation Units.
Total number of Brazilian subterranean fish species affected by each type of identified threat in the present study.
DISCUSSION
The distribution gaps observed to the sampling insufficiency in several Brazilian regions, which implies in a Wallacean shortfall, an ecological concept that refers to incomplete geographic distribution of most species (Hortal et al., 2015Hortal J, de Bello F, Diniz-Filho JAF, Lewinsohn TM, Lobo JM, Ladle RJ. Seven shortfalls that beset large-scale knowledge of biodiversity. Annu Rev Ecol Evol Syst. 2015; 46:523–49. https://doi.org/10.1146/annurev-ecolsys-112414-054400
https://doi.org/10.1146/annurev-ecolsys-...
). One of the most challenging bottlenecks in planning the conservation of this ichthyofauna is the fact that, for most of the species, geographic distributions are poorly known. This issue is related to the specificity of habitats where these fishes occur, which can be interconnected in the same outcrop/landscape, on a small scale or in extensive aquifers, on a large scale. Projects considering the possibility of connectivity between these populations can address the question of effective proposal areas for conservation.
A high number of threats identified for a given species does not necessarily represent the worst-case scenario, since, for example, physical habitat changes alone (one of the threats identified for Stygichthys typhlops, one of the 11 species of São Francisco basin, in upper and middle portions) might mean that the entire habitat may be suppressed, due, for example, to mining, hydroelectrical impacts or water exploitation for large irrigation projects. In addition, when the number of threats to cave habitats per river basin is considered, the upper rio Tocantins stands out by the high number of identified threats (eight), but this is a consequence of its highly diverse subterranean ichthyofauna, including species that occur in unique and particular cave habitats (e.g., epikarst, upper vadose tributaries, base-level streams) (Gallão, Bichuette, 2018Gallão JE, Bichuette ME. Brazilian obligatory subterranean fauna and threats to the hypogean environment. Zookeys. 2018; 746:1–23. https://doi.org/10.3897/zookeys.746.15140
https://doi.org/10.3897/zookeys.746.1514...
; Bichuette, Trajano, 2021Bichuette ME, Trajano E. Monitoring Brazilian cavefish: Ecology and conservation of four threatened catfish of genusItuglanis (Siluriformes: Trichomycteridae) from Central Brazil. Diversity. 2021; 13(2):91. https://doi.org/10.3390/d13020091
https://doi.org/10.3390/d13020091...
; Bichuette, 2021Bichuette ME. Ecologia de peixes de riachos de cavernas e outros habitat subterrâneos. Oecologia Australis. 2021; 25(2):620–41.https://doi.org/10.4257/oeco.2021.2502.24
https://doi.org/10.4257/oeco.2021.2502.2...
). However, this idea must be considered with caution, since the upper rio Paraguaçu presented six threats and harbor only three subterranean species, one of the species, Rhamdiopsis krugi Bockmann & Castro, 2010, causes this bias, since the threats are several in the 12 caves where this species occurs.
Different threats can affect from biological, ecological, and evolutionary aspects of these populations. For example, Stygichthys typhlops is probably a relict, representing an unique lineage (Moreira et al., 2010Moreira CR, Bichuette ME, Oyakawa OT, de Pinna MCC, Trajano E. Rediscovery and redescription of the unusual subterranean characiform Stygichthys typhlops, with notes on its life history. J Fish Biol. 2010; 76(7):1815–24. https://doi.org/10.1111/j.1095-8649.2010.02625.x
https://doi.org/10.1111/j.1095-8649.2010...
) and the loss of phylogenetic information in a possible extinction of Stygichthys typhlops can be worst than for other subterranean fishes in Brazil, which belongs to genera widely distributed or relatively widely distributed. Anyway, any loss must be avoided.
Considering the high number of troglobitic fishes in Brazil and the absence of specific plans for the conservation of this particular ichthyofauna, the scenario is very concerning. Only the electric cavefish Eigenmannia vicentespelaea Triques, 1996 (VU), the trichomycterid Trichomycterus itacarambiensis Trajano & de Pinna, 1996 (CR) and the characiform Stygichthys typhlops (EN) are included in PANs (“Planos de Ação Nacional”), which preconize and suggest effective actions to protect the Brazilian biodiversity. Eigenmannia vicentespelaea in the “Plano de Ação Nacional para a Conservação do Patrimônio Espeleológico nas Áreas Cársticas da Bacia do Rio São Francisco”; Trichomycterus itacarambiensis in the “Plano de Ação Nacional para a Conservação das Espécies Ameaçadas de Extinção da Fauna Aquática da Bacia do Rio São Francisco” and Stygichthys typhlops in the “Plano de Ação Nacional para a Conservação das Espécies Ameaçadas de Extinção da Fauna Aquática da Bacia do Rio São Francisco” and the “Plano de Ação Nacional para a Conservação do Patrimônio Espeleológico nas Áreas Cársticas da Bacia do rio São Francisco” (Portaria MMA N° 358, September 30, 2009Ministério do Meio Ambiente (MMA). Portaria Nº 358. September 30, 2009. Available from: https://www.icmbio.gov.br/cecav/images/download/Portaria_358_2009-MMA_PNCPE.pdf
https://www.icmbio.gov.br/cecav/images/d...
). None of these plans, however, was conceived with focus on one of these species,
Manjarrés-Hernández et al., (2021)Manjarrés-Hernández A, Guisande C, García-Roselló E, Heine J, Pelayo-Villamil P, Pérez-Costas E et al. Predicting the effects of climate change on future freshwater fish diversity at global scale. Nat Conserv. 2021; 43:1–24. https://doi.org/10.3897/natureconservation.43.58997
https://doi.org/10.3897/natureconservati...
discussed predictions of losses in the biodiversity of epigean freshwater fish species as consequences of the effects of climate change. They proposed a new and robust methodological approach to predict simple species distribution for future climatic scenarios (NOO3D, ModestR software). The authors predicted, from 16,825 freshwater fish species considered (1,464,232 occurrence records), the extinction of almost half the current freshwater fish species in the coming decades, with a pronounced decline in tropical regions and greater extinction likelihood for species with smaller body size and/or limited geographical ranges. These latter characteristics are the rule for subterranean fish populations in Brazil (Bichuette, Trajano, 2010Bichuette ME, Trajano E. Conservation of subterranean fishes. In: Trajano E, Bichuette ME, Kapoor BG, editors. Biology of subterranean fishes. Enfield: Science Publishers; 2010. p.65–80. https://doi.org/10.1201/EBK1578086702
https://doi.org/10.1201/EBK1578086702...
; Bichuette, 2021Bichuette ME. Ecologia de peixes de riachos de cavernas e outros habitat subterrâneos. Oecologia Australis. 2021; 25(2):620–41.https://doi.org/10.4257/oeco.2021.2502.24
https://doi.org/10.4257/oeco.2021.2502.2...
), and studies focusing on the effects of climate changes particularly for the subterranean ichthyofauna are scarce, the need to provide information about it is urgent.
The limits of the area proposed for the protection of a given subterranean fish species, in addition to encompassing the habitat itself, must also include the micro basins and associated aquifers in which the habitat is included. This is due to the important fact that a large part of the trophic resources present in the subterranean environment is of allochthonous origin, and broader landscape impacts exert strong influences on the subterranean biota. The possibility of including undescribed species in Red Lists should also be considered, at least in the case of undescribed species with already identified, unequivocal diagnoses, and that have testimony specimens deposited in accredited scientific collections, as discussed by Gallão, Bichuette, (2012)Gallão JE, Bichuette ME. The list of endangered fauna and impediments to inclusion of species - the example of Brazilian troglobitic fish. Nat Conserv. 2012; 10(1):83–87. https://doi.org/10.4322/natcon.2012.014
https://doi.org/10.4322/natcon.2012.014...
.
Trajano (1997Trajano E. Threatened fishes of the world: Pimelodella kronei (Ribeiro, 1907) (Pimelodidae). Environ Biol Fishes. 1997; 49(3):332. https://doi.org/10.1023/A:1007353902363
https://doi.org/10.1023/A:1007353902363...
, 2008aTrajano E. Pimelodella kronei (Ribeiro, 1907). In: Machado ABM, Drummond GM, Paglia AP, editors. Livro vermelho da fauna brasileira ameaçada de extinção. Belo Horizonte: Ministério do Meio Ambiente e Fundação Biodiversitas; 2008a. p.230–31.) addressed the concern about threats identified for Pimelodella kronei and remarked the necessity of protection of this species. Gallão, Bichuette, (2012)Gallão JE, Bichuette ME. The list of endangered fauna and impediments to inclusion of species - the example of Brazilian troglobitic fish. Nat Conserv. 2012; 10(1):83–87. https://doi.org/10.4322/natcon.2012.014
https://doi.org/10.4322/natcon.2012.014...
reinforced the importance of protection of the Brazilian subterranean ichthyofauna through the use of the IUCN Red List for effective actions. These alarming concerns, however, remain, exacerbated by the increase in the number of undescribed species (Linnean shortfall – a concept that considers most of the species on Earth have not been described and/or cataloged) (Hortal et al., 2015Hortal J, de Bello F, Diniz-Filho JAF, Lewinsohn TM, Lobo JM, Ladle RJ. Seven shortfalls that beset large-scale knowledge of biodiversity. Annu Rev Ecol Evol Syst. 2015; 46:523–49. https://doi.org/10.1146/annurev-ecolsys-112414-054400
https://doi.org/10.1146/annurev-ecolsys-...
) and not evaluated in the regional, national and global lists of threatened fauna, in addition to the recent increase in the number of threats for most Brazilian landscapes and their aquatic ecosystems, including the subterranean ones. Allied to this fact, we have the current dismantling and attacks to the environmental policies in Brazil, with a significant increase in fires, deforestation, and the transfer of areas to the production sector and other activities (Thomaz et al., 2019Thomaz SM, Bustamante MMC, Val VD, Pillar LA, Turra A, Viana BF et al. Biodiversity under concerted attack in Brazil. EFFS news, 25 June 2019. https://www.freshwatersciences.eu/effs/index.asp?page=NEWS&Id=6&IdItem=240&p=#Content
https://www.freshwatersciences.eu/effs/i...
).
A possible solution for proposing and taking actions towards the protection of such particular ecosystems and their communities, not limited to the evaluation of the species themselves, is a recent proposal by the IUCN of developing categories and criteria for a Red List of Ecosystems (RLE) aimed to ecosystem risk assessment at multiple scales (Keith et al., 2015Keith DA, Rodríguez JP, Brooks TM, Burgman MA, Barrow EG, Bland L et al. The IUCN red list of ecosystems: Motivations, challenges, and applications. Conserv Lett. 2015; 8(3):214–26. https://doi.org/10.1111/conl.12167
https://doi.org/10.1111/conl.12167...
). According to this proposal, the RLE would include eight categories of risk for each ecosystem based on five quantitative criteria designed to evaluate risk symptoms in terrestrial, subterranean, freshwater, and marine ecosystems (Keith et al., 2013Keith DA, Rodríguez JP, Rodríguez-Clark KM, Nicholson E, Aapala K, Alonso A et al. Scientific Foundations for an IUCN Red List of Ecosystems. PLoS ONE. 2013; 8(5):e62111. https://doi.org/10.1371/journal.pone.0062111
https://doi.org/10.1371/journal.pone.006...
). Subterranean ecosystems are being considered in the development of RLE criteria, which has 2025 as a target date to achieve global coverage of ecosystems. The authors hope that the Brazilian subterranean fishes resist and survive until that aim is achieved.
Finally, we reinforce the importance of long-term monitoring and functional approach projects, still scarce, in conservation program proposals, allied to education projects aiming to develop public awareness.
ACKNOWLEDGEMENTS
The authors thank the members of the Laboratório de Estudos Subterrâneos (LES), Universidade Federal de São Carlos, São Carlos, Brazil, for sharing unpublished data on Brazilian cavefish species, and for their ideas and concerns about the conservation of this singular fauna. The authors also thank: L. de Assis for preparing the maps of Figs. 1 and 3; A. Gambarini for the permission to use the photos on Figs. 5A and C; Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Fundação o Boticário de Proteção à Natureza (FBPN) for financial support to MEB; the field guides E. Calvo, J. A. Santos, R. H. dos Santos, R. C. dos Santos, R. J. Silva, and S. O. do Nascimento; Grupo Bambuí de Pesquisas Espeleológicas (GBPE) and Grupo Pierre Martin de Espeleologia (GPME) for their support and indications of caves, many times resulting in ichthyological discoveries. To the three anonymnous reviewers and to the associate editor for suggestions and cristicism to improve this work.
REFERENCES
- Bichuette ME Eigenmannia vicentespelaea Triques, 1996. In: Machado ABM, Drummond GM, Paglia AP, editors. Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. Belo Horizonte: Ministério do Meio Ambiente e Fundação Biodiversitas; 2008. p.176–77.
- Bichuette ME. Ecologia de peixes de riachos de cavernas e outros habitat subterrâneos. Oecologia Australis. 2021; 25(2):620–41.https://doi.org/10.4257/oeco.2021.2502.24
» https://doi.org/10.4257/oeco.2021.2502.24 - Bichuette ME, de Pinna MCC, Trajano E. A new species of Glaphyropoma: the first subterranean copionodontine catfish and the first occurrence of opercular odontodes in the subfamily (Siluriformes, Trichomycteridae). Neotrop Ichthyol. 2008; 6(3):301–06. https://doi.org/10.1590/S1679-62252008000300002
» https://doi.org/10.1590/S1679-62252008000300002 - Bichuette ME, Trajano E. Epigean and subterranean ichthyofauna from the São Domingos karst area, upper Tocantins River basin, Central Brazil. J Fish Biol. 2003; 63(5):1100–21. https://doi.org/10.1046/j.1095-8649.2003.00227.x
» https://doi.org/10.1046/j.1095-8649.2003.00227.x - Bichuette ME, Trajano E. Conservation of subterranean fishes. In: Trajano E, Bichuette ME, Kapoor BG, editors. Biology of subterranean fishes. Enfield: Science Publishers; 2010. p.65–80. https://doi.org/10.1201/EBK1578086702
» https://doi.org/10.1201/EBK1578086702 - Bichuette ME, Trajano E. Population density and habitat of an endangered cave fish Eigenmannia vicentespelaea Triques, 1996 (Ostariophysi: Gymnotiformes) from a karst area in central Brazil. Neotrop Ichthyol. 2015; 13(1):113–22. https://doi.org/10.1590/1982-0224-20140095
» https://doi.org/10.1590/1982-0224-20140095 - Bichuette ME, Trajano E. Monitoring Brazilian cavefish: Ecology and conservation of four threatened catfish of genusItuglanis (Siluriformes: Trichomycteridae) from Central Brazil. Diversity. 2021; 13(2):91. https://doi.org/10.3390/d13020091
» https://doi.org/10.3390/d13020091 - Borghezan R. 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). [Master Dissertation]. São Paulo: Universidade de São Paulo; 2013. Available from:https://teses.usp.br/teses/disponiveis/41/41133/tde-12062013-090146/fr.php
» https://teses.usp.br/teses/disponiveis/41/41133/tde-12062013-090146/fr.php - Brasil. 2008. Decreto no 6.640, de 7 de novembro de 2008. Dá nova redação aos arts. 1°, 2°, 3°, 4° e 5o e acrescenta os arts. 5-A e 5-B ao Decreto n° 99.556, de 1 de outubro de 1990, que dispõe sobre a proteção das cavidades naturais subterrâneas existentes no território nacional. Brasília, DF, 7 de novembro de 2008. Available from: http://www.planalto.gov.br/ccivil_03/_Ato2007-2010/2008/Decreto/D6640.htm
» http://www.planalto.gov.br/ccivil_03/_Ato2007-2010/2008/Decreto/D6640.htm - Culver DC, Pipan T. The biology of caves and other subterranean habitats. Acta Carsologica. 2009; 38(2–3):309–11. https://doi.org/10.3986/ac.v38i2-3.168
» https://doi.org/10.3986/ac.v38i2-3.168 - Culver DC, Pipan T. The biology of caves and other subterranean habitats. Oxford: Oxford University Press; 2019. Available from: https://doi.org/10.1093/oso/9780198820765.001.0001
» https://doi.org/10.1093/oso/9780198820765.001.0001 - Elliott WR. Protecting caves and cave life. In: Culver DC, White WB, editors. Encyclopedia of Caves Vol. 1. Amsterdam: Elsevier; 2005. p.458–67.
- Fernandes CS, Batalha MA, Bichuette ME. Does the cave environment reduce functional diversity? PLoS ONE. 2016; 11(3):e0151958. https://doi.org/10.1371/journal.pone.0151958
» https://doi.org/10.1371/journal.pone.0151958 - Gallão JE, Bichuette ME. The list of endangered fauna and impediments to inclusion of species - the example of Brazilian troglobitic fish. Nat Conserv. 2012; 10(1):83–87. https://doi.org/10.4322/natcon.2012.014
» https://doi.org/10.4322/natcon.2012.014 - Gallão JE, Bichuette ME. Brazilian obligatory subterranean fauna and threats to the hypogean environment. Zookeys. 2018; 746:1–23. https://doi.org/10.3897/zookeys.746.15140
» https://doi.org/10.3897/zookeys.746.15140 - Hortal J, de Bello F, Diniz-Filho JAF, Lewinsohn TM, Lobo JM, Ladle RJ. Seven shortfalls that beset large-scale knowledge of biodiversity. Annu Rev Ecol Evol Syst. 2015; 46:523–49. https://doi.org/10.1146/annurev-ecolsys-112414-054400
» https://doi.org/10.1146/annurev-ecolsys-112414-054400 - Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). Livro vermelho da fauna brasileira ameaçada de extinção: Volume VI - Peixes. In: Instituto Chico Mendes de Conservação da Biodiversidade, organizers. Livro vermelho da fauna brasileira ameaçada de extinção. Brasília: ICMBio/MMA; 2018.
- Jones W, Culver DC, Herman JS. Epikarst, Karst Waters Institute. Special Publication Vol. 9. Charles Town: Karst Waters Institute; 2004. 160p.
- Juberthie C. The diversity of the karstic and pseudokarstic hypogean habitats in the world. In: Wilkens H, Culver D, Humphreys WF, editors. Ecosystems of the world Vol. 30 Subterranean Ecosystems. Amsterdam: Elsevier; 2000a. p.17–39.
- Juberthie C. Conservation of subterranean habitats and species. In: Wilkens W, Culver DC, Humphreys WF, editors. Ecosystems of the World Vol. 30 Subterranean Ecosystems. Amsterdam: Elsevier; 2000b. p.691–700.
- Keith DA, Rodríguez JP, Brooks TM, Burgman MA, Barrow EG, Bland L et al The IUCN red list of ecosystems: Motivations, challenges, and applications. Conserv Lett. 2015; 8(3):214–26. https://doi.org/10.1111/conl.12167
» https://doi.org/10.1111/conl.12167 - Keith DA, Rodríguez JP, Rodríguez-Clark KM, Nicholson E, Aapala K, Alonso A et al Scientific Foundations for an IUCN Red List of Ecosystems. PLoS ONE. 2013; 8(5):e62111. https://doi.org/10.1371/journal.pone.0062111
» https://doi.org/10.1371/journal.pone.0062111 - Mammola S, Cardoso P, Culver DC, Deharveng L, Ferreira RL, Fisër C et al Scientists’ warning on the conservation of subterranean ecosystems. Bioscience. 2019; 69(8):641–50. https://doi.org/10.1093/biosci/biz064
» https://doi.org/10.1093/biosci/biz064 - Manjarrés-Hernández A, Guisande C, García-Roselló E, Heine J, Pelayo-Villamil P, Pérez-Costas E et al Predicting the effects of climate change on future freshwater fish diversity at global scale. Nat Conserv. 2021; 43:1–24. https://doi.org/10.3897/natureconservation.43.58997
» https://doi.org/10.3897/natureconservation.43.58997 - Ministério do Meio Ambiente (MMA). Portaria Nº 358. September 30, 2009. Available from: https://www.icmbio.gov.br/cecav/images/download/Portaria_358_2009-MMA_PNCPE.pdf
» https://www.icmbio.gov.br/cecav/images/download/Portaria_358_2009-MMA_PNCPE.pdf - Moreira CR, Bichuette ME, Oyakawa OT, de Pinna MCC, Trajano E. Rediscovery and redescription of the unusual subterranean characiform Stygichthys typhlops, with notes on its life history. J Fish Biol. 2010; 76(7):1815–24. https://doi.org/10.1111/j.1095-8649.2010.02625.x
» https://doi.org/10.1111/j.1095-8649.2010.02625.x - Mugnai R, Messana G, Di Lorenzo T. The hyporheic zone and its functions: revision and research status in Neotropical regions. Braz J Biol. 2015; 75(3):524–34. https://dx.doi.org/10.1590/1519-6984.15413
» https://dx.doi.org/10.1590/1519-6984.15413 - Muriel-Cunha J, de Pinna M. New data on cistern catfish, Phreatobius cisternarum, from subterranean waters at the mouth of the Amazon River (Siluriformes, Incertae Sedis). Pap Avulsos Zool. 2005; 45(26):327–39.https://doi.org/10.1590/S0031-10492005002600001
» https://doi.org/10.1590/S0031-10492005002600001 - Niemiller ML, Bichuette ME, Chakrabarty P, Fenolio DB, Gluesenkamp AG, Soares D et al Cavefishes. In: White WB, Culver DC, Pipan T, editors. Encyclopedia of Caves. Amsterdam: Elsevier; 2019. p.227–36.
- Ohara WM, Fonseca ML, Da Costa ID. Behaviour, feeding habits and ecology of the blind catfish Phreatobius sanguijuela (Ostariophysi: Siluriformes). J Fish Biol. 2016; 89(2):1295–301. https://doi.org/10.1111/jfb.13037
» https://doi.org/10.1111/jfb.13037 - Poulson TL, White WB. The cave environment. Science. 1969; 3897(165):971–80.
- Rabello GCR. Ictiofauna da região da Serra da Canastra, Minas Gerais: cavernas são filtros ambientais considerando-se riqueza, diversidade e comportamento alimentar? [Master Dissertation]. São Carlos: Universidade Federal de São Carlos; 2021. Available from: https://repositorio.ufscar.br/handle/ufscar/14060
» https://repositorio.ufscar.br/handle/ufscar/14060 - Ratton P, Ferreira RL, Pompeu PS. Fish community of a small karstic Neotropical drainage and its relationship with the physical habitat. Mar Freshwater Res. 2018; 69(8):1312–20. https://doi.org/10.1071/MF17167
» https://doi.org/10.1071/MF17167 - Thomaz SM, Bustamante MMC, Val VD, Pillar LA, Turra A, Viana BF et al Biodiversity under concerted attack in Brazil. EFFS news, 25 June 2019. https://www.freshwatersciences.eu/effs/index.asp?page=NEWS&Id=6&IdItem=240&p=#Content
» https://www.freshwatersciences.eu/effs/index.asp?page=NEWS&Id=6&IdItem=240&p=#Content - Trajano E. Threatened fishes of the world: Pimelodella kronei (Ribeiro, 1907) (Pimelodidae). Environ Biol Fishes. 1997; 49(3):332. https://doi.org/10.1023/A:1007353902363
» https://doi.org/10.1023/A:1007353902363 - Trajano E Pimelodella kronei (Ribeiro, 1907). In: Machado ABM, Drummond GM, Paglia AP, editors. Livro vermelho da fauna brasileira ameaçada de extinção. Belo Horizonte: Ministério do Meio Ambiente e Fundação Biodiversitas; 2008a. p.230–31.
- Trajano E Trichomycterus itacarambiensis Trajano & de Pinna, 1996. In: Machado ABM, Drummond GM, Paglia AP, editors. Livro vermelho da fauna brasileira ameaçada de extinção. Belo Horizonte: Ministério do Meio Ambiente e Fundação Biodiversitas; 2008b. p.252–53.
- Trajano E. Ecological classification of subterranean organisms. In: White WB, Culver DC, editors. Encyclopedia of Caves. Amsterdam: Elsevier; 2012. p.275–77.
- Trajano E, Bichuette ME. Subterranean fishes of Brazil. In: Trajano E, Bichuette ME, Kapoor BG, editors. Biology of Subterranean Fishes. Enfield: Science Publishers; 2010. p.331–56.
- Trajano E, Gallão JE, Bichuette ME. Spots of high diversity of troglobites in Brazil: the challenge of measuring subterranean diversity. Biodivers Conserv. 2016; 25:1805–28. https://doi.org/10.1007/s10531-016-1151-5
» https://doi.org/10.1007/s10531-016-1151-5
ADDITIONAL NOTES
-
HOW TO CITE THIS ARTICLE
Bichuette ME, Gallão JE. Under the surface: what we know about the threats to subterranean fishes in Brazil. Neotrop Ichthyol. 2021; 19(3):e210089. https://doi.org/10.1590/1982-0224-2021-0089
Edited-by
Publication Dates
-
Publication in this collection
08 Oct 2021 -
Date of issue
2021
History
-
Received
28 Jan 2021 -
Accepted
23 Aug 2021