Subterranean Communities Research Articles

Exploring Biodiversity and Food Webs in Sulfur Cave in the Vromoner Canyon on the Greek–Albanian Border

Sulfidic caves support diverse and abundant subterranean communities, including numerous endemic species and complex food webs, though the full extent of species diversity and resource utilization in these ecosystems remains largely unexplored. This paper presents the results of biological surveys conducted from 2023 to 2024 in Sulfur Cave, located in the Vromoner Canyon on the Greek–Albanian border, focusing on microbial, vertebrate, and invertebrate communities and investigating the structure of the subterranean food web. The microbial communities from the different biofilms are dominated by chemosynthetic sulfur-oxidizing microorganisms, specifically filamentous bacteria such as Thiotrix and Beggiatoa. Two species of fish, an eel (Anguilla sp.) and a Cyprinid (Alburnoides sp.), and six bat species from three families (Rhinolophidae, Miniopteridae, and Vespertilionidae) were documented. The invertebrate fauna includes five aquatic species, 25 terrestrial species, and four amphibiotic species. Among these, eight species are endemic, and seven species exhibit troglomorphic traits. Stable isotope analysis showed light carbon and nitrogen values for the terrestrial and aquatic invertebrates, suggesting that subterranean communities rely on food produced in situ by chemoautotrophic microorganisms. Our results identified cave areas of significant biological relevance and provided reference data to inform conservation actions aimed at preserving the biodiversity of this sulfidic cave.

Pronounced changes of subterranean biodiversity patterns along a Late Pleistocene glaciation gradient

Understanding spatial patterns of biodiversity within the context of long‐term climatic shifts is of high importance, particularly in the face of contemporary climate change. In comparison to aboveground taxa, subterranean organisms respond to changing climates with generally much lower dispersal and recolonization potential, yet possible persistence in refugial groundwater habitats under ice‐shields. However, knowledge on general and geographically large‐scale effects of glaciation on contemporary groundwater biodiversity patterns is still very limited. Here, we tested how Late Pleistocene glaciation influenced the diversity and distribution of 36 groundwater amphipod species in Alpine and peri‐Alpine regions, characterized by extensive glaciation cycles, and how its legacy explains contemporary diversity patterns. We based our analysis on an unprecedented density of ~ 1000 systematic sampling sites across Switzerland. Using presence–absence data, we assessed biodiversity and species' ranges, and calculated for each site within‐catchment distance to the Last Glacial Maximum (LGM) glacier extent. We then applied a sliding window approach along the obtained distance gradient from LGM ice‐covered to ice‐free sites to compute biodiversity indices reflecting local richness, regional richness, and differentiation, respectively. We found a strong signal of the LGM ice extent on the present‐day distribution of groundwater amphipods. Our findings revealed pronounced species turnover and spatial envelopes of individual species' occurrences in formerly ice‐covered, ice‐free, or transitional zones, respectively. While local richness remained constant and low along the LGM distance gradient, groundwater communities in LGM ice‐covered areas were more similar to each other and had lower gamma diversities and decreased occurrence probabilities per sliding window compared to communities in Pleistocene ice‐free areas. These results highlight the significant impact of Pleistocene glaciation on shaping biodiversity patterns of subterranean communities and imprinting contemporary distribution of groundwater organisms.

Functional convergence underground? The scale‐dependency of community assembly processes in European cave spiders

AbstractAimQuantifying the relative contribution of environmental filtering versus limiting similarity in shaping communities is challenging because these processes often act simultaneously and their effect is scale‐dependent. Focusing on caves, island‐like natural laboratories with limited environmental variability and species diversity, we tested: (i) the relative contribution of environmental filtering and limiting similarity in determining community assembly in caves; (ii) how the relative contribution of these driving forces changes along environmental gradients.LocationEurope.Time periodPresent.Major taxa studiedSubterranean spiders.MethodsWe used data on distribution and traits for European cave spiders (n = 475 communities). We estimated the trait space of each community using probabilistic hypervolumes, and obtained estimations of functional richness independent of the species richness of each community via null modelling. We model functional diversity change along environmental gradients using generalized dissimilarity modelling.ResultsSixty‐three percent of subterranean spider communities exhibited a prevalence of trait underdispersion. However, most communities displayed trait dispersion that did not depart significantly from random, suggesting that environmental filtering and limiting similarity were both exerting equally weak or strong, yet opposing influences. Overdispersed communities were primarily concentrated in southern latitudes, particularly in the Dinaric karst, where there is greater subterranean habitat availability. Pairwise comparisons of functional richness across caves revealed these effects to be strongly scale‐dependent, largely varying across gradients of cave development, elevation, precipitation, entrance size and annual temperature range. Conversely, geographical distance weakly affected trait composition, suggesting convergence in traits among communities that are far apart.Main conclusionsEven systems with stringent environmental conditions maintain the potential for trait differentiation, especially in areas of greater habitat availability. Yet, the relative influence of environmental filtering and limiting similarity change with scale, along clear environmental gradients. The interplay of these processes may explain the assembly of species‐poor subterranean communities displaying high functional specialization.

The Subterranean Species of the Vjetrenica Cave System in Bosnia and Herzegovina

The Western Balkan’s Vjetrenica Cave in southern Bosnia and Herzegovina is renowned for high richness of subterranean species. However, the data on its fauna have been published only in monographs printed in a small number of copies, making them hardly accessible to the wider scientific community. To overcome this issue, we compiled the data from published monographs with the data from our own recent field surveys. Further, as they are connected via water channels or small crevices in bedrock, we defined the Vjetrenica Cave System as a system comprising Vjetrenica and Bjelušica Caves and Lukavac Spring. Altogether, 93 troglobiotic, i.e., obligate subterranean aquatic (48) and terrestrial (45), taxa were reported for the system, verifying the Vjetrenica Cave System as the second richest locality in subterranean biodiversity in the world. The global uniqueness of the system is also reflected in the fact that as many as 40 troglobiotic species were described from the system. Finally, we reviewed the factors endangering this unique subterranean community and questioned whether it will withstand human-induced changes and pressures due to infrastructural development in southern Bosnia and Herzegovina.

Persisting while changing over time: modelling the historical biogeographic of cave crickets (Orthoptera, Grylloidea) in Neotropics

Abstract Using species distribution modelling (SDMs) techniques, we predicted the biogeographic history of crickets commonly found in Neotropical caves as a way to detect potential long-term environmental refuges in South America. Our models were built based on a thorough investigation of existing database regarding the genus Endecous Saussure, 1878 (Ensifera: Phalangopsidae) occurrences. The predictions of their distribution were obtained for two paleoclimate scenarios (LGM — 21 ka and Mid-Holocene — 6 ka), the current climate scenario (0 ka) and one future global warming climate scenario (RCP8.5, 2080–2100). Our findings suggest that in the past, the potential distribution of the crickets was wider, with potential forest corridors connecting different karst areas with caves within their occupancy area. The future prediction indicates a drastic reduction in their spatial distribution with an increased potential for isolation in subterranean ecosystems. Atlantic humid forest patches and caves represent the main environmental refuges for these crickets. Considering the ongoing impacts on surface environments and future climate change, the conservation of caves and karst landscapes has become one of the main strategies for the maintenance of these crickets and all the correlated subterranean communities.

Dark biosphere: Just at the very tip of the iceberg.

Dark biosphere: Just at the very tip of the iceberg.

Pilbarana, a new subterranean amphipod genus (Hadzioidea: Eriopisidae) of environmental assessment importance from the Pilbara, Western Australia

The Pilbara and nearby regions in north-western Western Australia have an exceptionally high diversity of short-range endemic invertebrates inhabiting threatened groundwater-dependent habitats. Amphipod crustaceans, in particular, are dominant in these communities, but are poorly understood taxonomically, with many undescribed species. Recent molecular phylogenetic analyses of Pilbara eriopisid amphipods have, nonetheless, uncovered a previously unknown biodiversity. In this study, we formally establish a new genus, Pilbarana Stringer & King gen. nov., and describe two new species, P. grandis Stringer & King sp. nov. from Cane River Conservation Park and P. lowryi Stringer & King sp. nov. from the Fortescue River Basin near the Hamersley Range, using a combination of molecular and morphological data. The new genus is similar morphologically to the two additional Western Australian eriopisid genera, Nedsia Barnard & Williams, 1995 and Norcapensis Bradbury & Williams, 1997, but represents a genetically divergent, reciprocally monophyletic lineage, which can be differentiated by its vermiform body shape, the presence of an antennal sinus, and by the length and form of the antennae and uropods. This research signifies an important contribution to knowledge of Pilbara subterranean communities and has critical implications for future environmental impact assessments and conservation management.

From light to darkness: the duality of influence of habitat heterogeneity on Neotropical terrestrial cave invertebrate communities

ABSTRACT The theory of habitat heterogeneity, which treats one of the global drivers of biodiversity, is valid for several taxonomic groups and distinct ecosystems, including subterranean environments. However, knowledge about the factors that influence the structure of subterranean communities remains limited, especially in Neotropical regions. We sought to understand the main drivers of invertebrate species richness and composition. For that, we compared the substrate elements of twilight and deep-cave zones and their associated invertebrate communities. Variations in habitat heterogeneity were significantly related to richness in the deep cave zone, but had no effect on the fauna associated with the twilight zone. The local heterogeneity enhanced the richness in the deep cave zone due to the increase in the number of available habitats and the effect on decreasing niche overlap. For communities’ composition, the geographic distribution of caves explained the similarity between the twilight zone of different caves. Therefore, nearby caves have a more similar fauna in the entrance regions but conversely, exhibit a higher dissimilarity between communities associated with the deep-cave zone. This study highlights the influence of local habitat heterogeneity on the invertebrate communities associated with different zones of the cave.

Arthropod communities and drivers of their species diversity and composition in caves

Understanding the drivers of diversity patterns in ecological communities remains a major challenge in ecology. Moreover, few studies have considered invertebrate or subterranean communities and little is known about which factors are responsible for structuring arthropod communities in caves. In this study we: assessed the abundance, richness, and composition of arthropod communities from eight caves located in Banat and Mehedinti region, Romania; and determined whether altitude, cave physical characteristics (temperature, relative humidity, light intensity) and features (cave extension, hight, width, heterogeneity, substrate (wall versus floor)) influence cave arthropod communities along the horizontal development of the cave (i.e. from the cave entrance, through the intermediate zone, to the aphotic zone). assessed the abundance, richness, and composition of arthropod communities from eight caves located in Banat and Mehedinti region, Romania; and determined whether altitude, cave physical characteristics (temperature, relative humidity, light intensity) and features (cave extension, hight, width, heterogeneity, substrate (wall versus floor)) influence cave arthropod communities along the horizontal development of the cave (i.e. from the cave entrance, through the intermediate zone, to the aphotic zone). Overall, 89 species were found, of which three were obligate subterranean dwellers and 17 were endemic species. Species abundance distributions showed evident variation in species numbers among cave zones and between the wall and floor substrate. Species abundance was influenced by cave extension, relative humidity and light intensity. Species richness was related to cave extension while relative humidity and cave heterogeneity affected the species diversity. The results also indicated differences in species abundance, richness and diversity among cave zones and between substrate types. The arthropod community structure and composition was determined by altitude, relative humidity, temperature and substrate. The floor and wall substrate had different species composition while the species composition of the three cave zones largely overlapped. We conclude that several biotic and abiotic factors explain the diversity and composition of cave arthropods communities and that our results may be relevant to other types of island-like habitats.

From Slave to Bishop. Callixtus’ Early Ecclesial Career and Mechanisms of Clerical Promotion

Abstract Bishop Callixtus I of Rome (217?–222?) is well known for his position as manager of the κοιμητήριον, the earliest subterranean community burial ground, today known as the Catacombs of Callixtus. Less well documented, but particularly formative is, however, Callixtus’ early ecclesial career starting with his recognition as an authentic confessor shortly after his return from the mines of Sardinia. This contribution aims to shed some light on this formative period and explores the mechanisms behind Callixtus’ promotion to paid ecclesial ministry. It argues that Callixtus’ association with the clergy was neither an honorary, that is, automatic admission, nor merely a pious act to honour his individual and spiritual achievement. It seems, it was also a powerful instrument to financially support, integrate, and if necessary, control independent spiritual authorities. Moreover, Callixtus’ installation in active ministry, as well as that of other confessors, show typical patterns of client-patron relationship.

Do different relevance attributes indicate the same conservation priorities? A case study in caves of southeastern Brazil

In the last decade, the scientific community brought to the debate gaps that slow down the advance of knowledge regarding global biodiversity. More recently, this discussion has reached subterranean environments, where these gaps are even more dramatic due to the relict and vulnerable nature of their species. In this context, we tested ecological metrics related to some of these gaps, checking if the biological relevance of the caves would change depending on ecological attributes related to each metric. The study was carried out in caves from southeastern Brazil, located in a region presenting a high richness of troglobitic species restricted to a narrow geographical extent. Thus, we verified: (a) the cave invertebrate communities’ vulnerability with the Vulnerability Index and the Importance Value for Cave Conservation; (b) the distribution and endemicity of the troglobitic species with the Endemicity Index; (c) the phylogenetic diversity of the troglobitic species considering the average taxonomic distinction (∆+), their richness and evenness. We observed a considerable change in the ordering of the caves’ biological relevance according to each tested attribute (index). We discussed how each of these metrics and their attributes indirectly relate to: (a) the preservation and maintenance of the phylogenetic diversity of subterranean communities; (b) the spatial restrictions of different groups, where the greater their restrictions, the greater their vulnerability; (c) the preservation of caves with high biological relevance considering these different attributes together. Thus, we recommend the use of different metrics so that different ecological attributes can be considered, supporting actions that aim to preserve caves in highly altered regions. Finally, we find that the most biologically important cave in the region is not protected (Gruta da Morena cave). We warn that this cave needs to be contemplated by a conservation unit in the region urgently.

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

Abstract The present work brings information on threats to the subterranean fishes in Brazil. Currently, at least 36 species are known, 22 of which are already formally described. Endemism is the rule for most of them. Regarding their conservation, these fishes are in general considered threatened: and most of the already formally described species are included in national lists of threatened fauna, and only four of them are included in the global list of the IUCN. Regarding habitats, Brazilian subterranean fishes occur in alluvial sediments (part of the hyporheic zone), shallow base-level streams, flooded caves, lakes in the water table, upper vadose tributaries, and epikarst aquifers. We detected 11 main threats, mainly related to agriculture, pasture, and hydroelectric plans, but unmanaged tourism and pollution are also significant threats. Two threats affect a high number of species (physical change of the habitat and food restriction). The river basins with the higher number of identified threats are the upper Tocantins (eight) followed by the upper Paraguaçu (six). Effective proposals to protect this neglected component of the Brazilian biodiversity are still scarce, such as monitoring projects and their function in the subterranean communities, besides education projects aiming to develop public awareness.

Environmental factors structuring the assemblage of aquatic insects in an epigean and hypogean stretch of a Neotropical karst stream

The aim of the present study was to identify which variables structure the assemblage of aquatic insects in the subterranean environment, because knowledge about how subterranean communities are structured in rivers with hypogean sections is still emerging. In addition to identifying whether the hypogean assemblage is structured in the same way as the epigean assemblage, we sought to identify whether the environmental restrictions caused by the subterranean habitat resulted in reduced species richness and abundance compared with the epigean habitat. We sampled a 345-m stretch of a stream in Brazil and collected aquatic insects from both the epigean and hypogean environments. In the stream stretch investigated, there was a positive relationship between richness and the percentage of immersion, fine substrate and organic matter, and a negative relationship between richness and conductivity. We also verified differences between the epigean and hypogean environments regarding composition. The variables that best explained the overall assemblage structure included the epigean–hypogean environment and the percentage of coarse and fine substrate. Given the differences between these environments, we emphasise the need for management actions in karst regions that consider the discontinuity of these regions’ river communities to conserve all components of diversity.

Epigean and hypogean drivers of Neotropical subterranean communities

AbstractAimIn addition to cave size and other subterranean habitat characteristics, cave entrances are important structurers of neotropical cave communities. However, little is known about the epigean ecosystems factors that might dictate the influence of entrances and the relationship among surface and cave communities, as entrance regions are ecotonal zones between the epigean and hypogean ecosystems. We aimed to assess the influence of epigean and hypogean factors as potential drivers of invertebrate species richness in Neotropical caves as well as the influence of the regional pool of invertebrate diversity on cave invertebrate diversity.LocationLimestone caves in south‐eastern Brazil.TaxonInvertebratesMethodsData were collected in 48 caves within the Cerrado biome (Brazilian Savanna). The fauna sampling was performed by a direct intuitive search (DIS). Landscape characteristics and climatic parameters were accessed using geographic information systems. The characterization of the caves occurred during each sampling event. Regional diversity was based on the Taxonomic Catalog of Brazilian Fauna. To clarify the factors that significantly influence invertebrate species richness of the caves, we used generalized linear models (GLM). The relationship between regional diversity and cave diversity was evaluated based on linear models (LM).ResultsOverall, 1,173 species were found, of which 72 were obligate subterranean dwellers. The cave total species richness was influenced by hypogean factors and epigean factors. The species richness of obligate cave dwellers was significantly explained only by cave size. The regional pool of invertebrate species influenced the levels of biodiversity in the studied caves. The taxa with troglobitic species tended to be more diverse in caves than expected.Main conclusionsIn addition to the influences of intrinsic cave variables, we highlight the importance of epigean factors on subterranean diversity in the Neotropics. The study shows the significant influence of the regional species pool on cave faunal composition. These findings reinforce the importance of considering the surrounding areas in actions regarding cave biodiversity conservation.

Under the karst: detecting hidden subterranean assemblages using eDNA metabarcoding in the caves of Christmas Island, Australia

Subterranean ecosystems are understudied and challenging to conventionally survey given the inaccessibility of underground voids and networks. In this study, we conducted a eukaryotic environmental DNA (eDNA) metabarcoding survey across the karst landscape of Christmas Island, (Indian Ocean, Australia) to evaluate the utility of this non-invasive technique to detect subterranean aquatic ‘stygofauna’ assemblages. Three metabarcoding assays targeting the mitochondrial 16S rRNA and nuclear 18S genes were applied to 159 water and sediment samples collected from 23 caves and springs across the island. Taken together, our assays detected a wide diversity of chordates, cnidarians, porifera, arthropods, molluscs, annelids and bryozoans from 71 families across 60 orders. We report a high level of variation between cave and spring subterranean community compositions which are significantly influenced by varying levels of salinity. Additionally, we show that dissolved oxygen and longitudinal gradients significantly affect biotic assemblages within cave communities. Lastly, we combined eDNA-derived community composition and environmental (water quality) data to predict potential underground interconnectivity across Christmas Island. We identified three cave and spring groups that showed a high degree of biotic and abiotic similarity indicating likely local connectivity. This study demonstrates the applicability of eDNA metabarcoding to detect subterranean eukaryotic communities and explore underground interconnectivity.

Distribution of cyclopoid copepods in different subterranean habitats (southern Poland)

Abstract The majority of Polish studies on freshwater cyclopoids focused on surface water fauna. There are relatively few data on copepods of subterranean waters. Thus, in our research, copepods were collected from 37 different, mostly groundwater-dependent habitats (i.e. caves, springs, wells, interstitial and overhead environments) over a period of five years between 2005 and 2010. A total of 22 species belonging to eight genera were found. Some species, previously not recorded or known only from a few sites in Poland, proved to be a frequent component of subterranean communities.

Exploring the homogeneity of terrestrial subterranean communities at a local spatial scale

1. Although caves are generally perceived as isolated habitats, at the local scale, they are often interconnected via a network of fissures in the bedrock. Accordingly, caves in close proximity are expected to host the same, or very similar, animal communities.2. We explored the extent to which subterranean arthropod communities are homogenous at a local spatial scale of less than 1 km2, along with which cave‐specific environmental features result in a departure from the expected homogeneous pattern. We approached this question by studying richness and turnover in terrestrial invertebrate communities of 27 caves in a small karst massif in the Western Italian Alps.3. Specialised subterranean species were homogeneously distributed among caves and were not influenced by seasonality. The only factor driving their distribution was the distance from the cave entrance, with deeper caves yielding a greater diversity of species.4. Significant spatio‐temporal turnover in species not specialised to subterranean life was observed. In summer, there was a significant homogenisation of the community and a more even distribution of species among sites; in winter, these species were missing or found exclusively at greater depths, where environmental conditions were more stable. Furthermore, caves at lower elevations yielded, on average, a greater diversity and abundance of these species.5. This study demonstrated that the theoretical expectation of no turnover in community composition in caves in close proximity is not always met. Turnover can be mostly attributed to seasonal patterns and sampling depth; thus, our findings have implications for planning sampling and monitoring activities in caves.

Do Salamanders Limit the Abundance of Groundwater Invertebrates in Subterranean Habitats?

Several species of surface salamanders exploit underground environments; in Europe, one of the most common is the fire salamander (Salamandra salamandra). In this study, we investigated if fire salamander larvae occurring in groundwater habitats can affect the abundance of some cave-adapted species. We analyzed the data of abundance of three target taxa (genera Niphargus (Amphipoda; Niphargidae), Monolistra (Isopoda; Sphaeromatidae) and Dendrocoelum (Tricladida; Dedrocoelidae)) collected in 386 surveys performed on 117 sites (pools and distinct subterranean stream sectors), within 17 natural and 24 artificial subterranean habitats, between 2012 and 2019. Generalized linear mixed models were used to assess the relationship between target taxa abundance, fire salamander larvae occurrence, and environmental features. The presence of salamander larvae negatively affected the abundance of all the target taxa. Monolistra abundance was positively related with the distance from the cave entrance of the sites and by their surface. Our study revealed that surface salamanders may have a negative effect on the abundance of cave-adapted animals, and highlited the importance of further investigations on the diet and on the top-down effects of salamanders on the subterranean communities.

Specialized aquatic subterranean communities are probably most species-rich in the thickest epikarst

Stygobionts are aquatic troglobionts, i.e., organisms that are specialized for living in subterranean environment. It has been demonstrated that the epikarst above caves harbors a stygobiont fauna that is as rich as that in deeper caves. The abiotic parameters affecting the aquatic fauna in drip water have been relatively well explored, while aquatic troglobionts alone are not frequently the focus of such studies; consequently, many crucial questions remain insufficiently studied. We hypothesized that the epikarst stygobiont fauna may occur locally in deeper zones of the epikarst, since environmental conditions are more stable there. For this purpose, we studied the composition and annual dynamics of the epikarst stygobiont community from ten water drips in the cave Zguba jama in Slovenia. Copepoda predominated among eight stygobiont taxa. The high total and between-sites dissimilarity of stygobiont communities among the drips was mainly the consequence of species turnover. We found that the greater the distance from the entrance and the ceiling thickness, and the higher the water temperature, the greater was the chance of finding aquatic troglobionts and the higher thier diversity. Our study suggests that locally, owing to specific lithology and geomorphology, epikarst stygobionts can extend from the shallow layers into deeper epikarst layers, where voids with more suitable environmental conditions exists.

Taxonomic Distinctness of the subterranean fauna from Peruaçu Caves National Park, state of Minas Gerais, eastern Brazil

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