No longer safe in the darkness: ecological and conservation perspectives on troglobitic species in a disturbed Neotropical karst landscapeABSTRACT
Cave-restricted fauna is highly specialized, endemic, and particularly vulnerable to extinction. Nevertheless, the biodiversity of many karst regions remains poorly documented due to limited scientific research, restricted accessibility, and inefficient data collection methods, resulting in substantial knowledge gaps and conservation challenges. In this study, we reviewed existing literature and applied fine-scale sampling techniques in caves within the Capiru, Itaiacoca, and Votuverava limestone formations to investigate the composition, species richness, and taxonomic distinctness of troglobitic invertebrates. These caves are located in the northern region of Paraná state, Brazil, an area under considerable environmental pressure from human activities. We hypothesized that geographically distinct limestone formations support different troglobitic communities as a result of spatial separation, environmental variation, and differing anthropogenic disturbances. Across 23 sampled limestone caves, we recorded 28 troglomorphic invertebrate species, substantially exceeding the nine species previously reported for the state of Paraná. No significant differences were detected in species composition, richness, or taxonomic distinctness among the Votuverava, Capiru, and Itaiacoca limestone belts. The most frequent human impacts observed inside caves were trampling (78.2%), littering (65.2%), graffiti (65.2%), pasture encroachment (60.8%), and speleothem vandalism (60.8%). Our results indicate that greater taxonomic distinctness among troglobitic species is positively associated with higher species richness. In addition, caves subjected to higher levels of human disturbance tended to harbor a greater number of troglobitic species, highlighting the paradoxical occurrence of biological richness in environments under substantial anthropogenic pressure. This study considerably expands the known diversity of troglobitic invertebrates in the Paraná state and improves current knowledge of subterranean biodiversity and faunal composition within the Capiru, Itaiacoca, and Votuverava limestone belts. These findings underscore the urgent need for targeted conservation actions to protect these fragile subterranean ecosystems.
KEYWORDS:
Cave ecology; cave fauna invertebrate conservation; karst conservation; limestone caves; troglobites
INTRODUCTION
Understanding the ecological, biogeographical, and environmental threats to biodiversity is essential for effective conservation. It is critical to determine how many species exist, where they are located, how they interact with one another and with their environment, and how habitat changes affect them (Venter et al. 2014, Pollock et al. 2017, McKerrow et al. 2018, Belote et al. 2021). This foundational knowledge underpins the development of sound conservation strategies, including the identification of priority areas, implementation of protective measures, mitigation of threats, and promotion of sustainable practices (Da Rocha Melo et al. 2025). Public awareness and education about the value of biodiversity also play vital roles in its preservation. As people gain a deeper understanding of the importance of biodiversity and how their actions impact the environment, they are more likely to support and engage in conservation efforts (Newing et al. 2011).
Global conservation priority frameworks have significantly influenced how resources are allocated at broad geographic scales. However, several researchers have pointed out that these global prioritization efforts often fall short in driving effective, on-the-ground conservation outcomes (Mace et al. 2000, Brummitt and Lughadha 2003, Whittaker et al. 2005, Brooks et al. 2010). Consequently, it is necessary to establish conservation targets and priorities at much finer spatial scales, as conservation relevance can vary greatly even within a single region (Whittaker et al. 2005). In the context of subterranean biodiversity, Culver and Sket (2000) proposed that areas harboring 20 or more troglobitic species should be considered hotspots, warranting focused conservation action. As more high-diversity subterranean areas were documented globally, this threshold was later revised to 25 species (Culver et al. 2021). However, this criterion has been criticized for its arbitrary nature and for failing to account for geographic, ecological, and climatic differences across regions (Ferreira et al. 2023).
Troglobionts are obligate cave-dwelling species and often exhibit troglomorphic features such as eye reduction, depigmentation, body elongation, and enhanced sensory appendages (Racovitz 1907, Schiner 1854, Culver and Pipan 2019). However, some cave-restricted species may lack pronounced troglomorphic traits due to factors such as habitat size, exposure to twilight zones, or genetic variability. In such cases, species may be preliminarily classified as “potential troglobionts” or even as “troglophiles” (Deharveng et al. 2024), pending further ecological, morphological, or molecular analyses to clarify their status.
Although relatively few subterranean biodiversity hotspots have been identified in tropical regions to date, continued biological surveys and the discovery of new species are expected to lead to the recognition of additional hotspots in these areas (Culver et al. 2021, Souza-Silva et al. 2021, Ferreira and Souza-Silva 2023). Accurately quantifying subterranean invertebrate biodiversity has long posed substantial challenges (Culver et al. 2004, Wynne et al. 2019, Mammola et al. 2021). These difficulties stem from the inherent complexity of subterranean ecosystems and the logistical constraints associated with accessing and studying underground habitats (Mammola et al. 2021).
One of the key limitations has been the lack of detailed observation within specific cave microhabitats. Many traditional sampling techniques overlook the small body size of numerous invertebrates, making visual detection and collection particularly challenging. Additionally, troglobitic species often exhibit highly localized distributions, strongly associated with specific microhabitat conditions, such as high humidity, the presence of resources like plant debris, guano, or microbial biofilms, and locations situated farther from cave entrances (Pacheco et al. 2020, Nicolosi et al. 2021, Souza-Silva et al. 2021). These factors underscore the importance of adopting targeted, microhabitat-focused sampling strategies. Prioritizing the investigation of ecologically relevant microhabitats is essential to uncover the full extent of troglobitic diversity within cave systems (Pacheco et al. 2020, Reis-Venâncio et al. 2024).
Recent studies have demonstrated that the spatial distribution of terrestrial invertebrate communities within caves is strongly influenced by the availability of food resources and specific microhabitat conditions (Prous et al. 2015, Pacheco et al. 2020, Souza-Silva et al. 2021). As a result, sampling methods that focus on targeted microhabitats tend to detect a substantially greater number of troglobitic species, even when the number of sampling events is limited (Bento et al. 2021, Cardoso et al. 2021, Souza-Silva et al. 2021). This approach not only increases the efficiency of biodiversity assessments but is also essential in contexts where extended inventories are logistically challenging or infeasible.
In the state of Paraná, Brazil, extensive carbonate belts host numerous caves that have been the focus of faunal studies for decades, revealing the presence of several endemic and threatened invertebrate species (Pinto-da-Rocha 1995, Sessegolo et al. 2006, Bená and Vanin 2014). However, knowledge of troglobitic species remains limited, particularly given the high biodiversity potential of these regions. This study aims to update and expand our understanding of troglobitic diversity within the caves of the Capiru, Itaiacoca, and Votuverava limestone belts (Açungui Group), located located in the northern region of Paraná state, by employing fine-scale sampling methods targeted at specific microhabitats. We hypothesize that the three limestone belts support distinct communities of troglobitic invertebrates due to differences in environmental conditions. Moreover, factors such as proximity to urban centers, population density, elevation, and mining activity are expected to reflect varying degrees of landscape conservation and anthropogenic pressure.
Given that the study region is subject to intense human disturbance, including unregulated urban expansion, environmental pollution, and natural resource exploitation (Macedo 2004), subterranean biodiversity, particularly troglobitic species, may be significantly impacted. Documenting the diversity of these organisms in the Paraná limestone belts underscores the ecological value of these subterranean ecosystems and informs more effective conservation and management strategies. This research also contributes to identifying priority areas for protection and guiding future policy development aimed at safeguarding subterranean life in highly modified landscapes.
MATERIAL AND METHODS
Study area
The study was conducted in 23 caves distributed across three contiguous limestone belts (Itaiacoca, Votuverava, and Capiru), Paraná State, Brazil (Fig. 1). This region is situated within the Atlantic Rainforest biome. For this study, caves were sampled in the following cities: Colombo, Sengés, Castro, Campo Largo, Rio Branco do Sul, Almirante Tamandaré, Itaperuçu, Cerro Azul, Adrianópolis, and Doutor Ulysses (Fig. 1).
Map of Brazilian territory (A) and the location of municipalities (B and D) that make up the Metropolitan region of Curitiba (capital of the state of Paraná, with 1,773,718 people) [Source 1]. The Itaiacoca, Votuverava, and Capiru limestone belts (D). The red dots are the sampled caves. For more details see Table 2. 1) Varzeão; 2) Arco de Pedra; 3) Casa de Pedra; 4) Ressurgência do Feital; 5) Dá a Volta; 6) Pocinho; 7) Pocinho II; 8) Malfazido; 9) Toquinhas; 10) Piedade; 11) Bromados; 12) Lancinha; 13) Fadas; 14) Jesuítas; 15) Bom Sucesso; 16) Chiquinho; 17) Chiquinho II; 18) Pinheiro Seco; 19) Ermida; 20) Itaperussu; 21) Pinheirinho; 22) Pinhalzinho; 23) Bacaetava.
Specifically, six caves were sampled in the Capiru belt, five in the Votuverava belt, and twelve in the Itaiacoca belt (Table 1). These limestone belts consist of metasedimentary rocks from the Açungui Carbonatic Group, dating to the Late Proterozoic (1,000-570 million years ago, Fiori 1994). The region’s humid subtropical climate is characterized by mild winters and rainfall evenly distributed throughout the year. The vegetation comprises both mixed ombrophilous forest (dominated by Araucaria spp.) and dense ombrophilous forest (Morellato and Haddad 2000, IAT 2024).
Limestone belt (Belt), cave names, UTM coordinates (zone 22J), latitude (LAT), longitude (Long), Altitude asl (Alt), distance from urban center (DUC), distance from mining activities (DMA), Population density (PD), Human impacts weight (HI), troglobitic species richness (S), and taxonomic distinctness (TD) of the 23 limestone caves placed at the northern region of Paraná, Brazil. Ressurgência do Feital (Ress. do Feit.), Bom Sucesso (B. Sucesso), Pinheiro Seco (P. Seco).
The study area encompasses a karst aquifer of appro ximately 5,740 km2 and falls entirely within the Ribeira watershed (IAT 2024). The location of these caves in a heavily impacted landscape subjects them to significant anthropogenic threats, including urban expansion, mining, agriculture, tourism, and deforestation (Gondim et al. 2002, Macedo 2004, Fritzsons et al. 2009, Mohebalian et al. 2022).
Sampling and identification of obligate cave invertebrates
Invertebrate sampling was performed within standardized sectors (3 × 10 m) and quadrats (1 × 1 m) using active search and collection methods, aided by tweezers and fine brushes (Souza-Silva et al. 2021). To maximize the detection of cave-restricted species, additional active searches were conducted throughout all accessible areas of the caves. Fieldwork was carried out during three separate campaigns (November 2022, April 2023, and July 2023), with each cave surveyed once during one of these periods.
Microhabitats were thoroughly inspected to maximize recorded species richness. Cave floor habitats were classified according to their structural features and resource availabi lity (Souza-Silva et al. 2021), including: organic substrates (e.g., guano, leaf litter, woody debris, and animal carcasses); mineral and structural substrates (e.g., bedrock, blocks, boulders, gravel, sand, silt/clay/mud, hardpan, and contraction cracks); aquatic environments; smooth rock surfaces; and speleothems. All collected specimens were preserved in 70% ethanol and transported to the Centro de Estudos em Biologia Subterrânea (CEBS) at the Universidade Federal de Lavras (UFLA) for sorting and morphotyping.
Potential troglobiont species were identified based on troglomorphic traits-morphological adaptations indicating evolutionary isolation in subterranean environments (Culver and Pipan 2019). Selected specimens were subsequently submitted to taxonomic specialists for further evaluation (see Acknowledgments). Voucher specimens were deposited in the Coleção de Invertebrados Subterrâneos de Lavras (ISLA) at CEBS/UFLA, Minas Gerais, Brazil (https://www.biologiasubterranea.com.br).
Literature search and data compilation
A bibliographic review was conducted in July 2023 and updated in March 2025 to compile records of troglobitic species reported from caves in Paraná State. Searches were performed in the SciELO, Web of Science, and Google Scholar databases using combinations of keywords in both Portuguese and English, including: “cave fauna”, “troglobites”, and “Paraná”. Additionally, the Red Book of Threatened Brazilian Fauna (ICMBio 2018) was consulted to identify further records of cave-restricted species. These data provided a comparative baseline for evaluating the species richness recorded in the present study.
To contextualize our findings, we expanded the search to compare and rank species richness at both local and national levels. Using the same databases and targeted search terms, we compiled diversity data from other karst regions in Brazil. This allowed for a robust comparison between the troglobitic richness of the northern region of Paraná (local relevance) and other Brazilian hotspots of subterranean biodiversity (national relevance).
Cave and surroundings impact assessment
The degree of anthropogenic impact on the caves was assessed using the Cave Conservation Priority Index (CCPi; Souza-Silva et al. 2015). This index evaluates both types of human use and their resultant environmental impacts. While activities such as tourism and religious practices were considered forms of use, their associated effects-including trampling, artificial lighting, and construction-were treated as direct modifications of the subterranean environment.
According to the CCPi framework, impacts are categorized into three types based on their alteration potential: impoverishment (decline in organic resources and biodiversity), enrichment (anthropogenic increase in organic matter), and physical modification (structural changes without necessarily affecting trophic dynamics). Each impact was scored by its extent and temporal permanence, with weights from 1 to 3 reflecting their severity or persistence.
The modification potential of each impact was further assessed: intense potential (causing significant disturbances to fauna or physical structures) was assigned a weight of 2, while tenuous potential (minor disturbances) received a weight of 1. Regarding spatial extent, localized impacts were classified as short-range (weight 1), whereas those affecting broader areas were considered widespread (weight 2). For temporal permanence, occasional impacts were assigned a weight of 1, while those persisting over long periods or permanently were weighted 3.
All 23 sampled caves were classified based on their cumulative impact scores. Using the highest observed score (55) as a reference, four categories were defined: extremely high (≥ 28), high (20-27), medium (14-19), and low (≤ 13). These were converted into ordinal values (4, 3, 2, and 1, respectively) for further analysis. Notably, deforestation and agricultural activities were consistently assigned a weight of 1, as their direct impact on subterranean environments is often difficult to quantify precisely (Souza-Silva et al. 2015).
Geomorphological and spatial features
Most caves were surveyed following the methodology of Sessegolo et al. (2006) and complied with the British Cave Research Association (BCRA) survey grade 4C. Geographic coordinates and altitude were recorded via GPS and are presented in Table 1. These spatial data were processed in QGIS 3.34.6 (https://qgis.org/pt_BR/site/) to calculate the shortest linear distances from each cave to the nearest mining site, urban center, and road.
Socio-demographic and mineral economy data
Population estimates for the studied municipalities were retrieved from the Instituto Brasileiro de Geografia e Estatística (IBGE) database as of March 2024 (https://www.ibge.gov.br/estatisticas/sociais/populacao/9103-estimativas-de-populacao.html). Information regarding the mineral economy, including active mining concessions, types of minerals extracted, and the names of operating companies, was obtained from the 2019 database of the Instituto Água e Terra do Paraná (IAT, https://www.iat.pr.gov.br/Pagina/Economia-Mineral).
Data analysis
Alpha diversity was determined by calculating troglobitic invertebrate richness for each sampling unit, quadrant, sector, and cave. We analyzed average taxonomic distinctness (Δ+) using a distribution matrix of morphotypes among sampling units, assigning weights to Phylum (100), Class (80), Order (60), Family (40), and morphotypes (20) (Anderson et al. 2008). This analysis was performed using PRIMER-E version 7.
Faunal compositional similarity among caves was assessed via the Bray-Curtis dissimilarity index and visualized through non-metric multidimensional scaling (nMDS). Bootstrap resampling was applied to evaluate pattern robustness, and an Analysis of Similarities (ANOSIM) was conducted to test for significant differences in species composition among the three limestone belts.
To investigate environmental and anthropogenic drivers of troglobitic richness, we fitted generalized linear models (GLMs) with a Poisson distribution. The full model (Model 1) included human impact, average taxonomic distinctness (∆+), population density, altitude, distance to mining areas, and distance to roads as predictor variables. Due to multicollinearity between “distance to mining areas” and “distance to urban centers” -identified via Variance Inflation Factor (VIF) and correlation matrices-two alternative models were constructed. Model 2 excluded “distance to mining areas” while retaining “distance to urban centers”, whereas Model 3 retained “distance to mining areas” and excluded “distance to urban centers”.This approach allowed for an evaluation of each variable’s influence on species richness while effectively controlling for collinearity.
Model diagnostics were performed using residual plots and simulations via the DHARMa package (Hartig 2024) to evaluate residual distributions formally. Overdispersion was assessed to confirm the suitability of the Poisson distribution. Multicollinearity was further examined using VIF and correlation matrices to ensure model integrity. Model performance was compared using the coefficient of determination (R2) and the Akaike Information Criterion (AIC), with the final model selected based on the principle of parsimony.
Spatial distribution was visualized using a shaded plot of square-root-transformed data. The matrix was reordered through cluster analysis using the Whittaker Association Index (Whittaker 1952; Clarke et al. 2014) to highlight compositional patterns Statistical analyses were executed in PRIMER-E version 7 and RStudio version 4.4.1.
RESULTS
Literature data
Our literature review retrieved 107 articles, eight of which met the criteria for inclusion by specifically addressing troglobitic species in Paraná caves. We also incorporated data from the Red Book of Threatened Brazilian Fauna and the regional survey “Conhecendo cavernas da região metropolitana de Curitiba” (Sessegolo et al. 2006).
Historical studies on Paraná caves have documented nine troglobitic species. A seminal survey by Pinto-da-Rocha (1995) highlighted two of these: the springtail Acherontides aff. eleonorae and the millipede Katantodesmus sp., both associated with bat guano deposits. Notably, Katantodesmus was subsequently recognized as a junior synonym of Crypturodesmus (Trajano et al. 2000).
Subsequent investigations expanded this list with the records of the pseudoscorpion Ideoroncus cavicola Mahnert, 2001, the springtail Arrhopalites paranaensis Zeppelini, 2006, the millipede Peridontodesmella alba Schubart, 1957, and the pseudoscorpion Pseudochthonius strinatii Beier, 1969 (Table 2).
Sampled caves, municipalities names, and troglobitic species occurrence registered by Pinto-da-Rocha (1995), Sessegolo et al. (2006) and Bená and Vanin (2014). Species occurrence after our samples in 2022 and 2023.
Further studies identified the harvestman Tricommatinae sp. in Gruta do Varzeão (Sessegolo et al. 2006), a cave that also yielded the description of the carabid beetle Coarazuphium ricardoi Bená & Vanin, 2014. Finally, the amphipod Hyalella formosa Cardoso, Araujo, Bueno & Ferreira, 2014 was described from a sandstone cave in Ponta Grossa. Although nine troglobitic species were documented in Paraná by 2023, H. formosa was excluded from our faunal comparisons as it occurs outside the Açungui Group.
Current troglobitic richness
A total of 28 troglobitic species were identified in this study (Fig. 2). These comprise four species of Palpigradi (Eukoeneniidae: Eukoenenia spp. 1-4); two Pseudoscorpiones (Chthoniidae: Pseudochthonius spp. 1-2); and four Opiliones, including Gonyleptidae spp. 1-2 and Cryptogeobiidae spp. 1-2. Araneae was represented by three species: Hahniidae sp. 1 and Prodidomidae spp. 1-2.
Some of the troglobitic species collected in Northern Paraná between the years 2022 and 2023: (A) Peridontodesmella sp. 1; (B) Crypturodesmus sp. 1; (C) Pyrgodesmidae sp. 1; (D) Gonyleptidae sp. 1; (E) Gonyleptidae sp. 2; (F) Cryptogeobiidae sp. 1; (G) Cryptogeobiidae sp. 2; (H) Pseudochtonius sp. 1; (I) Prodidomidae sp. 1; (J) Eukoenenia sp. 1; (K) Eukoenenia sp. 2; (L) Eukoenenia sp. 3; (M) Cylindroniscus sp. 1; (N) Trichorhina sp. 1; (O) Philosciidae sp. 1; (P) Acherontides aff. eleonorae; (Q) Arrhopalites sp. 1; (R) Happia sp. 1.
The Collembola were the most diverse group with seven recorded species: Acherontides aff. eleonorae (Hypogastruridae), Arrhopalites spp. 1-2 (Arrhopalitidae), Entomobryomorpha spp. 1-2, and Symphypleona spp. 1-2. Among Isopoda, three species were identified: Philosciidae sp. 1, Cylindroniscus sp. 1 (Styloniscidae), and Trichorhina sp. 1 (Platyarthridae). Diplopoda was represented by four species: Peridontodesmella spp. 1-2 (Cryptodesmidae), Pyrgodesmidae sp. 1, and Crypturodesmus sp. 1 (Oniscodesmidae). Finally, one Gastropoda species was identified: Happia sp. 1 (Systrophiidae).
The richness recorded in this study equaled or exceeded all previously reported values for the assessed caves. The caves of Pinheiro Seco, Pinhalzinho, Bom Sucesso, and Varzeão stood out for their high diversity of obligate invertebrates (Fig. 3A). Specifically, Pinheiro Seco and Bom Sucesso each hosted seven troglobitic species, Pinhalzinho contained eight, and Varzeão harbored nine. In comparison, historical records indicated only four troglobitic species for Varzeão, two for Bom Sucesso, and a single species for both Pinheiro Seco and Pinhalzinho (Fig. 4).
(A) Number of troglobitic species recorded in each cave. (B) Occurrence of each troglobitic species across the 20 sampled caves; the Y-axis represents the percentage of caves in which each species was recorded.
Spatial distribution of some caves and their troglobitic species richness (TgbR) in Northern Paraná, State, Brazil. 1) Varzeão; 2) Arco de Pedra; 3) Casa de Pedra; 4) Ressurgência do Feital; 5) Dá a Volta; 6) Pocinho; 7) Pocinho II; 8) Malfa zido; 9) Toquinhas; 10) Piedade; 11) Bromados; 12) Lancinha; 13) Fadas; 14) Jesuítas; 15) Bom Sucesso; 16) Chiquinho; 17) Chiquinho II; 18) Pinheiro Seco; 19) Ermida; 20) Itaperussu; 21) Pinheirinho; 22) Pinhalzinho; 23) Bacaetava.
Thirteen caves that previously lacked troglobitic records now harbor at least one obligate species (Table 2). Among these, Acherontides aff. eleonorae exhibited the widest distribution, occurring in 14 of the 23 surveyed caves (61%). This species was commonly associated with guano deposits and decaying wood, often in high abundance (Fig. 2P). Troglobitic species were absent in only three caves (13%): Gruta Dá a Volta, Ponte de Pedra, and Casa de Pedra; thus, 87% of the surveyed caves contained at least one troglobiont (Table 2).
Faunal distribution and similarity
No significant differences were found in the faunal composition of troglobitic species. The global test revealed no significant differences among the three limestone belts (R = 0.022, p = 0.388). Pairwise comparisons supported this result, showing no significant differentiation between Itaiacoca and Votuverava (R = 0.017, p = 0.405), Itaiacoca and Capiru (R = 0.035, p = 0.365), or Votuverava and Capiru (R = 0.035, p = 0.325).
Among the three belts, the Itaiacoca range exhibited the highest richness of troglobitic species, with a total of 20 recorded species. The Capiru range followed with 14 species, while the Votuverava range had the lowest diversity, with 11 species. Four species were shared across all three ranges: Trichorhina sp., Crypturodesmus sp., Happia sp., and Acherontides aff. eleonorae.
Additionally, five species were recorded in two of the three ranges: Pseudochthonius sp. 1, Entomobryomorpha sp. 1, Symphypleona sp. 1, Symphypleona sp. 2, and Arrhopalites sp. 1. The remaining 23 species were exclusive to a single limestone range, with 16 of them occurring in only one cave.
Regional relevance of the troglobite species richness
Of the 32 troglobitic species recorded in the state of Paraná, only seven have been formally described: Coarazuphium ricardoi Bená & Vanin, 2014; Acherontides aff. eleonorae Palacios-Vargas and Gnaspini-Netto, 1992; Ideoroncus cavicola Mahnert, 2001; Arrhopalites paranaensis Zeppelini, 2006; Hyalella formosa Cardoso, Araujo, Bueno and Ferreira, 2014; Peridontodesmella alba Schubart, 1957; and Pseudochthonius strinatii Beier, 1969.
With the new records obtained in the present study, the northern region of Paraná now ranks twelfth in Brazil in terms of total troglobitic species richness, emphasizing the previously underestimated diversity of subterranean fauna in the region (Fig. 5). When considering relative richness (i.e., species per cave sampled), the region ranks eleventh nationally (Table 3).
Brazilian areas of great biospeleological relevance. The numbers represent the total species richness. Some regions, such as Chapada Diamantina, have more than one lithology. Quadrilátero ferrífero and Carajás are iron ore and Ibitipoca is quartzite. Açungui-Northern Paraná (PR). States name: Pará (PA), Ceará (CE), Minas Gerais (MG), Goias (GO), Bahia (BA), Paraná (PR), São Paulo (SP), Mato grosso do Sul (MS), Rio Grande do Norte (RN), Parque Estadual Turístico do Alto Ribeira (PETAR), Parque Estadual Intervales (PEI).
National relevance in troglobite species richness in some areas of Brazil. Açungui Paraná (AP), lithology (Lito), richness (troglobite richness), relative species richness (S/N), number of sampled caves (n), coordinates (UTM), altitude asl (Alt). Places with caves considered hotspots of subterranean biodiversity (#), according to Culver and Sket (2000). Ferruginous rocks (Fe), Carbonates (Ca), and quartzite (Qua).
Economic development, impacts, and social conflicts
At least 56 companies carry out limestone extraction activities in the study region. The number of companies engaged in mining varies by municipality, with the highest concentration in Rio Branco do Sul (42 companies), followed by Almirante Tamandaré (24), Castro (18), Itaperuçu (8), Cerro Azul (7), Colombo (5), Jaguariaíva (5), Sengés (4), Campo Largo (3), Adrianópolis (2), Bocaiúva do Sul (1), and Doutor Ulysses (1). As of 2019, the number of formal mining concessions per municipality was as follows: Rio Branco do Sul (35), Castro (14), Almirante Tamandaré (12), Cerro Azul (7), Itaperuçu (7), Jaguariaíva (5), Colombo (4), Sengés (4), Campo Largo (3), Adrianópolis (2), Bocaiúva do Sul (1), and Doutor Ulysses (1).
The mineral products extracted vary by location. Adrianópolis exploits limestone; Almirante Tamandaré, dolomitic limestone and dolomite; Bocaiúva do Sul, dolomite; Campo Largo, limestone; Castro, limestone, dolomitic limestone, dolomite, and marble; Cerro Azul, limestone and marble; Colombo, limestone and dolomitic limestone; Doutor Ulysses, marble; Itaperuçu, limestone and dolomitic limestone; Jaguariaíva, limestone and dolomitic limestone; Rio Branco do Sul, a variety including calcitic limestone, dolomitic limestone, dolomite, and marble; and Sengés, limestone and dolomite.
Given its geomorphological characteristics, limestone plays a central role in the local economy of the studied municipalities. However, its extraction also has significant environmental consequences. In addition to contributing to the loss of native vegetation, which indirectly affects subterranean ecosystems, mining can cause siltation of caves. Gruta Itaperussu and Gruta Ermida are likely examples where siltation appears to be linked to nearby mining operations and deforestation. The mean distance from the caves to the nearest urban center was 16.5 km (SD = 6.3), and to mining areas, 8.9 km (SD = 5.9) (Table 1).
Population estimates for the municipalities where the studied caves are located, based on IBGE (2024) data, are as follows: Colombo - 249,277; Sengés - 19,441; Castro - 72,125; Campo Largo - 135,678; Rio Branco do Sul - 32,635; Almirante Tamandaré - 121,420; Itaperuçu - 29,493; Cerro Azul - 17,884; Adrianópolis - 5,797; and Doutor Ulysses - 5,525.
Across the 23 caves investigated, a total of 14 distinct types of anthropogenic impacts were recorded (Table 1, Fig. 6). The most frequently observed were trampling (78.2%), trash deposition (65.2%), graffiti (65.2%), pasture cultivation (60.8%), and vandalism of speleothems (60.8%). Four of the sampled caves are located within protected conservation units: Gruta da Lancinha, Gruta Jesuítas, Gruta Fadas, and Gruta Bacaetava. Among them, only Gruta da Lancinha lacks infrastructure for tourist management and environmental education activities.
Human impacts (HI) were observed on the surrounding epigean areas of the caves in the Northern Paraná, state, Brazil. Large-scale monoculture of Eucalyptus sp. (A), substitution of Araucária angustifolia forest (right side in picture B) by Eucalyptus sp. forest (left side in picture B), mining activities (C), urbanization (D), Construction and tourism inside a cave (E), Trampling on the cave floor (F), rock fragmentation inside a cave (G) and plastic bottle in the groundwater (H).
Troglobite diversity, distribution, and abiotic correlates
The richness of troglobitic species was significantly and positively associated with taxonomic distinctness (β = 0.0205, p < 0.001), indicating that caves with greater taxonomic distinctness among species tend to support higher troglobite richness. Human impact also exhibited a positive effect (β = 0.0136); however, the association was only marginally significant (p = 0.086), suggesting a trend that does not meet the conventional threshold for statistical significance. None of the other predictor variables in the model showed a significant effect (p > 0.05), suggesting that they may not individually influence troglobitic richness or that unmeasured factors and interactions may obscure their effects.
The generalized linear model showed a good overall fit, with a residual deviance of 15.305 on 16 degrees of freedom. Nagelkerke’s R2 value of 0.876 indicates that the model explains a substantial proportion of the variance in troglobite richness. Additionally, variance inflation factor (VIF) values were below 2 for all predictors, confirming the absence of multicollinearity and supporting the robustness of the model estimates.
DISCUSSION
The results of this study reveal a substantial increase in the number of known troglobitic species compared to previous records. Until 2023, historical surveys had documented only nine troglobitic species in Paraná, with early contributions by Pinto-da-Rocha (1995) identifying key taxa such as Acherontides aff. eleonorae and Katantodesmus sp. (the latter now a junior synonym of Crypturodesmus). Subsequent studies expanded this list through descriptions from caves like Lancinha and Varzeão, including the amphipod Hyalella formosa from a sandstone cave (Cardoso et al. 2014). In contrast, our study documented 28 troglomorphic or troglobitic species, a considerable increase in known subterranean biodiversity. The presence of genera such as Eukoenenia and Pseudochthonius, alongside various Collembola and Diplopoda, reflects a richer assemblage of invertebrates adapted to cave life. Notably, at least one troglobitic species was found in 13 caves that previously lacked such records, significantly expanding our understanding of the region’s subterranean fauna.
Systematic studies are crucial for characterizing cave biodiversity, a conclusion supported by global research (Deharveng and Bedos 2012, White and Culver 2011). In addition to careful sampling design and effective collection techniques, sampling frequency plays a pivotal role in determining observed species richness (Souza-Silva and Ferreira 2016). Due to the complexity and heterogeneity of subterranean habitats, complete species inventories are rarely achieved. Species accumulation curves in these environments often fail to reach an asymptote, suggesting that many species remain undocumented (Souza-Silva and Ferreira 2016).
Sampling cave environments is inherently challenging, especially given the limited accessibility of fissures and interstitial microhabitats where many specialized species reside (Culver and Pipan 2019). Consequently, repeated sampling is often necessary to capture the true extent of subterranean biodiversity. Nevertheless, rapid assessment protocols can provide meaningful insights for comparative analyses, provided that standardized sampling procedures are rigorously followed (Simões et al. 2015, Souza-Silva et al. 2015, Souza-Silva and Ferreira 2016, Moutaouakil et al. 2024).
Subterranean connectivity and troglobite distribution
In examining troglobitic composition, we hypothesized that geographical distances and distinct environmental conditions would differentiate the three limestone belts. However, this was not supported by the data, which revealed no significant differences in invertebrate community composition among the belts.
Environmental heterogeneity-including microhabi tat variation and trophic conditions-is known to foster diverse and complex communities (Souza-Silva et al. 2011, Lunghi et al. 2014, Simões et al. 2015). Habitat complexity and resource availability increase niche diversity, enabling species coexistence (Stein et al. 2014). Therefore, the relative similarity in environmental conditions across the belts likely explains the lack of significant differentiation.
Other factors commonly influencing subterranean composition include distance between caves, which can limit dispersal, and lithological variation, which shapes habitat structure even among caves in proximity (Souza-Silva et al. 2020). While water bodies and trophic resource availability also drive faunal differentiation (Bento et al. 2016, Pacheco et al. 2020, Souza-Silva et al. 2021), the sampled caves lie within geologically similar limestone formations and carbonate ranges.
The absence of compositional differences suggests a degree of subterranean connectivity. As highlighted by Mammola et al. (2020), connectivity is a key driver of biodiversity patterns and ecological interactions. Enhanced connectivity facilitates species dispersal, leading to more homogeneous assemblages. In line with Sovie et al. (2022), biological communities can serve as proxies for landscape connectivity: similar compositions reflect high levels of connectivity, whereas dissimilarity suggests ecological isolation. Thus, the observed faunal similarity provides essential insights into the current and potentially historical connectivity of these karst systems.
Regional significance of troglobite diversity
Although other regions of Brazil report higher troglobitic richness, this is largely the result of broader sampling efforts and the exploration of a greater number of caves (Trevellin et al. 2019, Bento et al. 2021, Ferreira and Souza-Silva 2023). We hypothesize that continued systematic surveys will substantially expand the regional inventory. As these caves are located within the Atlantic Forest-a global biodiversity hotspot with exceptional endemism (Tabarelli et al. 2010, Joly et al. 2014)-expanding research in this biome is essential.
Surface factors such as climate and primary productivity are major drivers of cave species richness (Culver et al. 2006, Bregović and Zagmajster 2016, Christman et al. 2016, Mammola et al. 2019). In both tropical and temperate systems, productivity shapes trophic dynamics (Culver and Pipan 2019). While low-productivity regions support fewer species due to resource limitation, Atlantic Forest caves have the potential to sustain richer assemblages due to high surface productivity.
Our results also demonstrate that the detailed microhabitat-based approach used here significantly improved the detection of small-bodied taxa compared to previous, less systematic protocols (Pinto-da-Rocha 1995, Sessegolo et al. 2006, Pacheco et al. 2020, Souza-Silva et al. 2021). Evidence from other regions indicates that species inventories continue to expand even after long-term exploration. For example, the Areias system (SP) has yielded new records after more than a century of study (Souza-Silva and Ferreira 2016), while the Águas Claras system (BA) required ten campaigns to document 31 troglobitic species (Ferreira et al. 2023).
Economic development and conservation
Tropical karst regions are particularly vulnerable to mining (Auler and Piló 2015, Souza-Silva et al. 2017). In the northern region of Paraná, limestone extraction by at least 56 companies poses a direct threat to cave structures and surrounding vegetation, altering microclimatic and trophic dynamics. These changes reduce the organic resources entering subterranean environments, directly impacting cave-dependent biota (Prous et al. 2015, Culver and Pipan 2019).
Interestingly, our findings reveal a positive association between troglobitic richness and human impact levels, underscoring the vulnerability of these organisms. Many troglobitic species are concentrated in areas experiencing intense anthropogenic pressures such as mining, deforestation, and agriculture-factors widely recognized for their negative influence on richness (Beynen and Townsend 2005, Schiesari et al. 2013, Ferreira et al. 2022a). With only seven of the 32 troglobitic species in Paraná formally described, there is an urgent need for conservation measures, taxonomic work, and long-term monitoring.
Protection remains limited; only four sampled caves lie within conservation units. Even within protected areas, status alone is insufficient without management. While Gruta Jesuítas, Gruta Fadas, and Gruta Bacaetava benefit from infrastructure and active programs (Menin et al. 2022, Antic et al. 2022), Gruta da Lancinha lacks active enforcement to prevent degradation despite its protected status. Consequently, only 28.1% of the troglobitic species recorded in Paraná are in areas with functional conservation status, a figure that reflects the national trend where only 11.6% of caves fall within protected areas (Sugai et al. 2015, Souza-Silva et al. 2015). Given the economic and political pressures from urbanization, systematic studies are essential to prioritize protection (White and Culver 2011, Deharveng and Bedos 2018).
Based on our results, we propose the establishment of a conservation unit in the Itaiacoca limestone belt, which harbors high troglobitic richness and faces less pressure from mining than areas closer to Curitiba. Incorporating emerging technologies and refined sampling will be vital to overcoming the limitations of studying these environments and fostering effective conservation strategies.
In summary, this study highlights the ecological importance of the Atlantic Forest’s subterranean systems, revealing a specialized fauna that has been historically overlooked. The significant increase in recorded species underscores the efficacy of standardized, microhabitat-based methodologies and the urgent need for systematic documentation. Given the intensification of mining and urbanization, integrating subterranean biodiversity into regional land-use planning and establishing new protected areas are essential steps to preserve the ecological integrity of these fragile ecosystems and mitigate the impacts of anthropogenic pressures.
ACKNOWLEDGMENTS
We thank Mater Natura and Margem Mineração for their financial support in compliance with the Speleological Compensation Commitment Term TCCE No. 01/2021/ICMBio. We also extend our gratitude to the Programa de Pós-Graduação em Ecologia Aplicada (PPGEco-UFLA), the Centro Nacional de Pesquisa e Conservação de Cavernas (CECAV), Instituto Água e Terra (IAT). Special thanks to the Grupo de Estudos Espeleológicos do Paraná (GEEP Açungui), especially Gisele Sessegolo, Darci Paulo Zakrzewski, and Kleber Mise, for their assistance in locating the caves. We acknowledge Pedro Henrique Mendes, Gabriel Vaz, Felipe Carvajal, Paulo César Reis, and Priscila Emanuela for their help in the invertebrate collection. We also thank Giovanna Monticelli (Isopoda), Julio Vaz (Hemiptera), Natália Soares Reategui (Psocoptera), Guilherme Prado (Pseudoscorpiones), Luiz Simone (Gastropoda), Douglas Zeppelini Filho (Collembola), Juan Romero (Diplopoda) and Leopoldo Ferreira (Acari) for their assistance in invertebrate identification.
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ADDITIONAL NOTES
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Data Availability
Datasets generated or analyzed in this study are available from the corresponding author on reasonable request.
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Funding
Financial support was provided by Mater Natura and Margem Mineração, in compliance with the Speleological Compensation Commitment Term (TCCE 01/2021/ICMBio). This work was also supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), including productivity scholarships to RLF (grant 302925/2022-8) and MSS (grant 303434/2025).
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AI Statement
Artificial intelligence tools were used solely to assist with language editing and grammar.
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How to cite this article
da Rocha Melo LM, Ferreira RL, Souza-Silva M (2026) No longer safe in the darkness: ecological and conservation perspectives on troglobitic species in a disturbed Neotropical karst landscape. Zoologia 43: e25031. https://doi.org/10.1590/S1984-4689.v43.e25031
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Published by
Sociedade Brasileira de Zoologia at Scientific Electronic Library Online - https://www.scielo.br/zool
Datasets generated or analyzed in this study are available from the corresponding author on reasonable request.
