Abstract:

Limiting factors of subterranean environments, high relative air humidity and, especially, permanent darkness, represent ecological filters for organisms and biodiversity patterns of surface and subterranean communities display wide disparities. Subterranean diversity and singularity are, thus, better expressed when the common presence of rare and endemic species are considered. Our study aimed to describe the diversity of the cave fauna from 14 caves from Peruaçu Caves National Park (PCNP), eastern Brazil. We analyzed the regional diversity using the index that includes the average taxonomic distinction (TD - Δ +, AvTD). We recorded 1,674 individuals belonging to 10 Classes and 237 morphotypes, 11 troglobitic and two troglomorphic and possible troglobites. Greatest species abundance (N=330) and richness (s=76) were recorded at Lapa do Cipó cave, followed by Gruta Olhos d’Água (N=330, s=71), which shows the highest TD value (Δ + = 90.18) in relation to the others, including the richest Lapa do Cipó (Δ + = 85.24), consequence of the several taxonomic units with large number of species. The below-expected values of TD (Δ + = 87.70) may indicate anthropic impacts on these communities. Our results demonstrate that Gruta Olhos d’ Água and Lapa do Cipó caves are the most important sites for the occurrence of endemic and troglobitic species and may be part of a complex system that should be considered for a more efficient conservation planning.

Keywords:
Diversity; Gruta Olhos d’ Água cave; troglobites; subterranean environment

Resumo:

Fatores limitantes dos ambientes subterrâneos como alta umidade relativa do ar e, principalmente, a falta de luz, representam filtros ecológicos para organismos e padrões de biodiversidade de comunidades superficiais e subterrâneas, nas quais mostram grandes disparidades. Diversidade e singularidade subterrâneas são, portanto, mais bem expressas quando os presença de espécies raras e endêmicas. Nosso estudo teve como objetivo descrever a diversidade da fauna da caverna de 14 cavernas do Parque Nacional das Cavernas de Peruaçu (PCNP), leste do Brasil. Analisamos a diversidade regional usando o índice que inclui a distinção taxonômica média (TD - Δ +, AvTD). Registramos 1,674 indivíduos pertencentes a 10 classes e 237 morfotipos, 11 troglóbios e dois troglomórficos e possíveis troglóbios. A maior abundância de espécies (N = 330) e riqueza (s = 76) foram registradas na caverna da Lapa do Cipó, seguida por Gruta Olhos d´Água (N = 330, s = 71), que mostra o maior valor de DT (Δ + = 90,18) em relação aos outros, incluindo a Lapa do Cipó mais rica (Δ + = 85,24), consequência das várias unidades taxonômicas com grande número de espécies. Os valores abaixo do esperado de TD (Δ + = 87,70) podem indicar impactos antrópicos nessas comunidades. Nossos resultados demonstram que as cavernas Gruta Olhos d ‘Água e Lapa do Cipó são os locais mais importantes para a ocorrência de espécies endêmicas e troglóbias e pode fazer parte de um sistema complexo que deve ser considerado por mais planejamento eficiente de conservação.

Palavras-chave:
Diversidade; Gruta Olhos d’ Água; troglóbios; ambiente subterrâneo

Introduction

Subterranean or hypogean environments have striking features which represent environmental filters, because selective regimen contrasts sharply with those of surface environments. Permanent darkness at deeper zones is the main difference (Hoenen 2005HOENEN, S. 2005. Circadian patterns in the activity of the Brazilian cave cricket Strinatia brevipennis Ensifera Phalangopsidae. Eur. J. Entomol. 102(4): 663-668., Hervant et al. 2000HERVANT, F. MATHIEU, J. DURAND, J. P. 2000. Metabolism and circadian rhythms of the European blind cave salamander Proteus anguinus and a facultative cave dweller, the Pyrenean newt Euproctusasper. Can. J. Zool. 78(8): 1427-1432., Poulson & White 1969POULSON, T. L. WHITE, W. B. The cave environment. Science, Washington/Cambridge, v. 3897, p. 971-980, 1969.), leading to the dependence of allochthonous energy inputs because photoautotrophic organisms do not thrive there (Poulson & Lavoie 2000POULSON, T. L. LAVOIE, K. The trophic basis of subsurface ecosystems. 2000.). Environmental stability is other noteworthy aspect of subterranean ecosystems. Unlike surface communities, little variation occurs in parameters such temperature and air humidity, due to the isolation caused by the surrounding rock (Juberthie 2000JUBERTHIE, C. 2000. The diversity of the karstic and pseudokarstic hypogean habitats in the world. In:, Culver & Pipan 2009CULVER, D. C., PIPAN, T. 2009. The biology of caves and other subterranean habitats. Oxford University Press, USA.). Such contrasts between subterranean and superficial environments are related to processes of colonisation and reproductive isolation of subterranean species (Trajano 2012TRAJANO, E. 2012. Ecological classification of subterranean organisms. In: CULVER, D.C. WHITE W.B. San Diego, Academic. The encyclopedia of caves. 275-277.).

Subterranean communities are formed by populations which present distinct ecological-evolutionary relationships with the environment and, consequently, may be classified at three categories (Racovitza 1907RACOVITZA, E. G. 1907. Essai sur les problèmes biospéologiques. Arch. zool. exp. gen. 6. 371-488., Trajano 2012TRAJANO, E. 2012. Ecological classification of subterranean organisms. In: CULVER, D.C. WHITE W.B. San Diego, Academic. The encyclopedia of caves. 275-277.), according to its degree of specialisation to the subterranean realm: trogloxenes are those who need to leave the cave periodically in order to complete its life cycle because subterranean resources are insufficient (Racovitza 1907RACOVITZA, E. G. 1907. Essai sur les problèmes biospéologiques. Arch. zool. exp. gen. 6. 371-488.). Troglophiles are those capable of completing its life cycle inside as well as outside subterranean environments. They represent the majority of the taxa found at subterranean communities (Racovitza 1907RACOVITZA, E. G. 1907. Essai sur les problèmes biospéologiques. Arch. zool. exp. gen. 6. 371-488.). Some species only live at subterranean environments (Racovitza 1907RACOVITZA, E. G. 1907. Essai sur les problèmes biospéologiques. Arch. zool. exp. gen. 6. 371-488.), not being able to colonise surface environments anymore, because they evolved isolated at subterranean environments and, during this period, accumulated specialisations that hampers survival or reproduction in surface environments. They are called troglobites (Racovitza, 1907RACOVITZA, E. G. 1907. Essai sur les problèmes biospéologiques. Arch. zool. exp. gen. 6. 371-488.). This condition is recognised by the presence of autapomorphies acquired throughout evolutionary process, known as troglomorphisms (Holsinger & Culver 1988HOLSINGER, J. R & CULVER, D. C. 1988. The invertebrate cave fauna of virginia and a part of eastern tennessee-zoogeography and ecology. Brimleyana. 14: 1-162., Holsinger 1988HOLSINGER, J. R. 1988. Troglobites: The evolution of cave-dwelling organisms. American Scientist. 76: 146-153., Trajano & Bichuette 2010TRAJANO, E. & BICHUETTE, M. E. 2010. Diversity of Brazilian subterranean invertebrates with a list of troglomorphic taxa. Subterranean Biology. 7, 1-16.). Even though the term troglomorphism (sensuChristiansen 1962CHRISTIANSEN, K. 1962. Proposition pour la classification des animaux cavernicoles. Spelunca 2: 76-78.) had been originally proposed for morphological characteristics, it has been applying to behavioural and physiological characteristics as well (Barr 1968BARR, T. C. 1968. Cave ecology and the evolution of troglobites. In Evolutionary biology. Springer, Boston, MA, p. 35-102.). This classification has been extended and discussed by Trajano and Cobolli (2012)TRAJANO, E. & COBOLLI, M. 2012. Evolution of lineages. In: WHITE, W. B. CULVER, D.C. Encyclopedia of Caves. Amsterdam: Elsevier Academic Press. 2012 p. 230-234. to include source-population concept and, thus, population characteristics has been included for recognizing the troglobitic status of a given species.

Diversity patterns of subterranean and superficial communities show significant disparities. Even though richness of subterranean communities is much lower when compared to superficial communities, it can be considered high on a global scale (Gibert & Deharveng 2002GIBERT, J., DEHARVENG, L. 2002. Subterranean Ecosystems: a Truncated Functional Biodiversity. BioScience. 52: 473-481.). In addition, when lineages that colonised both habitats at the same geographical area are compared, subterranean communities have much higher proportion of endemic species than superficial communities (Gibert & Deharveng 2002GIBERT, J., DEHARVENG, L. 2002. Subterranean Ecosystems: a Truncated Functional Biodiversity. BioScience. 52: 473-481.). Recognition of such patterns is essential to support conservation proposals (Trajano 2010TRAJANO, E. 2010. Políticas de conservação e critérios ambientais: princípios, conceitos e protocolos. Estudos avançados. 24. 135-146.).

Knowledge about Brazilian subterranean fauna has been broadened at the last two decades. The first faunistic lists were produced for the karst area of Ribeira Valley (Trajano & Gnaspini 1991TRAJANO, E. & GNASPINI, P. 1991. Notes on the food webs in caves of southeastern Brazil. Mémories de Biospéologie. Moulis. 8. 75-79.), states of São Paulo and Paraná (Trajano & Bichuette 2010TRAJANO, E. & BICHUETTE, M. E. 2010. Diversity of Brazilian subterranean invertebrates with a list of troglomorphic taxa. Subterranean Biology. 7, 1-16.). Later, other regions had their diversity assessed, including karst areas at the states of Minas Gerais, Bahia, Mato Grosso do Sul, Goiás and Rio Grande do Norte (Gnaspini & Trajano 1994GNASPINI, P. TRAJANO, E. 1994. Brazilian cave invertebrates, with a checklist of troglomorphic taxa. Rev. Bras. Entomol. 38: 549-584., Pinto-da-Rocha 1993PINTO-DA-ROCHA, R. 1993. Invertebrados cavernícolas da porção meridional da Provincia Espeleológica do Vale do Ribeira, Sul do Brasil. Rev. Bras. Zool. 10: 229-255., Trajano & Bichuette 2010TRAJANO, E. & BICHUETTE, M. E. 2010. Diversity of Brazilian subterranean invertebrates with a list of troglomorphic taxa. Subterranean Biology. 7, 1-16., Ferreira et al. 2010FERREIRA, R.L., PROUS, X., BERNARDI, L.F.O., SOUAZ-SILVA, M. 2010. Fauna subterrânea do Estado do Rio Grande do Norte: caracterização e impactos. Rev. Bras. Esp. 1: 25-51., Gallão & Bichuette 2018GALLÃO, J. E., BICHUETTE, M. E. 2018. Brazilian obligatory subterranean fauna and threats to the hypogean environment. ZooKeys 746: 1-23. https://doi.org/10.3897/zookeys.746.15140.
https://doi.org/10.3897/zookeys.746.1514... ).

Some are important because they have high species richness, presence of phylogenetic indicators or high genetic diversity. (Trajano et al. 2016TRAJANO, E., GALLÃO, J. E., BICHUETTE, M. E. 2016. Spots of high diversity of troglobites in Brazil: the challenge of measuring subterranean diversity. Biodiversity & Conservation. 25, 1805-1828.). High genetic diversity is based on the degree of specialisation of individual species, with accumulation of autapomorphies, that may evolve into a troglobitic species, while phylogenetic indicators are related to the presence of biogeographical relicts (Trajano et al. 2016TRAJANO, E., GALLÃO, J. E., BICHUETTE, M. E. 2016. Spots of high diversity of troglobites in Brazil: the challenge of measuring subterranean diversity. Biodiversity & Conservation. 25, 1805-1828.). Exclusively subterranean populations are generally fragile and represent one of the main arguments in favour of the conservation of caves and its systems (Trajano 2010TRAJANO, E. 2010. Políticas de conservação e critérios ambientais: princípios, conceitos e protocolos. Estudos avançados. 24. 135-146., Trajano et al. 2016TRAJANO, E., GALLÃO, J. E., BICHUETTE, M. E. 2016. Spots of high diversity of troglobites in Brazil: the challenge of measuring subterranean diversity. Biodiversity & Conservation. 25, 1805-1828., Gallão & Bichuette 2018GALLÃO, J. E., BICHUETTE, M. E. 2018. Brazilian obligatory subterranean fauna and threats to the hypogean environment. ZooKeys 746: 1-23. https://doi.org/10.3897/zookeys.746.15140.
https://doi.org/10.3897/zookeys.746.1514... ). For this reason, to understand the evolutionary processes and patterns that occur in underground environments, faunal studies are needed to identify high diversity spots and to propose actions and political for conservation. (Trajano et al. 2016TRAJANO, E., GALLÃO, J. E., BICHUETTE, M. E. 2016. Spots of high diversity of troglobites in Brazil: the challenge of measuring subterranean diversity. Biodiversity & Conservation. 25, 1805-1828.).

We investigated the biodiversity of caves located at Peruaçu Caves National Park (PCNP), northern state of Minas Gerais, taking into account not only the number of species, but its identity as well. The region has 140 caves registered so far, of which, Gruta Olhos d’ Água cave is the largest one, with approximately 9,100 m of conduits and passageways, and harbors the highest number of troglobites (Trajano et al. 2016TRAJANO, E., GALLÃO, J. E., BICHUETTE, M. E. 2016. Spots of high diversity of troglobites in Brazil: the challenge of measuring subterranean diversity. Biodiversity & Conservation. 25, 1805-1828., Gallão & Bichuette 2018GALLÃO, J. E., BICHUETTE, M. E. 2018. Brazilian obligatory subterranean fauna and threats to the hypogean environment. ZooKeys 746: 1-23. https://doi.org/10.3897/zookeys.746.15140.
https://doi.org/10.3897/zookeys.746.1514... ). For this, two main questions were considered: 1) Do the PCNP caves have high phylogenetic diversity? 2) Does Gruta Olhos d ‘Água cave present higher diversity compared to the other caves of the PCNP?

Materials and Methods

Study Area

We conducted the study herein presented in 14 caves located at Peruaçu Caves National Park (PCNP), municipalities of Itacarambi and Januária, northern of Minas Gerais state (Figure 1). The region has outcrops composed by carbonate rocks from Bambuí Group, more precisely laminated limestone and dolomites from Januária-Itacarambi Formation (Piló & Kohler 1991PILÓ, L. B. & KÖHLER, H.C. 1991. Do Vale do Peruaçu ao São Francisco : uma viagem ao interior da terra. Anais do III Congresso da Associação Brasileira do Estudo do Quaternário. Belo Horizonte. 2: 57-73.). Inside the limits of PCNP, Peruaçu river traverses about 17 Km of its valley surrounded by enormous rocky walls, channels and dolines, forming the Peruaçu river, left tributary of the upper-middle São Francisco River.

Peruaçu Valley, where PCNP is located, occurs in a transition zone between Cerrado and Caatinga morphoclimatic Domains (Ab’Saber 1977AB’SABER, A. N. 1977. Os domínios morfoclimáticos na América do Sul. Primeira aproximação. São Paulo, Geomorfologia.). Climate covering Peruaçu, according to Köppen-Geiger, is tropical humid with dry winters (“Aw”) (Peel et al. 2007PEEL, M. C. FINLAYSON, B. L. MCMAHON T. A. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrol. Earth Syst. Sc. 42: 439-473.), characterised by dry winters, between March and October, and rainy summers, between April and November, with annual average temperature of 24°C and average annual rainfall of 800 mm (INMET 2010Instituto Nacional de Metereologia. http://www.inmet.gov.br/portal/. Acessado em Abril de 2010.
http://www.inmet.gov.br/portal/... ).

Samplings

We conducted field campaigns between the years along the years of 2013 and 2015 at the following caves: Lapa da Onça, Lapa d’ Água, Lapa do Branco I, Lapa do Branco IV, Toca do Pedrinho, Toca Mina d’Água, Gruta Olhos d’ Água, Lapa do Cipó, Lapa do Mogno, Gruta Troncos, Caverna dos Cascudos, Caverna Janelão, Caverna Boquete and Caverna Bonita (Figure 2). During this period, we visited Gruta Olhos d’ Água seven times, Lapa do Cipó four times and only once the other caves.

We sampled potential microhabitats by active search and then the collected specimens were euthanized and preserved in 50% and 70% alcohol. We then identified morphotypes at the least inclusive taxonomic level we could reach using specialised literature (Borror et al., 1989; Adis, 2002; Costa et al., 2006). In addition, we consulted specialists in order to refine identification: Bolfarini, M.P. (Orthoptera - LES/UFSCar), Brescovit, A. (Ctenidae - Instituto Butantan), Carvalho, L.S. (Pholcidae - UFMG), Chagas-Jr, A. (Chilopoda - UFMT), Fernandes, C.S. (Isopoda - LES/UFSCar), Gallão, J.E. (Scorpiones - LES/UFSCar), Gallo, J.S. (Diplopoda - LES/UFSCar), Prado, L.P. (Formicidae - Museu de Zoologia/USP), Cizauskas, I. (Araneae - Museu de Zoologia/USP), von Schimonsky, D.M. (Pseudoscorpiones - LES/UFSCar) and Salvador, R.D. (Gastropoda - State Museum of Natural History Stuttgart, Germany).

Data analysis

We used Taxonomic Distinctness index (TD) (Δ+, AvTD) for diversity analysis, defined as the mean distance between two randomly chosen species, traced by means of a Linnean or phylogenetic classification of all the species in the data-set (Warwick & Clarke 1998WARWICK, R.M. CLARKE K.R. 1998. Taxonomic distinctness and environmental assessment. J Appl Ecol. 35. 532-543., Clarke & Warwick 2001CLARKE, K.R. & WARWICK, R.M. 2001. A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Mar. Ecol. Prog. Ser. 216: 265-278.).

Differently of a traditional diversity index, the Taxonomic Distinctness TD (Δ+, AvTD) take into account the abundance of rare and common species by giving them different weights (Warwick & Clarke 1998WARWICK, R.M. CLARKE K.R. 1998. Taxonomic distinctness and environmental assessment. J Appl Ecol. 35. 532-543., Cianciaruso et al. 2009CIANCIARUSO, M. V. SILVA, I. A. BATALHA, M. A. 2009. Diversidades filogenética e funcional: novas abordagens para a Ecologia de comunidades. Biota Neotrop. 93: http://www.biotaneotropica.org.br/v9n3/en/abstract?article+bn01309032009.
http://www.biotaneotropica.org.br/v9n3/e... ). Besides considering the relative contribution of each species at a given community by using the number of species and the distribution of individuals, TD also includes the taxonomic value of each species.

Taxonomic distinctness is, thus, estimated by the expected number of nodes between any two individuals of different species randomly drawn from the full species set. The biggest number of nodes or links among them, the higher will be the distinctness of a given species (Warwick & Clarke 1998WARWICK, R.M. CLARKE K.R. 1998. Taxonomic distinctness and environmental assessment. J Appl Ecol. 35. 532-543., Cianciaruso et al. 2009CIANCIARUSO, M. V. SILVA, I. A. BATALHA, M. A. 2009. Diversidades filogenética e funcional: novas abordagens para a Ecologia de comunidades. Biota Neotrop. 93: http://www.biotaneotropica.org.br/v9n3/en/abstract?article+bn01309032009.
http://www.biotaneotropica.org.br/v9n3/e... ). Also, Taxonomic Distinctness index is a robust measure, when compared to traditional indexes of diversity, because it is independent of sampling effort (Warwick & Clarke 1998WARWICK, R.M. CLARKE K.R. 1998. Taxonomic distinctness and environmental assessment. J Appl Ecol. 35. 532-543.). We used PRIMER 7 statistical package to calculate TD (Δ+, AvTD) (Clarke & Gorley 2015CLARKE, K. R. & GORLEY, R. N. 2015. Primer v7: User manual/tutorial. Plymouth, UK: PRIMER-E.) using the data-set.

Results

We recorded a total abundance of 1,674 individuals inside all caves we visited, from 237 morphotypes inside ten Classes: Actinopterygii (Osteichthyes), Amphibia, Arachnida, Chilopoda, Clitellata, Diplopoda, Entognatha, Gastropoda, Insecta and Malacostraca. Both Arachnida and Insecta were richer (42.2% and 38.5%, respectively) and more abundant (46.6% and 35.9%, respectively) than the other recorded Classes.

The sole representative of Actinopterygii was the troglobitic catfish T. itacarambiensis, endemic from Gruta Olhos d’ Água cave. Entognatha and Mammalia presented equal relative abundance of 1.06% and richness at 0.81% and 1.63%, respectively. Mammals were represented by the bats Carollia perspicillata, Desmodus rotundus, Diphylla ecaudata and an unidentified Glossophaginae, all recorded at Gruta Olhos d’ Água. Amphibia, Clitellata and Actinopterygii, were the less abundant, with 0.22%, 0.28% and 0.67%, respectively and the less rich, with 0.81%, 0.81% and 0.4%, respectively. Diplopoda had an abundance of 1.63% and a richness of 2.04%, while Chilopoda had abundance of 1.23% and richness of 2.86%. Diplopods Katantodesmus showed a small abundance in several stretches of Gruta Olhos d’ Água, particularly at sediment banks.

Relative abundance of Malacostraca and Gastropoda represented 8.65% and 2.58% out of the total, respectively. When considering relative richness, Gastropoda had 6.55% and Malacostraca, 3.27%. Spiders, herein including both infraorders Araneomorphae and Mygalomorphae, represented 60.7% of all arachnids recorded, with predominance of Araneomorphae. Less representative but not least important, were the arachnids of the following Orders: Opiliones (14.3%), Amblypygi (1.3%), Pseudoscorpiones (12.1%), Scorpiones (1.2%), Acari (5.4%) and Opilioacarida (0.9%) (Figure 3). Insects were represented by 13 Orders with the predominance of Coleoptera (19.3%), followed by Lepidoptera (16.6%) and Diptera (19.3%).

The PCNP has 11 troglobitic species described (Table 1), such as the amphibious isopod Xangoniscus odaraCampos-Filho, Araujo & Taiti, 2014CAMPOS-FILHO, I. S. BICHUETTE, M. E. TAITI, S. 2016. Three new species of terrestrial isopods Crustacea, Isopoda, Oniscidea from Brazilian caves. Nauplius. 24. (Figure 4a), found at small puddles (Campos-Filho et al. 2014CAMPOS-FILHO, I. S. BICHUETTE, M. E. TAITI, S. 2016. Three new species of terrestrial isopods Crustacea, Isopoda, Oniscidea from Brazilian caves. Nauplius. 24.) and under submerged rocks inside Lapa do Cipó cave; the cricket Endecous peruassuensisBolfarini & Bichuette, 2015BOLFARINI, M. P. BICHUETTE, M. E. 2015. Endecous peruassuensis n. sp. Orthoptera: Grylloidea: Phalangopsidae from caves of Eastern Brazil: evidence of isolation in the subterranean realm and discussion about troglomorphisms. Zootaxa. 4032 (3): 297-308. (Figure 4b) from Gruta Olhos d’ Água and Lapa do Cipó caves (Bolfarini & Bichuette 2015BOLFARINI, M. P. BICHUETTE, M. E. 2015. Endecous peruassuensis n. sp. Orthoptera: Grylloidea: Phalangopsidae from caves of Eastern Brazil: evidence of isolation in the subterranean realm and discussion about troglomorphisms. Zootaxa. 4032 (3): 297-308.), the relict Kimulidae harvestmen, Relictopiolus galadrielPérez-González, Monte & Bichuette, 2017PÉREZ-GONZÁLEZ, A., CECCARELLI. F.S., MONTE, B.G.O., PROUD, D.N., DASILVA, M.B., BICHUETTE, M.E. 2017. Light from dark: A relictual troglobite reveals a broader ancestral distribution for kimulid harvestmen Opiliones: Laniatores: Kimulidae in South America. PLoS ONE 1211: e0187919. https://doi.org/10.1371/journal.pone.0187919.
https://doi.org/10.1371/journal.pone.018... (Pérez-González et al. 2017PÉREZ-GONZÁLEZ, A., CECCARELLI. F.S., MONTE, B.G.O., PROUD, D.N., DASILVA, M.B., BICHUETTE, M.E. 2017. Light from dark: A relictual troglobite reveals a broader ancestral distribution for kimulid harvestmen Opiliones: Laniatores: Kimulidae in South America. PLoS ONE 1211: e0187919. https://doi.org/10.1371/journal.pone.0187919.
https://doi.org/10.1371/journal.pone.018... ) (Figures 4c), the pseudoscorpion Pseudochthonius biseriatusMahnert, 2001MAHNERT, V. 2001. Cave-dwelling pseudoscorpions Arachnida, Pseudoscorpiones from Brazil. Rev. Suisse. Zool. 108: 95-148. (Figure 4d) and the recently described centipede from Gruta do Janelão cave, Schendylops janelaoNunes, Chagas-Jr & Bichuette, 2019NUNES G. A., CHAGAS-JR A., BICHUETTE M. E. 2019. A new centipede Schendylops Cook from eastern Brazil: the first troglobitic geophilomorph for South America (Geophilomorpha, Schendylidae). Zootaxa. 4691 (4): 386-400. (Nunes et al. 2019NUNES G. A., CHAGAS-JR A., BICHUETTE M. E. 2019. A new centipede Schendylops Cook from eastern Brazil: the first troglobitic geophilomorph for South America (Geophilomorpha, Schendylidae). Zootaxa. 4691 (4): 386-400.) (Table 1). In addition to those described, we recorded species with conspicuous troglomorphisms such as the Diplopoda of family Oniscodesmidae (Figure 4f) and one species of Collembola (Entognatha). For troglophile category, a new spider of genus Plato was recorded (I. Cizauskas, pers. comm).

Development and extension of aphotic zones were the most contrasting physical parameters when comparing the caves (Table 2). Gruta Olhos d’ Água is the longest cave with an extensive aphotic zone in the region, Gruta do Janelão presents large galleries and an extensive twilight zone with several openings to the epigean environment. The other caves show small extensions, some without aphotic zones or perennial drainages, such as Lapa do Sonho, Toca do Pedrinho and Gruta Mina d’ Água. A general characterization of each cave is presented at Table 2.

Expected Taxonomic Distinctness (TD, Δ+) was 87.7. The highest value of TD (Δ+) was of Gruta Olhos d’ Água (Δ+ = 90.18) (Figure 5). Four caves presented values of TD lower than expected and outside the confidence interval: Caverna Cascudo (Δ+ = 71.21), Caverna Boquete (Δ+ = 81.54) and Lapa dos Sonhos (Δ+ = 83.07) (Figure 5, Table 3).

Discussion

Subterranean fauna of PCNP is remarkable. Our results corroborate the hypothesis that Gruta Olhos d’Água cave is a spot of subterranean biodiversity (Trajano et al. 2016TRAJANO, E., GALLÃO, J. E., BICHUETTE, M. E. 2016. Spots of high diversity of troglobites in Brazil: the challenge of measuring subterranean diversity. Biodiversity & Conservation. 25, 1805-1828.) probably due the long period of environmental stability, as evidenced by its high troglobitic species richness, at least 13 so far (Perez-González et al. 2017, Gallão & Bichuette 2018GALLÃO, J. E., BICHUETTE, M. E. 2018. Brazilian obligatory subterranean fauna and threats to the hypogean environment. ZooKeys 746: 1-23. https://doi.org/10.3897/zookeys.746.15140.
https://doi.org/10.3897/zookeys.746.1514... ). In addition, we identified another important locality of endemic and troglobitic species, the Lapa do Cipó cave (Table 4).

Besides the great number of taxa, we also recorded a significant number of troglobites at Peruaçu region. For Brazil, the highest number of troglobites is recorded at Areias System, located at the Alto Ribeira karst area, state of São Paulo, accounting for 20 species described so far, followed by Alambari de Cima cave, at the same region, with 10 troglobites (Trajano & Bichuette 2010TRAJANO, E. & BICHUETTE, M. E. 2010. Diversity of Brazilian subterranean invertebrates with a list of troglomorphic taxa. Subterranean Biology. 7, 1-16., Trajano et al. 2016TRAJANO, E., GALLÃO, J. E., BICHUETTE, M. E. 2016. Spots of high diversity of troglobites in Brazil: the challenge of measuring subterranean diversity. Biodiversity & Conservation. 25, 1805-1828.). Other spot of high subterranean diversity (Gallão & Bichuette 2015GALLAO, J. E., BICHUETTE, M. E. 2015. Taxonomic distinctness and conservation of a new high biodiversity subterranean area in Brazil. An. Acad. Bras. Ciênc. 87: 209-217., Trajano et al. 2016TRAJANO, E., GALLÃO, J. E., BICHUETTE, M. E. 2016. Spots of high diversity of troglobites in Brazil: the challenge of measuring subterranean diversity. Biodiversity & Conservation. 25, 1805-1828.) has been identified at Chapada Diamantina region, at the state of Bahia, with 23 troglobites recorded at 11 caves, 13 of them from a single cave.

The analysis of taxonomic distinction (Δ+, AvTD) takes into account that the more phylogenetically distinguishes species in a given community, the greater the diversity (Cianciaruso et al. 2009CIANCIARUSO, M. V. SILVA, I. A. BATALHA, M. A. 2009. Diversidades filogenética e funcional: novas abordagens para a Ecologia de comunidades. Biota Neotrop. 93: http://www.biotaneotropica.org.br/v9n3/en/abstract?article+bn01309032009.
http://www.biotaneotropica.org.br/v9n3/e... ). However, when taxonomic relationships are taken into account, high TD values (Δ+, AvTD) indicate high diversity preserved spots (Clarke & Warwick 2001CLARKE, K.R. & WARWICK, R.M. 2001. A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Mar. Ecol. Prog. Ser. 216: 265-278.), as we observed for Gruta Olhos d ‘Água (s = 71, Δ+ = 90.18) (Figure 5). On the other hand, despite presenting higher richness, Lapa do Cipó presented a lower than expected TD (s = 76, Δ+ = 85.24), indicating possible degradation and / or the existence of some genera with many species (Figure 5).

Among the 14 caves we studied, Gruta Olhos d’ Água is remarkable by its high faunistic singularity, as shown by the high value of Taxonomic Distinctness. This value also indicates the presence of singular taxa as, for instance, troglobitic species (Cianciaruso et al. 2009CIANCIARUSO, M. V. SILVA, I. A. BATALHA, M. A. 2009. Diversidades filogenética e funcional: novas abordagens para a Ecologia de comunidades. Biota Neotrop. 93: http://www.biotaneotropica.org.br/v9n3/en/abstract?article+bn01309032009.
http://www.biotaneotropica.org.br/v9n3/e... , Gallão & Bichuette 2015GALLAO, J. E., BICHUETTE, M. E. 2015. Taxonomic distinctness and conservation of a new high biodiversity subterranean area in Brazil. An. Acad. Bras. Ciênc. 87: 209-217.).

A relict species (Relictopiolus galadriel) recorded at Gruta Olhos d’Água corroborates environmental stability, enabling survival and evolution of species whilst its populations and sister groups outside caves were extinct by several factors as, for instance, climatic changes, competitive exclusion and stochastic factors.

The Lapa do Cipó cave presented the highest species richness, among which the troglobitic populations of I. uai, C. eleonorae (Monte et al. 2015MONTE, B. G. O., GALLÃO, J. E., VON SCHIMONSKY, D. M., BICHUETTE, M. E. 2015. New records of two endemic troglobitic & threatened arachnids Amblypygi & Opiliones from limestone caves of Minas Gerais state, southeast Brazil. Biodivers. Data J. 3.), E. peruassuenssis (Bolfarini & Bichuette 2015BOLFARINI, M. P. BICHUETTE, M. E. 2015. Endecous peruassuensis n. sp. Orthoptera: Grylloidea: Phalangopsidae from caves of Eastern Brazil: evidence of isolation in the subterranean realm and discussion about troglomorphisms. Zootaxa. 4032 (3): 297-308.) and X. odara (Campos-Filho et al. 2014CAMPOS-FILHO, I. S. BICHUETTE, M. E. TAITI, S. 2016. Three new species of terrestrial isopods Crustacea, Isopoda, Oniscidea from Brazilian caves. Nauplius. 24.). Besides the importance of its fauna, species richness is also high. Even more, these three troglobitic populations occur at Lapa do Cipó and Gruta Olhos d’ Água caves, suggesting that both caves are part of a complex system. However, Lapa do Cipó showed a low TD value, probably because of its faunistic similarity with other caves.

In a study conducted at Chapada Diamantina, state of Bahia, a highest value of TD was recorded for the lowest richness cave, followed by the cave with the highest number of troglobitic species (Gallão & Bichuette 2015GALLAO, J. E., BICHUETTE, M. E. 2015. Taxonomic distinctness and conservation of a new high biodiversity subterranean area in Brazil. An. Acad. Bras. Ciênc. 87: 209-217.). In the region of Presidente Olegário, state of Minas Gerais, the highest TD value among seven caves studied is related to the presence of frugivorous guano patches and the presence of some animals that have a preference for this type of substrate such as Chilopoda of the genus Lamyctes (Zepon 2015ZEPON, T. 2015. Zonação e estratificação da fauna subterrânea de Presidente Olegário, noroeste de Minas Gerais. Dissertação de mestrado, Universidade Federal de São Carlos, São Carlos.).

Lower values of TD may indicate severe environmental degradation and pollution (Warwick & Clarke 1998WARWICK, R.M. CLARKE K.R. 1998. Taxonomic distinctness and environmental assessment. J Appl Ecol. 35. 532-543.). TD values at Caverna Cascudo, Caverna Boquete, Lapa dos Sonhos and Gruta Mina d’ Água caves were significantly lower than expected at least for one of these, Caverna Boquete, we can state that this value may be related to anthropic impacts because of visitation. Non-significant values of TD were also found at caves from other localities. Zepon (2015)ZEPON, T. 2015. Zonação e estratificação da fauna subterrânea de Presidente Olegário, noroeste de Minas Gerais. Dissertação de mestrado, Universidade Federal de São Carlos, São Carlos., for instance, argued that the low value found at Gruta Juruva cave, Presidente Olegário, state of Minas Gerais, was due to low variety and quality of resources. In caves from Bahia, Gallão & Bichuette (2015)GALLAO, J. E., BICHUETTE, M. E. 2015. Taxonomic distinctness and conservation of a new high biodiversity subterranean area in Brazil. An. Acad. Bras. Ciênc. 87: 209-217. associated the low values of TD to extensive diamond mining in the past, which continues nowadays as a residual and clandestine activity.

Our results show that contextualized studies of diversity are indispensable to conservation policies because, more than only characterize the fauna and spots of troglobitic occurrence, they also help the identification of complex subterranean systems and expand the potential for subsequent studies. Those discoveries are fundamental to conservation of the entire subterranean systems and its area of influence, a much more efficient approach to subterranean conservation than those focusing only in a given cave.

Acknowledgements

We are grateful to Vandeir B. de Jesus (“Branco”) for help in the fieldtrips; to Tamires Zepon, Camile S. Fernandes, Márcio P. Bolfarini, Ives Arnoni, Diego monteiro von schimonsky and Jonas Eduardo Gallão for help in the fieldtrips, to Peruaçu Caves National Park administrators for support during the work. This study was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior Code 001 (CAPES, BGOM doctoral scholarship); to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for grants to MEB (productivity fellowship - processes 303715/2011-1, 308557/2014-0 and 310378/2017-6); to LBR Fernandes, biologist of Departamento de Ecologia e Biologia Evolutiva/Universidade Federal de São Carlos, for taking the stereomicroscope images of Figures 4c and 4d; To AMPM Dias, coordinator of the Instituto Nacional de Ciência e Tecnologia dos Hymenoptera Parasitoides from Brazilian Southwestern region (INCT Hympar Sudeste - Processes FAPESP 2008/57949-4 and CNPq 573802/2008-4) for availability of use of stereomicroscope; to M.P. Bolfarini and I. Arnone for photographies of cave entrances; to the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for collection permit (28992-4) and to the Programa de Pós-graduação em Ecologia e Recursos Naturais da Universidade Federal de São Carlos (PPGERN/ UFSCar) for the infrastructure to develop this work.

References

Publication Dates

History