Under the surface: what we know about the threats to subterranean fishes in Brazil

Maria Elina Bichuette¹ and Jonas Eduardo Gallão¹

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Abstract​

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, 2000a). 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, 2009). 

It is widely accepted that organisms with abilities to explore dark and food-scarce habitats are potential colonizers of subterranean environments (Poulson, White, 1969; Culver, Pipan, 2009). 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) 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, 2003, 2021; Trajano, Bichuette, 2010; Ratton et al., 2018; Rabello, 2021); 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, 2005; Culver, Pipan, 2019; Mammola et al., 2019). Troglobites, in particular, are intrinsically fragile and vulnerable to environmental changes, given their small populations with low resilience (Culver, Pipan, 2009). 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, 2000b; Bichuette, Trajano, 2010, 2021; Fernandes et al., 2016; Trajano et al., 2016; Gallão, Bichuette, 2018; Culver, Pipan, 2019; Mammola et al., 2019; Bichuette, 2021).

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, 2008) that classifies caves by their levels of relevance (see Gallão, Bichuette, 2018). 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, 2012, 2018). 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, 2012). 

Furthermore, it is a worldwide consensus that subterranean habitats are highly singular, and one of the most threatened in the world (Culver, Pipan, 2019). 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., 2015), 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, 2000a), 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, 2021). However, the phylogenetic diversity in China, 10 genera in four families (Niemiller et al., 2019) 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, 2010; Bichuette, 2021).

By considering also the several Brazilian fish species that have troglophilic populations, about 50 (Bichuette, Trajano, 2003; Trajano, Bichuette, 2010; Bichuette, 2021), 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, 2008; Trajano, 2008a,b; Bichuette, Trajano, 2010, 2015, 2021; Gallão, Bichuette, 2012, 2018; Borghezan, 2013; ICMBio, 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.

TABLE 1 | 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.

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., 2004). 

FIGURE 1 | Map of Brazil showing the distribution of the subterranean fish species according to the basins included in the country’s territory.

FIGURE 2 | Distribution of Brazilian subterranean fish species according to basin.

FIGURE 3 | 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.

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, 2009; Bichuette, 2021), 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., 2008). 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., 2010) or submerged litter banks in the hyporheic zone (Muriel-Cunha, Pinna, 2005; Ohara et al., 2016), respectively. Such fragile environments are rarely reported in the literature.

Sixteen subterranean fish species were evaluated in the most recent edition of the Brazilian Red List (ICMBio, 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). 

FIGURE 4 | Distribution of Brazilian subterranean fish species according to the type of habitat

FIGURE 5 | A. Ituglanis epikarsticus 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.

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).

TABLE 2 |  Brazilian subterranean fishes: threats, possible causes, IUCN categories, and occurrence in Conservation Units.

FIGURE 6 |  Total number of Brazilian subterranean fish species affected by each type of identified threat in the present study.

FIGURE 7 | Total number of threats recorded for each basin.

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., 2015). 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, 2018; Bichuette, Trajano, 2021; Bichuette, 2021). 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., 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, 2009). None of these plans, however, was conceived with focus on one of these species, 

Manjarrés-Hernández et al. (2021) 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, 2010; Bichuette, 2021), 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). 

Trajano (1997, 2008a) addressed the concern about threats identified for Pimelodella kronei and remarked the necessity of protection of this species. Gallão, Bichuette (2012) 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., 2015) 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., 2019).

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., 2015). 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., 2013). 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.

Acknowledgments​

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.

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Authors

Maria Elina Bichuette¹ and Jonas Eduardo Gallão¹

^[1]    Instituto Brasileiro de Geografia e Estatística – Reserva Ecológica do IBGE, DF 001, km 3Laboratório de Estudos Subterrâneos, Universidade Federal de São Carlos, Rodovia Washington Luís km 235, Caixa Postal 606, 13565-905 São Carlos, SP, Brazil. (MEB) bichuette@ufscar.br (corresponding author), (JEG) jonasgallao@gmail.com.

Authors Contribution

Maria Elina Bichuette: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Writing-original draf.

Jonas Eduardo Gallão: Writing-original draf, Writing-review and editing.

Ethical Statement​

Not applicable.

Competing Interests

The authors declare no competing interests. 

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

Copyright​

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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