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Patterns of endemism of the eastern North American cave fauna
Abstract
Aim Over 250 species of obligate terrestrial cave‐dwelling animals (troglobionts) are known from single caves in the eastern United States. We investigate their geographical distribution, especially in relation to other troglobionts. We relate these patterns to taxonomic group, opportunities for dispersal and geographical location.
Location Caves of the United States east of the Mississippi River.
Methods We associated over 3000 records of more than 450 troglobiotic species and subspecies with hexagons of 1000, 5000 and 10,000 km ² in size. We calculated Moran's I , black–white joins and cubic regression of endemics on non‐endemics at all three spatial scales. For 5000 km ² hexagons, we modelled the spatial autocorrelation of the residuals of the cubic regression of endemics on non‐endemics.
Results Differences among orders in percentage single‐cave endemism were not significant, except for Pseudoscorpionida, which was higher (69%) than any other order. At all three scales, Moran's I and black–white joins were significant, indicating a clumped distribution of both single‐cave endemics and other troglobionts. Spatial patterns were similar at all three scales and Moran's I was highest at 5000 km ² . The cubic fit of endemics to non‐endemics was consistently better, with less systematic error or residuals, than were linear or quadratic models. Residuals showed a significant geographical pattern with excess endemics in more southerly locations.
Main conclusions There was both a non‐spatial and spatial component to the pattern of single‐cave endemism. The non‐spatial component was the association of high levels of single‐cave endemism with areas of high diversity of non‐endemics. It may be that both are high because of high secondary productivity. Spatially, single‐cave endemism is high in central rather than peripheral areas and in the southern part of the range. It is not higher in areas of more dissected limestone, which would reduce migration rates; if anything endemism is lower. Regional spatial effects are important, indicating that cave communities cannot be understood (or protected) in isolation.
... Only a few localities harbor a high number of species to the point that differences in species richness among grid cells within a region can largely depend upon the distribution of species-rich localities among cells (Culver et al., 2004a;Pipan et al., 2018). Species-rich localities are due to the overlap of ranges of "widespread" species rather than from the occurrence of many species endemic to these localities (Culver et al., 2004a;Christman et al., 2005;Bregovi c et al., 2019). Local biodiversity hotspots have been reported from several regions in the World (Culver et al., 2021), having high numbers of obligate groundwater species too: these includes the Postojna Planina Cave System, Slovenia (72 species), the Walsingham Cave, Bermuda (65 species), the San Marcos Artesian Well, USA (55 species), and the Robe Valley wells, Australia (48 species). ...
... If subterranean dispersal is important, then species richness in adjoining areas should influence diversity locally. The difficulty is that LSR may be spatially autocorrelated because of some factors that influence species dispersal or because some unmeasured environmental parameters influencing LSR are themselves spatially autocorrelated (Christman et al., 2005). The problem trying to understand spatial patterns in LSR within a region is not deciding among a number of explanations but rather quantifying the relative contributions of different explanations. ...
... Studies documenting variation in groundwater species richness over large spatial extents have used a coarse spatial grain size corresponding either to biogeographical regions (Hof et al., 2008), geological regions (Culver et al., 2003), or grid cells of 100e10,000 km 2 in size (most often 400 km 2 ; Christman et al., 2005;Niemiller and Zigler, 2013;Zagmajster et al., 2014;Eme et al., 2015Eme et al., , 2018Bregovi c et al., 2019). Not surprisingly, patterns of regional species richness and the mechanisms put forward to explain them are sensitive to the spatial grain size used to map species richness ( Fig. 6.4). ...
Understanding patterns of groundwater biodiversity is a challenging task because of the inherent difficulty in drawing links between environmental factors, eco-evolutionary processes, and patterns. Using studies in Europe, the Americas, and Australia, we focus on patterns that are common enough among taxonomic groups and continents in species richness and taxonomic composition of the groundwater fauna to be potentially recognized as “rules”. The obligate groundwater fauna is dominated by crustaceans, which represent 65%–78% of species at continental to global scales. Local species richness of groundwater species communities is low, at least compared to surface aquatic communities; however, regional to continental species richness is high due to strong spatial turnover characteristic of groundwater species composition. Macroecological studies have challenged the long-held view that historical factors primarily drive continental-scale patterns of regional species richness by reviving the importance of energy resources and spatial heterogeneity in controlling speciation and extinction. Aquifer properties, such as the size of voids, their interconnectedness, and hydrological connection to the surface environment, drive differences in species composition among localities of a region. Continental-scale patterns in community turnover may essentially be controlled by historical climates: species replacement is higher in European regions of stable climates where ecological and/or nonecological speciation events can accumulate over time, whereas community nestedness is higher in regions where variable climates can promote extinction and recolonization. However, we still lack a quantitative understanding of the contribution of environmental filtering and dispersal limitations to patterns of species richness and community turnover at regional to continental scales. Groundwater biologists are increasingly incorporating the phylogenetic and functional facets of biodiversity for understanding the mechanisms contributing to the assembly of communities. This multifaceted approach is revealing the importance of niche specialization and ecological specialization–dispersal trade-off in shaping geographic patterns of subterranean biodiversity.
... Typically, Collembola are considered able to disperse easily due to their ability to float on the surface of water and the possible use of the furcula for leverage and mobility. Individual species might therefore be regionally widespread; however, truly troglobitic/ cavernicolous species are potentially restricted in their distributions due to the highly specialised and isolating soil horizon that they occupy (Christman et al. 2005;Niemiller and Zigler 2013;Kováč et al. 2016;Fiera et al. 2018). ...
... Two of these genera occur in Western Australia (Greenslade 2002) including Pseudosinella Schäffer (Entomobryidae: Lepidocyrtini), a known troglobitic/cavernicolous genus (i.e., lacking eyes and pigment, possessing elongate legs, furca, and antennae) (e.g., Soto-Adames 2010), which has been found within the calcrete aquifers of the Yilgarn region. It is thought that a subterranean lifestyle restricts dispersal, with local adaptation and diversification being common in subterranean Collembola from other locations around the world (Christman et al. 2005;Soto-Adames 2010;Niemiller and Zigler 2013;Kováč et al. 2016;Fiera et al. 2018;B. Zhang et al. 2018;F. ...
... Local adaptation to favourable pockets of habitat are a common observation in less mobile species. For those that we have shown are trapped in the subterranean soil habitats above aquifers and show limited evidence of historical dispersal, we consider these restricted lineages biologically consistent with other collembolan groups (Christman et al. 2005;Niemiller and Zigler 2013;Kováč et al. 2016;Fiera et al. 2018). Whilst it is possible that we have not sampled these haplotypes well enough to detect long-distance gene flow and extensive sampling might reveal haplotypes with larger distributions, we observed that even well-sampled calcretes, such as SM and LDS, have restricted lineages (Table 1). ...
The subterranean islands hypothesis for calcretes of the Yilgarn region in Western Australia applies to many stygobitic (subterranean–aquatic) species that are “trapped” evolutionarily within isolated aquifers due to their aquatic lifestyles. In contrast, little is known about the distribution of terrestrial–subterranean invertebrates associated with the calcretes. We used subterranean Collembola from the Yilgarn calcretes to test the hypothesis that troglobitic species, those inhabiting the subterranean unsaturated (non-aquatic) zone of calcretes, are also restricted in their distribution and represent reciprocally monophyletic and endemic lineages. We used the barcoding fragment of the mtDNA cytochrome c oxidase subunit 1 (COI) gene from 183 individuals to reconstruct the phylogenetic history of the genus Pseudosinella Schäffer (Collembola, Lepidocyrtidae) from 10 calcretes in the Yilgarn. These calcretes represent less than 5% of the total possible calcretes in this region, yet we show that their diversity for subterranean Collembola comprises a minimum of 25 new species. Regionally, multiple levels of diversity exist in Pseudosinella, indicative of a complex evolutionary history for this genus in the Yilgarn. These species have probably been impacted by climatic oscillations, facilitating their dispersal across the landscape. The results represent a small proportion of the undiscovered diversity in Australia’s arid zone.
... Consequently, we expect differences in the pattern of richness and community structure between troglobionts that cannot survive outside caves and facultative cave dwellers (troglophiles) that might also occur in the matrix outside caves. Troglobionts should also tend to occur in restricted geographical areas (Christman et al., 2005). The high degree of habitat specialization in combination with stable habitat conditions may increase the role of competitive exclusion, leading to reduced local species richness compared to less specialized species (Cardoso, 2012). ...
... Niemiller & Zigler (2013) found that 24% of Tennessee cave arthropods are endemics to one single cave. Christman et al. (2005) reported between 23% and 67% single cave endemics of North American arthropods, with the highest proportions found for Arachnida and Coleoptera (> 40%), and the lowest proportions found for Collembola (23%). However, cave arthropods, and Collembola in particular, are taxonomically and ecologically still poorly studied, and probably still include numerous cryptic species. ...
... This high proportion of species with restricted distributions needs to be discussed in terms of extinction/speciation dynamics (Christman et al., 2005). Cave endemics show little ecological plasticity and are often unable to respond even to small environmental changes. ...
Geographical isolation, habitat quality and habitat size are known as driving factors shaping species communities and richness. We analysed cave-dwelling springtail communities from 187 caves of the Carpathian Mountains and the Dobrogea Region across Romania. These caves differ in size, geographical isolation, habitat heterogeneity and age, and in the surrounding environmental conditions. Based on these data we tested for potential effects of environmental factors on species composition and richness. Despite high species turnover we found that caves which are geographically close to each other, at similar altitudes and with similar climatic conditions tend to have a more similar species composition than expected from random colonization. Particularly important for current species spatial distributions were past (glacial) environmental conditions. We found that co-occurring species are taxonomically more clustered than expected by chance. In turn, species traits, namely dispersal ability and body size and shape, were only of minor influence and did not significantly affect community assembly. These findings are consistent with long-term isolation and cave specific speciation/extinction dynamics. Our study adds to the increasing evidence that isolated habitat islands might maintain a stable although species-poor fauna due to a trade-off between past colonization, speciation and extinction. © 2018 The Linnean Society of London, Biological Journal of the Linnean Society.
... The south-central Kentucky karst system is among the top 10 most endangered karst systems in the world (Romero, 2009), and the interior plateau is home to among the largest assemblages of obligate cave fauna in North America (Christman et al., 2005;Lewis and Lewis, 2005;Niemiller and Zigler, 2013). Further, eastern North American cave ecosystems are home to 170 described trechine cave beetle species with some endemic to single caves, as well as several critically endangered species (Barr, 1979;Christman et al., 2005). ...
... The south-central Kentucky karst system is among the top 10 most endangered karst systems in the world (Romero, 2009), and the interior plateau is home to among the largest assemblages of obligate cave fauna in North America (Christman et al., 2005;Lewis and Lewis, 2005;Niemiller and Zigler, 2013). Further, eastern North American cave ecosystems are home to 170 described trechine cave beetle species with some endemic to single caves, as well as several critically endangered species (Barr, 1979;Christman et al., 2005). North American cave beetles are extremely diverse, with over 250 species estimated in the genus Pseudanophthalmus alone (Peck, 1998). ...
Rising temperatures and diminishing groundwater availability due to the current climate crisis are predicted to expose cave faunas in eastern North America to unprecedented environmental conditions that could prove detrimental to their unique ecosystems. Organisms that inhabit relatively stable environments like caves are known to develop narrow physiological tolerances. Cave habitats with their organisms are simple ecosystems whose homogeneity offers an ideal system for testing the ability of a highly specialized fauna to tolerate abiotic changes. We tested the capability of a cave-specialized beetle in the eastern United States, Darlingtonea kentuckensis Valentine, to withstand future climatic shifts in its environment. We exposed individuals to a range of relative humidities and temperatures for 10 days. The data strongly suggest that there is a temperature threshold for the survival of D. kentuckensis, but it is a higher thermal tolerance than would be expected in an environment that has not fluctuated in recent evolutionary time and suggests remnant physiological characteristics of ancestral epigean carabids. Decreasing the relative humidity in the environment resulted in a much more dramatic decline in survival, indicating highly evolved specialization for constant high-humidity environments. The narrow humidity threshold in which troglobionts can survive may be a much more apparent limiting factor than temperature in adapting to climatic shifts within a cave environment.
... Unlike surface habitats, deep caves are completely devoid of sunlight, with neither photosynthesis nor plant growth, and have constant temperatures and a limited food supply (Culver & Pipan, 2009). Biologists have long been fascinated by the peculiarities of typical subterranean organisms (e.g., Darwin, 1859;Jeannel, 1943;Racovitza, 1907), especially troglobite animals (terrestrial troglobites and aquatic stygobites), as they can serve as models for understanding endemism and its causes (Christman et al., 2005). Cave invertebrates are classically categorized as troglobites, troglophiles, and trogloxenes. ...
... Most troglobites represent evolutionary products of separate invasions of surface-dwelling species rather than a single colonization followed by subsequent dispersal. Endemism may result, not from the lack of dispersal, but from subterranean dispersal followed by speciation (Christman et al., 2005). Allopatric speciation based on geographic isolation has been shown to occur among cave Collembola species (Katz et al., 2018). ...
en This paper provides an overview on troglobitic springtails found in European caves, including a checklist at species level. The paper also reviews what is currently known about Collembola, which occur in caves of the most important mountain ranges in Europe. Only troglobitic species were included since many troglophiles were of uncertain ecological status. A total of 338 troglobitic species of Collembola is recorded from European caves, distributed across 12 families. Spain and France appear to host the highest richness of species, including endemics. From a biogeographic perspective, troglobitic species are unevenly distributed in Europe, especially in the most important mountain ranges, like the Alps, the Carpathians, the Pyrenees, the Caucasus, and other European mountains. Troglobitic springtails are far more abundant in temperate zones than in the tropics. Despite this, several genera of Collembola appear to be well represented, while some are poorly represented (or lacking) in European caves. Many advances in knowledge of subterranean springtails have been made, particularly in the description of new species. However, there are still major gaps in the knowledge of the biology, environmental requirements, and impacts on subterranean fauna. This paper highlights the need for further research and provides baseline data for such efforts.
Resumen
es En este trabajo se proporciona una visión general de los colémbolos troglobios encontrados en las cuevas europeas, incluyendo un listado a nivel de especie. También se revisa lo que hasta ahora se conoce sobre los colémbolos que se encuentran en las cuevas de las cadenas montañosas más importantes de Europa. Se incluyen solamente las especies troglobias ya que el estado ecológico de muchos troglófilos es dudoso. Se registran 338 especies troglobias de Collembola en cuevas europeas, distribuidas en 12 familias. España y Francia parecen albergar la mayor riqueza de especies, incluidas las endémicas. Desde una perspectiva biogeográfica, las especies troglobias se distribuyen de forma desigual en Europa, especialmente en las cadenas montañosas más importantes, como los Alpes, los Cárpatos, los Pirineos, el Cáucaso y otras montañas europeas. Los colémbolos troglobios son mucho más abundantes en las zonas templadas que en los trópicos. A pesar de esto, varios géneros de Collembola parecen estar bien representados, mientras que otros están poco representados (o no existen) en las cuevas europeas. Últimamente se han realizado muchos avances en el conocimiento de los colémbolos subterráneos, particularmente en la descripción de nuevas especies. Sin embargo, aún existen importantes lagunas sobre su biología, los requisitos ambientales y los impactos sobre la fauna subterránea. Este trabajo destaca la necesidad de realizar más investigaciones y aporta datos de referencia en este sentido.
... However, in most cases, the tests of hypotheses related to the ecological patterns of subterranean communities have involved invertebrate fauna restricted to these environments (troglobites) [25][26][27] , strictly aquatic fauna (stygobites) 14,28,29 , or speci c taxonomic groups 30,31 . This leaves a huge gap that has not been extensively explored yet, regarding the search for more general patterns of subterranean fauna, composed mainly of organisms not restricted to subterranean environments 15 . ...
... To form spatial aggregations of caves based on the factors that best represent variations in compositional similarity, we explored ve different factors, both separately and combined, with their different number of levels in parentheses (infographic in gure 6): biogeographic domain (2), lithology (3), biome (5), ecoregion (16), and drainage basin (26). We have selected these ve factors due to their reported in uence on cave communities, where in some ways subterranean communities can be in uenced by cave lithology 37 ; by the regional pool of surface species 24 , an in uence that was tested here using the boundaries of the biogeographic domains, biomes, and ecoregions; and nally, by the drainage ows in the landscape, which in uence had been only reported acting on strictly aquatic cave organisms until then 29,54 . ...
Studies regarding macroecological patterns involving subterranean fauna are challenging, since the environments where such species are found generally do not have the same ecological patterns observed on the surface, due to their isolation. Therefore, using data on the occurrence of invertebrate families, we tested the influence of ecological regions already established for surface environments (biogeographic domains, biomes, and ecoregions), lithology, and drainage basins as potential drivers of the similarity on the invertebrates communities. We observed that within the surface ecoregions there might still be subdivisions due to different drainage basins, a pattern that was repeated in both aquatic and terrestrial fauna. Thus, we present different bioregions in the Afrotropics and Neotropics, in which caves have distinct faunistic identities. We discuss the biogeographic relationships between the epigean and hypogean environments that may be behind these patterns. We believe that these results can assist in conservation strategies, in which these different compositions are considered.
... Patterns of gene flow among caves in karst areas vary mostly in accordance with the geographical distribution of subterranean limestone (e.g., Caccone 1985, Katz et al. 2018. In limestone-rich parts of the Eastern United States (Fig. 1) where karst exposure is patchy, structurally fragmented, and discontinuous, caves are generally smaller and more isolated from one another (e.g., Currens 2002, Christman et al. 2005. One such region is the Appalachian Valley (AV), located primarily in eastern Tennessee and Virginia, which supports a high diversity of endemic cave beetles and other troglobites per unit area, many of which are limited in range to one or a few caves (Barr 1967, 1981, Christman et al. 2005, Niemiller and Zigler 2013. ...
... In limestone-rich parts of the Eastern United States (Fig. 1) where karst exposure is patchy, structurally fragmented, and discontinuous, caves are generally smaller and more isolated from one another (e.g., Currens 2002, Christman et al. 2005. One such region is the Appalachian Valley (AV), located primarily in eastern Tennessee and Virginia, which supports a high diversity of endemic cave beetles and other troglobites per unit area, many of which are limited in range to one or a few caves (Barr 1967, 1981, Christman et al. 2005, Niemiller and Zigler 2013. Conversely, troglobiotic invertebrates that inhabit large and highly interconnected cave systems which have permeated the large and uninterrupted exposures of limestone in the Mississippian Plateau (MP) region have comparatively broader ranges and less predictable distributional boundaries (e.g., Barr 1979). ...
Cave beetles of the eastern USA are one of many poorly studied groups of insects and nearly all previous work delimiting species is based solely on morphology. This study assesses genetic diversity in the monotypic cave carabid beetle genus Darlingtonea Valentine 1952, to test the relationship between putative geographical barriers to subterranean dispersal and the boundaries of genetically distinct groups. Approximately 400bp of the mitochondrial cytochrome oxidase I (COI) gene was sequenced from up to four individuals from each of 27 populations, sampled from caves along the escarpments of the Mississippian and Cumberland plateaus in eastern Kentucky, USA. The 81 individuals sequenced yielded 28 unique haplotypes. Hierarchical analyses of molecular variance (AMOVA) within and among geographically defined groups tested two a priori hypotheses of structure based on major and minor river drainages, as well as genetic distance clusters defined a posteriori from an unrooted analysis. High genetic differentiation (F ST ) between populations was found across analyses. The influence of isolation by distance could potentially account for much but not all of the variation found among geographically defined groups at both levels. High variability among the three northernmost genetic clusters (F CT ), low variability among populations within clusters (F SC ), and low within-cluster Mantel correlations indicate the importance of unidentified likely intra-karst barriers to gene flow separating closely grouped cave populations. Overall phylogeographic patterns are consistent with previous evidence of population isolation among cave systems in the region, revealing geographically structured cryptic diversity in Darlingtonea over its distribution. The landscape features considered a priori in this study were not predictive of the genetic breaks among the three northern clusters, which are genetically distinct despite their close geographic proximity.
... A striking characteristic of subterranean fauna is an exceptionally high proportion of extreme endemics, that is, species limited to few square kilometers or even one site Niemiller & Zigler, 2013;Trontelj et al., 2009;Zagmajster et al., 2014). For example, in different parts of United States, 20%-45% of subterranean species are single-site endemics (Christman, Culver, Madden, & White, 2005;Niemiller & Zigler, 2013), while in France, 38% of aquatic subterranean species have latitudinal linear range extents <3 km (Ferreira, Malard, Dole-Olivier, & Gibert, 2007). In general, aquatic subterranean species with linear range extents above 200 km are an exception (Copilaș-Ciocianu et al., 2017;Eme et al., 2018;Trontelj et al., 2009;Zagmajster et al., 2014). ...
... Note also that this effect is more pronounced in beetles overall species diversity (Bonn, Rodrigues, & Gaston, 2002), given that the areas of the highest species richness and the areas of the highest number of rare species do not always overlap (Orme et al., 2005). The problem is new to conservation of subterranean diversity, as hitherto studied hotspots contained also high shares of rare species (Christman et al., 2005;Niemiller & Zigler, 2013). ...
Aim:
Common species contribute more to species richness patterns (SRPs) than rare species in most studies. Our aim was to test this hypothesis using a novel model system, species living exclusively in subterranean habitats. They consist of mainly rare species (small ranges), only a few of them being common (large ranges), and challenge whether rare species are less important for the development of SRPs in this environment. We separately analyzed aquatic and terrestrial species.
Location:
Western Balkans in southeastern Europe.
Methods:
We assembled two datasets comprising 431 beetle and 145 amphipod species, representing the model groups of subterranean terrestrial and aquatic diversity, respectively. We assessed the importance of rare and common species using the stepwise reconstruction of SRPs and subsequent correlation analyses, corrected also for the cumulative information content of the subsets based on species prevalence. We applied generalized linear regression models to evaluate the importance of rare and common species in forming SRPs. Additionally, we analyzed the contribution of rare and common species in species-rich cells.
Results:
Patterns of subterranean aquatic and terrestrial species richness overlapped only weakly, with aquatic species having larger ranges than terrestrial ones. Our analyses supported higher importance of common species for forming overall SRPs in both beetles and amphipods. However, in stepwise analysis corrected for information content, results were ambiguous. Common species presented a higher proportion of species than rare species in species-rich cells.
Main conclusion:
We have shown that even in habitats with the domination of rare species, it is still common species that drive SRPs. This may be due to an even spatial distribution of rare species or spatial mismatch in hotspots of rare and common species. SRPs of aquatic and terrestrial subterranean organisms overlap very little, so the conservation approaches need to be habitat specific.
... For example, less than 7% of caves in Tennessee, the most cave-rich state in United States, have been surveyed for biological resources and even fewer have been repeatedly and comprehensively bioinventoried (Niemiller and Zigler 2013). Moreover, most troglobionts and stygobionts are endemic to a single site or known from very few (<5) cave systems (Christman et al. 2005;Deharveng et al. 2009;Niemiller and Zigler 2013) in a small geographical region (i.e., short-range endemism; Harvey 2002) and inherently assumed to be at higher extinction risk. However, uncertainly often exists whether such species are truly rare or if presumed rarity reflects inadequate surveying effort historically. ...
... First, P. alabamae may in fact be quite rare with an extremely restricted distribution. Many troglobionts and stygobionts are considered short-range endemics (sensu Harvey 2002) with small ranges and re-ported from a single or few cave systems (Christman et al. 2005;Niemiller and Zigler 2013;Niemiller et al. 2017). In Alabama alone, several species have more restricted ranges than P. alabamae, such as three cave crayfishes (Cooper and Cooper 1997a,b;Buhay and Crandall 2009), a cavefish (Cooper and Kuehne 1974), and several cave pseudoscorpions (Muchmore and Chamberlain 1995;Muchmore 1996) that are all single-site endemics. ...
The Alabama Cave Shrimp Palaemonias alabamae Smalley, 1961 is a federally endangered cave shrimp endemic to just four cave systems within and near the greater Huntsville metropolitan area in Madison County, Alabama USA. It is one of two described atyid cave shrimp in the Interior Low Plateau karst region. Here we report the discovery of a new population of P. alabamae from the Fern Cave system in western Jackson County, Alabama. We observed four cave shrimp in August 2018 in an isolated pool in the base-level stream passage of the longest cave system in Alabama. Two cave shrimp were observed during a subsequent survey in July 2019: one in the same isolated pool and a second shrimp in a pool in the main stream passage. Morphological and genetic analyses confirm that this population is closely allied with other populations in Madison County. This new population expands the known distribution of the species into a new county and watershed (Lower Paint Rock River). The potential exists to discover additional populations in Paint Rock River valley and other nearby regions.
... Understanding changes in conditions in these subterranean ecosystems is crucial, as karst and cave systems have unparalleled levels of endemism, with many karst systems hosting site endemic taxa (Christman et al., 2005;Nitzu et al., 2018). Caves also provide interesting sites for a multitude of fields, their isolation creating "island" ecosystems for evolutionary research. ...
... Several studies agree that caves contain some of the most vulnerable ecosystems on Earth (Noss & Peters, 1995;Elliott, 2000;Wynne & Pleytez, 2005;Wynne et al., 2007;Wood et al., 2008;Caraka et al., 2018;Reboleira et al., 2022), with numerous cave-dwelling organisms being endemic to a small region or even to a single cave (Barr & Holsinger, 1985;Reddell, 1994;Sarbu et al., 1996;Culver et al., 2000;Zhao et al., 2011;Monro et al., 2018;Nitzu et al., 2018). In times of rapid global climate and environmental change (Mannion, 2014;Rahmstorf & Schellnhuber, 2019;IPCC, 2021IPCC, , 2022, the relatively stable environmental and climatic conditions of caves increasingly make them refuge and archive for many endangered animal and plant species, which can no longer survive elsewhere (LaVal et al., 1977;Humphreys, 2000;Krajick, 2001;Christman et al., 2005;Judson, 2007). ...
... The distribution of three undescribed Pseudosinella species in southern karst areas contradicts the observation of Christman et al. (2005) that single-cave endemism is not high in isolated cave areas on the periphery. To obtain an overall picture, it is important to note that troglomorphic Pseudosinella representatives do not occur in the karst of the Tatras Mts. that form the northern ridges of the Western Carpathians (Kováč et al., 2016). ...
IntroductionUsing an integrative taxonomic approach, we investigated the morphological and molecular characters to identify the species of the genus Pseudosinella occurring in caves of the Western Carpathians and to clarify their phylogenetic relationships. Based on morphological characters, we hypothesized that Pseudosinella aggtelekiensis (Stach, 1929) and Pseudosinella paclti (Rusek, 1961) originated from different phyletic lineages.Methods
We used the barcoding fragment of the mtDNA COI gene from 87 individuals from 16 caves to reconstruct the phylogenetic history of the genus Pseudosinella.ResultsThe molecular phylogenetic tree revealed two distinct species groups with allopatric distributions. The first group consisted of P. aggtelekiensis populations from the Slovak Karst and three undescribed species from fragmented and isolated karst areas in southeastern Slovakia. The second group, P. paclti populations in the Central Western Carpathians, was merged. This group included Pseudosinellamuranensis, a new species taxonomically described in this work. It is characterized by highly developed troglomorphic features and is restricted to a small karst area, the Muranska planina Plateau. The phylogeny of the genus Pseudosinella from the caves of the Western Carpathians revealed a Miocene diversification. According to molecular calibration, the two distinct Pseudosinella lineages were separated in the Middle Miocene, about 14.51 Mya, followed by further diversification in the P. paclti lineage 10.89 Mya and in the P. aggtelekiensis lineage 11.14 Mya.DiscussionThis phylogeny is consistent with the uplift of Triassic limestones during the early formation of the Western Carpathians in the Paratethys region and the initial development of caves during this period. The study provides further important evidence that the Western Carpathians played a significant role as an independent speciation center of the obligate cave fauna in Europe.
... Similar abiotic conditions in different cave systems have resulted in convergent evolution of troglobitic species spanning the kingdom Animalia (Barr & Holsinger, 1985;Mammola & Isaia, 2017). These animals possess similar traits, such as unpigmented skin and non-functional eyes (Christman et al., 2005;Culver & Pipan, 2015). Dispersal into caves and selection for traits required to live in these extreme environments are driving forces of speciation, ecologically isolating these populations from their surfacedwelling relatives (Christiansen, 1961;Barr & Holsinger, 1985;Strecker et al., 2012). ...
Insular habitats have played an important role in developing evolutionary theory, including natural selection and island biogeography. Caves are insular habitats that place extreme selective pressures on organisms due to the absence of light and food scarcity. Therefore, cave organisms present an excellent opportunity for studying colonization and speciation in response to the unique abiotic conditions that require extreme adaptations. One vertebrate family, the North American catfishes (Ictaluridae), includes four troglodytic species that inhabit the karst region bordering the western Gulf of Mexico. The phylogenetic relationships of these species have been contentious, and conflicting hypotheses have been proposed to explain their origins. The purpose of our study was to construct a time-calibrated phylogeny of Ictaluridae using first-occurrence fossil data and the largest molecular dataset on the group to date. We test the hypothesis that troglodytic ictalurids have evolved in parallel, thus resulting from repeated cave colonization events. We found that Prietella lundbergi is sister to surface-dwelling Ictalurus and that Prietella phreatophila + Trogloglanis pattersoni are sister to surface-dwelling Ameiurus, suggesting that ictalurids colonized subterranean habitats at least twice in evolutionary history. The sister relationship between Prietella phreatophila and Trogloglanis pattersoni may indicate that these two species diverged from a common ancestor following a subterranean dispersal event between Texas and Coahuila aquifers. We recovered Prietella as a polyphyletic genus and recommend P. lundbergi be removed from this genus. With respect to Ameiurus, we found evidence for a potentially undescribed species sister to A. platycephalus, which warrants further investigation of Atlantic and Gulf slope Ameiurus species. In Ictalurus, we identified shallow divergence between I. dugesii and I. ochoterenai, I. australis and I. mexicanus, and I. furcatus and I. meridionalis, indicating a need to reexamine the validity of each species. Lastly, we propose minor revisions to the intrageneric classification of Noturus including the restriction of subgenus Schilbeodes to N. gyrinus (type species), N. lachneri, N. leptacanthus, and N. nocturnus.
... La fragmentation de la distribution et les faibles capacités de dispersion Exemplaire réservé à Isabel Sanmartin conduisent à une forte structuration des populations chez les organismes souterrains, comme cela a été démontré dans de nombreux groupes tels que les coléoptères (Faille et al. 2015 ;Balogh et al. 2020 ;Boyd et al. 2020) ou les amphipodes Niphargus (Lefébure et al. 2007). Cela souligne le rôle clé tant de la vicariance que de la dispersion dans le façonnement des patrons biogéographiques actuels observés chez la faune souterraine (Christman et al. 2005 ; Jurado-Rivera et al. 2017). ...
Les progrès récents des méthodes d’analyse en biologie, impliquant différentes disciplines, ouvrent un large panel d’études qui fait aujourd’hui de la biogéographie une approche intégrative de l’évolution du vivant. En tant que telle, la biogéographie va bien au-delà d’une simple description de la répartition des espèces vivantes sur Terre.La biogéographie est une discipline où écologistes et évolutionnistes cherchent à comprendre la manière dont les espèces vivantes s’organisent en relation avec leur environnement. Face aux défis majeurs tels que le réchauffement climatique, l’extinction massive d’espèces ou les pandémies, la biogéographie fournit les éléments indispensables à l’élaboration des solutions.La biogéographie présente un large aperçu des différents domaines de cette discipline. Les auteurs internationaux y développent différentes analyses sur la base de leurs connaissances et de leur expérience, illustrant les vastes domaines couverts par la biogéographie.
... Three additional subterranean-adapted species occurred in multiple caves with maximum distances ranging from 81.27 and 137.6 km ( Table 3). As many troglomorphic arthropods are identified as short-range endemic species, occurring in a single cave or geological formation (Reddell 1994, Culver et al. 2000, Christman et al. 2005, Deharveng et al. 2008, Tian 2011, Harvey and Wynne 2014, Gao et al. 2018, Nitzu et al. 2018 and that rivers and valleys/ lowland areas often result in vicariance (Barr 1985, Faille et al. 2015, Katz et al. 2018, the genetic relatedness of at least these three species should be further examined using genetic techniques. While these species may be morphological similar, we suggest they may be genetically distinct -potentially representing different subspecies or lineages. ...
We synthesized the current knowledge of cave-dwelling millipede diversity from Guangxi Zhuang Autonomous Region (Guangxi), South China Karst, China and described six new millipede species from four caves from the Guilin area, northeastern Guangxi. Fifty-two cave-dwelling millipedes are known for the region consisting of 38 troglobionts and 14 troglophiles. Of the troglobionts, 24 are presently considered single-cave endemics. New species described here include Hyleoglomerisrukouqu sp. nov. and Hyleoglomerisxuxiakei sp. nov. (Family Glomeridae), Hylomusyuani sp. nov. (Family Paradoxosomatidae), Eutrichodesmusjianjia sp. nov. (Family Haplodesmidae), Trichopeltisliangfengdong sp. nov. (Family Cryptodesmidae), and Glyphiulusmaocun sp. nov. (Family Cambalopsidae). Our work also resulted in range expansions of Pacidesmustrifidus Golovatch & Geoffroy, 2014, Blingulussinicus Zhang & Li, 1981 and Glyphiulusmelanoporus Mauriès & Nguyen Duy-Jacquemin, 1997. As with many hypogean animals in Southeast Asia, intensive human activities threaten the persistence of both cave habitats and species. We provide both assessments on the newly described species’ distributions and recommendations for future research and conservation efforts.
... Species inhabiting subterranean waters are usually isolated, with a limited capacity of dispersal. These conditions may drive large differences in species composition between regional sites (high β diversity) [10,11]. Speciation and endemicity are therefore common in these environments and are promoted by events such as vicariance and spatial ecological partition of the environment [11][12][13]. ...
We studied benthic assemblages through X-Batún, a continental freshwater cenote and its associated submerged cave located in San Antonio Mulix (Yucatán, Mexico). Using cave diving techniques, we collected sediment samples at four zones of the system. We extracted and counted individuals of benthic species in three replicates of 5 grams of wet sediment at each site. The biological composition was integrated by 15 species from eight higher taxonomic groups. Non-metric multidimensional scaling distinguished four assemblages that coincided with surface, open water, cavern and cave zones. ANOSIM test revealed significant differences between the assemblages. In the deeper zones of the cenote characterized by twilight and total darkness, Ostracoda and Gastropoda show the highest diversity and abundance, with practical absence in surface sediments. This pattern may suggest ecological interactions with chemosynthetic bacterial activity. Surface shows an assemblage typical of epigean environments. Environmental variables along the cenote varied little from the upper layers to bottom. Linear correlation and detrended canonical analysis revealed that light is the main driver of benthic species assemblages. Temperature, pH, and dissolved oxygen exert higher influence at individual biological benthic assemblage in X-Batún.
... Fragmentation of the distribution and low dispersal abilities lead to strong population structure in cave biota, as evidenced in many groups such as beetles (Faille et al. 2015;Boyd et al. 2020;Balogh et al. 2020) or Niphargus amphipods (Lefébure et al. 2007). This suggests that both vicariance and dispersal have a key role in shaping the current biogeographic patterns observed in the subterranean fauna (Christman et al. 2005;Jurado-Rivera et al. 2017). ...
Freshwater ecosystems occupy only 2.3% of Earth's surface, yet they support an excessive portion of the world's most speciose and endemic taxa. They are estimated to harbor 12% of the world's fauna and one third (18,000 species) of the global vertebrate species richness. In this chapter, the author draws together threads of recent theoretical and empirical results and patterns at multiple scales; both may offer a useful roadmap of theoretical background for identifying new paths of investigation and future challenges into the field of freshwater biogeography, which needs to be considered to safeguard the status of aquatic ecosystems. Neotropics and Afrotropics are among the global hotspots of freshwater fish endemism. Recent findings in freshwaters underscore the importance of studying simultaneously historical processes, drainage basin characteristics and local environmental conditions to understand variation in species richness. Freshwater species richness and endemism patterns are the result of climate, productivity and biogeographical history.
... Caves also represent important habitats for cave-restricted animals. These systems often support troglomorphic (subterranean-adapted) species with narrow geographic ranges (i.e., occurring within a single cave or watershed [6][7][8][9][10][11][12][13][14][15]) and are often represented by small populations [16,17]. Cave entrances have also been identified as important habitats for relict arthropod species from the last glaciation [18][19][20][21][22] and extensive surface disturbance [23][24][25]. ...
Since the initial experiments nearly 50 years ago, techniques for detecting caves using airborne and spacecraft acquired thermal imagery have improved markedly. These advances are largely due to a combination of higher instrument sensitivity, modern computing systems, and processor intensive analytical techniques. Through applying these advancements, our goals were to: (1) Determine the efficacy of methods designed for terrain analysis and applied to thermal imagery; (2) evaluate the usefulness of predawn and midday imagery for detecting caves; and (3) ascertain which imagery type (predawn, midday, or the difference between those two times) was most informative. Using forward stepwise logistic (FSL) and Least Absolute Shrinkage and Selection Operator (LASSO) regression analyses for model selection, and a thermal imagery dataset acquired from the Mojave Desert, California, we examined the efficacy of three well-known terrain descriptors (i.e., slope, topographic position index (TPI), and curvature) on thermal imagery for cave detection. We also included the actual, untransformed thermal DN values (hereafter "unenhanced thermal") as a fourth dataset. Thereafter, we compared the thermal signatures of known cave entrances to all non-cave surface locations. We determined these terrain-based analytical methods, which described the "shape" of the thermal landscape hold significant promise for cave detection. All imagery types produced similar results. Down-selected covariates per imagery type, based upon the FSL models, were: Predawn-slope, TPI, curvature at 0 m from cave entrance, as well as slope at 1 m from cave entrance; midday-slope, TPI, and unenhanced thermal at 0 m from cave entrance; and difference-TPI and slope at 0 m from cave entrance, as well as unenhanced thermal and TPI at 3.5 m from cave entrance. Finally, we provide recommendations for future research directions in terrestrial and planetary cave detection using thermal imagery.
... Thus, it is worth noting that both species described in this study show high abundance in their type-localities, which are not effectively protected. Cave habitats have characteristics that favor high endemism, with species being restricted even to a single cave (Christman et al., 2005;Trajano & Bichuette 2010;Trajano et al., 2016;Gallão & Bichuette 2018), as seems to be the case of both species described in this study. However, caves can be threatened by diverse human activities, including tourism, mining, agriculture or livestock, deforestation, causing changes in the hydrical conditions and water pollution in the surroundings and other nearby caves (Gallão & Bichuette 2018). ...
The diversity of freshwater triclads of the suborder Continenticola in the Neotropical region is poorly known, with few studies in South America. In this work, we describe two new cave-dwelling species of Girardia: G. corumbataiensis sp. nov. is described from a single sandstone cave located in an area covered by semi-deciduous vegetation, southeastern Brazil; G. nobresis sp. nov. is described from a single flooded limestone cave located in an area of Cerrado vegetation, central-western Brazil. Specimens of G. corumbataiensis sp. nov. have a slight pigmented dorsal surface with highly triangular head and two eyes, whereas specimens of G. nobresis sp. nov. lack body pigmentation and eyes and have pointed auricles. Girardia corumbataiensis sp. nov. shows a pear-shaped bulbar cavity with forked portions turned dorsally and a slightly bent bursal canal. Girardia nobresis sp. nov. has an ample bulbar cavity with numerous folds and an angled bursal canal. The two new species are categorized as troglobites and easily recognized by a unique combination of characters of their external morphology and copulatory apparatus. G. corumbataiensis sp. nov. occurs in a cave inserted in a protected area, but no effective action for preservation has been provided. This species is abundant in a single stream crossing the cave, which is subject to intensive visitation and control of bat populations, besides Eucalyptus plantations nearby. The type-locality of G. nobresis sp. nov., a single flooded cave near a municipal road, has no legal protection. There are impacts, such as intensive visitation for fishing and deforestation in its surroundings.
... Species inhabiting subterranean waters are usually isolated, with a limited capacity of dispersal. These conditions may drive large differences in species composition between regional sites (high β diversity) [10,11]. Speciation and endemicity are therefore common in these environments and are promoted by events such as vicariance and spatial ecological partition of the environment [11][12][13]. ...
The Yucatán Peninsula is a karstic region, rich in subterranean environments with a diverse crustacean stygobiont fauna. In order to gain insights into the biological evolution of the subterranean environments of this region, we evaluated the ostracode species composition of caves and cenotes in five independent sampling campaigns (2008, 2013, 2017–2019). Using morphometric analyses, we evaluated inter-population morphological variability; using molecular analysis based on mitochondrial COI and nuclear 18S rDNA, we evaluated genetic differentiation in selected species. The observed fauna is composed of 20 (epigean) species, presenting a lack of strict stygobionts. Morphometric analyses discriminated up to three morphotypes in each of the three most abundant species: Cytheridella ilosvayi, Alicenula sp. and Cypridopsis vidua. High intraspecific morphological variability was found either in shape or size. Phylogenetic analysis based on COI demonstrated the existence of three lineages on C. ilosvayi, with high support (>0.9). The 18S rDNA sequences were identical among individuals of different populations. A lack of congruence between the genetic markers precluded us from postulating speciation in subterranean environments. It is likely that Late Pleistocene—Early Holocene climate variation related to sea level and precipitation was forcing agent for epigean ostracode dominance in subterranean environments of the Peninsula.
... Cave ecosystems and the associated species are considered particularly vulnerable to anthropogenic impacts (Furey and Racey, 2016;Medellín et al., 2017;Smith and Burns, 2011;. Their clumped distribution within landscapes has given rise to extraordinary levels of endemism, particularly that of troglobites characterized by limited dispersal (Christman et al., 2005;Medellín et al., 2017). As a consequence of manifold human pressures, not only changes in water flow regimes, groundwater pollution, novel microclimate patterns, fragmentation, and destruction of the surface ecosystems, but also doline recreational use, soil erosion, mining, and vandalism are detrimental to cave ecosystems (Silva et al., 2015;Furey and Racey, 2016;Phelps et al., 2016;Medellín et al., 2017;Cajaiba et al., 2016). ...
Neotropical caves located in pristine ecosystems harbor high biodiversity but face functional shifts and degradation interlinked with aboveground changes. Cave-roosting bats have been proposed as integrity indicators of karst landscapes considering their sensitive to both the underground and aboveground characteristics and resources. In the present study, the selection of caves by bats in karst areas across a landscape gradient in the Brazilian Amazon was investigated. We envisioned that taxonomic and guild diversity should respond dissimilarly to disturbance at different scales, namely by a selective offsetting of the bat community. To test our hypothesis , we accordingly selected caves spanning a gradient of disturbance, located in old growth forests, secondary forests, forest fragments, agricultural landscapes, and pastures. Species and traits showing responses to the gradient of caves and aboveground ecosystems were identified. On the basis of patterns of occurrence, we determined those communities unique to or primarily associated with undisturbed caves located in pristine ecosystems and landscapes. Disturbed caves, which are generally located in areas of agriculture and pastures, were found to have detrimental effects on specialized species and functional guilds diversity. Our preliminary results reveal that bat communities are particularly sensitive to gradients of cave and ecosystem disturbance, and consequently might add ecological information to the currently used indicators for assessing the ecological status of landscapes in the Neotropics.
... As caves are colonized by surface species capable of overcoming cave environmental filters (Rivera et al., 2002;Wessel et al., 2013), richer epigean areas may therefore present richer caves, in both temperate and Neotropical areas. Hence, the limits proposed for ecoregions, which were primarily based on epigean attributes (such as richness and composition of distinct communities), can also be significant for Neotropical cave communities, as already shown in temperate regions (Christman et al., 2005;Moldovan et al., 2018;Niemiller & Zigler, 2013). ...
Aim: In addition to cave size and other subterranean habitat characteristics, cave entrances are important structurers of neotropical cave communities. However, little is known about the epigean ecosystems factors that might dictate the influence of entrances and the relationship among surface and cave communities, as entrance regions are ecotonal zones between the epigean and hypogean ecosystems. We aimed to assess the influence of epigean and hypogean factors as potential drivers of invertebrate species richness in Neotropical caves as well as the influence of the regional pool of invertebrate diversity on cave invertebrate diversity. Location: Limestone caves in southeastern Brazil. Taxon: Invertebrates Methods: Data were collected in 48 caves within the Cerrado biome (Brazilian Savanna). The fauna sampling was performed by a direct intuitive search (DIS). Landscape characteristics and climatic parameters were accessed using geographic information systems. The characterization of the caves occurred during each sampling event. Regional diversity was based on the Taxonomic Catalog of Brazilian Fauna. To clarify the factors that significantly influence invertebrate species richness of the caves, we used generalized linear models (GLM). The relationship between regional diversity and cave diversity was evaluated based on linear models (LM). Results: Overall, 1,173 species were found, of which 72 were obligate subterranean dwellers. The cave total species richness was influenced by hypogean factors and epigean factors. The species richness of obligate cave dwellers was significantly explained only by cave size. The regional pool of invertebrate species influenced the levels of biodiversity in the studied caves. The taxa with troglobitic species tended to be more diverse in caves than expected. Main conclusions: In addition to the influences of intrinsic cave variables, we highlight the importance of epigean factors on subterranean diversity in the Neotropics. The study shows the significant influence of the regional species pool on cave faunal composition. These findings reinforce the importance of considering the surrounding areas in actions regarding cave biodiversity conservation. K E Y W O R D S cave, diversity, ecology, invertebrates, karst, speleobiology
... To investigate spatial patterns in endemism, species are often weighted by the inverse of their range (1 / number of grid cells occupied by an organism; Crisp et al. 2001, Kessler 2002, Christman et al. 2005, Zuloaga et al. 2019. When summed for all species in a cell of a defined area, the resulting metric is called weighted endemism (Crisp et al. 2001). ...
... Concordantly, litter species in Alabama are comparatively rare, and the local fauna of Anillinus is dominated by representatives of the subterranean lineages, especially those from cave habitats. The dominant role of the troglobitic lineages when compared to other lineages of Anillinus is also in accord with the fact that Alabama has one of the highest diversities of troglobitic arthropods in the USA (Peck 1989(Peck , 1995(Peck , 1998, and is considered to be one of the hotspots of cave endemism (Christman et al. 2005;Culver et al. 2006). Taking in account that subterranean fauna of Anillinus is insufficiently explored and more new species are to be discovered, the proportion of endemics in faunas of Tennessee and North Carolina may grow up in the future. ...
Four new species of anilline ground beetles are described from Alabama. Two species from Jackson County, Anillinus clinei new species, and Anillinus folkertsioides new species, are troglobitic and litter species, respectively. Anillinus hildebrandti new species, is a troglobitic species from a cave in Morgan County. Anillinus humicolus new species, from Jefferson County is supposedly an endogean species. All new species are illustrated with images and drawings; a distribution map and a modified key to the Alabama species are provided. With these new discoveries, the known fauna of Anillinus of Alabama now includes twelve species. Species compositions of Anillinus based on habitat preferences of taxa satisfactorily explain the variations in total species numbers and number of endemics among Alabama and other eastern American states.
... Troglobionts typically exhibit high rates of endemism (Christman et al., 2005), and we noted this pattern in the Georgia fauna. Seventeen of the 51 (33 %) troglobionts known from Georgia are endemic to the state ( Table 2). ...
We provide an annotated checklist of species recorded from caves and other subterranean habitats in the state of Georgia, USA. We report 281 species (228 invertebrates and 53 vertebrates), including 51 troglobionts (cave-obligate species), from more than 150 sites (caves, springs, and wells). Endemism is high; of the troglobionts, 17 (33 % of those known from the state) are endemic to Georgia and seven (14 %) are known from a single cave. We identified three biogeographic clusters of troglobionts. Two clusters are located in the northwestern part of the state, west of Lookout Mountain in Lookout Valley and east of Lookout Mountain in the Valley and Ridge. In addition, there is a group of tro-globionts found only in the southwestern corner of the state and associated with the Upper Floridan Aquifer. At least two dozen potentially undescribed species have been collected from caves; clarifying the taxonomic status of these organisms would improve our understanding of cave biodiversity in the state. Conservation concerns related to species found in Georgia caves are significant, with fourteen species (including 13 vertebrates) considered "High Priority Spe-cies" under the Georgia State Wildlife Action Plan, many of these species have additional state or federal protections. In addition, 17 invertebrate troglobionts (33 % of those known in the state) are considered "Critically Imperiled" by Nature-Serve. Several biologically important caves are not protected, these are an important conservation concern. However, remarkably, around one third of all caves in the state are on protected lands, including seven of the eight caves known to host ten or more troglobionts.
... In contrast to their surface relatives, many cave-dwelling species have morphological, physiological, and behavioral adaptations that limit or prevent surface dispersal (White & Culver, 2012). Often restricted to small, discontinuous ranges, these species can exhibit high levels of population structure, short-range endemism, and morphologically cryptic species (e.g., Christman et al., 2005;Zagmajster et al., 2008;Niemiller et al., 2012;Faille et al., 2015). ...
Vicariance and dispersal are major drivers of the evolution of biodiversity, yet the relative impact of these processes, and the factors that influence them, often remain elusive. Identifying and understanding evolutionary processes responsible for generating diversity is essential for understanding ecological patterns and for the development and implementation of management strategies intended to conserve biodiversity. My dissertation research is focused on the historical, ecological and evolutionary underpinnings driving the origin, diversification, and maintenance of biodiversity in springtails (Collembola). This class of tiny, wingless insect-like hexapods includes some of the most abundant (and perhaps, most diverse) arthropods on earth. They have colonized, diversified, and adapted to nearly every terrestrial habitat from marine intertidal zones and tropical rainforests to polar deserts and caves, yet the evolutionary mechanisms behind their ecological success are poorly understood.
Ecological specialization is a central theme in my first two chapters. Species with obligate ecological associations offer simple systems to evaluate biogeographical hypotheses and also provide an ecological context to test the effects and consequences of specialization on patterns of diversity. In Chapter 1, I identify and compare spatial and temporal patterns of molecular diversity for two ecologically distinct and codistributed genera of cavernicolous springtails (cave-obligate vs. cave-facultative species) from a regional cave-bearing karst system spanning the Mississippi River in Illinois and Missouri. Phylogeographic analysis revealed that evolutionary processes of vicariance and dispersal were both major influences on patterns of cave springtail diversity, but the effects of these processes are also strongly influenced by intrinsic ecological factors, in this case, the degree of cave-dependence. Estimates of genetic structure and divergence times also implicated climatic and geological processes involved in the formation of the modern Mississippi River valley as major factors driving the isolation of cave-obligate species, but cave-facultative species have been able to maintain genetic connectivity across this barrier.
In Chapter 2, I developed a molecular dataset for marine littoral-obligate springtails collected along the Pacific and Atlantic coasts of Panama to identify transisthmian sister taxa, determine processes driving and maintaining their isolation, and to evaluate their timing of origin. I was able to identify multiple geminate species pairs spanning the Isthmus and molecular analyses revealed examples of pre-Pliocene vicariance, post-closure dispersal, and cryptic diversification across the Isthmus of Panama. This study not only demonstrates that ecological specialization can (but not always) reduce genetic connectivity across geographic barriers, but also corroborates recent (and controversial) geological and biogeographical estimates of an early Miocene closure of the Panama Isthmus.
These works demonstrate the utility of incorporating ecologically specialized springtails in evolutionary investigations. However, independent timing information is essential for assessing historical factors influencing contemporary patterns of diversity. Unfortunately, springtails (and most other small, soft-bodied organisms) lack a useful fossil record for this purpose. As a result, employing “universal” rates of molecular evolution to estimate divergence times is common, even though evolutionary rates can vary considerable across taxa. In Chapter 3, I assess the validity of the generalized arthropod rate assumption by conducting a Bayesian phylogenetic analysis to evaluate the relative rate of molecular evolution across all major hexapod groups. I found that substitution rates in Collembola are not significantly different from most other hexapod groups and suggest that the use of “universal” insect molecular clocks are appropriate for estimating collembolan evolutionary timescales. An additional yet fundamental challenge impacting all fields of biology is the fact that most biodiversity remains to be discovered or is poorly understood—including many species that are of potential conservation concern. This is exacerbated in collembolan taxonomy, due to the lack of variation in discrete morphological characters, and the general shortage of taxonomic expertise in North America, reflected in the limited number of taxonomic tools available to researchers (and the public) for identifying species in this region. To help address this challenge, I produced detailed morphological taxonomic descriptions for all New World species of the springtail genus Willowsia, including a new species that is endemic to Florida in Chapter 4. Most members in this genus are from Asia, but comparative morphological analysis revealed two unique character states shared only by endemic New World Willowsia and Americabrya, providing prima facie evidence of their independent evolution from a common New World ancestor.
... There are at least two caves within a radius of 5 km in the Magang cave, and at least three caves in the radius of 5 km in the Shenxian cave. As with many subterranean-adapted taxa (e.g., Culver et al., 2000;Christman et al., 2005;Kováč et al. 2005;Borges et al. 2012), these two pseudoscorpion species may indeed have restricted distributions. However, they may have wider distributions than a single cave and are likely restricted to a geologic formation rather than the caves in which they were found. ...
Two new troglomorphic pseudoscorpion species, Parobisium magangensis sp. n. and P. yuantongi sp. n., belonging to the family Neobisiidae, are described based on specimens collected in karst caves from Beijing, China. These are the first troglomorphic pseudoscorpions discovered from caves in northern China. Detailed diagnosis, descriptions, and illustrations are provided. We also offer future research and management recommendations for these two new pseudoscorpion species.
... Consequently, the subterranean fauna mostly depends on organic matter input from surface habitats (Gers, 1998;Poulson & Lavoie, 2000) and is generally poorly diversified (Gibert & Deharveng, 2002). In spite of this, numerous investigations have disclosed a much higher biodiversity and a higher degree of endemism among subterranean species than predicted previously (e.g., Christman et al., 2005;Culver & Sket, 2000;Deharveng et al., 2012;Elliott, 2000;Peck, 1998;Pipan & Culver, 2007a, 2007bReboleira et al., 2011;Zagmajster et al., 2008). ...
Troglobionts are organisms that are specialized for living in a subterranean environment. These organisms reside prevalently in the deepest zones of caves and in shallow subterranean habitats, and complete their entire life cycles therein. Because troglobionts in most caves depend on organic matter resources from the surface, we hypothesized that they would also select the sections of caves nearest the surface, as long as environmental conditions were favorable. Over 1 year, we analyzed, in monthly intervals, the annual distributional dynamics of a subterranean community consisting of 17 troglobiont species, in relation to multiple environmental factors. Cumulative standardized annual species richness and diversity clearly indicated the existence of two ecotones within the cave: between soil and shallow subterranean habitats, inhabited by soil and shallow troglobionts; and between the transition and inner cave zones, where the spatial niches of shallow and deep troglobionts overlap. The mean standardized annual species richness and diversity showed inverse relationships, but both contributed to a better insight into the dynamics of subterranean fauna. Regression analyses revealed that temperatures in the range 7–10°C, high moisture content of substrate, large cross section of the cave, and high pH of substrate were the most important ecological drivers governing the spatiotemporal dynamics of troglobionts. Overall, this study shows general trends in the annual distributional dynamics of troglobionts in shallow caves and reveals that the distribution patterns of troglobionts within subterranean habitats may be more complex than commonly assumed.
... Three additional subterranean-adapted species occurred in multiple caves with maximum distances ranging from 81.27 and 137.6 km ( Table 3). As many troglomorphic arthropods are identified as short-range endemic species, occurring in a single cave or geological formation (Reddell 1994, Culver et al. 2000, Christman et al. 2005, Deharveng et al. 2008, Tian 2011, Harvey and Wynne 2014, Gao et al. 2018, Nitzu et al. 2018 and that rivers and valleys/ lowland areas often result in vicariance (Barr 1985, Faille et al. 2015, Katz et al. 2018, the genetic relatedness of at least these three species should be further examined using genetic techniques. While these species may be morphological similar, we suggest they may be genetically distinct -potentially representing different subspecies or lineages. ...
We synthesized the current knowledge of cave-dwelling millipede diversity from Guangxi Zhuang Autonomous Region (Guangxi), South China Karst, China and described six new millipede species from four caves from the Guilin area, northeastern Guangxi. Fifty-two cave-dwelling millipedes are known for the region consisting of 38 troglobionts and 14 troglophiles. Of the troglobionts, 24 are presently considered single-cave endemics. New species described here include Hyleoglomeris rukouqu sp. nov. and Hyleoglomeris xuxiakei sp. nov. (Family Glomeridae), Hylomus yuani sp. nov. (Family Paradoxosomatidae), Eutrichodesmus jianjia sp. nov. (Family Haplodesmidae), Trichopeltis liangfengdong sp. nov. (Family Cryptodesmidae), and Glyphiulus maocun sp. nov. (Family Cambalopsidae). Our work also resulted in range expansions of Pacidesmus trifidus Golovatch & Geoffroy, 2014, Blingulus sinicus Zhang & Li, 1981 and Glyphiulus melanoporus Mauriès & Nguyen Duy-Jacquemin, 1997. As with many hypogean animals in Southeast Asia, intensive human activities threaten the persistence of both cave habitats and species. We provide both assessments on the newly described species’ distributions and recommendations for future research and conservation efforts.
... In Japan, several centipede species can be found in both the inside and outside cave, and Shinohara (1966) referred two species were considered to be troglobiotic centipedes; Brachygeophilus polyporus Takakuwa, 1942 (Geophilomorpha) and Monotarsobius minor Takakuwa, 1942 (Lithobiomorpha). Commonly, the troglobiotic fauna has a high proportion of endemic species in each cave or cave group (Gibert and Deharveng 2002;Christman et al. 2005). Many endemic species with small geographic ranges may occur in isolated caves (Barr Jr and Holsinger 1985); therefore, the inventory of the troglobiotic fauna is important to clarify the formulation of endemism. ...
Arrupakiyoshiensis Tsukamoto & Shimano, sp. n. is described from a limestone cave, Kagekiyo-ana, in Akiyoshi-dai, one of the largest karst regions in Japan, Yamaguchi prefecture. It is distinguishable from 14 valid named congeners by some unique characteristics including entire areolation on the cephalic pleurite, elongation of distal part of female gonopod, and a tubercle on forcipular segment II. In addition, the 18S rRNA gene sequences of A.akiyoshiensis Tsukamoto & Shimano, sp. n. and A.ishiianus , one of the most morphologically similar species, differed by four bp out of 1821 bp. The fact that only troglobionts and troglophilic species are found in the collection site suggests that this new species might be a cave-dweller.
... First, most subterranean species are geographically rare, often having small, highly restricted geographic ranges (Culver et al. 2006;Zagmajster et al. 2008;Deharveng et al. 2009;Gallão and Bichuette 2018). These animals often are endemic to a single or few cave systems (Christman et al. 2005;Deharveng et al. 2009;Niemiller and Zigler 2013). Many species also may be numerically rare. ...
We review significant conservation and management legislation, policies, and other actions that have been implemented or proposed to protect and conserve subterranean biodiversity in Europe, North America, Central America, and South America. In particular, we focus on legislation at the national and international levels that has been passed or proposed to directly or indirectly protect subterranean biodiversity. Other conservation initiatives, such as the IUCN Red List and NatureServe conservation assessment, also have conservation implications for to subterranean biodiversity. However, there remain several limitations of legislation, policies, and other initiatives to protect and conserve subterranean biodiversity on these continents. Several suggestions are set forth to overcome these shortcomings and better facilitate subterranean biodiversity conservation in Europe, North America, Central America, and South America.
... In other words, it is theoretically expected that communities in caves relatively close to each other should exhibit faunal differences. The high level of endemism of most subterranean species seems to confirm this hypothesis in most cases (Sharratt et al. 2000;Christman et al. 2005). ...
Despite subterranean communities being relatively simple, their precise characterization still represents an interesting ecological challenge. This is mostly because, due to the inaccessibility of most subterranean habitats, the spatial boundaries and the species composition of the communities are difficult to define. In this chapter, we describe the general structure and composition of a cave community, keeping in mind different theoretical approaches. We discuss how spatial and temporal turnover occur within most cave biocoenosis, leading to complex species interactions among the resident species. Particular attention is paid to characterizing the ecological niche and the interspecific competition dynamics in cave ecosystems, showing how competition often arises from niche overlaps in species exploiting similar resources and microhabitats. The use of caves as model systems to study basic ecological concepts such as communities, niche, and species interactions has great potential for advancing ecological knowledge.
... Western Carpathian distributions, were smaller compared to more tolerant groups with broad distribution ranges (Cosmopolitan, Holarctic, Palearctic, European and Carpathian distributions). Generally, specialised obligate subterranean species tend to have small distribution ranges (Christman et al., 2005;Culver and Pipan, 2009) and show a high level of endemism (e.g. Bregović and Zagmajster, 2016;Nitzu et al., 2018). ...
... Formam ambientes únicos, com uma fauna peculiar, consideradas sítios de especial interesse científico, apresentando uma fauna frágil e vulnerável aos impactos causados no ambiente físico por interferências de ações humanas ou fenômenos naturais (ALVES, 2007;CAJAIBA, 2013). Os animais que ali habitam são limitados em sua capacidade de dispersão, devido à descontinuidade no habitat apropriado e, como consequência, apresentam altos níveis de endemismos (CHRISTMAN et al., 2005). São particularmente vulneráveis à perturbação por causa de sua raridade em habitats (SLANEY; WEINSTEIN, 1997), por isso a necessidade de divulgação desse potencial para a sociedade e sua devida proteção (CAJAIBA, 2012). ...
graduação (lato sensu) em Ciências Biológicas, Mestre em Engenharia do Ambiente pela Utad/Portugal, Doutorando em Ambiente e Desenvolvimento pela Univates. reinaldocajaiba@hotmail.com RESUMO Este trabalho teve como objetivo avaliar os principais impactos ambientais existentes em sete cavernas no município de Uruará-PA. Os dados foram compilados numa matriz de Leopoldo, o qual leva em consideração a frequência, duração, extensão, reversibilidade, origem, sentido e o grau de impacto. Como resultado, encontraram-se ações de grandes impactos, como queimadas, trilhas, compactação do solo, erosão, desmatamentos, visitação turísticas desordenadas, presença de lixo, poluição luminosa, atividades madeireira, desvio curso d'água e atividades agropecuárias. Nossos resultados sugerem que sejam implantados programas de Educação Ambiental para concientização da população e dos proprietários dos imóveis rurais onde as cavernas estão localizadas, além de maior controle e fiscalização por parte dos gestores públicos para proteção desses ambientes, junto com a implantação de projetos de recuperação das áreas já degradadas. Palavras-chave: Diagnóstico Ambiental. Impacto cavernícola. Conservação. ABSTRACT This study aimed to assess the main environmental impacts in seven caves on Uruará-PA. The data were compiled in a Leopold's matrix, which takes into account the frequency, duration, extent, reversibility, origin, direction and degree of impact. As a result, we found high-impact actions such as fire, trails, soil compaction, erosion, deforestation, disordered sightseeing, presence of litter, light pollution, logging activities, diversion of watercourses and agricultural activities. The results suggest that should be displayed environmental education programs to raise awareness on population and the owners of rural properties where the caves are located, greater control and supervision of public managers to protect these environments and the implementation of projects for recovering degraded areas. RESUMEN Este estudio tuvo como objetivo evaluar los principales impactos ambientales en siete cuevas existentes en el municipio de Uruará-PA. Los datos fueron compilados en una matriz de Leopold, que tiene en cuenta la frecuencia, la duración, el alcance, la reversibilidad, origen, dirección y el grado de impacto. Como resultado,
... This pattern is empirically confirmed by the documented greater proportion of subterranean endemic species relative to their surface counterparts (e.g. Sharratt et al. 2000;Christman et al. 2005;Cardoso 2012;Niemiller and Zigler 2013;Wynne et al. 2014). Nevertheless, mechanisms other than geographic isolation have sometimes been invoked to explain the origin of subterranean organisms (Juan et al. 2010). ...
Speciation in subterranean habitats is commonly explained as the result of divergent selection in geographically isolated populations; conversely, the contribution of niche partitioning in driving subterranean species diversification has been rarely quantified. The present study integrated molecular and morphological data with a hypervolume analysis based on functional traits to investigate a potential case of parapatric speciation by means of niche differentiation in two sibling spiders inhabiting contiguous subterranean habitats within a small alpine hypogean site. Troglohyphantes giachinoi, sp. nov. and T. bornensis are diagnosed by small details of the genitalia, which are likely to be involved in a reproductive barrier. Molecular analysis recovered the two species as sister, and revealed a deep genetic divergence that may trace back to the Messinian (~6 million years ago). The hypervolume analysis highlighted a marginal overlap in their ecological niches, coupled with morphological character displacement. Specifically, T. giachinoi, sp. nov. exhibits morphological traits suitable for thriving in the smaller pores of the superficial network of underground fissures (Milieu Souterrain Superficiel, MSS), whereas T. bornensis shows a greater adaptation to the deep subterranean habitat. Our results suggest that different selective regimes within the subterranean environment, i.e. deep caves v. MSS, may either drive local speciation or facilitate contiguous distributions of independently subterranean adapted species.
Caves host a wide variety of highly adapted endemic species which are vulnerable to disturbances and environmental changes, but are poorly understood, especially for the conditions, past and current, that affect their distribution. Particularly intriguing for biogeography are the freshwater cave-dwelling isopods of the genus Monolistra, which are spread in numerous karst areas from the south-eastern parts of Dinaric karst to south-eastern Switzerland. They inhabit different typologies of groundwater habitats, where they can be an important fraction of the biomass. The aims of this study are: to perform an extensive and repeated survey to characterise the microhabitats use of the westernmost populations of this genus, which have never been thoroughly investigated; to assess if these isopods can resist long periods of droughts; to study the habitat suitability for this genus in Italy; to understand which past and current conditions better explain their distribution.
From November 2021 to February 2023, I surveyed multiple times 13 caves, divided into 42 plots, in the western part of the Monolistra range (Val d’Intelvi and surroundings, including Monte Generoso and Monte Bisbino, between Italy and Switzerland). Occupancy models were used to estimate the relationships between environmental covariates, detection probability and occupancy in the surveyed caves. In 5 of these caves and in 3 caves near the town of Erba (Como district), during the drought of Spring 2022, I performed rinsing tests of individuals found in dried sectors. Occurrences of different Monolistra species in Italy were retrieved for the period 1934-2023, by personal observations and review of academic and grey literature. Species distribution models were used to establish relationships between environmental variables and species occurrences. Qualitative maps of the Last Glacial Maximum and of the shoreline during Miocene were produced.
Caves surveys revealed that detection probability was influenced by hour and date, with higher probabilities in the morning and early summer. The plots that were connected to a larger part of the aquifer and without light from outside had a higher probability to be occupied. A new behaviour was recorded: during the drought of Spring 2022, all the individuals found in dry areas were rolled up and completely motionless above the substrate, with 72 % of the individuals able to reactivate; the percentage of reactivated individuals was negatively related to the estimated time of dryness but not with sex; individuals that experienced longer dryness took longer to reactivate. The presence of carbonate rocks strongly drove the habitat suitability, which had as well a positive relationship with vegetation and temperature, and a negative relationship with climatic instability; habitat suitability resulted generally high in all the carbonate Prealps.
Two new populations in close geographic proximity were discovered in the western part of the range, and genetic analyses are still necessary, along with the other westernmost populations. The fact the detection probability was influenced by microclimatic conditions suggests sensitivity to small variations in the generally constant cave climate. Even if the rolling-up capability allowed resistance to droughts, prolonged variations and perturbations of subterranean aquifers can affect the survival of groundwater invertebrates. My results show that current ecological conditions strongly affect freshwater cave-dwelling isopods, both at the microhabitat scale and at a broader scale, with their distribution shaped by current conditions and by palaeogeographic history, including survival in glacial refugia.
Karst systems represents a typical dissolution morphology, frequently present in carbonate-type rocks, with significant water activity. Due to the large number of resources and services it provides and because it is widely distributed on our planet, it has become the source of many resources for human beings, making it a precious but vulnerable element. In the present work, the level of disturbance and impact existing in six karstic sites of two municipalities located in the Amazon region (Archidona) and Litoral (Pedro Carbo) of the Republic of Ecuador, was analyzed. Both municipalities are different, due to their geographical location, geological origin and age of the calcareous rocks that make up the dissolution areas, however presented the same relative impacts and uses of karst. Evaluation matrices for Karst Disturbance Index (KDI) were applied, with which it was known that the disturbance levels correspond to relatively low valuations, coinciding with the evolutionary levels of karst, which defined that the study areas correspond to young and juvenile karst elements. Was observed that there are currently low levels of degradation of the karst, however recommended to establish specific conservation strategies for the karst in the future, to strengthen its protection against the tourist activities that are constantly developed in the karst sites of both municipalities.
Background
Caves are special natural laboratories for most biota and the cave communities are unique. Establishing population in cave is accompanied with modifications in adaptability for most animals. To date, little is known about the survival mechanisms of soil animals in cave environments, albeit they play vital roles in most terrestrial ecosystems. Here, we investigated whether and how gut microbes would contribute to the adaptation of earthworms by comparing the gut microbiome of two earthworm species from the surface and caves.
Results
Two dominant earthworm species inhabited caves, i.e., Allolobophora chlorotica and Aporrectodea rosea . Compared with the counterparts on the surface, A. rosea significantly decreased population in the cave, while A. chlorotica didn’t change. Microbial taxonomic and phylogenetic diversities between the earthworm gut and soil environment were asynchronic with functional diversity, with functional gene diversity been always higher in earthworm gut than in soil, but species richness and phylogenetic diversity lower. In addition, earthworm gut microbiome were characterized by higher rrn operon numbers and lower network complexity than soil microbiota.
Conclusions
Different fitness of the two earthworm species in cave is likely to coincide with gut microbiota, suggesting interactions between host and gut microbiome are essential for soil animals in adapting to new environments. The functional gene diversity provided by gut microbiome is more important than taxonomic or phylogenetic diversity in regulating host adaptability. A stable and high-efficient gut microbiome, including microbiota and metabolism genes, encoded potential functions required by the animal hosts during the processes of adapting to and establishing in the cave environments. Our study also demonstrates how the applications of microbial functional traits analysis may advance our understanding of animal-microbe interactions that may aid animals to survive in extreme ecosystems.
The subterranean environment comprises voids of any size in which life can develop in aphotic, aseasonal and largely oligotrophic conditions. A small proportion of living organisms have been able to evolve and adapt to such conditions. Some of them have become strictly dependent on this harsh environment, at the price of a set of profound biological adaptations. Key new discoveries shed light on ancient biogeographical patterns but challenge our views regarding the origin and history of the extant fauna, as illustrated by the recently discovered monospecific genus Iberotrechodes in a cave in Cantabria, Spain. Vicariance by plate tectonics remains the main explanatory factor for the amphi‐Atlantic distribution displayed by many groups of subterranean Crustacea. An accurate knowledge of subterranean diversity at the species level, combined with a comprehensive overview of the geological and paleoclimatic histories of the areas of interest, is a prerequisite to the understanding of biogeographic patterns.
The subterranean aquatic snails may serve as a model of endemism and isolation vs. migration in subterranean habitats. The aim of the present paper is to verify the hypothesis that subterranean aquatic snails can migrate through diverse subterranean habitats, applying four molecular markers as well as a RAPD technique and shell morphometry. They were used to estimate the differences and gene flow between populations of the hydrobiid subterranean aquatic species Montenegrospeum bogici, collected in the Dinaric karst region. Three molecularly distinct taxonomic units were distinguished. The mOTU B was found at single locality, mOTU C at two, but the mOTU A at ten localities, scattered along 236 km distance, at two of them in sympatry with either mOTU B or C. Within mOTU A, the estimated levels of the gene flow were high. The pairwise measures of genetic differentiation were statistically significantly associated with geographic distances between the populations. In general, neither the infinite-island model of interpopulation differentiation, expected for isolated populations, nor the stepping-stone one, but rather the isolation-by-distance model explained the observed pattern. Our results suggest that interstitial habitats provide ways of migration for the stygobiont M. bogici, as has been already suggested for other subterranean gastropods.
Biogeography is a multidisciplinary field that is concerned with delimiting and explaining the geographic distributions of organisms in space and time. Due to their distribution patterns and interesting biology (e.g., ancient lineage with a nearly cosmopolitan distribution, sedentary lifestyle with limited dispersal capabilities), tarantulas are an appealing taxonomic group for addressing a variety of biogeographic questions concerning the Earth’s history. In this chapter, we discuss some biogeographic basic concepts, delve into the distribution patterns of New World tarantulas, and explore some of the historical explanations that may have led to these distributions. We mostly review and highlight the results of recent studies but also include personal observations and unpublished data. The distributions of higher-level taxonomic groups (subfamilies and tribes) are described and we detail their latitudinal and elevational limits. We also review the distributions of groups with unique insular habitats such as those found on islands surrounded by seas, forested “islands” surrounded by “seas” of deserts, and caves. Furthermore, we discuss the distribution of some unique morphological characters of taxonomic importance such as urticating setae. Finally, we review a handful of studies that have explicitly investigated the biogeography of New World tarantulas using a variety of different analytical methods.
Background. Aquatic subterranean species often exhibit disjunct distributions, with high level of endemism and small range, shaped by vicariance, limited dispersal, and evolutionary rates. We studied the disjunct biogeographic patterns of an endangered blind cave shrimp, Typhlocaris , and identified the geological and evolutionary processes that have shaped its divergence pattern.
Methods. We collected Typlocaris specimens of three species ( T. galilea , T. ayyaloni , and T. salentina ), originating from subterranean groundwater caves by the Mediterranean Sea, and used three mitochondrial genes (12S, 16S, COI) and four nuclear genes (18S, 28S, ITS, H3) to infer their phylogenetic relationships. Using the radiometric dating of a geological formation (Bira) as a calibration node, we estimated the divergence times of the Typhlocaris species and the molecular evolution rates.
Results. The multi-locus ML/Bayesian trees of the concatenated seven gene sequences showed that T. salentina (Italy) and T. ayyaloni (Israel) are more closely related than T. galilea (Israel). The divergence time of T. ayyaloni and T. salentina from T. galilea was according to COI – 6.0 [4.5-7.2] Ma and according to 16S – 5.9 [3.6-7.4] Ma. The computed interspecific evolutionary rates for COI – 0.0074 substitutions/Myr and for 16S – 0.0041 substitutions/Myr.
Discussion. Two consecutive vicariant events have shaped the phylogeographic patterns of Typhlocaris species. First, T. galilea was tectonically isolated from its siblings in the Mediterranean Sea by the arching uplift of the central mountain range of Israel ca. 7 Ma. Secondly, T. ayyaloni and T. salentina were stranded and separated by a marine transgression ca. 6 Ma, occurring just before the Messinian Salinity Crisis. Our estimated molecular evolution rates were in one order of magnitude lower than the rates of closely related crustaceans, as well as of other stygobiont species. We suggest that this slow evolution reflects the ecological conditions prevailing in the highly isolated subterranean enclosures inhabited by Typhlocaris .
Caves offer selective pressures that are distinct from the surface. Organisms that have evolved to exist under these pressures typically exhibit a suite of convergent characteristics, including a loss or reduction of eyes and pigmentation. As a result, cave-obligate taxa, termed troglobionts, are no longer viable on the surface. This circumstance has led to an understanding of highly constrained dispersal capabilities, and the prediction that, in the absence of subterranean connections, extreme genetic divergence between cave populations. An effective test of this model would involve (1) common troglobionts from (2) nearby caves in a cave-dense region, (3) good sample sizes per cave, (4) multiple taxa, and (5) genome-wide characterization. With these criteria in mind, we used RAD-seq to genotype an average of ten individuals of the troglobiotic spider Nesticus barri and the troglobiotic beetle Ptomaphagus hatchi, each from four closely located caves (ranging from 3 to 13 km apart) in the cave-rich southern Cumberland Plateau of Tennessee, USA. Consistent with the hypothesis of highly restricted dispersal, we find that populations from separate caves are indeed highly genetically isolated. Our results support the idea of caves as natural laboratories for the study of parallel evolutionary processes.
Caves offer selective pressures that are distinct from the surface. Organisms that have evolved to exist under these pressures typically exhibit a suite of convergent characteristics, including a loss or reduction of eyes and pigmentation. As a result, cave-obligate taxa, termed troglobionts, are no longer viable on the surface. This circumstance has led to a ″caves as islands″ model of troglobiont evolution that predicts extreme genetic divergence between cave populations even across relatively small areas. An effective test of this model would involve (1) common troglobionts from (2) nearby caves in a cave-dense region, (3) good sample sizes per cave, (4) multiple taxa, and (5) genome-wide characterization. With these criteria in mind, we used RAD-seq to genotype an average of ten individuals of the troglobiotic spider Nesticus barri and the troglobiotic beetle Ptomaphagus hatchi , each from four closely located caves (ranging from 3-13 km apart) in the cave-rich southern Cumberland Plateau of Tennessee, USA. Consistent with the caves as islands model, we find that populations from separate caves are indeed highly genetically isolated. In addition, nucleotide diversity was correlated to cave length, suggesting that cave size is a dominant force shaping troglobiont population size and genetic diversity. Our results support the idea of caves as natural laboratories for the study of parallel evolutionary processes.
We summarize and discuss the 29 known cave-dwelling pseudoscorpion species from China. Four new troglomorphic pseudoscorpion species, Parobisium motianense sp. nov., P. qiangzhuang sp. nov., P. san- louense sp. nov., and P. tiani sp. nov., belonging to the family Neobisiidae, are described based on speci- mens collected in karst caves in Guizhou, China. Detailed diagnosis, descriptions, and illustrations are presented. We also provide recommendations for management of caves where they occur, as well as the cave arthropod communities and the habitats that support them.
Ever-increasing human pressures on cave biodiversity have amplified the need for systematic, repeatable, and intensive surveys of cave-dwelling arthropods to formulate evidence-based management decisions. We examined 110 papers (from 1967 to 2018) to: (i) understand how cave-dwelling invertebrates have been sampled; (ii) provide a summary of techniques most commonly applied and appropriateness of these techniques, and; (iii) make recommendations for sampling design improvement. Of the studies reviewed, over half (56) were biological inventories, 43 ecologically focused, seven were techniques papers, and four were conservation studies. Nearly one-half (48) of the papers applied systematic techniques. Few papers (24) provided enough information to repeat the study; of these, only 11 studies included cave maps. Most studies (56) used two or more techniques for sampling cave-dwelling invertebrates. Ten studies conducted ≥10 site visits per cave. The use of quantitative techniques was applied in 43 of the studies assessed. More than one-third (42) included some level of discussion on management. Future studies should employ a systematic study design, describe their methods in sufficient detail as to be repeatable, and apply multiple techniques and site visits. This level of effort and detail is required to obtain the most complete inventories, facilitate monitoring of sensitive cave arthropod populations, and make informed decisions regarding the management of cave habitats. We also identified naming inconsistencies of sampling techniques and provide recommendations towards standardization.
In the last two decades, there has been a substantial progress in the availability of records for several subterranean taxa, as well as in mapping and statistical modeling of biodiversity patterns. Currently, there is still a large bias toward analyses of aquatic compared to terrestrial subterranean taxa. We provide the first global map of species richness for groundwater crustaceans, indicating that tropics are not hotspots of species richness. Detailed analyses of subterranean biodiversity patterns in Europe show that species richness peaks in regions of mid-latitude, where the beneficial effects of a high productive energy and high habitat heterogeneity have not been counteracted by cold or arid historical events. The range size of European groundwater crustacean species increases northward, a pattern which is best explained by long-term climatic changes. Subterranean species have narrow distribution ranges, which results in a high spatial turnover in species composition across regions and a disproportionally high contribution of regional diversity to total species richness. Within regions, biodiversity patterns are diverse, and their explanations vary across regions, but hotspots contribute only a small proportion of the regional species pool. Molecular approaches to biodiversity studies offer promising research avenues for further documenting and understanding subterranean biodiversity patterns.
Energy (carbon) availability is considered the primary mechanism influencing both evolutionary and ecological processes in cave ecosystems, and both experimental and observational studies broadly support this hypothesis. However, we suggest that this conceptual model overlooks several factors that also influence cave community dynamics. In this chapter we explore these additional factors in two types of cave food webs, those supported by energy from detritus (dead animal or plant matter) and chemolithoautotrophic bacteria. We begin by examining the origin of each energy source and then explore what factors influence the input and/or productivity rates of each energy source, including the strength of surface connectivity, the productivity of surface habitats, and the compounds available for oxidation. We then explore how several factors are influencing cave community dynamics, including resource quantity and quality, size of resource surpluses, spatial distribution of resources, consumer-resource stoichiometry, top-down forces, and the relative harshness of certain cave environments. We hope this discussion both provides a broad overview of how food web dynamics influence cave community structure and highlights areas of future research.
Stygobites are thought to be wider ranging than troglobites in the contiguous 48 United States. This
assumption is confirmed by showing that stygobite species are recorded from more counties than troglobite
species (Mann Whitney U = 80189, Z = −6.781, P < 0.0001). The properties of water flow through
caves may allow greater dispersal opportunities for stygobites above the normal water table during
floods and could be one reason for the larger ranges of these species.
A comprehensive environmental monitoring program based on a sound statistical design is necessary to provide estimates of the status of, and changes or trends in, the condition of ecological resources. A sampling design based upon a systematic grid can adequately assess the condition of many types of resources and retain flexibility for addressing new issues as they arise. The randomization of this grid requires that it be regular and retain equal-area cells when projected on the surface of the earth. After review of existing approaches to constructing regular subdivisions of the earth's surface, we propose the development of the sampling grid on the Lambert azimuthal equal-area map projection of the earth's surface to the face of a truncated icosahedron fit to the globe. This geometric model has less deviation in area when subdivided as a spherical tessellation than any of the spherical Platonic solids, and less distortion in shape over the extent of a face when used for a projection surface by the Lambert azimuthal projection. A hexagon face of the truncated icosahedron covers the entire conterminous United States, and can be decomposed into a triangular grid at an appropriate density for sampling. The geometry of the triangular grid provides for varying the density, and points on the grid can be addressed in several ways.
In recent years a number of methods have been developed for subdividing the surface of the earth to meet the needs of applications in dynamic modeling, survey sampling, and information storage and display. One set of methods uses the surfaces of Platonic solids, or regular polyhedra, as approximations to the surface of the earth. Diamond partitions are similar to recursive subdivisions of the triangular faces of either the octahedron or icosahedron. This method views the surface as either four (octahedron) or ten (icosahedron) tessellated diamonds, where each diamond is composed of two adjacent triangular faces of the figure. The method allows for a recursive partition on each diamond, creating nested sub-dimaonds, that is implementable as a quadtree, including the provision for a Peano or Morton type coding system for addressing the hierarchical pattern of diamonds and their neighborhoods, and for linearizing storage. Furthermore, diamond partitions, in an aperture-4 hierarchy, provide direct access through the addressing system to the aperture-4 hierarchy of hexagons developed on the figure. Diamond partitions provide a nested hierarchy of grid cells for applications that require nesting and diamond cells have radial symmetry for those that require this property. Finally, diamond partitions can be cross-referenced with hierarchical triangle partitions used in other methods.
Two troglobitic fishes of conservation concern that inhabit Missouri are the Ozark and southern cavefishes, Amblyopsis rosae and Typhlichthys subterraneus, respectively. These species inhabit the groundwater of karstified bedrock in the Springfield and Salem plateau regions of the state, respectively. These two areas differ substantially – geographically, geologically, and hydrologically. This paper explores how these differences interact in shaping (1) the habitat in which these two species dwell, (2) the resulting ecological constraints that the fishes face, (3) how their ecologies and populations reflect these constraints, and (4) how conservation and management efforts may need to be tailored to best compliment the unique challenges that each species presents.
Caves harbor a rich fauna unique to subterranean environments. Although extensive records of cave animals are available, only a small fraction of known caves in any region have been biologically assessed. We investigated the impact of incomplete sampling using one of the richest, best documented cave faunas in the world – that of the Dinaric karst of Slovenia. We utilized time snapshots (1940, 1970, and 2000) of the caves and cave fauna to analyze stability of hotspots, spatial pattern, and relationship between number of species and number of caves. Using data aggregated into 100km2 hexagons, the location of hotspots, black–white joins, Moran's I, and spatial autocorrelation all remained constant, at least from 1970 on. The linear regression coefficient of the relationship between number of caves and number of species declined with time. Most hexagons had been sampled, but there was no indication that any hexagon had been sampled intensively enough for the accumulation curve of number of caves versus number of species within a hexagon to reach an asymptote. This appeared to be the result of a highly skewed distribution of species richness among caves. Number and position of hotspots can be predicted from information on these few high diversity caves.
This chapter briefly reviews all subphyla and classes of Arthropoda, with its nearly one million described species, and provides information about major arthropod taxa not covered in other entries of this encyclopedia. It also discusses aspects of arthropod evolutionary relationships, diversity, anatomy, physiology, and ecology. The preponderance of molecular evidence links arthropods with other phyla that must shed their cuticle during ecdysis to grow. This clade of “Ecdysozoa” also includes the phyla Tardigrada, Onychophora, Nematoda, and Nematomorpha, along with the more distantly related Priapulida and Kinorhyncha. Arthropoda is a more diverse phylum than any other living or extinct animal taxon. Counted among this immense assemblage are spiders, ticks, millipedes, butterflies, beetles, ants, silverfish, fairy shrimp, barnacles, sea spiders, lobsters, pill bugs, and many other common animals–—too numerous to mention. They colonize virtually every conceivable habitat–—from the equator to the poles, from high mountains to deep ocean trenches, and from rain forests to deserts and hot springs–—and fill all consumers food web levels. Except for molluscan cephalopods, arthropods surpass all invertebrates in internal organ complexity. Although they are a coelomate phylum, the coelom no longer functions as a hydrostatic skeleton but persists only as a cavity surrounding reproductive and/or excretory organs.
Speoplatyrhinus poulsoni, n. gen., n. sp., is a distinctive troglobitic (obligate cavernicole) fish of the family Amblyopsidae. It is known from 9 specimens, all collected at the type locality, a cave in northwestern Alabama where it is apparently an endemic relict. Among its unique morphological features are a long, anteriorly-depressed head with flat snout, absence of bifurcate fin rays, notably incised fin membranes, and unusual size, number and arrangement of caudal sensory papillae. The type locality supports a comparatively diverse aquatic fauna, a rich terrestrial fauna (especially guanobies), and a summer colony of an aggregative species of bat.
The geographic variation of 25 populations of the troglobitic collembolan Pseudosinella hirsuta was analyzed. Preliminary studies showed 12 cave-dependent (convergent) and three cave-independent (non-convergent) features with significant geographic variation. All cave-dependent features for each cave population show similar states of advanced or primitive cave adaptation, with the exception of the extremely phenoplastic mesothorax. On this basis each population can be placed in one of several sequences of advanced to primitive conditions. Each sequence is largely or entirely limited to a single geological region with a single evolutionarily advanced region, and one to five, generally marginal, primitive regions. The cave-independent features do not follow the same pattern, but do give some indication of decreasing variability from the advanced to the primitive populations. Each sequence of caves contains within it most or all of the variation seen within the species. The main conclusions from this study are as follows: 1) The characteristics of P. hirsuta have evolved independently in at least four different places. 2) Similarly, P. christianseni represents a continuation of the evolutionary trends seen in P. hirsuta and this form has also evolved independently in at least four different places. 3) Dispersal of P. hirsuta occurred primarily via underground routes. 4) There is no indication of morphological discontinuity between populations of a given cave sequence. 5) There is morphological evidence for genetic discontinuity between different cave sequences. 6) The nature of the deduced genetic interchange, and the precise morphological parallelisms makes the biological species concept inapplicable in this group. The morphological species concept is applied and is envisioned here not merely as a useful taxonomic device, but as a functional evolutionary unit.
The species Ligidium longicaudatum Stoller is shown to be a synonym of L. elrodii Packard, and four new subspecies of L. elrodii are described from caves in eastern United States. The other species of the genus and the general trend towards cave adaptation among the species and subspecies are discussed. Three common species not adapted to caves were also encountered in the caves.
The distributions ojenearly 45,000 caves and 924 obligate cave species and subspecies (stygobites and troglobites) in the 48 contiguous states of the United States were mapped by county. Both maps show a highly clumped distribution. Approximately one-half of the variance in the number of species in a county is explained by variance in the number of caves per county. While several maps of karst and pseudo-karst areas of the 48 contiguous states are available, most notably that of Davies et al. (1986) and its variants (Culver 1999), we know of no similar map of cave locations. We have a special interest in the distribution of caves since we have compiled a list of the oblig-ate cave-dwelling species by county for each of the 3100 coun-ties in the 48 contiguous states (available at www.karstwa-ters.org). In particular, we were interested in the explanatory power the distribution of caves has in accounting for the distri-bution of obligate cave-dwelling species. Therefore, we have assembled data on the number of caves by county, based on information in the National Speleological Society cave fries and from records of state cave surveys. The list includes not only solution caves, but lava tubes, sea caves, etc. The purpose of this brief communication is to present dot maps of the distribution of caves by county and the distribution of obligate cave species by county, and briefly to compare the two. A more complete analysis of the spatial distribution of cave species will appear elsewhere at a later date. The maps presented below were generated using the Geographic Information System software package, MapView . Each cave (or species) in a county is represented by a dot so that, for example, a county with 10 caves has 10 dots. The position of the dot within the county is assigned at random by MapView . While this produces some loss of accuracy, it also ensures that no precise location information can be determined from the maps. For some counties, the number of caves is so great that the dots completely fill the county, and individual dots are indistinguishable and superim-posed. Figure 1. Dot map of the number of caves per county. Each dot represents one cave. Figure 2. Dot map of the number of stygobites and troglo-bites per county. Each dot represents one county record of a stygobite or troglobite.
AimThe goal of this study was to determine the role habitat availability plays in the distribution of obligate subterranean cave fauna in eastern North America.LocationThe numbers of stygobites, troglobites and caves in the counties of the south-eastern USA were analysed.Methods
The data were characterized by large numbers of zeroes and by spatial clustering of non-zeroes in five regions. Regression and conditional autoregressive (CAR) models were used to elucidate the patterns and relationships between numbers of species and numbers of caves both locally and regionally.ResultsLocal effects (regions and numbers of caves in counties) accounted for 45% of the variation in troglobite counts (P=< 0.001) and 24% of the variation in stygobite counts (P=< 0.001). Significant spatial autocorrelation among both stygobites and troglobites (P=< 0.0001) was found as well.Conclusion
Overall, habitat availability as measured by cave numbers influenced species richness. Spatial and regional effects also played an important role in determining the observed distributions of the subterranean fauna. Terrestrial and aquatic communities showed very different patterns in their relationship to habitat and within the different regions.
The following description deals with a unique genus of small, eyeless ground beetle, a single specimen of which was taken by the author from a tiny cave near Lewisburg, W. Va. Situated in the valley of the Greenbrier River, this cave is in richly cavernous country featuring numerous sink-holes, tunnellike subterranean waterways and passages—caverns in early stages of formation. The author has visited 7 of the many caves known to occur within 20 miles of this spot, but in spite of diligent searches and extensive trapping here and elsewhere, no second representative of the genus has yet been brought to light. Since the habits of this beetle are not sufficiently well known to assure the collector of success in its capture, and because it is such an aberrant form, the author has taken the liberty of presenting it from the material at hand—a single, perfect male specimen.
Thesis (Ph. D.)--Old Dominion University, 1997. Includes bibliographical references.
Karst hydrology atlas of West Virginia Stygobites are more wide-ranging than troglobites
- Elsevier
- Amsterdam
- W K Jones
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- J Lamoreux
Elsevier, Amsterdam. Jones, W.K. (1997) Karst hydrology atlas of West Virginia. Special Publication 4, Karst Waters Institute, Charles Town, WV. Lamoreux, J. (2004) Stygobites are more wide-ranging than troglobites. Journal of Cave and Karst Studies, 66, 18–19.
Colonization. Encyclopedia of cave and karst science
- F Stoch
Stoch, F. (2004) Colonization. Encyclopedia of cave and karst science (ed. by J. Gunn), pp. 235–238.
Spatial processes, models and applications. Pion Limited Speoplatyrhinus poulsoni, a new genus and species of subterranean fish from Alabama
- A D Cliff
- J K Ord
Cliff, A.D. & Ord, J.K. (1981) Spatial processes, models and applications. Pion Limited, London. Cooper, J.E. & Kuehne, R.E. (1974) Speoplatyrhinus poulsoni, a new genus and species of subterranean fish from Alabama.
III (2005) Crustacea. Encyclopedia of caves Ecological derivation, colonization, and speciation. Subterranean ecosystems
- H H Hobbs
Hobbs, H.H., III (2005) Crustacea. Encyclopedia of caves (ed. by D.C. Culver and W.B. White), pp. 141–153. Elsevier Academic Press, Burlington, MA. Holsinger, J.R. (2000) Ecological derivation, colonization, and speciation. Subterranean ecosystems (ed. by H. Wilkens, D.C. Culver and W.F. Humphreys), pp. 399–415.
Onychophora, encyclopaedia biospeologica, tome I
- H Ruhberg
Ruhberg, H. (1994) Onychophora, encyclopaedia biospeologica,
tome I (ed. by C. Juberthie and V. Decu), pp. 81-85. Société
de Biospéologie, Moulis, France.
Diversity patterns in the tropics. Encyc-lopedia of caves
- L Deharveng
Deharveng, L. (2005) Diversity patterns in the tropics. Encyc-lopedia of caves (ed. by D.C. Culver and W.B. White), pp.
Biospé. La biologie des animaux caver-nicoles. Gauthier-Villars Global grids from recursive diamond sub-divisions of an octahedron or icosahedron. Environmental Monitoring Assessment
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Endemism in cave fauna Vandel, A. (1964) Biospé. La biologie des animaux caver-nicoles. Gauthier-Villars, Paris. White, D. (2000) Global grids from recursive diamond sub-divisions of an octahedron or icosahedron. Environmental Monitoring Assessment, 64, 93–103.
Niphargobates orophobata n. gen. n. sp. (Amphipoda Gammaridae s.l.) from caves waters in Slovenia
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Sket, B. (1981) Niphargobates orophobata n. gen. n. sp.
(Amphipoda Gammaridae s.l.) from caves waters in Slovenia
(NW Yugoslavia). Biološki Vestnik, 29, 105-118.
Critical review of the relevant theories of the evolution of subterranean animals. Subterranean ecosystems
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Culver, D.C. & Wilkens, H. (2000) Critical review of the
relevant theories of the evolution of subterranean animals.
Subterranean ecosystems (ed. by H. Wilkens, D.C. Culver and
W.F. Humphreys), pp. 381-398. Elsevier, Amsterdam.
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Jones, W.K. (1997) Karst hydrology atlas of West Virginia.
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Her interests include modeling zoogeography, biodiversity, population dynamics, and behavioural studies and developing sampling designs and estimators for rare and elusive species
- C Mary
Mary C. Christman is an Associate Professor in the Department of Statistics, University of Florida, Gainesville, FL. She is active in
statistical modeling for environmental studies and biological research. Her interests include modeling zoogeography, biodiversity,
population dynamics, and behavioural studies and developing sampling designs and estimators for rare and elusive species.
He is currently Professor of Biology at American University. He has studied caves and cave fauna for 40 years. His main research interests include biodiversity patterns of subterranean animals, ecology of shallow groundwater inverterbrates
- C David
David C. Culver has a PhD in Biology from Yale University. He is currently Professor of Biology at American University. He has
studied caves and cave fauna for 40 years. His main research interests include biodiversity patterns of subterranean animals, ecology
of shallow groundwater inverterbrates, and conservation biology of cave animals.
Madden has a MS in Environmental Science from American University. She currently has an ORISE Fellowship working on ocean dumping and dredged material issues in coordination with the Environmental Protection Agency
- K Molly
Molly K. Madden has a MS in Environmental Science from American University. She currently has an ORISE Fellowship working
on ocean dumping and dredged material issues in coordination with the Environmental Protection Agency.
Niphargobates orophobata n. gen. n. sp. (Amphipoda Gammaridae s.l.) from caves waters in Slovenia (NW Yugoslavia)
- Sket B.