The karst area of the northeastern state of Goiás comprises two main municipalities: São Domingos and Posse. São Domingos is inside the limits of a Full Protection Conservation Unit known as Parque Estadual de Terra Ronca (PETeR), where a high number of caves occurs, some of them surpassing 10 km in length. Despite their protection by law, uncontrolled tourism has been threatening the integrity of the unique and fragile cave systems of São Domingos. On the other hand, the caves of Posse are much less visited, with its subterranean fauna poorly unknown and are strongly threatened by the urban areas and mining activities in the vicinity. We conducted six systematic surveys of invertebrates in 12 caves, seven of which are located in São Domingos and five in Posse, between 2010 and 2012. Immediately outside the caves, we sampled several microhabitats for comparison. We estimated richness, abundance, and taxonomic distinctness of the communities. We recorded 1,941 individuals of 344 morphospecies. Caves from São Domingos showed a higher species richness and were more taxonomic distinct than caves from Posse. Most morphospecies were considered troglophiles (188). We also found one trogloxene and one troglobite, as well as nine troglomorphic taxa that possibly are troglobitic as well. Both regions have markedly singular caves regarding its subterranean fauna, with high values of taxonomic distinctness. However, the richer caves were not necessarily the most taxonomic distinct. Conservation measures are especially necessary in the region of Posse, where caves are not legally protected and are within an area of significant urbanization. Cave entrances of Posse are near deforested vicinities, in some cases with domestic wastes and cement plants nearby.

caves, conservation, phylogenetic diversity, subterranean fauna, São Domingos, Posse, Goiás

The subterranean fauna consists of organisms able to survive in peculiar conditions of the environment, as the permanent darkness, the high relative humidity of the air and stable temperatures at the deepest zones (Barr 1968). These inherent features may act as an environmental filter (see Fernandes et al. 2016 to opposite view) in such a way that only part of the epigean taxa is capable to colonize and establish hypogean populations. So, the organisms found inside caves can be sorted in three ecological-evolutionary categories, considering its degree of specialization and dependence of surface environments: trogloxenes, troglophiles and troglobites.

Because of its unique conditions and the high degree of endemism, subterranean environments are fragile and sensitive to environmental changes, especially those regarding anthropic activities (Culver 1986, Gibert and Deharveng 2002, Trajano and Bichuette 2006). Among the main human interference in Brazilian caves, we may stress mining, construction of hydroelectric dams, deforestation for agriculture and uncontrolled tourism (Ferreira et al. 2014, Gallão and Bichuette 2018).

Brazil has about 17,000 registered caves (CECAV 2018). Some heterogeneity exists in the knowledge about the subterranean fauna regarding different Brazilian karst and non-karst areas. Some are well known, as the Vale do Ribeira (southeastern) (e.g., Trajano 1991, Bichuette and Trajano 2003, Rodrigues et al. 2014) and Chapada Diamantina (eastern-northeastern) (Gregorin and Mendes 1999, Bockmann and Castro 2010, Gallão and Bichuette 2015). Others, however, have its knowledge limited to preliminary data about species richness and abundance, which was obtained on a few sampling occasions (e.g. Altamira, northern) (Trajano and Moreira 2001). Besides this, only a few approaches covered long-term samplings, with replicas enough to contemplate more than one annual cycle (e.g. Trajano 1991, Gallão and Bichuette 2015, Resende and Bichuette 2016, Zepon and Bichuette 2017). Most often in tropical caves, the seasonal oscillation is of great importance in the dynamics of the subterranean environments (Trajano 2000).

Some studies have shown that phylogenetic diversity, a measure of species relatedness considering the phylogenetic relationship among species, are more sensitive to detecting responses of communities to environmental changes (Cianciaruso et al. 2009). This is because traditional diversity indexes have limited prediction about ecosystems functioning. According to Faith (1992), the emphasis on conservation regards preserving as much of this hierarchical variation as possible, no matter what the taxonomic identity involved. In this sense, a phylogenetic diversity index has been shown more efficient to proposals of conservation strategies than traditional indexes (Cianciaruso et al. 2009) and was used also for conservation purposes comparing taxonomic distinctness with α indexes (Gallão and Bichuette 2015).

In the present study, we sampled subterranean invertebrates at the karst area of the northeastern Goiás state, central Brazil, encompassing the municipalities of São Domingos and Posse. We estimated species richness and abundance by each cave and by each region, as well as by the karst area. Finally, we compared the fauna of these caves regarding geographical position and taxonomic distinctness of the communities. We expected that phylogenetic component of diversity would indicate those most singular caves in the region better than traditional indexes of diversity. Our purpose was to improve the knowledge about components of biological diversity in the region and, through a better knowledge of the ecological-evolutionary processes underlying these communities, provide best arguments for better conservation decisions.

We collected a total of 1,941 individuals of 344 morphospecies belonging to 128 families, 37 orders and ten classes (Appendix 1) in both regions: 287 morphospecies and 1,554 individuals were from São Domingos and 122 morphospecies and 387 individuals were from Posse. Whether we consider São Domingos and Posse singly or combined as a larger karst area, insects and arachnids were the richest and more abundant taxa (Figure 2–4).

Figure 2. 

A Richness and B abundance of subterranean terrestrial invertebrate (by Class) from the São Domingos and Posse karst areas, state of Goiás, and from both regions combined.

Figure 3. 

Fauna from caves of northeastern Goiás, central Brazil: A Heterophrynus longicornis (Amblypygi) preying a cricket Endecous sp. (Orthoptera: Phalangopsidae) B Nesticodes rufipes (Araneae: Theridiidae) C Scolopendra viridicornis (Chilopoda: Scolopendromorpha) DChernetidae (Pseudoscorpiones) E Flirtea batman (Opiliones: Cosmetidae) F Stenochrus portoricensis (Schizomida: Hubbardiidae).

Figure 4. 

Fauna from caves of northeastern Goiás, central Brazil: AMesostigmata (Acari) BEmesinae (Hemiptera: Reduviidae) C Venezillo congener (Isopoda: Armadillidae) DDubioniscidae (Isopoda) E Trogolaphysa (Collembola: Paronellidae) F Paratachys sp. (Coleoptera: Carabidae).

Of the 344 morphospecies, we classified one as a trogloxene (TX) (Araneae: Ctenidae: Enoploctenus sp.), 188 as troglophiles (TF), one as a troglobite (TB) (Pseudoscorpiones: Chernetidae: Spelaeochernes sp.), nine as troglomorphic and, being such, possibly troglobitic (TM/TB?) and 48 as accidentals (AC). Due to lack of data, we considered the classification of 97 morphospecies as uncertain concerning their ecological-evolutionary relationship with caves.

In São Domingos, Lapa Angélica was the richest and most abundant cave, with 203 morphospecies and 865 individuals, followed by Terra Ronca II cave with 88 morphospecies and 274 individuals. Pau Pombo cave was the least rich and abundant with 11 morphospecies and 22 individuals (Table 1). In Posse, Revolucionários cave was the richest and the most abundant, with 43 morphospecies and 112 individuals, followed by Doralino cave system with 40 morphospecies and 95 individuals. The least rich and abundant was Nova Esperança cave with 17 morphospecies and 42 individuals.

For São Domingos, the expected TD (Δ+) value was 72.517, and the cave with the highest TD was São Bernardo (Δ+= 73.566), followed by Terra Ronca I (Δ+=72.110), Lapa Angélica (Δ+= 71.966), Lapa do Bezerra (Δ+= 71.760), São Mateus (Δ+=71.541), Terra Ronca II (Δ+= 69.669) and Pau Pombo (Δ+= 69.237) (Figure 5A, Table 1). Values of TD close to expected as shown herein revealed that caves from São Domingos share many taxa (morphospecies). One exception is São Bernardo, which shows higher TD in relation to other caves, above the expected value, which means that São Bernardo is the most singular cave in São Domingos. In this cave some morphospecies were unique: one isopod (Dubioniscidae sp. 1), one spider (Mysmena sp. 1), one millipede (Pseudonannolenidae sp. 1), one dipteran (Mycetophilidae sp. 1), one Nematoda (sp.1) (Appendix 1).

Figure 5. 

Taxonomic distinctness (TD) for caves from A São Domingos and B Posse karst areas. Horinzontal line presents the expected TD for the region and funnel graph means 95% confidence limits. Legend: SBer= São Bernardo cave system, Ang= Lapa Angélica, Bez= Lapa do Bezerra, SMat= São Mateus cave system, TR_I= Terra Ronca I cave, TR_II= Terra Ronca II cave, PPom= Pau Pombo cave, Rus= Russão cave system, Bom= Bombas cave system, Dor= Doralino cave system, NEsp= Nova Esperança cave, Rev= Revolucionários cave.

For Posse, the expected TD (Δ+) value was 73.206, and the cave with the highest TD was Revolucionários (Δ+=78.649), followed by Bombas system (Δ+= 73.006), Russão (Δ+= 67.847), Doralino system (Δ+= 67.955) and Nova Esperança (Δ+= 64.680) (Figure 5B, Table 1). Contrasting to observed to São Domingos, most TD values for Posse caves were far from expected, with some caves showing TDs much lower than expected (Russão, Doralino and Nova Esperança caves), sharing many taxa (morphospecies). Bombas cave presented a TD value near the expected, showing a singularity in relation to the others and Revolucionários cave showed the highest TD value, being the most singular cave in the region (unique taxa/morphospecies). In this cave some morphospecies were unique: one centipede (Newportia (Tidops) balzanii), one pseudoscorpiones (Chthoniidae sp. 1), two isopods (Platyarthridae sp. 1 and Dubioniscidae sp. 2), one orthopteran (Endecous sp. 1), one opilionid (Pachylinae sp. 2), one scorpion (Tityus sp.), one collembolan (Trogolaphysa sp. 3), one coleopteran (Tachys sp. 1) and eight gastropods (Appendix 1).

According to simple linear regression, the richness and TD values are not correlated in both areas: São Domingos (r = 0.001972, r² = 0.007384, F = 0.03719, p = 0.8547) and Posse (r = 0.2147, r² = 0.2044, F = 0.7708, p = 0.4446), i.e., the richest caves not necessarily present the higher TD value, as observed in the São Domingos area (Figure 6A, B).

Figure 6. 

Simple linear regression between richness and Taxonomic distinctness (TD) values of caves from A São Domingos and B Posse karst areas. Legend: SBer= São Bernardo cave system, Ang= Lapa Angélica, Bez= Lapa do Bezerra, SMat= São Mateus cave system, TR_I= Terra Ronca I cave, TR_II= Terra Ronca II cave, PPom= Pau Pombo cave, Rus= Russão cave system, Bom= Bombas cave system, Dor= Doralino cave system, NEsp= Nova Esperança cave, Rev= Revolucionários cave.

Our data show high species richness for both the São Domingos and Posse karst areas, which has been also observed for other Brazilian karst areas, such as Chapada Diamantina with c.a. 160 morphospecies (Gallão and Bichuette 2015) and Presidente Olegário with 382 morphospecies (Zepon and Bichuette 2017). Many species that we found during this study were often reported from other limestone caves whether in the same karst area or in other Brazilian karst areas (Trajano 1987, Pinto-da-Rocha 1995, Zepon and Bichuette 2017). As expected for Brazilian caves, most species we found are troglophiles (Trajano and Bichuette 2010).

In São Domingos karst area, Lapa Angélica cave was the richest and the most abundant. Although we sampled this cave on more occasions, its high richness is likely due to the high input of nutrients brought by the extense rivers crossing the cave systems and, consequently, to the high amount of dissolved organic carbon in subterranean terrestrial substrates (62.2 mgC.L^-1); the same was observed for Terra Ronca II cave (111.12 mgC.L^-1) (Paula 2018), which, in addition, has skylights along its length through which more organic matter may enter the system (Bichuette et al. 2017). In relation to Pau Pombo cave, the low richness and abundance values may be explained by the limited habitat we searched compared to other caves, as well as this is a typicall dry cave.

In Posse karst area, the higher species richness and abundance we found inside the cave Revolucionários is also attributable to the drainage traversing its length, as well as the high humidity of the terrestrial substrates and the high amount of trophic resources, composed mainly of leaf litter, frugivorous and hematophagous bat guano (Gnaspini-Neto 1992, Poulson and Lavoie 2000). Low diversity and abundance at Nova Esperança can be attributed to low amount of organic matter found inside the cave, mainly leaf litter and guano (ME Bichuette pers. obs). It is a small cave, crossed by a river and with few terrestrial habitats available for fauna, most of which contain rocky or clay substrates. There are several skylights at the ceiling and its epigean environs are impacted by the presence of cattle and pastures.

São Bernardo (São Domingos region) and Revolucionários (Posse region) were the most singular caves in Goiás karst area. Gallão and Bichuette (2015) also observed a high singularity for two caves from Bahia state, northeastern Brazil (Gruna Parede Vermelha and Morro de Alvo caves). Not necessarily the richest caves had higher TD. In other words, the richest caves hadn’t the highest singularities in their faunistic compositions. For instance, Lapa Angélica, the richest cave of São Domingos, had a value of TD lower than the estimated mean for the region. This is related to the great number of morphospecies shared with other caves in the region. Our results reinforce that is inadequate to consider only the observed local diversity as the sole criterion for relevance attribution of an area, as this index by itself is not effective to compare different environments, regions, nor taxa (Pärtel et al. 2011). Numerical values of alpha diversity do not reflect the obvious singularities of the subterranean habitats, which is the main justification for its conservation (Trajano et al. 2012).

Lapa Angélica is also one of the most visited caves from PETeR and, on some occasions, visitors traverse its entire length. There has been no effective control of the number and frequency of tourist groups in the region since 2000 (ME Bichuette pers. obs.). We noted that there is only a few sparsely guano spots along the cave, probably reduced as a consequence of anthropic impacts (ground trampling and noise pollution, which drives off the bats). Disturbance diminishes the environmental heterogeneity and, consequently, reduces the offer of microhabitats and resources to the local community, as observed in Lapa Angélica in relation to bat guano along years (M.E. Bichuette pers. obs.). Environmental impacts (contamination) also cause reduction of taxonomic distinctness in marine species communities, while richness remained constant (Warwick and Clarke 1998).

We observed that some of the other richest caves which do not have high taxonomic distinctness, possibly because of anthropic impacts in the region. Taxonomic distinctness in the region may still be related to the trophic diversity of the community, in such a way that when there is a reduction in the number of guilds, TD decays (Clarke and Warwick 1999). The type of habitat affects trophic diversity. Consequently, more impacted areas are also more subject to a decrease in taxonomic distinctness.

Terra Ronca II cave, even with the second higher species richness, presented the lowest TD. The stretch of the cave we sampled has basically the same substratum type, which is predominantly composed of banks of sand and pebbles deposited at riverside. Despite its high species richness, the species are not taxonomically very distinct from each other (e.g., several morphospecies are from the beetle families Carabidae and Staphylinidae) when compared to other subterranean communities of the same region. In Posse, the richest cave (Revolucionários) also had the highest TD. Its high faunistic singularity is related to the presence of species and genera belonging to different families. Nova Esperança presented several common taxa and, therefore, low faunistic singularity.

São Domingos is remarkable for its high richness in troglobitic species of fishes that exhibit various degrees of specialization to subterranean life, including one species of Loricariidae catfish, four Trichomycteridae catfishes, one Heptapteridae catfish and one Sternopygidaeelectric fish (Reis 1987, Triques 1996, Fernández and Bichuette 2002, Bichuette and Trajano 2004, Trajano et al. 2004). Terrestrial invertebrates, such as Ctenidae, Scytodidae, and Symphytognathidae spiders, are also ubiquitous (Rheims and Pellegatti-Franco 2001). In Posse, only two troglobitic taxa are described to date: two catfishes of the families Callichthyidae and Trichomycteridae (Bichuette and Trajano 2008, Tencatt and Bichuette 2017).

If we excluded the troglophilic taxa and considered only troglobitic terrestrial invertebrates, species diversity recorded in northeastern Goiás would be considered poor when compared to other Brazilian regions, as has been demonstrated in this and in previous studies (Trajano and Bichuette 2010, Trajano et al. 2016). This poor troglobitic diversity can be related to the fact that this area comprises a relatively stable paleoclimatic zone (Barr 1973, Moore 1964). Under this model of climate fluctuations, areas where drastic climate fluctuations occurred in the past had greater troglobitic diversification, as can be found in the subterranean fauna in the northern Hemisphere (Barr 1968, Peck 1980). The most specialized Brazilian troglobites are found in caves of semiarid regions of Bahia state, as Chapada Diamantina and Campo Formoso (Trajano 1995).

As we corroborated in our study, a high degree of singularity is usually present in caves, even among those, which are geographically near other caves and inserted in the same rocky massif. To preserve as many singular caves as possible is urgent, because the ideal of environmental compensation is not applicable to these unique environments.

Even the caves from São Domingos are inside a legally protected area (PETeR), the tourist flow is intense and, several times, there is no adequate inspection. Thus, intense visitation may be affecting the subterranean communities we studied. Besides, part of the headwaters of rivers that crosses caves of São Domingos is outside the State Park limits. There, extensive cattle farming and monocultures are causing silting and pollution of rivers, bringing noxious materials to the caves and impacting the community (Simões et al. 2013). In February 2013, intense sedimentation occurred at the headwater of the São Vicente River (São Domingos), as a consequence of intensive agriculture upstream of the spring. In view of the above, it is difficult to preserve natural areas, even when legal reserve areas and parks are delimited. In Posse, the surroundings outside the caves are deforested and replaced by pastures and urban areas, while the rivers are being discharged from domestic sewage. Worryingly, Brazilian environmental laws do not legally protect the caves suffering these impacts.

In conclusion, caves of São Domingos and Posse karst areas exhibited a high taxonomic distinctness for terrestrial fauna, influenced by the high proportion of troglophilic, accidental and undetermined taxa. Our data show the relevance to considerer not only troglobitic taxa. Besides non-troglobionts, both areas showed a high diversity of troglobitic fish (Bichuette and Trajano 2003) and shelters highly important for bats (Bichuette et al. 2018). Anthropogenic impacts cause reduction of environmental heterogeneity and trophic diversity, and, consequently, diminishes faunistic singularity. Besides, these karst areas have high faunistic diversity when compared with other Brazilian regions. Therefore, protective measures should be taken, since the region is not totally preserved, even in the São Domingos area, where the surroundings of the headspring of rivers that enter on the caves (responsible for carrying food resources and increasing heterogeneity of habitats), are still outside the protection limits of the Park.

We are thankful to our colleagues of Laboratório de Estudos Subterrâneos who help in the field trips (CS Fernandes; PP Rizzato); to the helpful field guide in Terra Ronca, RH dos Santos; to the specialists who help in the identification of part of the material: A Brescovit (Araneae), JLC Mineiro (Acari), R Bessi (Carabidae), E Caron (Staphylinidae); RL Falaschi (Diptera), F Moreira (Hemiptera), H Gil-Santana (Heteroptera, Reduviidae), MP Bolfarini (Orthoptera), D Zeppelini (Collembola), JG Palacios-Vargas (Collembola), A Chagas-Jr. (Chilopoda), CS Fernandes (Isopoda), M Bartz (Haplotaxida), LRL Simone and R Salvador (Gastropoda), LP Prado (Formicidae), and JS Gallo (Diplopoda); to Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for the financial support to MEB (processes 98/13858-1 and 2010/08459-4), to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the Master scholarship to LBS (process 132981/2011-4) and productivity scholarships to MEB (processes 303715/2011-1, 308557/2014-0 and 310378/2017-6); to CS Fernandes for use permission of isopod images (Figures 3C and 3D); to Programa de Pós-Graduação em Ecologia e Recursos Naturais (PPGERN), for the infrastructure to develop part of this work (Master project of LBS). Collections were made in accordance with Brazilian environmental laws - State (authorization number SEMARH 063/2012) and Federal (authorization number SISBIO 28992). We also thank CS Fernandes for revision of the manuscript and English, and S Mammola, ML Niemiller and O Moldovan for the valuable suggestions to improve this work.