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Status and Distribution of the Cave-Obligate Land Snails in the Appalachians and Interior Low Plateau of the Eastern United States
Abstract and Figures
Cave-obligate (troglobiotic) land snails are among the most understudied taxa inhabiting cave systems because of their small size and cryptic nature. Other than locality records and general descriptions of species’ morphology, information regarding most cave snail taxa is minimal. Given the importance of land snails as indicator species and as important drivers of ecosystem processes, this lack of knowledge on cave-obligate taxa impedes conservation management of subterranean snails and subterranean ecosystems in general. As a first step, we compiled and georeferenced all available distributional records for troglobiotic snail species within two major karst regions in the United States: The Interior Low Plateau (ILP) and Appalachians. We identified 16 new localities among these species from caves in Alabama, Tennessee, and Georgia from 2012 to 2016, yielding 8 new occurrences of two species in the ILP and 8 new occurrences of three species in the Appalachians. In total, we report 143 occurrences for five species in 124 caves, representing the most comprehensive dataset on the distribution of cave-obligate snails in the eastern United States to date. We also provide the first IUCN Red List conservation assessments for all five troglobiotic
taxa and reexamine NatureServe conservation ranks. Our assessments indicate that three of the five species are considered at an elevated risk of extinction. Given these ranks and the threats identified to each species, we offer recommendations concerning the conservation and management of these cave snails and outline future areas of research for these taxa.
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May 2018
... Three troglobiotic snails occur in the Crystal-Wonder Cave System. Carychium stygium is a minute (<2 mm) terrestrial snail known from >75 caves throughout the Interior Low Plateau karst region of Kentucky and Tennessee [30,65,66], where it is often found in association with cricket guano [67]. Lewis [30] reported C. stygium from the Crystal Cave. ...
... Weigand et al. [68,69] suggested that C. stygium may be a morph of the troglophile C. exile based on mitochondrial COI sequence data. Glyphyalinia specus is a wide-ranging troglobiotic glyph known from twenty-seven caves in five states [66], including the Crystal Cave [26], in association with cricket guano [65]. Helicodiscus notius specus also has a broad distribution but is known from just four caves in Kentucky and Tennessee [66], including the Crystal Cave [30], where it is associated with cricket guano [65]. ...
... Glyphyalinia specus is a wide-ranging troglobiotic glyph known from twenty-seven caves in five states [66], including the Crystal Cave [26], in association with cricket guano [65]. Helicodiscus notius specus also has a broad distribution but is known from just four caves in Kentucky and Tennessee [66], including the Crystal Cave [30], where it is associated with cricket guano [65]. ...
The Crystal-Wonder Cave System developed in the Western Escarpment of the southern Cumberland Plateau in the Interior Low Plateau karst region of south-central Tennessee, USA is a global hotspot of cave-limited biodiversity. We combined historical literature, museum accessions, and database occurrences with new observations from bio-inventory efforts conducted between 2005 and 2022 to compile an updated list of troglobiotic and stygobiotic biodiversity for the Crystal-Wonder Cave System. The list of cave-limited fauna includes 31 species (23 troglobionts and 8 stygobionts) with 28 and 18 species documented from the Crystal and Wonder caves, respectively, which represents five phyla, ten classes, nineteen orders, and twenty-six families (six arachnids, three springtails, two diplurans, three millipedes, six insects, three terrestrial snails, one flatworm, five crustaceans, and two vertebrates, respectively). The Crystal-Wonder Cave System is the type locality for six species—Anillinus longiceps, Pseudanophthalmus humeralis, P. intermedius, Ptomaphagus hatchi, Tolus appalachius, and Chitrella archeri. The carabid beetle Anillinus longiceps is endemic to the Crystal-Wonder Cave System. Sixteen species are of conservation concern, including twelve taxa with NatureServe conservation ranks of G1–G3. The exceptional diversity of the Crystal-Wonder Cave System has been associated with several factors, including a high dispersal potential of cave fauna associated with expansive karst exposures along the Western Escarpment of the southern Cumberland Plateau, a high surface productivity, and a favorable climate throughout the Pleistocene.
... as troglobitic species. Besides their endemicity, there are other morphoanatomical features to support this, some of which are of particular importance for freshwater gastropods (Grego et al. 2020;Gladstone et al. 2018Gladstone et al. , 2021Salvador et al. 2022bSalvador et al. , 2024 as follows. Idiopyrgus meriadoci sp. ...
... has a white translucent and fragile shell and unpigmented body; it also has a minute size, smaller than all other congeners. These are features typical of specialised cave fauna (Gladstone et al. 2018(Gladstone et al. , 2021Grego et al. 2020). Likewise, I. eowynae sp. ...
The freshwater gastropod fauna in Brazil presently consists of circa 180 known species, though this is deemed an underestimate. The little-studied cavern faunas have been considered a potential source of undescribed species, particularly regarding the Truncatelloidea. Here, based on new collection efforts in caves in Bahia state, Brazil, we describe two new troglobitic species of Idiopyrgus (Tomichii-dae): Idiopyrgus eowynae sp. nov. and Idiopyrgus meriadoci sp. nov. We improve upon the previous molecular phylogeny of this genus and take the opportunity to reclassify Spiripockia umbraticola Simone & Salvador, 2021, as Idiopyrgus umbraticola (Simone & Sal-vador, 2021), comb. nov. The genus Idiopyrgus now contains ten species, reinforcing the presence of Tomichiidae in Brazil as a relict lineage that largely radiated into cave environments. Furthermore, considering that so far only snapshots of their biology are known, we have collated all the information currently available from the literature and field observations on the cavernicolous species of Idiopyr-gus. Notably, due to human action in the area where the two new species have been found, they can already be considered vulnerable.
... Regardless, these studies suggest that it is likely that C. stygium has recently colonized caves. Glyphyalinia specus is a wide-ranging snail known from 27 occurrences in five states [72]. Significant publications include Call [28], Hubricht [49,50,52,53], Barr [10], Poulson et al. [73], Dourson [74], Poulson [62], and Gladstone et al. [72]. ...
... Glyphyalinia specus is a wide-ranging snail known from 27 occurrences in five states [72]. Significant publications include Call [28], Hubricht [49,50,52,53], Barr [10], Poulson et al. [73], Dourson [74], Poulson [62], and Gladstone et al. [72]. ...
The Mammoth Cave System in the Interior Low Plateau karst region in central Kentucky, USA is a global hotspot of cave-limited biodiversity, particularly terrestrial species. We searched the literature, museum accessions, and database records to compile an updated list of troglobiotic and stygobiotic species for the Mammoth Cave System and compare our list with previously published checklists. Our list of cave-limited fauna totals 49 species, with 32 troglobionts and 17 stygobionts. Seven species are endemic to the Mammoth Cave System and other small caves in Mammoth Cave National Park. The Mammoth Cave System is the type locality for 33 cave-limited species. The exceptional diversity at Mammoth Cave is likely related to several factors, such as the high dispersal potential of cave fauna associated with expansive karst exposures, high surface productivity, and a long history of exploration and study. Nearly 80% of the cave-limited fauna is of conservation concern, many of which are at an elevated risk of extinction because of small ranges, few occurrences, and several potential threats.
... As Salvador (2019) pointed out, caves are among the least explored habitats in malacological studies in Brasil, a bias that is also common in other countries (e.g. Gladstone et al., 2018;Czaja et al., 2020). Sket, 2016;Bichuette & Trajano, 2018). ...
... Some studies point towards cryptic species in single caves or even cave systems: a local example may be the caves in the Ribeira Valley in southeastern Brasil. Bichuette & Trajano (2003, 2018 have identified several morphotypes of Potamolithus sp. in those caves, though species limits need to be investigated further, preferably using molecular data and more detailed morphological analysis (e.g. micro-CT). ...
The Brasilian territory is very extensive and harbors ~20,000caves, over half of which are calcareous (Fig. 1; CECAV, 2020). A reduced number of the ~ 700 terrestrial and nearly260 freshwater gastropod species reported from Brasil (Simone, 2006; Birckolz et al., 2016; Salvador, 2019) inhabit cave environments exclusively. Since the description of the first exclusively subterranean gastropod in the 1990s (Potamolithus troglobius Simone &Moracchioli, 1994), 17 land and three freshwater troglobitic snails have been described from Brasil (Table 1). Most of the descriptions stem from recent studies carried out over the past decade and several additional new species are in the process of being described (Table 1; Fig. 1).
... Several taxa are notably absent from the cavelimited fauna of Fern Cave, including terrestrial cavesnails, terrestrial woodlice, stygobiotic copepods, and stygobiotic salamanders, all of which may be discovered in the future. For example, three terrestrial cavesnails are known from Northern Alabama, including Helicodiscus barri, which has a broad distribution throughout the Interior Low Plateau karst region [66,67]. Twelve stygobiotic copepods occur in the Interior Low Plateau [68], but only one, Diacyclops alabamensis, has been reported from Alabama. ...
The Fern Cave System, developed in the western escarpment of the Southern Cumberland Plateau of the Interior Low Plateau karst region in Northeastern Alabama, USA, is a global hotspot of cave-limited biodiversity as well as home to the largest winter hibernaculum for the federally endangered Gray Bat (Myotis grisescens). We combined the existing literature, museum accessions, and database occurrences with new observations from bioinventory efforts conducted in 2018–2022 to generate an updated list of troglobiotic and stygobiotic species for the Fern Cave System. Our list of cave-limited fauna totals twenty-seven species, including nineteen troglobionts and eight stygobionts. Two pseudoscorpions are endemic to the Fern Cave System: Tyrannochthonius torodei and Alabamocreagris mortis. The exceptional diversity at Fern Cave is likely associated with several factors, such as the high dispersal potential of cave fauna associated with expansive karst exposures along the Southern Cumberland Plateau, high surface productivity, organic input from a large bat colony, favorable climate throughout the Pleistocene, and location within a larger regional hotspot of subterranean biodiversity. Nine species are of conservation concern, including the recently discovered Alabama cave shrimp Palaemonias alabamae, because of their small range sizes, few occurrences, and several potential threats.
... Moreover, given the extension of the Brazilian territory and a large number of caves (circa 20,000, over half of which are calcareous; CECAV 2020; Figs 23-28), this number is certainly a gross underestimation. As alluded to by Salvador (2019), caves are among the least explored habitats in malacological studies in Brazil, a bias that is also present in other countries (e.g., Gladstone et al. 2018, Czaja et al. 2020. In Brazil, our knowledge is biased toward a relatively low number of caves in the eastern portion of the country (44 caves, Fig. 29). ...
An up-to-date list of exclusively cave-dwelling gastropod species recorded in Brazil is presented including updated taxonomy, detailed geographic information, and illustration of types. The list includes 18 cave-exclusive (troglobitic) gastropods encompassing 15 land and three freshwater species, with the status of further species pending additional studies. Their unusual morphology and diversity are discussed, as well as their conservation status and prospects in the current Brazilian environmental and political scenario.
... As Salvador (2019) pointed out, caves are among the least explored habitats in malacological studies in Brasil, a bias that is also common in other countries (e.g. Gladstone et al., 2018;Czaja et al., 2020). ...
Recently, an Environmental Impact Assessment (EIA) was submitted for consideration to the National Environmental and Planning Agency (NEPA) of Jamaica by Noranda Jamaica Bauxite Partners II (NJBP II) in regards to a permit application to mine an area called SML-173 (Conrad Douglas & Associates Limited, 2020) (Fig. 1). SML-173 (SML standing for Special Mining Lease) is a part of Cockpit Country, which is the largest contiguous mesic limestone forest on the island and home to many endemic molluscan and other invertebrate species that cannot be found elsewhere on Jamaica. Cockpit Country has large reserves of aluminium-bearing soils (bauxite) and is constantly under threat of disturbance and mining despite protection measures. We provided critique and commentary to NEPA on the EIA, rejecting it for its inadequacies, including unclear reporting, lack of research and citations, unclear field methodologies and inaccurate results. We share a summary of some of these comments here to report on ongoing conservation issues and concerns for Jamaican terrestrial molluscs.
... As Salvador (2019) pointed out, caves are among the least explored habitats in malacological studies in Brasil, a bias that is also common in other countries (e.g. Gladstone et al., 2018;Czaja et al., 2020). ...
... As Salvador (2019) pointed out, caves are among the least explored habitats in malacological studies in Brasil, a bias that is also common in other countries (e.g. Gladstone et al., 2018;Czaja et al., 2020). ...
Subterranean ecosystems are among the most widespread environments on Earth, yet we still have poor knowledge of their biodiversity. To raise awareness of subterranean ecosystems, the essential services they provide, and their unique conservation challenges, 2021 and 2022 were designated International Years of Caves and Karst. As these ecosystems have traditionally been overlooked in global conservation agendas and multilateral agreements, a quantitative assessment of solution-based approaches to safeguard subterranean biota and associated habitats is timely. This assessment allows researchers and practitioners to understand the progress made and research needs in subterranean ecology and management. We conducted a systematic review of peer-reviewed and grey literature focused on subterranean ecosystems globally (terrestrial, freshwater, and saltwater systems), to quantify the available evidence-base for the effectiveness of conservation interventions. We selected 708 publications from the years 1964 to 2021 that discussed, recommended, or implemented 1,954 conservation interventions in subterranean ecosystems. We noted a steep increase in the number of studies from the 2000s while, surprisingly, the proportion of studies quantifying the impact of conservation interventions has steadily and significantly decreased in recent years. The effectiveness of 31% of conservation interventions has been tested statistically. We further highlight that 64% of the reported research occurred in the Palearctic and Nearctic biogeographic regions. Assessments of the effectiveness of conservation interventions were heavily biased towards indirect measures (monitoring and risk assessment), a limited sample of organisms (mostly arthropods and bats), and more accessible systems (terrestrial caves). Our results indicate that most conservation science in the field of subterranean biology does not apply a rigorous quantitative approach, resulting in sparse evidence for the effectiveness of interventions. This raises the important question of how to make conservation efforts more feasible to implement, cost-effective, and long-lasting. Although there is no single remedy, we propose a suite of potential solutions to focus our efforts better towards increasing statistical testing and stress the importance of standardising study reporting to facilitate meta-analytical exercises. We also provide a database summarising the available literature, which will help to build quantitative knowledge about interventions likely to yield the greatest impacts depending upon the subterranean species and habitats of interest. We view this as a starting point to shift away from the widespread tendency of recommending conservation interventions based on anecdotal and expert-based information rather than scientific evidence, without quantitatively testing their effectiveness.
The overexploitation of the world's biomes for natural products calls for the prioritization of biologically important ecosystems for conservation. Here we show that limestone karsts are “arks” of biodiversity and often contain high levels of endemism. Humans have exploited karsts for a variety of products and services, but unsustainable practices have caused population declines and extinctions among site-endemic taxa. Limestone quarrying is the primary threat to karst biodiversity in Southeast Asia, where quarrying rates exceed those in other tropical regions. Several socioeconomic, political, and scientific issues undermine the stewardship of these karsts. Mitigation of these problems will involve (a) better land-use planning to prevent karst resources from being exhausted in developing regions, (b) comprehensive assessments of a karst's economic and biological value before development, (c) improved legislation and enforcement to protect karst biodiversity, and (d) increased research and activities to promote public awareness of the importance of karsts and the threats facing them.
Biodiversity conservation requires an objective and consistent method for evaluating the conservation status of species. Conservation status assessments can identify conservation priorities and can highlight data gaps, effective conservation strategies, and groups of taxa that are underrepresented in conservation efforts relative to charismatic flagship and umbrella species. Groundwater invertebrates have a suite of traits that make them inherently vulnerable. But they go largely unnoticed by the general public and conservation practitioners, and comprehensive conservation status assessments are lacking for most species. In this article, the conservation status of all sixty-nine described groundwater-obligate invertebrates recorded from Texas, U.S.A. was assessed using NatureServe methodology. Some of the smallest taxa (e.g. copepods, ostracods, and mites) are too poorly known to evaluate their conservation status. Species restricted to springs were generally more at risk than species in other groundwater habitats, and beetles and snails were the most imperiled taxonomic groups. Most species faced low or medium severity threats, and only seven percent faced high or very high magnitude threats. Threat level varied among aquifers and among sites within aquifers and was primarily dependent on human population density and the adequacy of regulatory mechanisms protecting groundwater quality and quantity. Regardless of threat severity, fifty-five percent of evaluated species were ranked as imperiled or critically imperiled, largely due to extreme small-range endemism. Relative to other regions, Texas’ groundwater fauna is not unique in terms of rarity and threat, suggesting that as an ecological group, groundwater-obligate species are probably among the world’s most imperiled taxa.
The International Union for Conservation of Nature (IUCN) is the premier global biodiversity conservation organization. Its Red List is a rigorous vehicle for assessing the conservation status of plant and animal species. However, although all animal and bird species recognized by IUCN have been evaluated , only a tiny fraction of invertebrates have been evaluated. As a measure of the numbers of extinct species (since around the year 1500) the Red List is probably quite accurate for birds and mammals, but severely underestimates the numbers for invertebrates. Nonetheless, molluscs stand out as the major group most severely impacted by extinction, with 297 of the 744 animal species listed as extinct in the third issue of the 2016 Red List. Here we review efforts to obtain a more realistic , albeit less rigorous, assessment of the numbers of extinct mollusk species. Our approach has been based on biblio-graphic research and consultation with experts, rather than following the highly detailed but restrictive IUCN Categories and Criteria. In 2009, this led to an assessment that 533 mol-lusk species were extinct, far more than the number on the Red List. In the present study we revisited this approach and here list 638 species as extinct, 380 as possibly extinct, and 14 as extinct in the wild, a total of 1,032 species in these combined categories, and more than twice as many as listed by IUCN in these categories. However, this approach only considers species for which information is available; it is therefore biased. In a study published in 2015 we developed an alternative approach, based on a random global sample of land snails, and estimated that 3,000–5,100 mollusk species have gone extinct. We review the main reasons for these extinctions: habitat destruction, impacts of introduced species, exploitation and collecting, and, potentially, climate change, and discuss relevant case studies.
Subterranean ecosystems are among the most fragile and threatened worldwide. Among organisms living in the subterranean domain, source populations restricted to subterranean habitats are called troglobites, generally distinguished by sets of morphological, physiological, and ecological specializations. The singularities at both systemic (high dark and phylogenetic diversities) and species levels greatly contribute to regional and global biodiversity. However, good descriptive and interpretative knowledge about this diversity, which is important as a basis for effective conservation policies, is lacking especially for tropical areas. We describe and characterize Brazilian karst areas recognized as spots of high diversity of troglobites, highlighting particularly important cave systems. We considered not only taxonomic richness but also indicators of phylogenetic (e.g., presence of relictual taxa) and genetic diversities, the latter based on degree of specialization of individual species, i.e., accumulation of autapomorphies. For this, we used available literature and our own data, both published and unpublished. Only identifications validated by a taxonomist were considered, while all data based on parataxonomy were disregarded. We propose hypotheses based on models of origin of troglobites aiming to explain the differences between karst areas.
Caves and other subterranean habitats with their often strange (even bizarre) inhabitants have long been objects of fascination, curiosity, and debate. The question of how such organisms have evolved, and the relative roles of natural selection and genetic drift, has engaged subterranean biologists for decades. Indeed, these studies continue to inform the general theory of adaptation and evolution. Subterranean ecosystems generally exhibit little or no primary productivity and, as extreme ecosystems, provide general insights into ecosystem function. The Biology of Caves and other Subterranean Habitats offers a concise but comprehensive introduction to cave ecology and evolution. Whilst there is an emphasis on biological processes occurring in these unique environments, conservation and management aspects are also considered. The monograph includes a global range of examples from more than 25 countries, and case studies from both caves and non-cave subterranean habitats; it also provides a clear explanation of specialized terms used by speleologists. This accessible text will appeal to researchers new to the field and to the many professional ecologists and conservation practitioners requiring a concise but authoritative overview. Its engaging style will also make it suitable for undergraduate and graduate students taking courses in cave and subterranean biology. Its more than 650 references, 150 of which are new since the first edition, provide many entry points to the research literature.
Nonmarine molluscs are the major animal group with the greatest number of recorded extinctions due to anthropogenic impacts, and that number is certainly a serious underestimate. Land snails, particularly endemic land snails of oceanic islands, are the group of molluscs that have sustained the most extinctions. Understanding their ecology and the evolutionary processes that have led to their extreme vulnerability is crucial if we are to be able to conserve these diverse and important species. Oceanic island snails tend to have low α-diversity and high β-diversity, and divergence of habitat use among related species is known to occur in some radiations of land snails on oceanic islands. Processes of speciation and ecological interaction are possible major drivers of these patterns. The ecological opportunities available at the initial stage of insular evolution and the scarcity of effective predators may have led to divergence of habitat use and high β-diversity in oceanic island snails. Fewer and less diverse predators on oceanic islands lead to the evolution of fewer and less diverse defense traits in oceanic island snails, which results in their high vulnerability to non-native predators. High β-diversity of oceanic island snails also results in great vulnerability to habitat loss. Accordingly, the high susceptibility of oceanic island snails to extinction reflects their evolutionary history.