Article
To read the full-text of this research, you can request a copy directly from the authors.

Abstract

In light of recent alarming trends in human population growth, climate change, and other environmental modifications, a "Warning to humanity" manifesto was published in BioScience in 2017. This call reiterated most of the ideas originally expressed by the Union of Concerned Scientists in 1992, including the fear that we are "pushing Earth's ecosystems beyond their capacities to support the web of life. " As subterranean biologists, we take this opportunity to emphasize the global importance and the conservation challenges associated with subterranean ecosystems. They likely represent the most widespread nonmarine environments on Earth, but specialized subterranean organisms remain among the least documented and studied. Largely overlooked in conservation policies, subterranean habitats play a critical role in the function of the web of life and provide important ecosystem services. We highlight the main threats to subterranean ecosystems and propose a set of effective actions to protect this globally important natural heritage.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the authors.

... Intervention in the morphology and hydrology of surface waters via bank stabilization and the construction of dams disconnect the vital surface water-groundwater interface (Piégay et al. 2009). Threats from industry include, besides the improper storage of waste and direct release of contaminants, underground and surface mining activities (Mammola et al. 2019;Li et al. 2021). Increasing demands for drinking water supply may additionally drive overexploitation of groundwater resources. ...
... (1) Groundwater ecosystems do have a natural capacity to purify incoming water from organic matter and nutrients, including organic and inorganic contaminants. This ecosystem service is based on a sensitive balance between the low microbial biomass and activity in aquifers, the flux of matter to the aquifer, the comparatively long residence time of compounds introduced, as well as the large dimensions of aquifers (Griebler et al. 2019). Groundwater ecosystems can buffer inputs of dissolved organic carbon and nutrients to a certain degree by increasing microbial biomass and activity (Fillinger et al. 2023). ...
... Abstraction of groundwater from many aquifers worldwide by far exceeds the natural renewal rate (Gleeson et al. 2012). Regional declines of groundwater levels by several meters over the past years to decades are very common in many regions of the world (Mammola et al. 2019). At many sites, groundwater drawdown exceeds dozens of meters (Konikow & Kendy 2005). ...
Article
Full-text available
The terrestrial subsurface harbours the largest available freshwater reserves on our planet: In particular, shallow aquifers are home to a vast but insufficiently explored biodiversity. Whilst biodiversity research gained a strong momentum in the past decades, threats to groundwater ecosystems increased as well and we may lose species before their discovery and formal description. Negative impacts to groundwater fauna mainly encompass groundwater pollution, warming, and habitat loss. Given their peculiar adaptation to the usually dark and energy poor environment including a slow metabolism and low reproduction rates, as well as further special characteristics of groundwater fauna like their fragmented distribution, and high number of endemic species, groundwater invertebrates seem to be specifically at risk. We firmly propose to establish ecological measures in routine groundwater monitoring and to take action in the development of biodiversity conservation strategies and groundwater ecosystem protection.
... Normally, these environments are associated with a rock formation known as karst/pseudokarst, which enables the occurrence of chemical, physical and biological processes of dissolution of the rocks that originate them (Auler & Pilo, 2011;Travassos, 2019;Parker et al., 2022) (Poulson & White, 1969;Mammola, 2019), templos religiosos (Price & Travassos, 2016); fonte de registros e vestígios arqueológicos (Damm & Young, 2013;Barra, 2020), paleontológicos (Burney et al., 2022), antropológicos (Détroit et al., 2019), paleoambientais (Novello et al., 2017;Cruz & Piló, 2019), fonte de serviços ecossistêmicos (Mammola et al., 2019a), e também utilizadas como fonte de informações sobre a saúde humana (Riddle et al., 2018;Yoshizawa et al., 2018), bem como locais para a prática de turismo, esportes e recreação. ...
... Estima-se que há um grande número de cavernas ainda desconhecidas (Auler & Pilo, 2011;Jansen et al., 2012;CECAV, 2022a), sendo parte dessa problemática, recentemente intitulada de lacuna Racovittzana, em homenagem ao naturalista Emil Racoviță (Ficetola et al., 2019). Ela se refere especificamente ao conhecimento desigual sobre a distribuição espacial de cavernas que, consequentemente, afeta também a conservação delas (Ficetola et al., 2019;Mammola et al., 2019a). Nesse contexto, a urbanização, a fragmentação da paisagem, a poluição e a extração de minerais têm se destacado como fatores intensificadores de tensões nas áreas com ocorrência de cavernas, o que podem gerar impactos irreversíveis sobre essas paisagens, os ecossistemas associados e os serviços ecossistêmicos locais (Ferreira et al., 2018;Mammola et al., 2019a;Ferreira et al., 2022;Mammola et al., 2022) principalmente em regiões de carste/ pseudocarste, onde ambientes cavernícolas são ainda desconhecidos. ...
... Ela se refere especificamente ao conhecimento desigual sobre a distribuição espacial de cavernas que, consequentemente, afeta também a conservação delas (Ficetola et al., 2019;Mammola et al., 2019a). Nesse contexto, a urbanização, a fragmentação da paisagem, a poluição e a extração de minerais têm se destacado como fatores intensificadores de tensões nas áreas com ocorrência de cavernas, o que podem gerar impactos irreversíveis sobre essas paisagens, os ecossistemas associados e os serviços ecossistêmicos locais (Ferreira et al., 2018;Mammola et al., 2019a;Ferreira et al., 2022;Mammola et al., 2022) principalmente em regiões de carste/ pseudocarste, onde ambientes cavernícolas são ainda desconhecidos. ...
Article
Full-text available
Many caves have yet to be discovered and/or mapped in Brazil. Various socio-economic and accessibility factors may be responsible for biasing the knowledge of Brazilian caves geographical distribution. In this study, using Bayesian modeling techniques, it was predicted that knowledge about the Brazilian caves geographic distribution is strongly biased towards locations close to urban centers and mining activities. More caves are known near mining environments and/or more accessible locations than far from them for instance. The models were built by associating the known occurrence data of digitally accessible caves in the Speleological Information National Register (Cadastro Nacional de Informações Espeleológicas (CANIE) with different accessibility and infrastructure variables. The findings suggest that the regions with the highest occurrence of known caves are mainly concentrated within the states of Minas Gerais, São Paulo, Goiás, Pará and Piauí. Meanwhile some Brazilian states, such as Amazonas, Roraima, Mato Grosso, Mato Grosso do Sul, Paraná and Maranhão are still under-explored. They have large gaps and high potential for the discovery of new caves. In conclusion, the economic exploitation has generated biased knowledge about the distribution of caves. This may be linked to the historical clashes between exploitation and conservation legislation, making it essential that new policies on the conservation of Brazil's speleological heritage consider the entire speleological landscape, its biases (better studied sites), Racovitzan shortfalls (less studied or possibly neglected sites), and the socio-economic processes that imply these.
... In fact, a long-term thermal variation study over 13 years in an ice cave has found a warming trend on cave temperatures 16 . Caves harbour unique organisms with specific adaptations to the peculiar conditions of subterranean habitats, including many short-range endemics, representing independent colonisations of surface ancestors, many ancient lineages and countless species yet to be discovered 5,17 . These ecosystems provide multiple benefits to humans 17,18 . ...
... Caves harbour unique organisms with specific adaptations to the peculiar conditions of subterranean habitats, including many short-range endemics, representing independent colonisations of surface ancestors, many ancient lineages and countless species yet to be discovered 5,17 . These ecosystems provide multiple benefits to humans 17,18 . They include the largest spaces for groundwater storage, but also water purification, in which subterranean biota plays the crucial role in the degradation of organic matter and pollutants 5,18,19 . ...
... They include the largest spaces for groundwater storage, but also water purification, in which subterranean biota plays the crucial role in the degradation of organic matter and pollutants 5,18,19 . In addition, caves are fundamental shelters for a variegated set of species, some of which are already known as being at risk of extinction, including bats 17 . Further, caves can provide opportunities for outdoor recreation, provide a unique environment for ecological end evolutionary scientific research, and have cultural and spiritual significance for indigenous communities and other groups 5,17 . ...
Article
Full-text available
Climate change affects all ecosystems, but subterranean ecosystems are repeatedly neglected from political and public agendas. Cave habitats are home to unknown and endangered species, with low trait variability and intrinsic vulnerability to recover from human-induced disturbances. We studied the annual variability and cyclicity of temperatures in caves vis-à-vis surface in different climatic areas. We hypothesize that cave temperatures follow the average temperature pattern at the surface for each location with a slight delay in the signal, but we found three different thermal patterns occurring in caves: (1) high positive correlation and a similar thermal pattern to the surface, (2) low correlation and a slight thermal delay of the signal from the surface, and (3) high negative correlation with an extreme delay from the surface. We found daily thermal cycles in some caves, which may potentially control the circadian rhythms of cave organisms. Our results show that caves had lower thermal amplitude than the surface, and that thermal averages within caves approximately correspond to the to the annual average of surface temperature. Caves buffer external temperature and act as refugia for biota in extreme climatic events. Likewise, temperature increases at surface will lead to increment in caves, threatening subterranean biota and ecosystem services.
... Highly adapted, exclusively subterranean terrestrial species are called troglobionts; stygobionts are aquatic species that are obligate and permanent residents of subterranean habitats (Culver and Pipan 2019;Gunn 2004). Due to the physical isolation in cave systems, such species often show a limited distribution (Howarth and Moldovan 2018a), and many subterranean species are endemic vulnerable (Mammola et al. 2019). Different microhabitats in caves promote a diverse composition of species (Bonacci et al. 2009;Howarth and Moldovan 2018b). ...
... The Encyclopedia Biospeleologica represents an extensive collection on cave species worldwide, including the Mediterranean, and illustrates the high biodiversity of underground habitats (Juberthie and Decu 1994). However, only a small percentage of caves and other subterranean habitats are protected with proper legislation (Culver and Pipan 2019;Mammola et al. 2019;Niemiller et al. 2018). ...
... Also, changes in water temperature and chemical composition can impact population dynamics and species assemblages (Chapin et al. 2011;Kløve et al. 2011a). Declining groundwater levels can impair ecosystem functions and lead to a loss of habitats and species Mammola et al. 2019). When the KGDE is disconnected from the aquifer, its groundwaterdependent vegetation is replaced by terrestrial vegetation. ...
Article
Full-text available
Karst groundwater-dependent ecosystems (KGDEs) in the Mediterranean region are important in terms of ecosystem services and biodiversity but are increasingly under anthropogenic pressures and climate-change constraints. For this study, the ecohydrological characteristics, threats, and protection status of 112 selected KGDEs around the Mediterranean Sea, including caves, springs, rivers and wetlands, were evaluated, based on local expert knowledge and scientific literature. Results demonstrate that KGDEs contribute considerably to regional biodiversity. The diversity of karst landscapes, combined with the groundwater emergence at springs, leads to exceptional habitat diversity, particularly in arid climates, where KGDEs serve as a refuge for species that could not thrive in the surrounding environment. The most common threats identified among the selected sites are direct human disturbances, such as mass tourism or overfishing, water-quality deterioration and water shortage from aquifer overdraft and/or climate change. Although most of the selected sites are under protection, conservation measures are frequently insufficient. Such shortcomings are often caused by poor data availability, little knowledge on conservation needs of invertebrate species, and conflicts of interest with the local population. For this purpose, it is necessary to raise environmental awareness and promote interdisciplinary research, in order to monitor water quality and quantity in addition to the status of the biocenoses.
... While groundwater has predominantly been studied and managed for its function as a freshwater resource, our understanding of groundwater as an ecosystem and its biotic communities remains limited (Mammola et al., 2019). To date, groundwater remains among the least documented ecosystems worldwide, mainly because of missing direct habitat accessibility and additional impediments (Ficetola et al., 2019;Mammola et al., 2021;Zagmajster et al., 2010). ...
... Given the tight linkage between shallow groundwater, soil, and surface ecosystems (Schneider et al., 2023), understanding cross-ecosystem effects on groundwater communities is crucial. This need is even more pressing given the increasing anthropogenic pressures on groundwater ecosystems, such as water and geothermal energy extraction, contamination, climate change, and habitat degradation (Mammola et al., 2019). We here identified signals of land use on groundwater organisms that exceed the spatial scale of present-day drinking water protection zones. ...
Article
Full-text available
Terrestrial and aquatic ecosystems are tightly linked, with direct implications for applied resource management and conservation. It is well known that human land use change and intensification of terrestrial systems can have large impacts on surface freshwater ecosystems. Contrastingly, the study and understanding of such land use impacts on groundwater communities is lagging behind. Both the impact strength of land use on groundwater communities and the spatial extents at which such interlinkages are operating are largely unknown, despite our reliance on groundwater for drinking water extraction as a key ecosystem service. Here, we analyzed groundwater amphipod occurrence from several hundred shallow groundwater aquifers used for drinking water extraction across a region of varying agricultural intensity and human population density in Switzerland. Despite drinking water extraction sites being generally built at locations with expected minimal aboveground impacts on water quality, we found a direct correlation between land use type and intensity within the surrounding catchment area and the locally measured nitrate concentrations, which is a direct proxy for drinking water quality. Furthermore, groundwater amphipods were more likely to be found at sites with higher forest coverage than at sites with higher crop and intensive pasture coverages, clearly indicating a tight connection between aboveground land use and groundwater biodiversity. Our results indicate that land use type effects on groundwater communities are most relevant and pronounced to spatial scales of about 400–1000 m around the groundwater sampling site. Importantly, the here identified spatial scale is 1.2‐ to 3‐fold exceeding the average extent of currently defined groundwater protection zones. We postulate that incorporating an ecosystem perspective into groundwater management strategies is needed for effective protection of groundwater quality and biodiversity.
... The analysis of the environmental data set indicated significant differences in environmental conditions among sampling sites (see Figure 2). The main synthetic environmental gradient (PCO1: variance explained: 61%) separated sites (08, [18][19][20] with relatively high values of parameters such as Sr, SO 4 We also observed concentration peaks for certain parameters during February: the highest value for Ni was recorded at 01F (5.9 mg L −1 ), and a peak of Al was detected at 07F (59 mg L −1 ); Ba had a maximum of 56.8 mg L −1 at sample 19F. The highest value for F (1.27 mg L −1 ) was recorded for sample 20M; sample 18F also had a high peak of Sr (9.70 mg L −1 ), followed by 19F (2.30 mg L −1 ); a peak concentration of PO 4 (0.93 mg L −1 ) was also recorded at 18F; at 20F, the highest concentration of Mn (7.1 mg L −1 ) was recorded. ...
... OTUs with low RDA1 values and thus found in sites with high relative values of ORP, OD1 and OD2 included OTUs 2,4,9,10,15,18,19,55 and 3070. These organisms assigned to taxa including the genera Limnohabitans and Acidovorax and the orders Sphingomonadales and Cytophagales were closely related (sequence similarity > 99%) to organisms obtained from river water, pumice, groundwater and lake water ( Table 3). ...
... Groundwater ecosystems harbour essential water resources for many people and other dependent ecosystems around the globe [1], yet the rare and mostly endemic species which are restricted to these environments are poorly understood, and consistently overlooked in management strategies [2][3][4]. Impacts of rapid climate change and anthropogenic activities that induce modifications in the physicochemical parameters of the environment (i.e. temperature, salinity and oxygen) are expected to affect groundwater communities [5][6][7][8][9], however, the impacts of these changes on groundwater species vary among species and the particular environmental change itself, which makes accurate projections for the future very difficult [4,6,[10][11][12][13]. ...
... Impacts of rapid climate change and anthropogenic activities that induce modifications in the physicochemical parameters of the environment (i.e. temperature, salinity and oxygen) are expected to affect groundwater communities [5][6][7][8][9], however, the impacts of these changes on groundwater species vary among species and the particular environmental change itself, which makes accurate projections for the future very difficult [4,6,[10][11][12][13]. Anchialine ecosystems (Box 1) in the Yucatan Peninsula (YP) are considered seasonally stable, with environmental changes occurring at broader timescales (such as glacial and interglacial epochs). ...
Article
Full-text available
Anchialine systems are coastal groundwater habitats around the world which host a unique community of cave adapted species (stygobionts). Such communities are expected to be separated by haloclines into either fresh or saline groundwater communities, hence climate changes (e.g., eustatic sea level shifts) and anthropic driven changes (e.g., salinization) may have a great impact on these stygobiont communities. Here we used cave-restricted species of Typhlatya from the Yucatan Peninsula as models to identify physiological capacities that enable the different species to thrive in marine groundwater (T. dzilamensis) or fresh groundwater (T. mitchelli and T. pearsei), and test if their distribution is limited by their salinity tolerance capacity. We used behavior, metabolic rates, indicators of the antioxidant system and cellular damage, and lactate content to evaluate the response of individuals to acute changes in salinity, as a recreation of crossing a halocline in the anchialine systems of the Yucatan Peninsula. Our results show that despite being sister species, some are restricted to the freshwater portion of the groundwater, while others appear to be euryhaline.
... The analysis of the environmental data set indicated significant differences in environmental conditions among sampling sites (see Figure 2). The main synthetic environmental gradient (PCO1: variance explained: 61%) separated sites (08, [18][19][20] with relatively high values of parameters such as Sr, SO 4 We also observed concentration peaks for certain parameters during February: the highest value for Ni was recorded at 01F (5.9 mg L −1 ), and a peak of Al was detected at 07F (59 mg L −1 ); Ba had a maximum of 56.8 mg L −1 at sample 19F. The highest value for F (1.27 mg L −1 ) was recorded for sample 20M; sample 18F also had a high peak of Sr (9.70 mg L −1 ), followed by 19F (2.30 mg L −1 ); a peak concentration of PO 4 (0.93 mg L −1 ) was also recorded at 18F; at 20F, the highest concentration of Mn (7.1 mg L −1 ) was recorded. ...
... OTUs with low RDA1 values and thus found in sites with high relative values of ORP, OD1 and OD2 included OTUs 2,4,9,10,15,18,19,55 and 3070. These organisms assigned to taxa including the genera Limnohabitans and Acidovorax and the orders Sphingomonadales and Cytophagales were closely related (sequence similarity > 99%) to organisms obtained from river water, pumice, groundwater and lake water ( Table 3). ...
... The analysis of the environmental data set indicated significant differences in environmental conditions among sampling sites (see Figure 2). The main synthetic environmental gradient (PCO1: variance explained: 61%) separated sites (08, [18][19][20] with relatively high values of parameters such as Sr, SO 4 We also observed concentration peaks for certain parameters during February: the highest value for Ni was recorded at 01F (5.9 mg L −1 ), and a peak of Al was detected at 07F (59 mg L −1 ); Ba had a maximum of 56.8 mg L −1 at sample 19F. The highest value for F (1.27 mg L −1 ) was recorded for sample 20M; sample 18F also had a high peak of Sr (9.70 mg L −1 ), followed by 19F (2.30 mg L −1 ); a peak concentration of PO 4 (0.93 mg L −1 ) was also recorded at 18F; at 20F, the highest concentration of Mn (7.1 mg L −1 ) was recorded. ...
... OTUs with low RDA1 values and thus found in sites with high relative values of ORP, OD1 and OD2 included OTUs 2,4,9,10,15,18,19,55 and 3070. These organisms assigned to taxa including the genera Limnohabitans and Acidovorax and the orders Sphingomonadales and Cytophagales were closely related (sequence similarity > 99%) to organisms obtained from river water, pumice, groundwater and lake water ( Table 3). ...
Article
Full-text available
Climate change may increase the vulnerability of aquifers to contamination through extreme precipitation and extended drought periods. Therefore, the understanding of groundwater ecosystem dynamics is crucial, with bacterial assemblages playing a major role in biogeochemical cycles. The present research describes a geospatial study targeting the bacterial community structure of groundwaters from the largest karst aquifer in Portugal (the Maciço Calcário Estremenho), integrating hydrogeochemical and bacterial diversity data. A total of 22 samples were analyzed from a set of 11 geographically sparsely distributed groundwater sources in dry vs. wet seasons. The 16S rRNA gene barcoding data revealed bacterial community variability across samples in space and time. The phylum Proteobacteria was dominant across all samples (from 44 to 92% of total sequence reads), mainly represented by the classes Alphaproteobacteria (). Variation in the bacterial community was primarily attributed to parameters such as redox conditions (DO, ORP), Fe, Mn, SO4, PO4, Sr and Cl, but also some minor and trace elements (Al, V, Cr, Cu, Pb). Our results provide novel insights into bacterial diversity in relation to groundwater hydrogeochemistry. The strong dominance of OTUs related to bacterial taxa associated with nitrifi-cation/denitrification also highlights a potentially important role of these assemblages on nutrients (nitrogen sources) and groundwater quality dynamics at this karstic aquifer system. Moreover, the integration of bacterial assemblages information is emphasized as central for water quality monitoring programs.
... Cave-adapted communities have high conservationist interest (Mammola et al. 2019), they are habitat specialists with high endemicity patterns, reduced population numbers and low fertility traits (Deharveng et al. 2024). Cave fauna face direct anthropogenic threats, such as groundwater contamination, habitat destruction due to quarrying activities and excessive cave visitation (Castaño-Sánchez et al. 2020). ...
... These species have reduced populations, inhabit habitats with specific environmental conditions and are very sensitive to anthropogenic pressure, such as climate change and pollution, being fundamental for global biodiversity conservation (Castaño-Sánchez et al. 2020). Therefore, they constitute a unique biodiversity heritage that is on the of extinction ( Mammola et al. 2019). The risk of extinction can be avoided by implementing protection figures for species and habitats specific for troglobionts (Wynne et al. 2021). ...
Article
Full-text available
Background Domitius lusitanicus (Fage, 1931) is a troglobiont spider, endemic from caves in the largest karst massif in Portugal, the Estremenho. It was the first described cave-adapted species from Portugal, but the male of the species was only described in 1988. New information Over the last two decades, the knowledge on the distribution of D. lusitanicus increased significantly. We assess the conservation status of D. lusitanicus, providing new information on its extent of occurrence and the anthropogenic threats and present a IUCN Red List profile. D. lusitanicus faces various anthropogenic threats, such as habitat loss, agriculture, pollution and tourism impacts. Despite a large part of its distribution is included in a Natural Park, it expands outside of the areas deemed for protection in the Natura 2000 network. This species has the widest spread distribution of all troglobionts in the Estremenho Massif; therefore, it may be used as an umbrella species for the protection of other cave-adapted species of invertebrates of the massif.
... Subterranean species produce fewer eggs; yet, they are typically larger than their closely related surface-dwelling counterparts [26]. These aspects have been subject to limited investigation in subterranean environments [5,27], partly due to the recent introduction of trait-based approaches in groundwater ecology and the inherent challenges posed by some taxa [16]. For example, copepods, a diverse group of small crustaceans found in various aquatic habitats and dominant in groundwater [28,29], exhibit closely resembling body shapes along a surface-subterranean gradient, indicating that groundwater habitats might not always filtrate body morphology alone [5]. ...
... On the other hand, the number of nonstygobiotic copepod individuals in an alluvial aquifer can be substantial [57,58], and these individuals may encounter suitable conditions for reproduction in aquifers contaminated by sewage wastes [59]. In addition, in a recent meta-analysis conducted by Vaccarelli et al. (2023) [60], an alarming concern came to light related to the possibility of surface-dwelling species infiltrating subterranean ecosystems as a consequence of climate change [27]. This migration could further disrupt the existing trophic dynamics, with surface copepod species, known for their higher metabolic activity [61] and fertility [28,29], expected to swiftly replace their subterranean counterparts in the organic-enriched groundwater habitat [59], thereby encroaching on their living spaces and depleting their energy resources [37]. ...
Article
Full-text available
Understanding trait selection factors is vital for decoding the processes shaping species’ assemblages. However, trait-based studies in freshwater crustacean copepod assemblages are scarce, especially in groundwater environments. We explored how environmental filtering influences functional traits in copepod assemblages across four freshwater habitats (an alluvial aquifer, a hyporheic zone, a stream benthic zone and a lake littoral) along a depth gradient. Each habitat had distinct environmental templates based on light, temperature and dissolved oxygen. We analysed 4898 individuals from 43 copepod species and examined 12 morphological and life history traits. The results revealed significant differences in copepod traits among habitats, notably in ovigerous female biomass, egg biomass and ovigerous female percentages. Furthermore, despite some statistical uncertainty, notable differences were also observed in the number of juveniles, male-to-female abundance ratios and overall biomass. No significant differences were observed in juvenile biomass, egg characteristics, body size dimorphism or juvenile-to-adult ratios among habitats. The trait variations offer insights into copepod-mediated ecosystem services, particularly carbon recycling. To gain a deeper understanding of copepod adaptations to environmental features and anthropogenic changes, future research should consider additional functional traits, such as locomotion and feeding habits.
... Caves host unique organisms with specific adaptations and specialized to survive in these extreme environments [15], some of which are endemism listed as Vulnerable in the IUCN Red List of Threatened Species (https://www.iucnredlist.org/, accessed on 15 September 2024), such as the olm Proteus anguinus (Laurenti 1768), the first obligate subterranean vertebrate described [16]. Show caves are important tourist attractions around the world, with a global commercial value of approximately EUR 2 billion per year [17]. ...
Article
Full-text available
In this study, a systematic review of the scientific literature was carried out to summarize the emerging evidence on microplastic pollution in natural caves. After the screening of 655 papers on the topic from a combined search on the Web of Knowledge and the Scopus databases, we found only 14 studies reporting quantitative data on microplastics from a total of 27 natural caves. Most of the assessments focused on water and sediment, with very limited investigations concerning the cave biota. Overall, the most common types of particles found in caves were small (<1 mm) fibers (~70–90% of items), transparent or light-colored, mostly made of polyethylene and polyethylene terephthalate. Anthropogenic cellulosic materials, however, represented a non-negligible portion of particles (i.e.,~20–30%). Microplastic concentrations in caves varied between 0.017 and 911 items/L for water and 7.9 and 4777 items/kg for sediment, thus falling within the levels of microplastic pollution found in other terrestrial, freshwater, and marine environments. Levels of microplastic pollution appear largely variable among caves, stressing the need to extend the geographic and environmental ranges of the assessments, which are currently concentrated on Italian caves on land, with very few case studies from other regions of the world and from marine caves. Despite their putative isolation, natural caves have a high vulnerability to microplastic contamination, requiring much more research effort to understand the potential risk that plastics pose to these fragile ecosystems.
... Subterranean environments are the largest non-marine habitat on Earth and include caves, aquifers, lava tubes, talus slopes, and fissures in bedrock. Contrary to popular belief, such habitats-which are frequently overlooked in conservation agendas-are not devoid of life and often act as biodiversity hotspots safeguarding relictual faunas (Mammola et al., 2019;Vaccarelli et al., 2023). Invertebrates represent the bulk of biodiversity in the subterranean realm (Humphreys, 2008;Souza-Silva et al., 2021;Trajano, 2000;Zigler et al., 2020), but in Australia an estimated 80% of species associated with caves are yet to be discovered (Guzik et al., 2010). ...
... Cave temperatures resemble the external annual average, while air humidity exceeds surface levels, potentially reaching saturation (H€ uppop, 2000). These patterns underscore the singularity and dynamics of these subterranean environments, serving as biological filters that select species with varying degrees of adaptation and persistence in such conditions (Culver & Pipan, 2009;Mammola et al., 2019;Poulson & White, 1969). ...
Article
Full-text available
The lack of understanding regarding how endogenous and behavioral factors affect the biological rhythms of amblypygid arachnids in cave environments underscores a gap in chronobiologic knowledge for this group. This study investigates the influence of specialization on subterranean habitats and the presence of biological rhythms on the locomotor activity patterns of the troglobitic and troglophilic species of the genus Charinus. Specimens collected from carbonate caves in Brazil were subjected to experimental treatments of constant light (LL), constant darkness (DD), and light–dark cycles (LD). The results revealed variations in the distribution of main periods among species, without a uniform pattern. Although some specimens showed greater variability in activity patterns in the DD and LL treatments, no significant differences were observed between troglobites and troglophiles. The lack of a clear distinction in rhythms between the two groups suggests the dynamic nature of circadian rhythms in these populations, where individual variations in activity patterns indicate this behavioral diversity. Additionally, intraspecific competition for food resources, probably intensified by the oligotrophic conditions of the cave environments, may play an important role in shaping these patterns and differences in activity phases. The presence of infradian rhythms and weak circadian rhythms in some individuals underscores the importance of considering non‐photic zeitgebers for a deeper understanding of these rhythms in cave organisms.
... One ecosystem with limited baseline knowledge on temporal dynamics is groundwater. Despite being the largest freshwater reservoir on earth and a keystone ecosystem (Ferguson et al. 2021;Saccò et al. 2024), it is one of the least studied ecosystems, mainly due to difficulties in accessibility (Mammola et al. 2019;). Yet, it harbors a unique range of organisms that are adapted to the dark and energy deprived conditions (Culver and Pipan 2019). ...
Article
Full-text available
Implementing and optimizing biodiversity monitoring is crucial given the current, worldwide biodiversity decline. Compared to other ecosystems, monitoring of biodiversity is lagging behind in groundwater ecosystems, both because of sparse taxonomic knowledge and methodological constraints. We here assessed temporal variation in the occurrence and abundance of macroinvertebrates collected systematically from shallow groundwater aquifers of Switzerland to establish general principles on seasonality and repeatability of assessment outcomes. We found no seasonal abundance pattern for obligate groundwater amphipods and isopods, indicating temporal consistency. In contrast, other macroinvertebrates (predominantly stygophiles and stygoxenes) showed pronounced seasonality in their detection rate. However, we found variability in detection rates across groundwater amphipod species and especially across sampling sites. For groundwater communities, characterized by narrowly-distributed and rare species, our results highlight the need for tailored and extensive sampling strategies. When setting up monitoring programs on groundwater fauna, detection probability, temporal autocorrelation, and standardization of sampling effort should be carefully considered. Applying novel, systematic approaches, can offer promising methodologies for understanding and conserving groundwater ecosystems.
... According to a recent review assessing global declines of arthropod diversity and abundance due to habitat loss and other factors, twice as many species show long-term population declines as those exhibiting population increases (Sánchez-Bayo and Wyckhuys 2020). Subterranean arthropods, and other low-mobility invertebrates, are at elevated risk of extinction due to high rates of endemism and physiological constraints on dispersal (Mammola et al. 2019). Arthropods constitute the most species-rich animal group on Earth, with an estimated 7 million species, of which 5.5 million belong to the class Insecta (Santos et al. 2020). ...
Article
Full-text available
Subterranean arthropods are important components of soils and contribute essential food-web functions and other ecosystem services, however, their diversity and community composition has scarcely been assessed. Subterranean pitfall traps are a commonly used method for sampling soil habitats in Europe but have never been widely implemented in the Americas. We used subterranean pitfall traps to sample previously unsurveyed arthropod communities in southwestern Virginia, U.S. Traps were placed in shallow subterranean habitats (SSHs), underground habitats close to the surface where light does not penetrate, and more specifically at the interface between the soil and underlying “milieu souterrain superficiel”—a microhabitat consisting of the air-filled interstitial spaces between rocks (abbreviated MSS). In total, 2,260 arthropod specimens were collected constituting 345 morphospecies from 8 classes, 33 orders, and 94 families. A region of the mitochondrial cytochrome c oxidase subunit I (COI) gene was amplified and sequenced, and objective sequence clustering of 3% was used to establish molecular operational taxonomic units (mOTUs) to infer observed species richness. In all, 272 COI barcodes representing 256 mOTUs were documented for rare soil-dwelling arthropod taxa and are published to build a molecular library for future research in this system. This work is the first taxonomically extensive survey of North American soil-dwelling arthropods greater than 10 cm below the soil surface.
... Como queda patente en el presente trabajo, el estudio sistematizado e intensivo del medio subterráneo en general, y del MSS en particular, puede proporcionar avances significativos en la reducción de estos déficits del conocimiento. Sin embargo, el medio subterráneo, debido a su condición de medio inhóspito, oculto y desconocido, se enfrenta a no pocas amenazas y es urgente adoptar medidas para su protección (Mammola et al. 2019). ...
Article
Full-text available
Típicamente, cuando se habla del ecosistema subterráneo, la mayoría de la gente piensa en cuevas y en animales con llamativas adaptaciones morfológicas. Sin embargo, existen otros hábitats subterráneos a parte de las cuevas. El medio subterráneo superficial (MSS) es uno de esos hábitats, con las características ambientales típicas de un medio subterráneo (afótico, elevada humedad) pero muy cercano a la superficie y formado por pequeñas fisuras y no por grandes espacios. En esta contribución repasamos los estudios más intensivos y sistemáticos del MSS que se han llevado hasta a cabo en la península ibérica, y repasamos los principales descubrimientos referidos a la fauna de este singular hábitat.
... All species considered extensively pre-date the LGM and are relicts of a major pre-ice age radiation . While having persisted through subsequent ice-ages and glaciation cycles (McInerney et al. 2014), contemporary climate change may pose a new, unprecedented challenge with respect to warming and depletion of groundwater systems (Mammola et al. 2019a). ...
Article
Full-text available
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.
... Within Zygentoma, members of Nicoletiidae typically live in habitats lacking light, with distinctive characteristics for a subterranean existence, such as lack of pigment and eyes. While intrinsically interesting because of their specialized ecology, our understanding of their biodiversity has been greatly constrained, like many troglobionts (Niemiller et al. 2018;Mammola et al. 2019;Niemiller and Taylor 2019), by the difficulties inherent in collecting samples from subterranean environments. For example, the subfamily Cubacubaninae is a seldom encountered group of silverfish that were considered a minor group of little importance primarily restricted to the Neotropics, where they are found under rocks and logs (Espinasa et al. 2007). ...
Article
Full-text available
A new genus and species of troglobiotic nicoletiid (Insecta, Zygentoma, Nicoletiidae) is described from northern Alabama, USA. The type species was collected from three caves in the Highland Rim section of the Interior Low Plateau physiographic province on the northern side of the Tennessee River Valley. Morphological and genetic analysis using the mitochondrial 16S rRNA locus show that Spinanycta alabamensissp. nov. is quite distinct from related nicoletiids in North America. The species differs from members of other genera by its urosternum I, which in males is modified with a central pointy extension. The new species significantly extends the distribution of cave-dwelling members of the family into the southeastern United States and suggests that additional nicoletiid diversity remains to be discovered from karst regions of the eastern United States.
... Subterranean natural cavities in karst landscapes are intimately connected to soil and surface systems, offer shelter and feeding resources to several faunal groups (Ferreira and Martins 1999;Boyles et al. 2011;Sakoui et al. 2020), and play a critical role in the regulation and provision of ecosystem services, such as organic matter decomposition or contaminant filtering (Christensen et al. 2001;Lovley 2001;Röling and van Verseveld 2002). They may occur in a variety of carbonate rocks and non-carbonate rocks. ...
Article
Full-text available
A list of ant species collected in caves at different localities of Minas Gerais state, Brazil is presented, based on specimens deposited in the Entomological Collection Padre Jesus Santiago Moure (DZUP). Of the 51 species/morphospecies found, two are new records for the state. We encourage an increase in ant collection efforts in Brazilian caves using different sampling techniques and comparative approaches in order to improve the current knowledge of ant diversity in these environments.
... Climate change affects all ecosystems on Earth-terrestrial (Chen et al. 2011;Mammola et al. 2019a), freshwater (Woodward et al. 2010), and marine alike (Brito-Morales et al. 2020;Levin and Le Bris 2015)-being recognized as one of the five direct drivers responsible for global biodiversity loss (IPBES 2019). As the largest ecosystems on Earth, oceans are now experiencing dramatic changes due to multiple drivers, such as warming, acidification, and deoxygenation (Doney et al. 2012;Poloczanska et al. 2013). ...
Article
Full-text available
Correlative species distribution models (SDMs) are important tools to estimate species’ geographic distribution across space and time, but their reliability heavily relies on the availability and quality of occurrence data. Estimations can be biased when occurrences do not fully represent the environmental requirement of a species. We tested to what extent species’ physiological knowledge might influence SDM estimations. Focusing on the Japanese sea cucumber Apostichopus japonicus within the coastal ocean of East Asia, we compiled a comprehensive dataset of occurrence records. We then explored the importance of incorporating physiological knowledge into SDMs by calibrating two types of correlative SDMs: a naïve model that solely depends on environmental correlates, and a physiologically informed model that further incorporates physiological information as priors. We further tested the models’ sensitivity to calibration area choices by fitting them with different buffered areas around known presences. Compared with naïve models, the physiologically informed models successfully captured the negative influence of high temperature on A. japonicus and were less sensitive to the choice of calibration area. The naïve models resulted in more optimistic prediction of the changes of potential distributions under climate change (i.e., larger range expansion and less contraction) than the physiologically informed models. Our findings highlight benefits from incorporating physiological information into correlative SDMs, namely mitigating the uncertainties associated with the choice of calibration area. Given these promising features, we encourage future SDM studies to consider species physiological information where available. Supplementary Information The online version contains supplementary material available at 10.1007/s42995-024-00226-0.
... These environments harbor a specialized subterranean fauna, notably distinct from surface-dwelling species (Soriano-Morales et al. 2013). Furthermore, caves partially isolated from the surface, present unique opportunities for ecological and evolutionary studies, as well as for understanding the adaptation of biological rhythms (Mammola et al. 2019;Poulson and White 1969). Such opportunities arise from their unique traits as the absence of constant light or light-dark cycles, high humidity, low availability of trophic resources, and a consistent temperature close to the surface's annual average (Beale et al. 2016;Howarth 1983). ...
Article
Full-text available
Circadian clocks, internal mechanisms that generate 24-hour rhythms, play a crucial role in coordinating biological events with day-night cycles. In light-deprived environments such as caves, species, particularly isolated obligatory troglobites, may exhibit evolutionary adaptations in biological rhythms due to light exposure. To explore rhythm expression in these settings, we conducted a comprehensive literature review on invertebrate chronobiology in global subterranean ecosystems, analyzing 44 selected studies out of over 480 identified as of September 2023. These studies revealed significant taxonomic diversity, primarily among terrestrial species like Coleoptera, with research concentrated in the United States, Italy, France, Australia, and Brazil, and a notable gap in African records. Troglobite species displayed a higher incidence of aperiodic behavior, while troglophiles showed a robust association with rhythm expression. Locomotor activity was the most studied aspect (>60%). However, approximately 4% of studies lacked information on periodicity or rhythm asynchrony, and limited research under constant light conditions hindered definitive conclusions. This review underscores the need to expand chron-obiological research globally, encompassing diverse geographical regions and taxa, to deepen our understanding of biological rhythms in subterranean species. Such insights are crucial for preserving the resilience of subsurface ecosystems facing threats like climate change and habitat loss.
... These environments harbor a specialized subterranean fauna, notably distinct from surface-dwelling species (Soriano-Morales et al. 2013). Furthermore, caves partially isolated from the surface, present unique opportunities for ecological and evolutionary studies, as well as for understanding the adaptation of biological rhythms (Mammola et al. 2019;Poulson and White 1969). Such opportunities arise from their unique traits as the absence of constant light or light-dark cycles, high humidity, low availability of trophic resources, and a consistent temperature close to the surface's annual average (Beale et al. 2016;Howarth 1983). ...
Article
Full-text available
Circadian clocks, internal mechanisms that generate 24-hour rhythms, play a crucial role in coordinating biological events with day-night cycles. In light-deprived environments such as caves, species, particularly isolated obligatory troglobites, may exhibit evolutionary adaptations in biological rhythms due to light exposure. To explore rhythm expression in these settings, we conducted a comprehensive literature review on invertebrate chronobiology in global subterranean ecosystems, analyzing 44 selected studies out of over 480 identified as of September 2023. These studies revealed significant taxonomic diversity, primarily among terrestrial species like Coleoptera, with research concentrated in the United States, Italy, France, Australia, and Brazil, and a notable gap in African records. Troglobite species displayed a higher incidence of aperiodic behavior, while troglophiles showed a robust association with rhythm expression. Locomotor activity was the most studied aspect (>60%). However, approximately 4% of studies lacked information on periodicity or rhythm asynchrony, and limited research under constant light conditions hindered definitive conclusions. This review underscores the need to expand chron-obiological research globally, encompassing diverse geographical regions and taxa, to deepen our understanding of biological rhythms in subterranean species. Such insights are crucial for preserving the resilience of subsurface ecosystems facing threats like climate change and habitat loss.
... We currently have a limited quantitative understanding of population trends for subterranean insects and the threats affecting them (Mammola et al. 2019aWynne et al. 2021). Large-scale studies and long historical data series are missing, and our knowledge is biased in its geographic and taxonomic coverage (Nanni et al. 2023). ...
Chapter
This chapter addresses the multiple threats faced by subterranean insects and their conservation. Subterranean insects are intrinsically vulnerable to anthropogenic threats due to their small distribution ranges, small population size, restricted habitat, and limited physiological and behavioural plasticities. Although we lack a quantitative understanding of population trends and long-term series of data, experts agree that habitat modification at the surface and climate changes are the most pervasive threats that may negatively affect subterranean insects. Beyond acquiring basic knowledge about subterranean insects and establishing monitoring programmes, their future conservation will be best achieved by (i) expanding protected areas’ coverage of global hotspot of subterranean diversity; and (ii) increasing awareness about subterranean insects and the important nature’s contribution they provide to people.
... 11,12 Given these unique conditions, subterranean ecosystems are highly susceptible to anthropogenic pressures across all ecosystem components with synergistic impacts, often with difficult-to-predict consequences. 13 The need to obtain a nuanced understanding of such ecological complexity, allowing stakeholders to implement sound and effective management plans to ultimately guarantee the conservation of show caves, 14 has been recently highlighted as a lacking yet critical research area in subterranean biology. 15 In this review, we outline sustainable strategies for show cave management by quantitatively analyzing the literature published over the last 30 years 16 dedicated to the study of human-induced environmental changes in show caves. ...
... Adequate allocation of funds for monitoring and conservation is also essential to ensure comprehensive coverage of subterranean environments and their biodiversity, thereby contributing to regional and global conservation targets (e.g., Hermoso et al. 2017;Mammola et al. 2019). Furthermore, research efforts should focus on the Afrotropical, Neotropical, and Indo-Malayan regions to fill significant information gaps . ...
Article
Full-text available
Invasive alien species (IAS) are widely recognized as a major threat to ecosystems globally. Despite the growing interest and research effort on biological invasions, the impact of IAS on both terrestrial and aquatic subterranean habitats remains considerably under-studied in comparison to other environments. The Convention on Biological Diversity (CBD) has established global targets to mitigate the impacts of IAS, emphasizing the need for countries, organizations, and the scientific community to identify gaps in knowledge, monitoring, and management strategies for IAS. To this end, we mapped knowledge gaps in biological invasions of subterranean habitats that emerged from the first systematic surveys of the available information. We suggest that there are five main gaps restricting our ability to understand and tackle biological invasions in subterranean ecosystems. Given the vulnerability of subterranean ecosystems and the lack of attention they have received in conservation policies, it is crucial to increase research emphasis on IAS. This opinion paper aims to stimulate such efforts and contribute to the preservation of these ecosystems.
... The EU fares better than other regions with regard to subterranean protected areas, thanks to the Natura 2000 network. This is the largest transnational coordinated network of areas of conservation in the world, aiming to preserve Europe's most valuable and threatened species and habitats as defined in the annexes of the Habitats and Birds Directives (Council Directives Box 1. Main human pressures affecting subterranean ecosystems Subterranean ecosystems are threatened by human activities at the surface (indirect impacts) and underground (direct impacts), which may affect abiotic conditions, biodiversity, and ultimately ecological functioning and the delivery of ecosystem services 76 . While the magnitude and relevance of direct versus indirect effects have been evaluated for surface freshwater systems 77,78 , these have rarely been quantified in subterranean systems beyond local case studies, with expert opinion being the only available source of information at regional to global scales 79 ( Figure Box). ...
Article
Full-text available
Subterranean ecosystems (comprising terrestrial, semi-aquatic, and aquatic components) are increasingly threatened by human activities; however, the current network of surface-protected areas is inadequate to safeguard subterranean biodiversity. Establishing protected areas for subterranean ecosystems is challenging. First, there are technical obstacles in mapping threedimensional ecosystems with uncertain boundaries. Second, the rarity and endemism of subterranean organisms, combined with a scarcity of taxonomists, delays the accumulation of essential biodiversity knowledge. Third, establishing agreements to preserve subterranean ecosystems requires collaboration among multiple actors with often competing interests. This perspective addresses the challenges of preserving subterranean biodiversity through protected areas. Even in the face of uncertainties, we suggest it is both timely and critical to assess general criteria for subterranean biodiversity protection and implement them based on precautionary principles. To this end, we examine the current status of European protected areas and discuss solutions to improve their coverage of subterranean ecosystems.
... The groundwater ecosystem is facing mounting anthropogenic pressure (Castaño-Sánchez et al., 2020;Mammola et al., 2019;Vaccarelli et al., 2023). Water depletion driven by urbanization, industry, agriculture and exacerbated by climate change, has been documented on both regional and global scales (Wada et al., 2010). ...
Article
Groundwater is a vital ecosystem of the global water cycle, hosting unique biodiversity and providing essential services to societies. Despite being the largest unfrozen freshwater resource, in a period of depletion by extraction and pollution, groundwater environments have been repeatedly overlooked in global biodiversity conservation agendas. Disregarding the importance of groundwater as an ecosystem ignores its critical role in preserving surface biomes. To foster timely global conservation of groundwater, we propose elevating the concept of keystone species into the realm of ecosystems, claiming groundwater as a keystone ecosystem that influences the integrity of many dependent ecosystems. Our global analysis shows that over half of land surface areas (52.6%) has a medium-to-high interaction with groundwater, reaching up to 74.9% when deserts and high mountains are excluded. We postulate that the intrinsic transboundary features of groundwater are critical for shifting perspectives towards more holistic approaches in aquatic ecology and beyond. Furthermore, we
... Introduction Life on earth went through five big mass extinction events-short geological periods during which three quarters of existing species went extinct-and studies on extinction rates show that we are at the edge of causing the sixth one [1]. This high extinction rate can be observed across diverse types of ecosystems [2][3][4] and taxonomic groups [5][6][7]. Biodiversity crisis has multiple causes that are linked and reinforce each other in complex systems that act at both local and global levels [5]. ...
Article
Full-text available
On the edge of causing the sixth big mass extinction event, the development of positive attitudes towards the conservation of intraspecific diversity from early ages is essential to overcome the biodiversity crisis we currently face. However, there is no information available on elementary school students’ attitudes toward intraspecific diversity conservation nor is there a framework available to perform such analysis. For this study we designed, implemented, and evaluated an educational activity planned for third graders (8 to 13 years old) to explore the intraspecific diversity of vegetables and promote healthy eating habits. Additionally, a framework was developed to evaluate students’ attitudes towards intraspecific diversity conservation and applied to semi-structured interviews conducted with students before and after engaging in the educational activity. In this paper we present a reliable framework, developed aligned with the ABC model of attitudes, based on literature, and adapted to elementary school students’ responses, to evaluate students’ attitudes toward intraspecific diversity. Our results show that, before the educational activity, most students choose a non-biodiverse option, justifying this choice with the affective component of attitudes: mostly emotional factors but also aesthetic and social/cultural factors. After the educational activity, we observed a significant increase in the frequency of students that choose the biodiverse option and that justified it with the cognitive component of attitudes: mainly with biology and health knowledge factors, but also with economic and ethical knowledge factors. Our findings support the positive impact of educational activities that explore vegetable varieties on students’ attitudes toward intraspecific diversity conservation. This activity may also be used to foster education for sustainability and address socioscientific issues aligned with diverse sustainable development goals.
... Some of the country's most crucial subterranean bat roosts, Corredores, Gabinarraca, Damas, and Emus, lack any state of protection. Cave ecosystems are particularly vulnerable to anthropogenic threats such as pollution, disturbance due to tourist activities, and climate change (Mammola et al. 2019). With the rapid development of tourism and speleological activities (Ulloa and Goicoechea 2013), it is essential to preserve and protect the subterranean habitats and unique species assemblages that inhabit these sites. ...
Article
Full-text available
This study focused on the cave fauna of Costa Rica, which has remained relatively understudied despite the presence of more than 435 recorded natural caves and artificial subterranean sites. We collected and reviewed all available literature data on cave fauna in Costa Rica and created the first comprehensive review of the existing information. In addition, we report new records from field surveys conducted between 2015 and 2018. This study reported approximately 123 animal species, whereas the remaining records (n = 82) represented taxa that could not be identified at the species level. Data were collected from 127 locations throughout the country, with new cave fauna records from 41 sites. Notably, we reported the first occurrence of the true bug Amnestus subferrugineus (Westwood 1837) within Costa Rican caves, which represents an addition to the country's faunal inventory. As this study highlights the knowledge gaps in the subterranean fauna, it will serve as an important stepping stone for future research and conservation efforts related to caves in Costa Rica.
... Such widespread distribution elevates E. pallida among one of the most widely introduced spiders. In addition, being a generalist predator, this species represents a potential threat to the native fauna, including in the subterranean environment, a notorious delicate habitat (Mammola et al. 2019, Nicolosi et al. 2023 which this species can also exploit. Despite the potential importance of E. pallida as a conservation threat in non-native areas, the available records of this species outside the native range are still fragmented and not yet revised. ...
Article
Updated non-native distributional data of the invasive spider Eidmannella pallida (Emerton, 1875), Nesticidae, are herein summarized together with the morphological characters of the species. We report all the known localities from the literature. Furthermore, we present and discuss recent findings for the Italian peninsula. In particular, the species has been consistently found in vineyards and annual crop fields in North Italy and in olive groves in South Italy. We include a redescription of the species, and detailed illustrations of the diagnostic characters of both males and females, based on stereomicroscope and SEM images. The spreading potential of the species and its possible impacts on local communities are discussed. Our data suggest that E. pallida has high invasiveness potential and several new findings in non-native areas were recorded in the last years. We found that E. pallida can establish permanent populations in crop-dominated landscapes and has a tendency to exploit vulnerable ecosystems such as the subterranean environment. We thus recommend new and more comprehensive studies on this species to investigate in deeper detail its phylogeny, ecology, and micro-habitat preferences. A high effort should be placed to assess the potential negative effects of E. pallida on the endemic fauna in invaded areas, especially in caves.
... Climate change in general threatens groundwater ecosystems, but we do not know yet, how which groundwater ecosystems will react, and which will be the driving impacts (Mammola et al., 2019). Thus, we do not know what will happen to the ecosystem functions that the ecosystems deliver, e.g. ...
Preprint
Full-text available
Atmospherically rising temperature and CO2 impact all freshwater systems, including groundwater. Increasing CO2 leads to more intense weathering of silicate rocks. Here, we tested whether the increased levels, the weathering, or rather the increasing temperature, impacted on fauna and prokaryotes in the groundwater ecosystem. We conducted the analyses separately for deep, i.e. secluded, and shallow, quaternary aquifers which exchange with the surface more intensely. Organism abundances and relative composition did not correlate with temperature or CO2 levels. While many organisms rely on silica, in contrast, we found negative correlations between silica and fauna. The increases in silica over time, i.e. temporal trends, also partly correlated negatively with organisms. We hypothesize that the unexpected negative correlations are not direct effects, but indirectly indicate that groundwater communities do not adapt rapidly enough to changes. This jeopardizes future drinking water production which relies on the self-cleaning ecosystem services in groundwater.
... Moreover, most studies have focused on surface ecosystems and our understanding of decomposition in subterranean habitats such as caves along elevational gradients are lacking (Ravn et al., 2020). Cave ecosystems across the globe (Culver and Pipan, 2019) provide a window to explore the contributions to nutrient cycling in the vast dimensions of underground habitats (Mammola et al., 2019), otherwise inaccessible to humans. These ecosystems differ substantially from surface habitats as they exhibit stable diurnal and seasonal environmental conditions (Lauritzen, 2018, Castaño-Sánchez et al., 2020, limited nutrient availability (oligotrophic) (Simon et al., 2007), and invertebrate and microbial communities specialized to life in the dark (Simon et al., 2007, Ortiz et al., 2014, Gonzalez-Pimentel et al., 2018, Gonzalez-Pimentel et al., 2021, Hathaway et al., 2014b, Riquelme et al., 2015, Hathaway et al., 2014a, Simon et al., 2003. ...
Article
Full-text available
Decomposition is a major contributor to ecosystem respiration, determining the carbon emission and nutrient cycling rates. Our current understanding of decomposition dynamics and their underlying drivers has mainly focused on surface habitats but largely ignored in subterranean environments. Here we studied abiotic and microbial drivers of early-stage litter decomposition inside and outside caves along an elevational gradient in Tenerife. We found comparable decomposition rates (k) and litter stabilizing factors (S), with contrasting drivers and elevational variation. At the surface, we observed a mid-elevational trend in k, which tended to correlate with water availability, cooler temperatures, nutrient availability, and surface-specific bacterial taxa. In sharp contrast, caves showed no elevational impact nor influence of abiotic parameters and bacterial communities on k. Despite this, we found higher levels of S in caves, which were associated mainly with reduced water availability, lower temperatures and cave-specific bacterial taxa, indicating that conditions in caves are strongly linked with carbon storage. Our findings imply that our current perception of terrestrial habitat-based carbon cycling are underestimating the net carbon budget in areas with caves. Disentangling the role of the environment on decomposition in caves is key to fully characterize their roles in nutrient cycling and to understand how increasing anthropogenic pressures will affect fundamental processes in subterranean ecosystems.
... Despite providing important ecosystem services such as water storage, purification and active biodegradation of anthropogenic contaminants (Griebler and Avramov, 2015), groundwater biota is still poorly recognized as a priority for conservation (Mammola et al., 2019). Responses of subterranean groundwater-dependent biota to anthropogenic stressors (especially EOCs) remain poorly understood due to scarcity and limited research on their difficult-to-access habitats (Castaño-Sánchez et al., 2020, 2021. ...
Article
Emerging organic contaminants (EOCs) are a vast group of often (very)persistent, (very)mobile and toxic (PMT/vPvM) substances that are continuously released worldwide, posing environmental and human health risks. Research on occurrence and behavior of EOCs in karst is in its infancy, thus policy measures and legislative control of these compounds in groundwater are still lacking. The Dinaric karst aquifers are an essential source of drinking water for almost half of Croatia's territory. Intense karstification, complex heterogeneous characteristics, and high fracture-cavernous porosity result in rapid, far-reaching groundwater flow and large karst springs, but also high intrinsic vulnerability due to low contaminant attenuation. To prioritize future monitoring and establish appropriate thresholds for EOCs detected in Croatian karst drinking water resources, in silico tools based on quantitative structure-activity relationships were used in PBT (persistence, bioaccumulation, and toxicity) and PMT/vPvM analyzes, while toxicological assessment helped identify potential threats to human health. In 33 samples collected during two sampling campaigns in 2019 at 16 karst springs and one lake used for water supply, we detected 65 compounds (EOCs and some legacy chemicals), of which 7 were classified as potentially PBT or vPvB compounds (PFOS, PFHxS, PFHpA, PFOA, PFNA, boscalid, and azoxystrobin), while only 2 compounds were assessed as not PMT/vPvM. This finding underlines that most of detected EOCs potentially endanger karst (ground)water ecosystems and important drinking water sources in Croatia. Comparison of maximum concentrations with existing or derived drinking water guideline values revealed how 2 of 65 detected compounds represent a potential risk to human health at lifelong exposure (sulfadiazine and hydrochlorothiazide), while 5 chemicals warrant additional human health impacts studies and groundwater monitoring. Although most compounds do not individually pose a significant risk to human health at current environmental levels, their potential synergistic and long-term effects remain unknown.
Article
Several bat species have experienced rapid population declines in the northern United States and Canada in response to the white-nose syndrome (WNS) epizootic. The pathogen has since spread across the United States, including the Southeast, where relatively warm temperatures may change host–pathogen interactions. In the cave-rich Tennessee–Alabama–Georgia (TAG) region, we examined the impacts of WNS and forest cover on the Tricolored Bat (Perimyotis subflavus) metapopulation using a long-term data set of 832 cave surveys conducted in summer and winter from 2004 to 2022. Most bat colonies were small (<30 individuals), and bats were more likely to be present and abundant in caves surrounded by high percent forest cover, reiterating the importance of forest management for bat conservation. When comparing the years before and after the pathogen arrived in 2010 to 2012, bat presence and abundance during winter hibernation did not change. This stability contrasts with significant declines in other studies, suggesting that Tricolored Bat populations respond differently to WNS in small colonies in the TAG region. Fewer tricolored bats used caves in the summer than during hibernation, but across all years, we observed 1,021 tricolored bats in 121 caves during summer surveys. Unlike stable winter trends, bat presence and abundance declined in the post-WNS period in summer, when cave use is optional. This first broad geographical analysis of summer cave use highlights a potentially important change in bat behavior. Disease surveillance and conservation efforts that target caves with relatively small Tricolored Bat colonies in winter and/or summer may be important for regional population persistence of this threatened species.
Article
Aim Groundwater ecosystems harbour a unique biodiversity, but remain poorly studied, mainly due to difficulties in accessibility and imperfect species detection. Consequently, knowledge on the state and change of groundwater biodiversity remains highly deficient. In the context of global warming and excessive groundwater extraction, understanding groundwater from an ecosystem‐perspective, including organism diversity and distribution, is essential. This study presents the largest ever systematic assessment of groundwater amphipods, which are a key component of European groundwater biodiversity. Location Switzerland (41,285 km ² ), including data from 906 sampling sites. Taxon Groundwater amphipods, genera Niphargus and Crangonyx (Crustacea, Amphipoda). Methods We applied a highly standardized citizen science approach to collect repeated groundwater fauna samples in collaboration with municipal drinking water providers. Using detection–nondetection data of the genetically identified groundwater amphipod species, we assessed the overall species diversity of both rare and common species. The distribution of commonly found species was predicted using multispecies occupancy modelling. Results We retrieved 3882 samples from 906 sites, yielding 2350 groundwater amphipod individuals. We identified a remarkable species diversity, comprising few commonly and many rarely found species. Considering commonly found species, we identified distinct distribution ranges, low local species richness and a predominance of negative co‐occurrences. In contrast, a major portion of species were found rarely (generally at just one or two sites each), distributed uniformly throughout the study area and unrelated to common species' recognized hotspots. Many of these rarely found species are not yet formally described. Main Conclusions Our results give robust emphasis on the rare occurrence and narrow distribution of many groundwater dwellers. Our systematic and standardized sampling data of groundwater amphipods suggest that rarity is particularly prominent and inherent to groundwater organisms. We emphasize the need of systematic data to integrate rare groundwater species in biodiversity assessments, especially in times of global change.
Article
Full-text available
Aquifers contain the largest store of unfrozen freshwater, making groundwater critical for life on Earth. Surprisingly little is known about how groundwater responds to surface warming across spatial and temporal scales. Focusing on diffusive heat transport, we simulate current and projected groundwater temperatures at the global scale. We show that groundwater at the depth of the water table (excluding permafrost regions) is conservatively projected to warm on average by 2.1 °C between 2000 and 2100 under a medium emissions pathway. However, regional shallow groundwater warming patterns vary substantially due to spatial variability in climate change and water table depth. The lowest rates are projected in mountain regions such as the Andes or the Rocky Mountains. We illustrate that increasing groundwater temperatures influences stream thermal regimes, groundwater-dependent ecosystems, aquatic biogeochemical processes, groundwater quality and the geothermal potential. Results indicate that by 2100 following a medium emissions pathway, between 77 million and 188 million people are projected to live in areas where groundwater exceeds the highest threshold for drinking water temperatures set by any country.
Article
Desertification in karst is an effect of climate change and not sustainable anthropogenic activities, the combination of which, however, causes the gradual loss of karst natural resources, such as soil, vegetation, and groundwater. A considerable percentage of global karst areas is found in drylands, characterized by negative water balance and scarce presence of soils. High fragility of the karst environment, and its vulnerability to land degradation and pollution because of the peculiar anisotropic setting, environmental dynamics, and of the direct connection between the surface and the subsurface, are at the origin of the severe problems deriving from desertification processes in karst. In addition to natural drivers, such as geology and topography, karst desertification is generally due to four main factors, mostly or partly related to human activity: deforestation, improper land use, groundwater overexploitation, and climate changes. Through the analysis of a collection of studies conducted in several karst territories around the world, the present paper aims to provide an overview of the processes leading to desertification risks in karst areas. Emphasizing the need to preserve these fragile environments, characterized by peculiar features and precious freshwater resources, this review summarizes the main situations at the global scale of rocky desertification in karst, at the same time providing indications for developing innovative and multi-disciplinary approaches addressed toward mitigation of the risk related to desertification in karst.
Article
Full-text available
One of the most important steps in identifying priority areas for conservation is the assessment of species richness and their extinction risks. While most species remain undescribed, the identification of cryptic lineages is frequent in phylogenetic and phylogeographic studies. This is particularly common in troglobites, exclusively subterranean organisms. The Jandaíra Formation, in the Brazilian semiarid, combines the occurrence of extensive karstic areas with hundreds of caves and subterranean aquifers in a region with intense paleoclimatic changes. This region is recognized for the richness of troglobitic species, some of which are widely distributed in heterogeneous areas. This suggests cryptic lineages that can be differentially exposed to anthropogenic threats, with distinct extinction risks regarding the nominal taxa of which they putatively belong. To test it, a large sampling was conducted and, by means of lineage delimitation analyses, the genetic structure of four troglobitic taxa, three aquatic and one terrestrial, was evaluated. In addition, the extinction risk of these lineages was assessed and priority areas for conservation were identified. The results indicated that while Cirolanidae sp. 1 (Isopoda) is a single species widely distributed, Cirolanidae sp. 2, Potiberaba porakuara (Amphipoda) and Kinnapotiguara troglobia (Hemiptera) present an extensive diversity of cryptic and endemic lineages, most of which are likely new threatened species. Furthermore, two priority areas for conservation of these lineages were identified. Thus, comparative phylogeography may represent a first step in the conservation of subterranean taxa, indicating areas that should be prioritized in a context of increasing threats and dwindling conservation resources.
Preprint
Full-text available
Invasive non-native species are recognized as a serious threat to the native biodiversity of the areas they colonize. The subterranean spider Howaia mogera (Yaginuma 1972) (syn. Nesticella mogera) is considered a highly invasive non-native species rapidly expanding its geographical range from Asia across the European continent and to remote oceanic islands. Due to its preference for moist, dark, and climatically stable habitats, including caves, this spider represents a potential threat to the endemic fauna living in the forest litter and subterranean environments. Nevertheless, the origin, biogeography, patterns of colonization, and niche preference of H. mogera remain unexplored. In this study, we reconstructed the phylogeography of the species combining a multi-locus phylogenetic analysis and a niche modeling approach. Our results confirm the center of origin of H. mogera in southern China, from where the species naturally spread and diversified in eastern Asia during the Pleistocene Epoch. Its expansion into non-native areas occurred only recently, possibly as a consequence of human-mediated passive transportation and in conjunction with a shift in the habitat preference of the species. Non-native populations have shifted from an original preference for a subterranean lifestyle to more generalist conditions. This change has allowed them to exploit a wider breadth of habitats and has facilitated their expansion in Europe and remote oceanic islands. Yet, the retention of the original subterranean habitat preferences in these non-native populations poses a conservation threat to specialized and fragile subterranean ecosystems, which H. mogera can efficiently exploit in invaded areas. Our study underscores the importance of comprehending phylogeography and niche dynamics in invasive non-native species to predict and manage their future expansions. We further highlight the urgency of monitoring H. mogera's spread worldwide, particularly in Southern Europe, to protect fragile invaded ecosystems.
Article
Full-text available
Groundwater is a vital ecosystem of the global water cycle, hosting unique biodiversity and providing essential services to societies. Despite being the largest unfrozen freshwater resource, in a period of depletion by extraction and pollution, groundwater environments have been repeatedly overlooked in global biodiversity conservation agendas. Disregarding the importance of groundwater as an ecosystem ignores its critical role in preserving surface biomes. To foster timely global conservation of groundwater, we propose elevating the concept of keystone species into the realm of ecosystems, claiming groundwater as a keystone ecosystem that influences the integrity of many dependent ecosystems. Our global analysis shows that over half of land surface areas (52.6%) has a medium-to-high interaction with groundwater, reaching up to 74.9% when deserts and high mountains are excluded. We postulate that the intrinsic transboundary features of groundwater are critical for shifting perspectives towards more holistic approaches in aquatic ecology and beyond. Furthermore, we propose eight key themes to develop a science-policy integrated groundwater conservation agenda. Given ecosystems above and below the ground intersect at many levels, considering groundwater as an essential component of planetary health is pivotal to reduce biodiversity loss and buffer against climate change.
Article
Full-text available
Despite the study of subterranean biodiversity facing harsh sampling and mapping challenges, the huge diversity of taxa, ecological adaptations and evolutionary trajectories in subterranean environments is gaining increasing attention. Yet, the spatial and environmental factors driving the composition of groundwater communities are still poorly understood. To partially fill this knowledge gap, we collected copepod crustaceans from 12 caves along the Italian peninsula between 2019 and 2022, sampling each cave twice. The resulting presence-absence data were analysed to assess: (i) between-cave taxonomic beta diversity, also partitioning between turnover and nestedness-resultant dissimilarity; (ii) the relative weight of geographic distance and climatic differences in shaping observed beta diversity. Seventy-one species of copepods were collected overall. Pairwise beta diversity was high for most pairs of caves, with turnover being the major component. Geographic distance-decay models partially explained total beta diversity and turnover patterns. However, in Generalized Dissimilarity Models (GDM), including surface climatic conditions as predictors, the contribution of seasonal temperature averages was generally higher than that of geographic distance. Further, the explanatory and predictive performance of the GDMs notably increased, along with temperature contribution, when widening the spatial extent from which climate data were gathered. Our results confirmed a high spatial turnover in groundwater copepods’ assemblages and strengthened the link between regional climate and subterranean biodiversity.
Preprint
Full-text available
The seasonal use of caves by bats can be attributed to physiologically demanding activities like mating and reproductions or torpor. Although cave use varies intra- and inter-specifically in bats, the microclimatic characteristics of roost sites have significant implications for the fitness of bat populations. As these microclimates are increasingly influenced by surface level climatic changes, understanding the current patterns of cave utilization is crucial to assess the impact of climate change on bats. Therefore, we monitored cave temperatures and studied the diversity and abundance of bats in 41 caves across a seasonal (mid-winter, late-winter and early-spring) and an elevational (400 to 2700 meters above sea level) gradient in the Central Himalayas. The richness and abundance of bat species exhibited seasonal variations, with more species and individuals present during early spring (n = 15) compared to mid-winter (n = 9). Species richness exhibited a linear decline with elevation in mid-winter, but remained relatively stable until 900 msl and then declined in late-winter and early-spring. Furthermore, species such as Hipposideros armiger (20.14 ± 1.60°C in spring and 17.97 ± 0.88°C in mid-winter), Rhinolophus affinis (19.98 ± 1.76°C in spring and 16.18 ± 3.09°C in mid-winter) and Rhinolophus cf. pusillus (19.55 ± 1.64°C in spring and 15.43 ± 2.87°C in mid-winter) preferred warmer microclimates during early-spring compared to mid-winter. This season- and species- specific cave use suggests that even minor fluctuations in cave temperatures could potentially alter the composition of bat communities inside caves. We recommend that long-term studies in such highly diverse climate vulnerable areas would help understand and predict the responses of cave-dwelling bats to climate change.
Article
Full-text available
Caves are among the most important roosts of hundreds of bat species worldwide. However, caves can be formed in different lithologies. Cave structure and characteristics, which are shaped by lithology, can, in turn, influence roost preferences for different bat species. Therefore, cave lithology and characteristics can help us to better understand why some bat species may be rare in some caves and common in others. Brazil is a continental country, rich in bat species (181 spp.), lithologies and caves (>23 000). However, only a small fraction of the known caves has been sampled for bats so far, with no emphasis on the role lithology may have. Based on a literature review and using data on bat occurrence, in this study, we investigated the influence of lithology on bat species richness and rarity in Brazilian caves. We evaluated 117 studies, including data from 552 caves, and updated the number of bat species occurring in Brazilian caves to 81. Species richness differed between lithologies: carbonate caves had higher species richness, whereas iron caves had lower species richness. Richness was positively related to carbonate caves and with cave size: the bigger the cave, the more species‐rich it tends to be. Overall, caves in the Cerrado had the highest species richness, followed by Atlantic Forest, Caatinga caves and Amazonian caves. Thirteen species can be considered as primarily cave‐dwelling species, recorded in 10%–20% of the caves. Rarity was common among primarily cave‐dwelling species. Nearly 22% of the sampled caves harboured endangered species, reaching 53% of the species‐richest caves. Our analysis provides a comprehensive baseline for bat fauna in different types of caves in Brazil. Even so, we strongly recommend the establishment of long‐term monitoring of population trends for bats in Brazilian caves, which is necessary information but almost non‐existing for the country.
Article
Full-text available
Subterranean habitats can be considered harsh conditions with lack of light, low nutrients levels and constant high humidity. To thrive under such conditions, cave-adapted species have evolved a range of novel morphological, physiological and behavioural adaptations. These adaptations might have significant biomimetic potential. Biomimetics or biologically inspired design is a relatively new interdisciplinary field that aims to harness the processes and mechanisms in nature that have been optimised over millions of years’ evolution to improve our own technology. There are two main approaches to biologically inspired design—the problem-driven approach starting with an engineering problem and searching through biological equivalents and the solution-driven approach, which starts with a biological example or solution followed by the identification of a suitable engineering application. While the former approach is the most popular and is favoured by engineers, the latter remains the most successful and is typically driven by fundamental biological research. However, few biomimetic solutions or concepts have so far been described from subterranean habitats despite the rich potential. In this review paper, I first outline the theory behind biologically inspired design before I review the few biomimetic related studies of cave adapted organisms mainly based on the exceptional lateral line systems in blind cave fish. However, the main body of the review focuses on identifying and discussing subterranean adaptations with a particular strong potential including biomimetics sensors, adhesion in high humidity and wet conditions and biomaterials
Article
Full-text available
Cave-obligate aquatic organisms are difficult to monitor for conservation due to cryptic diversity, unknown subterranean hydrological connectivity, and accessibility to habitats. Conservation management practices have benefitted from evolutionary data; however, the evolutionary and biogeographic histories of most cave-obligate organisms are unknown. The modes and patterns leading to most cave-obligate organism distributions are also uncertain. The Southern Cavefish (Typhlichthys subterraneus, Amblyopsidae) is the largest ranging cavefish in the world but represents a species complex of which the distribution and relatedness within remains unclear. To explore modes of cave-adaptive evolution, we performed population genomic analyses on a dataset of single nucleotide polymorphisms harvested from ultraconserved elements. We found five to eight strongly delineated genetic clusters. Little to no genetic exchange occurred between clusters, indicating high genetic distinctiveness and low connectivity, a concerning result for the fitness and conservation of these fishes. Genetic clusters did not correspond to caves nor to other geographic boundaries examined. Unfortunately, one of the geographic units most easily communicated for conservation– caves– do not match the biological units of interest. Our results support multiple independent colonization events from a widespread surface ancestor with a small degree of cave connectivity among, but not between, clusters. We suggest whole cave system conservation.
Article
Full-text available
The impact of meteorological phenomena on ecosystem communities of karst subterranean estuaries (KSEs) remains unknown. KSEs are characterized by vertically stratified groundwater separated by a halocline and host endemic aquatic cave-adapted fauna (stygobionts). In October 2015, 8 days of heavy precipitation caused the first recorded mortality event in the KSE. This event was marked by a halocline shift 5 m deeper. The present study aimed to provide insights into resilience of KSEs faunal communities to temporal shifts in temperature and precipitation. Cave water temperature decreased on average 0.0068°C per mm of accumulated precipitation over 4 days, which can add up to, and surpass, the interannual temperature variation in cases of heavy precipitations. Biological surveys (2012-2021) conducted within cave systems El Aerolito and La Quebrada, in Cozumel, indicated that change in community structure was not detected and stygobionts were resilient; however, marine species inhabiting the caves were impacted. Overall, the faunal community at KSEs remains resilient within short-term meteorological phenomena despite shifts of non-stygobionts.
Article
Full-text available
Bats frequently inhabit caves and other subterranean habitats and play a critical role in subterranean food webs. With escalating threats to subterranean ecosystems, identifying the most effective measures to protect subterranean‐roosting bats is critical. We conducted a meta‐analysis to evaluate the effectiveness of conservation and management interventions for subterranean‐roosting bats. We used network analyses to determine to what extent interventions for bats overlap those used for other subterranean taxa. We conducted our analyses with data extracted from 345 papers recommending a total of 910 conservation interventions. Gating of roost entrances was applied to preserve bat populations in 21 studies, but its effectiveness was unclear. Habitat restoration and disturbance reduction positively affected bat populations and bat behavior, respectively, in ≤4 studies. Decontamination was assessed in 2 studies and positively affected bat populations, particularly in studies focused on reducing fungal spores associated with white‐nose syndrome in North America. Monitoring of bat populations as an effective conservation strategy was unclear and infrequently tested. Only 4% of bat studies simultaneously considered other subterranean organisms. However, effective interventions for bat conservation had similarities with all other organisms. If other subterranean organisms are considered when applying interventions to conserve bats, they might also benefit.
Article
Full-text available
1. Biodiversity conservation is a central imperative of the 21st century. Subterranean ecosystems deliver critical nature's contributions to people and harbour a broad diversity of poorly understood specialised organisms. However, the subterranean biome is still largely overlooked in global biodiversity targets. 2. We assessed how well subterranean biodiversity is represented in protected areas (Natura 2000 and Emerald networks) in two global hotspots of subterranean biodiversity (the Pyrenees and the Alps). For this, we used two comprehensive databases of terrestrial subterranean taxa, that is, leiodids (beetles) from the Pyrenees and spiders from the Alps, and identified priority areas in each region using both species richness and geographic rarity patterns. 3. Our results show the incapacity of surface-protected area networks to represent subterranean biodiversity, as more than 70% and 90% of the identified priority areas (and 40% and 22% of the species) are not effectively covered by protected areas in the Pyrenees and the Alps, respectively. 4. These findings call for developing an urgent plan for subterranean biodiversity conservation within the European Biodiversity Strategy for 2030.
Article
Full-text available
We report a functional switching valve within the female genitalia of the Brazilian cave insect Neotrogla. The valve complex is composed of two plate-like sclerites, a closure element, and in-and-outflow canals. Females have a penis-like intromittent organ to coercively anchor males and obtain voluminous semen. The semen is packed in a capsule, whose formation is initiated by seminal injection. It is not only used for fertilization but also consumed by the female as nutrition. The valve complex has two slots for insemination so that Neotrogla can continue mating while the first slot is occupied. In conjunction with the female penis, this switching valve is a morphological novelty enabling females to compete for seminal gifts in their nutrient-poor cave habitats through long copulation times and multiple seminal injections. The evolution of this switching valve may have been a prerequisite for the reversal of the intromittent organ in Neotrogla.
Article
Full-text available
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.
Article
Full-text available
The Second Warning to Humanity provides a clarion call for wetland researchers and practitioners given the loss and degradation of wetlands, the declining availability of fresh water, and the likely consequences of climate change. A coordinated response and approach to policies has the potential to prevent further degradation and support resilient wetlands that can provide a range of ecosystem services, including buffering wetlands from climate impacts, and avoiding major climate amplification from temperature-induced release of additional carbon dioxide and methane while addressing the causes and consequences of global climate change. The Warning to Humanity also provides an opportunity for organisations such as the Society of Wetland Scientists to raise the profile of wetlands and to initiate a discussion on how to respond and change direction from the destructive development trajectory that led to wetland loss and degradation. It also provides a signal for a reappraisal of the effectiveness of the implementation of the Ramsar Convention on Wetlands as an international mechanism for ensuring the sustainability of wetlands.
Article
Full-text available
Article impact statement: Biodiversity of unexplored and unmapped environments cannot be conserved until they have been described, mapped, and analyzed.
Article
Full-text available
https://rdcu.be/ZBWl (Direct link for BMC Evol Biol) Background: An essential question in evolutionary biology is whether shifts in a set of polygenic behaviors share a genetic basis across species. Such a behavioral shift is seen in the cave-dwelling Mexican tetra, Astyanax mexicanus. Relative to surface-dwelling conspecifics, cavefish do not school (asocial), are hyperactive and sleepless, adhere to a particular vibration stimulus (imbalanced attention), behave repetitively, and show elevated stress hormone levels. Interestingly, these traits largely overlap with the core symptoms of human autism spectrum disorder (ASD), raising the possibility that these behavioral traits are underpinned by a similar set of genes (i.e. a repeatedly used suite of genes).
Article
Full-text available
Landscapes in tropical regions have been greatly altered by human activities, as a product of growing demands for mineral and agricultural production, as well as those related to the generation of energy (e.g., hydroelectric, wind). In this scenario, caves have suffered several impacts, sometimes irreversible, as they are generally associated with rocks of high economic value and are closely related to epigean systems. Several indices have been proposed to guide conservation policies for the world’s speleological heritage, although few of them consider cave biodiversity as a criterion. To address this knowledge gap, we tested the applicability of four newly proposed indices to assist researchers and policy-makers select priority areas for global cave biodiversity conservation. To compare indices, we used data from 48 caves of the largest carbonate region of South America (Bambui geological group), all found within the Cerrado, a global biodiversity hotspot. Each of the four indices considered cave biodiversity as a criterion, although only three adequately evaluated this attribute. Based on results of Simões index and CCPi, which were the most appropriate in relation to indicate priority caves for biodiversity conservation in regions where the fauna and its distribution are not fully known, 15 of the 48 caves were identified as conservation priorities.
Article
Full-text available
Worldwide, there are at least 12 ILTER sites with an emphasis on karst, landforms arising from the combination of high rock solubility and well-developed solutional channel porosity underground, but the study of cave ecosystems has been largely neglected. Only two ILTER sites, both in Slovenia, are primarily caves. Caves are under-represented for several reasons, but especially because of the overall difficulty of access and the lack of a clear research agenda for cave ecosystem studies. We review several aspects of long-term studies in Postojna Planina Cave System (PPCS), proposing our approach as a model for ILTER research in caves. In PPCS, analysis of short-term temperature data shows a muted daily cycle and seasonality, and analysis of long-term temperature data shows an increase, largely the result of climate change. Changes in drip rate of epikarst aquifers above the cave are correlated with rainfall but with lags and complications resulting from differences in longer term rainfall patterns. Analysis of discharge rates indicates a rapid response to precipitation not only in the Pivka River at its sinking, but also at Unica Spring, where discharge is augmented from other parts of the aquifer, including epikarst. Quantitative analysis of the obligate epikarst-dwelling copepod community shows that, unlike most cave communities, complete sampling of the fauna is possible. Finally, organic carbon levels in PPCS indicate likely carbon limitation in the system. These five factors (temperature, drip rate, river discharge, epikarst copepod fauna, and organic carbon) are the appropriate variables for capturing the essential long-term trends in cave ecosystems and their causes.
Article
Full-text available
Periodic food shortages are a major challenge faced by organisms in natural habitats. Cave-dwelling animals must withstand long periods of nutrient deprivation, as-in the absence of photosynthesis-caves depend on external energy sources such as seasonal floods. Here we show that cave-adapted populations of the Mexican tetra, Astyanax mexicanus, have dysregulated blood glucose homeostasis and are insulin-resistant compared to river-adapted populations. We found that multiple cave populations carry a mutation in the insulin receptor that leads to decreased insulin binding in vitro and contributes to hyperglycaemia. Hybrid fish from surface-cave crosses carrying this mutation weigh more than non-carriers, and zebrafish genetically engineered to carry the mutation have increased body weight and insulin resistance. Higher body weight may be advantageous in caves as a strategy to cope with an infrequent food supply. In humans, the identical mutation in the insulin receptor leads to a severe form of insulin resistance and reduced lifespan. However, cavefish have a similar lifespan to surface fish and do not accumulate the advanced glycation end-products in the blood that are typically associated with the progression of diabetes-associated pathologies. Our findings suggest that diminished insulin signalling is beneficial in a nutrient-limited environment and that cavefish may have acquired compensatory mechanisms that enable them to circumvent the typical negative effects associated with failure to regulate blood glucose levels.
Article
Full-text available
The identification of important habitats for wildlife is essential in order to plan and promote strategies for longterm effective conservation. Caves and subterranean habitats are frequently overlooked habitats with diverse communities, which are frequently endemic to a region, karst outcrop or even a single cave. These cave species include a wide range of taxa adapted to cave environments. Within cave systems, bats are key providers of energy for other cave-dependent species. However, identifying caves for conservation prioritisation requires an understanding of cave-dwelling species diversity, patterns of endemism, and conservation status, in addition to a standard mechanism to evaluate risk. In this paper, we present the ‘Bat Cave Vulnerability Index’ (BCVI) as a standard index for evaluating bat caves for conservation prioritisation by determining Biotic Potential (BP) and Biotic Vulnerability (BV) of caves. The Biotic Potential is represented by various species diversity and rarity measurements. The Biotic Vulnerability is represented by the cave geophysical characteristics and human-induced disturbance present. Pilot testing in the southern Philippines has demonstrated that the index is an effective and practicable method to identify bat caves for conservation prioritisation. The biotic potential variables assess the presence of endemic, rare, and threatened bat species and assays the priority level based on an equation. Relative risk and vulnerability were assayed using landscape vulnerability variables, which showed anthropogenic activities were important factors in conservation prioritisation. The application and mechanism of the index potentially provides a valuable, rapid and simple assessment tool in cave conservation with special relevance to bat diversity and vulnerability. Furthermore, the multiple and holistic criteria of the BCVI, and the accessible information for both biotic and landscape features can be adapted to prioritise caves in a wider scale in the tropics, and in other regions with diverse cave ecosystems.
Article
Full-text available
Bats are unique among mammals, possessing some of the rarest mammalian adaptations, including true self-powered flight, laryngeal echolocation, exceptional longevity, unique immunity, contracted genomes, and vocal learning. They provide key ecosystem services, pollinating tropical plants, dispersing seeds, and controlling insect pest populations, thus driving healthy ecosystems. They account for more than 20% of all living mammalian diversity, and their crown-group evolutionary history dates back to the Eocene. Despite their great numbers and diversity, many species are threatened and endangered. Here we announce Bat1K, an initiative to sequence the genomes of all living bat species (n∼1,300) to chromosome-level assembly. The Bat1K genome consortium unites bat biologists (>132 members as of writing), computational scientists, conservation organizations, genome technologists, and any interested individuals committed to a better understanding of the genetic and evolutionary mechanisms that underlie the unique adaptations of bats. Our aim is to catalog the unique genetic diversity present in all living bats to better understand the molecular basis of their unique adaptations; uncover their evolutionary history; link genotype with phenotype; and ultimately better understand, promote, and conserve bats. Here we review the unique adaptations of bats and highlight how chromosome-level genome assemblies can uncover the molecular basis of these traits. We present a novel sequencing and assembly strategy and review the striking societal and scientific benefits that will result from the Bat1K initiative. Expected final online publication date for the Annual Review of Animal Biosciences Volume 6 is February 15, 2018. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Article
Full-text available
Twenty-five years ago, the Union of Concerned Scientists and more than 1700 independent scientists, including the majority of living Nobel laureates in the sciences, penned the 1992 “World Scientists’ Warning to Humanity” (see supplemental file S1). These concerned professionals called on humankind to curtail environmental destruction and cautioned that “a great change in our stewardship of the Earth and the life on it is required, if vast human misery is to be avoided.” In their manifesto, they showed that humans were on a collision course with the natural world. They expressed concern about current, impending, or potential damage on planet Earth involving ozone depletion, freshwater availability, marine life depletion, ocean dead zones, forest loss, biodiversity destruction, climate change, and continued human population growth. They proclaimed that fundamental changes were urgently needed to avoid the consequences our present course would bring. The authors of the 1992 declaration feared that humanity was pushing Earth's ecosystems beyond their capacities to support the web of life. They described how we are fast approaching many of the limits of what the ­biosphere can tolerate ­without ­substantial and irreversible harm. The scientists pleaded that we stabilize the human population, describing how our large numbers—swelled by another 2 billion people since 1992, a 35 percent increase—exert stresses on Earth that can overwhelm other efforts to realize a sustainable future (Crist et al. 2017). They implored that we cut greenhouse gas (GHG) emissions and phase out fossil fuels, reduce deforestation, and reverse the trend of collapsing biodiversity.
Article
Full-text available
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.
Article
Full-text available
Molecular taxonomy often uncovers cryptic species, reminding us that taxonomic incompleteness is even more severe than previous thought. The importance of cryptic species for conservation is poorly understood. Although some cryptic species may be seriously threatened or otherwise important, they are rarely included in conservation programs as most of them remain undescribed. We analysed the importance of cryptic species in conservation by scrutinizing the South European cryptic complex of the subterranean amphipod Niphargus stygius sensu lato. Using uni- and multilocus delineation methods we show that it consists of 15 parapatric and sympatric species, which we describe using molecular diagnoses. The new species are not mere “taxonomic inflation” as they originate from several distinct branches within the genus and coexist with no evidence of lineage sharing. They are as evolutionarily distinct as average nominal species of the same genus. Ignoring these cryptic species will underestimate the number of subterranean endemics in Slovenia by 12 and in Croatia by four species, although alpha diversity of single caves remains unchanged. The new taxonomy renders national Red Lists largely obsolete, as they list mostly large-ranged species but omit critically endangered single-site endemics. Formal naming of cryptic species is critical for them to be included in conservation policies and faunal listings.
Article
Full-text available
The genus Agave is one of the most diverse and rich groups of plants of Mexico. Mexican people have developed several technologies to extract products from Agave, and for many years they have consumed five different alcoholic beverages derived from Agave: Tequila, Mezcal, Bacanora, Raicilla, and Pulque. Additionally, Agave has coevolved with nectar-feeding bats, and in several cases, bats play the main role as functional pollinators in this ecological relationship. But with growth in the demand of agave derived products, management practices have reduced dependence on bat pollination, using instead clonal shoots to replant fields and harvesting plants before flowering, thereby negatively affecting both bats (by decreasing food availability) and agaves (by lowering their genetic diversity). We explore the possibility that bat-friendly practices may be incorporated into the production system. We compiled data about the pollination biology of Agave to infer how many bats could use the available resources, if Mezcal and Tequila producers allowed 5-10% of agave crop inflorescences to flower based on a linear projection using Agave angustifolia (a sister group of A. tequilana). If only 5% of the plants in one hectare were allowed to flower (approximately 222 individuals), then, depending on nectar concentration and total volume, a minimum of 89 individual bats could feed every night during flowering period. This means that allowing 5% of the current total population of A. tequilana reproductive agaves to flower could feed a total of 2,336,250 nectar feeding bats per month.
Chapter
Full-text available
Caves and other subterranean sites such as mines are critical to the survival of hundreds of bat species worldwide, since they often provide shelter for most of a nation’s bat fauna. In the temperate zone, caves provide roosts for hibernation and for some species, breeding in summer, whereas in warmer regions, they support high species richness year round and enormous colonies that maintain substantial ecosystem services. Due to the solubility of the substrate, the highest densities of caves occur in karst landscapes. Given their importance for bats, relatively few studies have investigated factors involved in cave selection, although current evidence suggests that the density and size of caves are the best predictors of species diversity and population sizes. Thermal preferences have been established for some cave-dwelling species as well as their vulnerability to disturbance, particularly during hibernation and reproduction. Growth in limestone quarrying and cave tourism industries worldwide severely threatens cave-dwelling bats, in addition to loss of foraging habitat, hunting for bushmeat, incidental disturbance and disruptive guano harvesting. Apparent declines of cave bats in Europe and North America also pose serious concerns, as do global climate change predictions. The main conservation response to threats to cave bats in these continents has been gating, but this remains relatively untested as a means of protecting colonies in other regions. Research on sustainable harvesting of bats as bushmeat and their responses to different types of human disturbance at caves and loss of surrounding foraging habitats is required. More caves of outstanding importance for bats at national and international levels also require protection.
Article
Full-text available
Ecologists and evolutionary biologists are increasingly using big-data approaches to tackle questions at large spatial, taxonomic, and temporal scales. However, despite recent efforts to gather two centuries of biodiversity inventories into comprehensive databases, many crucial research questions remain unanswered. Here, we update the concept of knowledge shortfalls and review the tradeoffs between generality and uncertainty. We present seven key shortfalls of current biodiversity data. Four previously proposed shortfalls pinpoint knowledge gaps for species taxonomy (Linnean), distribution (Wallacean), abundance (Prestonian), and evolutionary patterns (Darwinian). We also redefine the Hutchinsonian shortfall to apply to the abiotic tolerances of species and propose new shortfalls relating to limited knowledge of species traits (Raunkiæran) and biotic interactions (Eltonian). We conclude with a general framework for the combined impacts and consequences of shortfalls of large-scale biodiversity knowledge for evolutionary and ecological research and consider ways of overcoming the seven shortfalls and dealing with the uncertainty they generate.
Article
Full-text available
The disoovery of the Ursilor (Bear's) Cave (Apuseni Mountains, Romania) in the 70th was followed by climatic and biological studies, before its opening as a show cave. Twenty years later these researches were undertaken again The tourism has impacted on the populations of two endemic cave beetles: Pholeuon leptoderum and Drirneotus n. sp. The first one became extremely rare in the tourist part of the cave. Drimeotus has adapted different dynamics during the year in the two parts of the cave; near the tourist path the populations evolves depending on the affluence of the tourists in the summer months, and in the protected part has kept the same pattern as in the early studies.
Article
Full-text available
Caves are considered buffered environments in terms of their ability to sustain near-constant microclimatic conditions. However, cave entrance environments are expected to respond rapidly to changing conditions on the surface. Our study documents an assemblage of endemic arthropods that have persisted in Rapa Nui caves, despite a catastrophic ecological shift, overgrazing, and surface ecosystems dominated by invasive species. We discovered eight previously unknown endemic species now restricted to caves—a large contribution to the island's natural history, given its severely depauperate native fauna. Two additional species, identified from a small number of South Pacific islands, probably arrived with early Polynesian colonizers. All of these animals are considered disturbance relicts—species whose distributions are now limited to areas that experienced minimal historical human disturbance. Extinction debts and the interaction of global climate change and invasive species are likely to present an uncertain future for these endemic cavernicoles.
Article
Full-text available
Despite Brazil’s role as a global environmental leader, most of its megadiverse and unique biomes are at risk (Ferreira et al. 2014). Currently, the Brazilian Congress is debating political proposals (e.g. PL 3682/2012) for the expansion of mining and hydropower generation activities across the country, including areas within the system of Brazil’s protected areas. Ferreira et al. (2014) showed a detrimental perspective for the integrity of Brazil’s biomes in a scenario where the ongoing proposals are approved. Areas of mining interest overlap 20 % of Brazil’s protected areas and indigenous lands, threatening the coverage integrity of the largest system of protected areas worldwide. Although there are compelling arguments, the authors argue that Brazil’s newly elected government should maintain a consistent stance with its influential role as a leader in the conservation of natural areas by expanding the protected areas system and reducing deforestation.Although we fully agree with the ...
Article
Full-text available
BackgroundA key question in evolutionary biology is the relationship between species traits and their habitats. Caves offer an ideal model to test the adjustment of species to their surrounding temperature, as they provide homogeneous and simple environments. We compared two species living under different thermal conditions within a lineage of Pyrenean beetles highly modified for the subterranean life since the Miocene. One, Troglocharinus fonti, is found in caves at 4-11°C in the ancestral Pyrenean range. The second, T. ferreri, inhabits the coastal area of Catalonia since the early Pliocene, and lives at 14-16°C.ResultsWe found no differences in their short term upper thermal limit (ca. 50°C), similar to that of most organisms, or their lower thermal limit (ca. -2.5°C), higher than for most temperate insects and suggesting the absence of cryoprotectants. In longer term tests (7 days) survival between 6-20°C was almost 100% for both species plus two outgroups of the same lineage, but all four died between 23-25°C, without significant differences between them.Conclusions Our results suggest that species in this lineage have lost some of the thermoregulatory mechanisms common in temperate insects, as their inferred default tolerance range is larger than the thermal variation experienced through their whole evolutionary history.
Article
Full-text available
Cave environments are characterized by possessing specialized fauna living in high environmental stability with limited food conditions. These fauna are highly vulnerable to impacts, because this condition can frequently be easily altered. Moreover, environmental determinants of the biodiversity patterns of caves remain poorly understood and protected. Therefore, the main goal of this work is to propose a cave conservation priority index (CCPi) for a rapid assessment for troglobiotic and troglophile protection. Furthermore, the troglobiotic diversity, distribution and threats have been mapped in the Brazilian Atlantic forest. To propose the CCPi, the human impacts and richness of troglobiotic and troglophile species of 100 caves were associated. Data related to troglomorphic/troglobiotic fauna from another 200 caves were used to map the troglobiotic diversity and distribution. The CCPi reveals extremely high conservation priority for 15 % of the caves, high for 36 % and average for 46 % of the caves. Fourteen caves with extremely high priorities should have urgent conservation and management actions. The geographical distribution of the 221 known troglobiotic/troglomorphic species allowed us to select 19 karst areas that need conservation actions. Seven areas were considered to have urgent priority for conservation actions. The two richest areas correspond to the "iron quadrangle" with iron ore caves (67 spp.) and the "Açungui limestone group" (56 spp.). Both areas have several caves and are important aquifers. The use of the CCPi can prevent future losses because it helps assessors to select caves with priorities for conservation which should receive emergency attention in relation to protection, management and conservation actions.
Article
Full-text available
We investigated the upper and lower vertical limits of the distribution of inhabitants of the most abundant freshwater habitat—groundwater. Distribution in photic habitats is limited by competition, predation, and risks of exposure to ultraviolet radiation. Nonetheless, a number of eyeless, depigmented subterranean species occur in twilight habitats, taking advantage of the higher food resources available and modulating their distribution by photophobic behavior. We argue that the upper boundary is an interesting system in the study of classic ecological and evolutionary questions. The lower boundary of the distribution of groundwater species (approximately 2000—4000 meters) is likely controlled by physicochemical parameters, including temperature, pressure, and oxygen. The lower boundary warrants further research, and it is one of the most poorly explored areas of the biosphere.
Article
Full-text available
Most organisms are able to survive shorter or longer exposure to sub-zero temperatures. Hypothetically, trogloxenes characterized as not adapted, and troglophiles as not completely adapted to thermally stable subterranean environment, have retained or partially retained their ability to withstand freezing, while most troglobionts have not. We tested this hypothesis experimentally on 37 species inhabiting caves in Slovenia, analyzing their lower lethal temperatures in summer and winter, or for one season, if the species was not present in caves during both seasons. Specimens were exposed for 12 hrs to 1°C-stepwise descending temperatures with 48 hr breaks. In general, the resistance to freezing was in agreement with the hypothesis, decreasing from trogloxenes over troglophiles to troglobionts. However, weak resistance was preserved in nearly all troglobionts, which responded in two ways. One group, withstanding freezing to a limited degree, and increasing freezing tolerance in winter, belong to the troglobionts inhabiting the superficial subterranean habitats. The other group, which equally withstand freezing in summer and winter, inhabit deep subterranean or other thermally buffered subterranean habitats. Data on cold resistance can thus serve as an efficient additional measure of adaptation to particular hypogean environments.