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.     

Distributional dynamics of a specialized subterranean community oppose the classical understanding of the preferred subterranean habitats

Troglobionts are organisms that are specialized for living in a subterranean environment. These organisms reside prevalently in the deepest zones of caves and in shallow subterranean habitats, and complete their entire life cycles therein. Because troglobionts in most caves depend on organic matter resources from the surface, we hypothesized that they would also select the sections of caves nearest the surface, as long as environmental conditions were favorable. Over 1 year, we analyzed, in monthly intervals, the annual distributional dynamics of a subterranean community consisting of 17 troglobiont species, in relation to multiple environmental factors. Cumulative standardized annual species richness and diversity clearly indicated the existence of two ecotones within the cave: between soil and shallow subterranean habitats, inhabited by soil and shallow troglobionts; and between the transition and inner cave zones, where the spatial niches of shallow and deep troglobionts overlap. The mean standardized annual species richness and diversity showed inverse relationships, but both contributed to a better insight into the dynamics of subterranean fauna. Regression analyses revealed that temperatures in the range 7–10°C, high moisture content of substrate, large cross section of the cave, and high pH of substrate were the most important ecological drivers governing the spatiotemporal dynamics of troglobionts. Overall, this study shows general trends in the annual distributional dynamics of troglobionts in shallow caves and reveals that the distribution patterns of troglobionts within subterranean habitats may be more complex than commonly assumed.     

Six new cavernicolous cixiid planthoppers in the genus Solonaima from Australia (Homoptera: Fulgoroidea)

Abstract The monophyletic genus Solonaima , endemic to northern Queensland, is reviewed and six new species are described: S.sullivani sp.n., S.pholetor sp.n., S.stonei sp.n., S.halos sp.n., S.irvini sp.n. and S. baylissa sp.n. The previously known epigean species, S.solonaima Kirkaldy and S.pallesens (Distant) are illustrated and redescribed. The six new species represent four separate independent cave invasions and nearly double the number of known cavernicolous cixiids in the world. This is the first report of a closely related group of cave-dwelling Homoptera showing varying degrees of cave adaptation. One facultative cave species, S.sullivani , shows virtually no modification from surface relatives. Two species, S.pholetor and S.stonei , show some eye, colour, and wing-reduction, but they are still flighted and are considered facultative cave species. S.halos and S. irvini are nearly blind and have reduced, non-functional wings and are considered obligate cave species. S. baylissa , the most remarkable obligate cave species, is highly modified: eyeless, nearly wingless and colourless. The evolutionary trends displayed in cave adaptation are illustrated and discussed. These include reduction in body colour, eyes and wings, alteration of head and thorax shape, and possibly simplification of the male genitalia. The geology of the caves is complex and ranges from greater than 5-million-year-old caves in Silurian-aged metamorphosed limestone to 190,000-year-old lava tubes. The facultative species are generally found in the most open caves, the two intermediate obligate species are found in deeper caves, and the most highly modified species is restricted to damp cave passages with high CO₂ levels. There is no correlation between the ages of the caves and the degree of cave adaptation.     

Reduction in the metabolic levels due to phenotypic plasticity in the Pyrenean newt,Calotriton asper,during cave colonization

According to theories on cave adaptation, cave organisms are expected to develop a lower metabolic rate compared to surface organisms as an adaptation to food scarcity in the subterranean environments. To test this hypothesis, we compared the oxygen consumption rates of the surface and subterranean populations of a surface‐dwelling species, the newt Calotriton asper, occasionally found in caves. In this study, we designed a new experimental setup in which animals with free movement were monitored for several days in a respirometer. First, we measured the metabolic rates of individuals from the surface and subterranean populations, both maintained for eight years in captivity in a natural cave. We then tested individuals from these populations immediately after they were caught and one year later while being maintained in the cave. We found that the surface individuals that acclimated to the cave significantly reduced their oxygen consumption, whereas individuals from the subterranean population maintained in the cave under a light/dark cycle did not significantly modify their metabolic rates. Second, we compared these metabolic rates to those of an obligate subterranean salamander (Proteus anguinus), a surface aquatic Urodel (Ambystoma mexicanum), and a fish species (Gobio occitaniae) as references for surface organisms from different phyla. As predicted, we found differences between the subterranean and surface species, and the metabolic rates of surface and subterranean C. asper populations were between those of the obligate subterranean and surface species. These results suggest that the plasticity of the metabolism observed in surface C. asper was neither directly due to food availability in our experiments nor the light/dark conditions, but due to static temperatures. Moreover, we suggest that this adjustment of the metabolic level at a temperature close to the thermal optimum may further allow individual species to cope with the food limitations of the subterranean environment.     

Cave Fauna of Bermuda

Sea-level pools are found in most of Bermuda's known caves. Although the terrestrial fauna of the caves is sparse, a rich aquatic fauna inhabits the pools. While many of the marine cave animals are more or less regular immigrants from open littoral habitats, a number of new species have been discovered, including blind and probably subterranean ones. Zoogeographical connections exist between Bermuda's cave fauna and those of the West Indies and the Mediterranean.     

Energy and speleogenesis: Key determinants of terrestrial species richness in caves

The aim of this study was to unravel the relative role played by speleogenesis (i.e., the process in which a cave is formed), landscape‐scale variables, and geophysical factors in the determination of species richness in caves. Biological inventories from 21 caves located in the southeastern Iberian Peninsula along with partial least square (PLS) regression analysis were used to assess the relative importance of the different explanatory variables. The caves were grouped according to the similarity in their species composition; the effect that spatial distance could have on similarity was also studied using correlation between matrices. The energy and speleogenesis of caves accounted for 44.3% of the variation in species richness. The trophic level of each cave was the most significant factor in PLS regression analysis, and epigenic caves (i.e., those formed by the action of percolating water) had significantly more species than hypogenic ones (i.e., those formed by the action of upward flows in confined aquifers). Dissimilarity among the caves was very high (multiple‐site β_sim = 0.92). Two main groups of caves were revealed through the cluster analysis, one formed by the western caves and the other by the eastern ones. The significant—but low—correlation found between faunistic dissimilarity and geographical distance (r = .16) disappeared once the caves were split into the two groups. The extreme beta‐diversity suggests a very low connection among the caves and/or a very low dispersal capacity of the species. In the region under study, two main factors are intimately related to the richness of terrestrial subterranean species in caves: the amount of organic material (trophic level) and the formation process (genesis). This is the first time that the history of a cave genesis has been quantitatively considered to assess its importance in explaining richness patterns in comparison with other factors more widely recognized.     

ECOMORPHOLOGICAL CONVERGENCE OF CAVE COMMUNITIES

Extreme selective environments are commonly believed to funnel evolution toward a few predictable outcomes. Caves are well‐known extreme environments with characteristically adapted faunas that are similar in appearance, physiology, and behavior all over the world, even if not closely related. Morphological diversity between closely related cave species has been explained by difference in time since colonization and different ecological influence from the surface. Here, we tested a more classical hypothesis: morphological diversity is niche‐based, and different morphologies reflect properties of microhabitats within caves. We analyzed seven communities with altogether 30 species of the subterranean amphipod (crustacean) genus Niphargus using multivariate morphometrics, multinomial logit models cross‐validation, and phylogenetic reconstruction. Species clustered into four distinct ecomorph classes—small pore, cave stream, cave lake, and lake giants—associated with specific cave microhabitats and of multiple independent phylogenetic origins. Traits commonly regarded as adaptations to caves, such as antenna length, were shown to be related to microhabitat parameters, such as flow velocity. These results demonstrate that under the selection pressure of extreme environment, the ecomorphological structure of communities can converge. Thus, morphological diversity does not result from adaptive response to temporal and ecological gradients, but from fine‐level niche partitioning.     

Epigean and subterranean ichthyofauna from the São Domingos karst area, Upper Tocantins River basin, Central Brazil

In a survey of epigean and cave streams in the São Domingos karst area, 38 species were present in the stream reaches, including 10 characiforms, 19 siluriforms, seven gymnotiforms and two perciforms. One species of Astyanax and the new armoured catfish species Parotocinclus were the most common epigean fishes in São Domingos. The most conspicuous non-troglomorphic cave fishes were Hoplerythrinus unitaeniatus , Astyanax sp., Brycon sp. and two species of Imparfinis , with I. hollandi being the most common fish in most caves. São Domingos karst area has the most diverse and abundant Brazilian cavefish fauna, not only in terms of troglobitic species but also in general fish richness, with 22 non-troglomorphic species recorded in caves in addition to five troglobitic ones. Most fishes examined for stomach contents had at least partially full stomachs. The studied fishes were carnivorous, feeding primarily on aquatic insects. Fishes with developed gonads recorded in caves were I. hollandi , Rhamdia quelen , Pseudocetopsis plumbeus , Hoplerythrinus unitaeniatus and Cichlasoma araguaiensis , indicating a potential for reproduction in the subterranean habitat.     

The genus Camptochaeta in Nearctic caves, with the description of C. prolixa sp. n. (Diptera, Sciaridae)

Camptochaeta prolixasp. n. (Diptera, Sciaridae) is described from caves in Nevada, and three other congeneric species are recorded from caves in Nevada and Arkansas, United States. The new species shows some indication to a subterranean mode of life, including long antenna and legs, and in some specimens, reduction of the eye bridge.     

Multi-spatial analysis on cave ecosystems to predict the diversity of subterranean invertebrates

Subterranean habitats around the world can shelter diversified and threatened faunal communities. However, issues related to alterations in the landscape and structure of subterranean habitats still need to be better understood. Therefore, we used a multi-spatial scale analysis of land cover, land use, and cave habitats to predict the diversity of communities of subterranean invertebrates. We hypothesized that changes in land cover promote alterations in both faunal richness and composition and microhabitat diversity and that microhabitat features determined subterranean biodiversity. Sixteen limestone caves were sampled in Brazil at micro, meso, and macro scales using quadrats (1m²), transects (100 meters) as sample units inside caves and buffers with the radius of 100 and 250 meters in the surroundings of the cave entrances. Models performed showed that land cover and land use influenced cave environments, regarding both microhabitats traits and terrestrial invertebrate richness and composition. We also observed a relationship between microhabitat structure and terrestrial invertebrate richness and composition. Our results showed that deforested areas had negative effects on species richness and changed their composition, while natural areas had positive effects on microhabitat diversity. The same effects were observed for both 100 and 250 meters buffers. Invertebrate richness was negatively predicted by deforested areas while positively predicted by natural areas. Richness was also positively predicted by the combination of all microhabitat traits, and dissimilarity of fauna was influenced by microhabitat diversity in mesoscale and microscale by all microhabitat elements. The results highlight the importance of the landscape surrounding the caves to conserve the subterranean habitats and their fauna. Due to the spatial and temporal changes in the global environmental scenario, we argue the urgency of further detailed studies in fragmented landscapes to define minimum areas of protection for cave environments.     

Kotumsar Cave biodiversity: a review of cavernicoles and their troglobiotic traits

The evolutionary adaptations of the organisms which inhabit the unusual and fragile ecosystems within caves are of inherent interest to both biologists and laymen. Cave organisms generally develop a high degree of physiological and behavioural adaptation for survival in the subterranean environment. The Kotumsar Cave is biologically the best known cave in India and has attracted interest from researchers from all over the world. This paper assesses the ecological community and overall habitat of the cave. This is based on long-term field observations and the review of the extensive literature on Kotumsar. For each species, features indicative of evolutionary adaptation to the cave environment are noted and conclusions drawn regarding the status of the species as a cavernicole. Several species of this cave are yet to get a proper study for correct taxonomic position although they have apparent troglomorphic dispositions. Several species which are highly endemic to this cave are probably in verge of its extinction. A serious measure to conserve the whole biodiversity has been suggested.     

Applying species distribution models to caves and other subterranean habitats

Over the last two decades there has been an exponential increase in the use of correlative species distribution models (SDMs) to address a variety of topics in ecology, biogeography, evolution, and conservation biology. Conversely, the use of these statistical methods to study the potential distribution of subterranean organisms has lagged behind, relative to their above‐ground (epigean) counterparts. The reason for this is possibly related to a number of peculiarities of subterranean systems, which pose important limits, but also opportunities, for these correlative models. The aim of this forum is to explore the caveats that need to be made when generalizing these statistical techniques to caves and other subterranean habitats. We focus on the typical bias in spatial datasets of cave‐dwelling species, and provide advice for selecting the model calibration area. In parallel, we discuss the potential use of different large scale surface variables to represent the subterranean condition. A more widespread adoption of these statistical techniques in subterranean biology is highly attractive and has great potential in broadening our knowledge on a variety of ecological topics, especially in the fields of climate change and biodiversity conservation. Their use would especially benefit the study of the biogeographic patterns of subterranean fauna and the impact of past and future climate change on subterranean ecosystems.     

Sampling adequacy in an extreme environment: species richness patterns in Slovenian caves

Caves harbor a rich fauna unique to subterranean environments. Although extensive records of cave animals are available, only a small fraction of known caves in any region have been biologically assessed. We investigated the impact of incomplete sampling using one of the richest, best documented cave faunas in the world – that of the Dinaric karst of Slovenia. We utilized time snapshots (1940, 1970, and 2000) of the caves and cave fauna to analyze stability of hotspots, spatial pattern, and relationship between number of species and number of caves. Using data aggregated into 100km² hexagons, the location of hotspots, black–white joins, Moran's I, and spatial autocorrelation all remained constant, at least from 1970 on. The linear regression coefficient of the relationship between number of caves and number of species declined with time. Most hexagons had been sampled, but there was no indication that any hexagon had been sampled intensively enough for the accumulation curve of number of caves versus number of species within a hexagon to reach an asymptote. This appeared to be the result of a highly skewed distribution of species richness among caves. Number and position of hotspots can be predicted from information on these few high diversity caves.     

Finding answers in the dark: caves as models in ecology fifty years after Poulson and White

The use of semi‐isolated habitats such as oceanic islands, lakes and mountain summits as model systems has played a crucial role in the development of evolutionary and ecological theory. Soon after the discovery of life in caves, different pioneering authors similarly recognized the great potential of these peculiar habitats as biological model systems. In their 1969 paper in Science, ‘The cave environment’, Poulson and White discussed how caves can be used as natural laboratories in which to study the underlying principles governing the dynamics of more complex environments. Together with other seminal syntheses published at the time, this work contributed to establishing the conceptual foundation for expanding the scope and relevance of cave‐based studies. Fifty years after, the aim of this review is to show why and how caves and other subterranean habitats can be used as eco‐evolutionary laboratories. Recent advances and directions in different areas are provided, encompassing community ecology, trophic‐webs and ecological networks, conservation biology, macroecology and climate change biology. Special emphasis is given to discuss how caves are only part of the extended network of fissures and cracks that permeate most substrates and, thus, their ecological role as habitat islands is critically discussed. Numerous studies have quantified the relative contribution of abiotic, biotic and historical factors in driving species distributions and community turnovers in space and time, from local to regional scales. Conversely, knowledge of macroecological patterns of subterranean organisms at a global scale remains largely elusive, due to major geographical and taxonomical biases. Also, knowledge regarding subterranean trophic webs and the effect of anthropogenic climate change on deep subterranean ecosystems is still limited. In these research fields, the extensive use of novel molecular and statistical tools may hold promise for quickly producing relevant information not accessible hitherto.     

Big family,warm home,and lots of friends: Pteronotus large colonies affect species richness and occupation inside caves

Roosts are essential for the survival of most animals. Due to homothermic requirements, mammals are particularly dependent on roost quality and availability. Bats select their roosts in a species-specific way, likely related to species´ different physiological and adaptive needs. Unlike species whose individuals roost solitarily, roost selection is critical for bats forming large colonies due to the requirements for maintaining thousands of individuals in a single shelter. This is the case of Pteronotus (Mormoopidae), whose colonies reach hundreds of thousands of bats. Using captures, bioacoustics, and automated censuses, we evaluated how cave size, ceiling characteristics, environmental stability, temperature, and humidity influence the formation of exceptionally large colonies, species richness and composition in caves in north-eastern Brazil. We expected that colonies would be positively related to cave size and stability, internal cave selection would be species-specific, but larger and more environmentally stable caves would have higher richness. Pteronotus colonies were positively related to cave size, stability, and ceiling characteristics, and their presence strongly influenced cave temperature variation. Species richness was positively correlated to a cave stability index. Species other than Pteronotus preferred different climatic and ceiling characteristics. We detected an indirect influence of the large colonies of Pteronotus on the species richness and occupation inside caves. On the other hand, such caves favor species coexistence, as they offer a range of microenvironments, reducing niche overlap in their interior. Pteronotus gymnonotus and Pteronotus personatus are both key- and umbrella-species for cave ecosystems, stressing the need for specific conservation strategies in Brazil. Abstract in Portuguese is available with online material.     

Parallels between two geographically and ecologically disparate cave invasions by the same species,Asellus aquaticus (Isopoda,Crustacea)

Caves are long‐known examples of evolutionary replications where similar morphologies (troglomorphies) evolve independently as the result of strong natural selection of the extreme environment. Recently, this paradigm has been challenged based on observations that troglomorphies are inconsistent across taxa and different subterranean habitats. We investigated the degree of replicated phenotypic change in two independent cave invasions by the freshwater isopod Asellus aquaticus; the first in a sulphidic aquifer in Romania, the second in a sinking river in the Dinaric Karst in Slovenia. Both ancestral surface populations still live alongside the subterranean ones. Phylogenetic analyses show independence of the two colonization events, and microsatellite analysis shows no evidence of ongoing genetic exchange between surface and subterranean ecomorphs. The overall morphology has changed dramatically at both sites (50 of 62 morphometric traits). The amount of phenotypic change did not reflect differences in genetic diversity between the two ancestral populations. Multivariate analyses revealed divergent evolution in caves, not parallel or convergent as predicted by the current paradigm. Still, 18 traits changed in a parallel fashion, including eye and pigment loss and antennal elongation. These changes might be a consequence of darkness as the only common ecological feature, because Romanian caves are chemoautotrophic and rich in food, whereas Slovenian caves are not. Overall, these results show that morphologically alike surface populations can diverge after invading different subterranean habitats, and that only about one‐third of all changing traits behave as troglomorphies in the traditional sense.     

Do cave features affect underground habitat exploitation by non-troglobite species?

Many biospeleological studies focus on organisms that are exclusive inhabitants of the subterranean realm, but organisms that are not obligate cave-dwellers are frequent in caves, and may account for a substantial portion of biomass. Moreover, several taxa that are usually epigeous are regularly found inside caves, but for most of them it is unknown whether they accidentally enter them, or whether they actively select caves for specific environmental features. In this study we analysed the community of non-strict cave-dwelling organisms (amphibians, gastropods, spiders and orthopterans) in 33 caves from Central Italy, to assess how environmental factors determine community structure. Cave features strongly affected the distribution of the taxa considered. The combined effect of cave morphology and microclimate explained nearly 50% of the variation of community structure. Most of community variation occurred along a gradient from deep, dark and humid caves, to dry caves with wider entrances and extended photic areas. Most of species were associated with humid, deep and dark caves. Most of the non-troglobiont amphibians and invertebrates did not occur randomly in caves, but were associated to caves with specific environmental features. Analysing relationships between cave-dwelling species and environmental variables can allow a more ecological and objective classification of cave-dwelling organisms.     

Evidence for speciation underground in diving beetles (Dytiscidae) from a subterranean archipelago

Most subterranean animals are assumed to have evolved from surface ancestors following colonization of a cave system; however, very few studies have raised the possibility of “subterranean speciation” in underground habitats (i.e., obligate cave‐dwelling organisms [troglobionts] descended from troglobiotic ancestors). Numerous endemic subterranean diving beetle species from spatially discrete calcrete aquifers in Western Australia (stygobionts) have evolved independently from surface ancestors; however, several cases of sympatric sister species raise the possibility of subterranean speciation. We tested this hypothesis using vision (phototransduction) genes that are evolving under neutral processes in subterranean species and purifying selection in surface species. Using sequence data from 32 subterranean and five surface species in the genus Paroster (Dytiscidae), we identified deleterious mutations in long wavelength opsin (lwop), arrestin 1 (arr1), and arrestin 2 (arr2) shared by a sympatric sister‐species triplet, arr1 shared by a sympatric sister‐species pair, and lwop and arr2 shared among closely related species in adjacent calcrete aquifers. In all cases, a common ancestor possessed the function‐altering mutations, implying they were already adapted to aphotic environments. Our study represents one of the first confirmed cases of subterranean speciation in cave insects. The assessment of genes undergoing pseudogenization provides a novel way of testing modes of speciation and the history of diversification in blind cave animals.     

Ecological preferences of neotropical cave bats in roost site selection and their implications for conservation

Bats frequently use caves as roosts due to higher environmental stability and protection. However, species-specific ecological and physiological requirements and conditions of roosts and their surroundings can influence species presence. Little is known on cave choice by bats in the Neotropics, a species- and cave-rich region. Understanding how bats, cave characteristics and the surrounding landscape are related with each other helps the management and conservation of bats and caves. Based on sampling 19 caves using both diurnal observations and captures, we tested (1) whether bat richness was positively related to cave temperature, humidity, size, stability, and heterogeneity of microhabitats, and the preservation and heterogeneity of the surrounding landscape in central Brazil; (2) whether cave and landscape characteristics influenced on species composition; (3) how species responded to cave and landscape variables; and (4) whether these relationships changed between seasons. Temperature was a limiting factor, whereas environmental stability, humidity, and structural attributes of caves favored the occurrence of more species. Larger caves, rich in microhabitats – but more stable than the external environment – supported more species, especially in the dry season. Landscape context did not influence species richness and composition in the caves, but the percentage of vegetation around caves was important for certain species. Our results highlight the influence of environmental variables in the process of cave selection by Neotropical bat species. Moreover, we emphasize the importance of cave protection for bats and provide useful information for decision-making in processes of environmental licensing.