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Cave Communities: From the Surface Border to the Deep Darkness

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A special issue of Diversity (ISSN 1424-2818). This special issue belongs to the section "Biogeography and Macroecology".

Deadline for manuscript submissions: closed (30 November 2020) | Viewed by 36616

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Dr. Raoul Manenti

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Dipartimento di Scienze e Politiche Ambientali, Università degli Studi di Milano, 20133 Milan, Italy
Interests: zoology; herpetology; planarians; crayfish; cave biology
Special Issues, Collections and Topics in MDPI journals

Dr. Enrico Lunghi

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Co-Guest Editor

Division of Molecular Biology, Institut Ruđer Bošković, 10000 Zagreb, Croatia
Interests: herpetology; cave biology; ecology; evolution; conservation
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

From a biological perspective, the subterranean realm is one of the less studied but at the same time it is one of the most promising theatre for new findings and researches. Compared to those on the surface, the ecological conditions in subterranean habitats are relatively simple, and this may be an optimal scenario for understanding the mechanisms allowing the colonization, adaptation, and evolution of species, as well as their interactions within local communities. Diversity in subterranean habitats is often overlooked, and few studies embrace whole communities or try to assesses functional relationships between species.

This Special Issue will comprise papers covering a wide range of aspects related to the distribution, composition, and roles of subterranean communities, from bacteria and fungi to invertebrate and vertebrate animals, including papers addressing the effect of intraspecific interactions such as cannibalism among different developmental stages. All typologies of subterranean habitats will be covered, from artificial (tunnels, draining galleries, etc.) to natural (caves, interstices, and lava-tubes), including ecotonal and interfacial habitats (like springs, seepages, and cave entrances). Papers addressing the use of subterranean environments by surface species and how their presence integrates with obligate cave-dwelling species are especially welcome. Papers selected for this Special Issue can also be focused on the conservation of cave communities.

Dr. Raoul Manenti
Dr. Enrico Lunghi
Guest Editors

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Keywords

Cave biology
Subterranean
Biodiversity
Zoology
Ecology
Interaction
Hypogean
Spring
Karst

Published Papers (12 papers)

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Editorial

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5 pages, 197 KiB

Open AccessEditorial

Cave Communities: From the Surface Border to the Deep Darkness

by Enrico Lunghi and Raoul Manenti

Diversity 2020, 12(5), 167; https://0-doi-org.brum.beds.ac.uk/10.3390/d12050167 - 25 Apr 2020

Cited by 9 | Viewed by 3010

Abstract

The discipline of subterranean biology has provided us incredible information on the diversity, ecology and evolution of species living in different typologies of subterranean habitats. However, a general lack of information on the relationships between cave species still exists, leaving uncertainty regarding the dynamics that hold together cave communities and the roles of specific organisms (from the least to the most adapted species) for the community, as well as the entire ecosystem. This Special Issue aims to stimulate and gather studies which are focusing on cave communities belonging to all different typologies of subterranean habitats, with the overarching goal to corroborate the key role of the subterranean biology in ecological and evolutionary studies. Full article

(This article belongs to the Special Issue Cave Communities: From the Surface Border to the Deep Darkness)

Research

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25 pages, 5511 KiB

Open AccessArticle

A Primer on Spider Assemblages in Levantine Caves: The Neglected Subterranean Habitats of the Levant—A Biodiversity Mine

by Efrat Gavish-Regev, Shlomi Aharon, Igor Armiach Steinpress, Merav Seifan and Yael Lubin

Diversity 2021, 13(5), 179; https://0-doi-org.brum.beds.ac.uk/10.3390/d13050179 - 23 Apr 2021

Cited by 6 | Viewed by 2866

Abstract

Caves share unique conditions that have led to convergent adaptations of cave-dwelling animals. In addition, local factors act as filters on regional species-pools to shape the assemblage composition of local caves. Surveys of 35 Levantine caves, distributed along a climate gradient from the mesic in the north of Israel to hyper-arid areas in the south of Israel, were conducted to test the effect of cave characteristics, location, climate, bat presence, and guano level on the spider assemblage. We found 62 spider species and assigned four species as troglobites, 28 as troglophiles, and 30 as accidentals. Precipitation, elevation, latitude, minimum temperature, and guano levels significantly affected the composition of cave-dwelling spider assemblages. Caves situated in the Mediterranean region had higher species richness and abundance, as well as more troglobite and troglophile arachnids. These discoveries contribute to the knowledge of the local arachnofauna and are important for the conservation of cave ecosystems. By comparing spider assemblages of Levantine caves to European caves, we identified gaps in the taxonomic research, focusing our efforts on spider families that may have additional cryptic or yet to be described cave-dwelling spider species. Our faunistic surveys are crucial stages for understanding the evolutionary and ecological mechanisms of arachnid speciation in Levantine caves. Full article

(This article belongs to the Special Issue Cave Communities: From the Surface Border to the Deep Darkness)

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17 pages, 2034 KiB

Open AccessArticle

Updated Distribution of the Mysid Antromysis cenotensis (Crustacea: Peracarida), a Protected Key Species in Yucatan Peninsula Cenotes

by Luis Arturo Liévano-Beltrán and Nuno Simões

Diversity 2021, 13(4), 154; https://0-doi-org.brum.beds.ac.uk/10.3390/d13040154 - 31 Mar 2021

Cited by 1 | Viewed by 3696

Abstract

We present 52 new geographic location records for the peracarid crustacean Antromysis cenotensis Creaser, 1936, endemic in cenotes of the Yucatan Peninsula, Mexico. This species is currently considered threatened and, therefore, is protected by Mexican law. These results arise from several expeditions carried out between 2017 and 2020 in 75 locations within the cenote-ring, the interior, and coastal plains of the peninsula. A comprehensive literature review provided 84 geographic location records since the species was described in 1936. A map with 136 geographic location records that better describe the current species distribution is also included. With this information, plus some notes on the ecology of the species, a comprehensive literature and data review, and a brief analysis regarding the possible factors associated with the confirmed absence of the species in some locations in the state of Yucatan, we provide a brief and condensed summary of the actual knowledge on this particular species. The data in Darwin Core format can be retrieved in Zenodo. Full article

(This article belongs to the Special Issue Cave Communities: From the Surface Border to the Deep Darkness)

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19 pages, 1023 KiB

Open AccessArticle

Diversity of Brazilian Troglobitic Fishes: Models of Colonization and Differentiation in Subterranean Habitats

by Eleonora Trajano

Diversity 2021, 13(3), 106; https://0-doi-org.brum.beds.ac.uk/10.3390/d13030106 - 01 Mar 2021

Cited by 4 | Viewed by 2210

Abstract

The Brazilian subterranean ichthyofauna is distinguished worldwide by high taxonomic and phylogenetic diversity, involving at least 30 exclusively subterranean (troglobitic) lineages. This may be explained by high native epigean diversty, allied to opportunities for colonization and genetic isolation in the subterranean biotope, thence originating troglobites. An updated list of Brazilian troglobitic lineages and a review of previous hypotheses on modes of colonization and differentiation in subterranean habitats are presented with fresh data and models. Colonization of and isolation in the subterranean biotope are independent processes, usually separate over time. Access to subterranean habitats varies from the (sub)horizontal through sinkholes and resurgences of base-level streams and vadose tributaries to the vertical by shallow and deep phreatic waters through the hyporheic zone. Phenotypic differentiation of subterranean populations originating troglobites may be achieved by various, non-mutually exclusive modes of genetic isolation, e.g., directly in base-level streams and upper tributaries through the extinction of epigean populations, due to drainage discontinuation in dry paleoclimatic phases (or by other causes), by topographic isolation due to a lowering of the regional base level and karst catchments or by parapatric differentiation. Differentiation may also be a consequence of transition from lotic to lentic waters in flooded caves, and from shallow to deep phreatic habitats. Full article

(This article belongs to the Special Issue Cave Communities: From the Surface Border to the Deep Darkness)

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25 pages, 13307 KiB

Open AccessArticle

Monitoring Brazilian Cavefish: Ecology and Conservation of Four Threatened Catfish of Genus Ituglanis (Siluriformes: Trichomycteridae) from Central Brazil

by Maria Elina Bichuette and Eleonora Trajano

Diversity 2021, 13(2), 91; https://0-doi-org.brum.beds.ac.uk/10.3390/d13020091 - 20 Feb 2021

Cited by 4 | Viewed by 2375

Abstract

We investigated population parameters using the capture-mark-recapture method (Ituglanis passensis and I. bambui) and visual censuses (I. epikasrticus and I. ramiroi). The four species are regionally threatened (Brazilian Red List) and occur in caves of Terra Ronca State Park, São Domingos region, Central Brazil. We conducted seven fieldtrips across three years of dry seasons. For the capture-mark-recapture method, a 400 m long stream inside Passa Três cave, where I. passensis occurs and a 300 m long reach of an upper tributary where I. bambui occurs inside Angélica cave were divided into 20 and 17 study sections, respectively. Catfishes were hand-netted, measured (standard length), weighed, marked by subcutaneous injection of biocompatible pigments, and released. The four species show medium-to-low mean population densities (0.03 ind/m² 0.7 ind/m²). Capture-mark-recapture data pointed to a relatively small population size for I. passensis, restricted to a 1600 m long stream inside Passa Três cave (N = 719) and for I. bambui (N = 246; 300 m of epikarstic drainage). Ituglanis passensis and I. bambui move along relatively small areas with a restricted home range. We observed recruitment patterns and a trend of decrease in condition factor during the dry seasons for I. bambui but not for I. passensis, suggesting that epikarstic waters are probably more limiting concerning food input. Ituglanis passensis and I. bambui showed low growth and consequently high longevity, corroborated by captivity data (20 years). We suggest urgent actions and long-term monitoring projects to effectively protect this unique and endemic ichthyofauna. Full article

(This article belongs to the Special Issue Cave Communities: From the Surface Border to the Deep Darkness)

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24 pages, 3220 KiB

Open AccessArticle

Subterranean Waters of Yucatán Peninsula, Mexico Reveal Epigean Species Dominance and Intraspecific Variability in Freshwater Ostracodes (Crustacea: Ostracoda)

by Laura Macario-González, Sergio Cohuo, Dorottya Angyal, Liseth Pérez and Maite Mascaró

Diversity 2021, 13(2), 44; https://0-doi-org.brum.beds.ac.uk/10.3390/d13020044 - 24 Jan 2021

Cited by 6 | Viewed by 3164

Abstract

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. Full article

(This article belongs to the Special Issue Cave Communities: From the Surface Border to the Deep Darkness)

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12 pages, 229 KiB

Open AccessArticle

Hypogean Communities as Cybernetic Systems: Implications for the Evolution of Cave Biotas

by Aldemaro Romero, Jr.

Diversity 2020, 12(11), 413; https://0-doi-org.brum.beds.ac.uk/10.3390/d12110413 - 29 Oct 2020

Cited by 7 | Viewed by 2061

Abstract

Ramón Margalef proposed in 1968 that ecosystems could be better understood if they were viewed as cybernetic systems. I tested this hypothesis in the case of hypogean ecosystems using available pieces of evidence. I looked on how information on feedbacks, stability, succession, organization, diversity, and energy flows in the hypogean environment fit the cybernetics hypothesis. The results were that there are convincing arguments that the application of the concept of cybernetics in biospeleology can be beneficial to broadening our understanding of cave biota in terms of their structure. I also make the case that this approach can provide more clarity about how cave biota has evolved through time and the implications for their conservation. Full article

(This article belongs to the Special Issue Cave Communities: From the Surface Border to the Deep Darkness)

21 pages, 4895 KiB

Open AccessArticle

Diversity of Olfactory Responses and Skills in Astyanax Mexicanus Cavefish Populations Inhabiting different Caves

by Maryline Blin, Julien Fumey, Camille Lejeune, Maxime Policarpo, Julien Leclercq, Stéphane Père, Jorge Torres-Paz, Constance Pierre, Boudjema Imarazene and Sylvie Rétaux

Diversity 2020, 12(10), 395; https://0-doi-org.brum.beds.ac.uk/10.3390/d12100395 - 13 Oct 2020

Cited by 11 | Viewed by 3167

Abstract

Animals in many phyla are adapted to and thrive in the constant darkness of subterranean environments. To do so, cave animals have presumably evolved mechano- and chemosensory compensations to the loss of vision, as is the case for the blind characiform cavefish, Astyanax mexicanus. Here, we systematically assessed the olfactory capacities of cavefish and surface fish of this species in the lab as well as in the wild, in five different caves in northeastern Mexico, using an olfactory setup specially developed to test and record olfactory responses during fieldwork. Overall cavefish showed lower (i.e., better) olfactory detection thresholds than surface fish. However, wild adult cavefish from the Pachón, Sabinos, Tinaja, Chica and Subterráneo caves showed highly variable responses to the three different odorant molecules they were exposed to. Pachón and Subterráneo cavefish showed the highest olfactory capacities, and Chica cavefish showed no response to the odors presented. We discuss these data with regard to the environmental conditions in which these different cavefish populations live. Our experiments in natural settings document the diversity of cave environments inhabited by a single species of cavefish, A. mexicanus, and highlight the complexity of the plastic and genetic mechanisms that underlie cave adaptation. Full article

(This article belongs to the Special Issue Cave Communities: From the Surface Border to the Deep Darkness)

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21 pages, 7518 KiB

Open AccessFeature PaperArticle

Discovery of Two New Astyanax Cavefish Localities Leads to Further Understanding of the Species Biogeography

by Luis Espinasa, Claudia Patricia Ornelas-García, Laurent Legendre, Sylvie Rétaux, Alexandra Best, Ramses Gamboa-Miranda, Hector Espinosa-Pérez and Peter Sprouse

Diversity 2020, 12(10), 368; https://0-doi-org.brum.beds.ac.uk/10.3390/d12100368 - 24 Sep 2020

Cited by 19 | Viewed by 3626

Abstract

The Astyanax species complex has two morphs: a blind, depigmented morph which inhabits caves in México and an eyed, pigmented surface-dwelling morph. The eyed morph can also be found in a few caves, sometimes hybridizing with the cave morph. This species complex has arguably become the most prominent model system among cave organisms for the study of evolutionary development and genomics. Before this study, 32 caves were known to be inhabited by the cave morph, 30 of them within the El Abra region. The purpose of this study was to conduct new surveys of the area and to assess some unconfirmed reports of caves presumably inhabited by troglomorphic fish. We describe two new localities, Sótano del Toro #2 and Sótano de La Calera. These two caves comprise a single hydrologic system together with the previously described cave of Sótano del Toro. The system is inhabited by a mixed population of troglomorphic, epigeomorphic, and presumably hybrid fish. Furthermore, Astyanax cavefish and the mysid shrimp Spelaeomysis quinterensis show a phylogeographic convergence that supports the notion that the central Sierra de El Abra is a biogeographical region that has influenced the evolutionary history of its aquatic community across species. The presumptive location of the boundaries of this biogeographical region are identified. Full article

(This article belongs to the Special Issue Cave Communities: From the Surface Border to the Deep Darkness)

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11 pages, 1510 KiB

Open AccessArticle

Are the Neglected Tipuloidea Crane Flies (Diptera) an Important Component for Subterranean Environments?

by Enrico Lunghi, Gentile Francesco Ficetola, Yahui Zhao and Raoul Manenti

Diversity 2020, 12(9), 333; https://0-doi-org.brum.beds.ac.uk/10.3390/d12090333 - 31 Aug 2020

Cited by 11 | Viewed by 2943

Abstract

Usually, biospeleological studies focus on cave-specialist taxa showing strong adaptation to the subterranean environment, as their unusual morphological and ecological features represent intriguing case studies. On the other hand, species occurring in subterranean environments but without marked adaptations have been generally overlooked, probably because they are thought to be accidental and not very important for the ecosystem. Particularly exemplificative is the case of Tipuloidea crane flies (Diptera), which although abundant, are rarely considered in biospeleological studies. Here, by analyzing the crane fly occupancy, we observed that individuals occur within the shallowest areas of subterranean environments throughout the year, with a peak of presence during hot season. Crane flies occupy dark and warm areas close to the connection with surface and with smoother walls. Furthermore, we observed that the presence of crane flies is positively related to the abundance and the richness of cave predators, highlighting their importance for the sustainment of the local community. With this study we aim to stimulate future researches on these important, but still neglected cave species. Full article

(This article belongs to the Special Issue Cave Communities: From the Surface Border to the Deep Darkness)

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16 pages, 2361 KiB

Open AccessArticle

Abiotic Community Constraints in Extreme Environments: Epikarst Copepods as a Model System

by Tanja Pipan, Mary C. Christman and David C. Culver

Diversity 2020, 12(7), 269; https://0-doi-org.brum.beds.ac.uk/10.3390/d12070269 - 07 Jul 2020

Cited by 4 | Viewed by 2481

Abstract

The general hypothesis that the overall presence or absence of one or more species in an extreme habitat is determined by physico-chemical factors was investigated using epikarst copepod communities as a model system, an example of an extreme environment with specialized, often rare species. The relationship between the presence or absence of epikarst copepods from drips in six Slovenian caves and 12 physico-chemical factors (temperature, conductivity, pH, Ca²⁺, Na⁺, K⁺, Mg²⁺, NH₄⁺, and Cl⁻, NO₂⁻, NO₃⁻, and SO₄²⁻) was explored. Statistical analyses included principal components analysis, logistic mixed models, stepwise logistic multivariate regression, classification trees, and random forests. Parametric statistical analyses demonstrated the overall importance of two variables—temperature and conductivity. The more flexible statistical approaches, namely categorical trees and random forests, indicate that temperature and concentrations of Ca²⁺ and Mg²⁺ were important. This may be because they are essential nutrients or, at least in the case of Ca²⁺, its importance in molting. The correlation of Cl⁻ and NO₃⁻ with copepod abundance may be due to unmeasured variables that vary at the scale of individual cave, but in any case, the values have an anthropogenic component. This contrasts with factors important in individual species’ niche separation, which overlap with the community parameters only for NO₃⁻. Full article

(This article belongs to the Special Issue Cave Communities: From the Surface Border to the Deep Darkness)

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11 pages, 894 KiB

Open AccessEditor’s ChoiceReview

Reduced Oxygen as an Environmental Pressure in the Evolution of the Blind Mexican Cavefish

by Tyler Boggs and Joshua Gross

Diversity 2021, 13(1), 26; https://0-doi-org.brum.beds.ac.uk/10.3390/d13010026 - 12 Jan 2021

Cited by 11 | Viewed by 3409

Abstract

Extreme environmental features can drive the evolution of extreme phenotypes. Over the course of evolution, certain environmental changes may be so drastic that they lead to extinction. Conversely, if an organism adapts to harsh environmental changes, the adaptations may permit expansion of a novel niche. The interaction between environmental stressors and adaptive changes is well-illustrated by the blind Mexican cavefish, Astyanaxmexicanus, which has recurrently adapted to the stark subterranean environment. The transition from terrestrial rivers and streams (occupied by extant surface morphs of the same species) to the cave has been accompanied by the resorption of eyes, diminished pigmentation and reduced metabolism in cave-dwelling morphs. The principal features of caves most often associated with evolution of these common cave features are the absence of light and limited nutrition. However, a putatively essential cave feature that has received less attention is the frequently low concentration of oxygen within natural karst environments. Here, we review the potential role of limited oxygen as a critical environmental feature of caves in the Sierra de El Abra. Additionally, we review evidence that Astyanax cavefish may have evolved adaptive features enabling them to thrive in lower oxygen compared to their surface-dwelling counterparts. Full article

(This article belongs to the Special Issue Cave Communities: From the Surface Border to the Deep Darkness)

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