Recent Advances in the Diversity and Taxonomy of Subterranean Arthropods

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

Deadline for manuscript submissions: 31 December 2024 | Viewed by 19552

Special Issue Editors


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Guest Editor
Institute of Zoology, University of Belgrade - Faculty of Biology, Studentski Trg 16, Belgrade 11000, Serbia
Interests: diversity and faunistics of hypogean and soil-dwelling invertebrates; morphology, systematics, taxonomy, phylogeny, development, and ecology of Coleoptera; photonic structures in insects; secretion in ground beetles; antimicrobial action of the pygidial gland secretions of ground beetles

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Guest Editor
Montenegrin Academy of Sciences and Arts, Riste Stijovića 5, Podgorica 81000, Montenegro
Interests: taxonomy, biodiversity, ecology, zoogeography, and evolution of terrestrial, freshwater, subterranean, marine, and the world Amphipoda (Crustacea); marine and freshwater zoobenthos; cave-dwelling fauna; ecology of continental waters; marine fauna

Special Issue Information

Dear Colleagues,

The subterranean fauna of arthropods is one of the richest on the planet; however, at the same time, it is still insufficiently studied. The characteristics of the underground environment have conditioned hypogean arthropods to evolve both morphological and physiological adaptations, such as depigmentation, a complete loss of eyes, an elongation of appendages, slow metabolism, reduced energy consumption, and many others. These animals are excellent models to study the general principles of evolution and the mechanisms of adaptation to a novel environment. Given that the diversity of subterranean arthropods has not yet been sufficiently studied globally and that most previous studies have dealt with the faunal diversity, it is desirable to analyze other aspects of the diversity of this specific group of animals, including morphological, molecular, ecological, chemoecological, and behavioral diversity. Since the editors cover both troglobitic (associated with terrestrial subterranean environment) and stygobitic (associated with all types of subterranean waters) arthropods with their expertise, the Special Issue will be dedicated to the study of the diversity of both groups. We hope that it will contribute to a better knowledge of the diversity of subterranean arthropods within several biological disciplines, which would indicate their great importance within the habitats they inhabit, as well as for humans in general.

Prof. Dr. Srećko B. Ćurčić
Prof. Dr. Gordan S. Karaman
Guest Editors

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Keywords

  • underground environment
  • subterranean arthropods
  • troglobites
  • stygobites
  • taxonomy
  • biodiversity

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Published Papers (9 papers)

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12 pages, 2058 KiB  
Article
Exploring Biodiversity and Food Webs in Sulfur Cave in the Vromoner Canyon on the Greek–Albanian Border
by Serban M. Sarbu, Traian Brad, Raluca I. Băncilă and Andrei Ştefan
Diversity 2024, 16(8), 477; https://doi.org/10.3390/d16080477 - 6 Aug 2024
Cited by 1 | Viewed by 1248
Abstract
Sulfidic caves support diverse and abundant subterranean communities, including numerous endemic species and complex food webs, though the full extent of species diversity and resource utilization in these ecosystems remains largely unexplored. This paper presents the results of biological surveys conducted from 2023 [...] Read more.
Sulfidic caves support diverse and abundant subterranean communities, including numerous endemic species and complex food webs, though the full extent of species diversity and resource utilization in these ecosystems remains largely unexplored. This paper presents the results of biological surveys conducted from 2023 to 2024 in Sulfur Cave, located in the Vromoner Canyon on the Greek–Albanian border, focusing on microbial, vertebrate, and invertebrate communities and investigating the structure of the subterranean food web. The microbial communities from the different biofilms are dominated by chemosynthetic sulfur-oxidizing microorganisms, specifically filamentous bacteria such as Thiotrix and Beggiatoa. Two species of fish, an eel (Anguilla sp.) and a Cyprinid (Alburnoides sp.), and six bat species from three families (Rhinolophidae, Miniopteridae, and Vespertilionidae) were documented. The invertebrate fauna includes five aquatic species, 25 terrestrial species, and four amphibiotic species. Among these, eight species are endemic, and seven species exhibit troglomorphic traits. Stable isotope analysis showed light carbon and nitrogen values for the terrestrial and aquatic invertebrates, suggesting that subterranean communities rely on food produced in situ by chemoautotrophic microorganisms. Our results identified cave areas of significant biological relevance and provided reference data to inform conservation actions aimed at preserving the biodiversity of this sulfidic cave. Full article
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15 pages, 3171 KiB  
Article
Exploring Ice Cave Biodiversity in Northeastern Italy
by Leonardo Latella and Stefano Brighenti
Diversity 2024, 16(7), 364; https://doi.org/10.3390/d16070364 - 26 Jun 2024
Viewed by 1211
Abstract
The ice stored in caves is a widespread yet neglected cryospheric component. The cold-adapted biodiversity of ice caves has received very little attention from research, despite the potential abundance of endemic troglobiotic and cryophilic species and their consequent sensitivity to the changing climate. [...] Read more.
The ice stored in caves is a widespread yet neglected cryospheric component. The cold-adapted biodiversity of ice caves has received very little attention from research, despite the potential abundance of endemic troglobiotic and cryophilic species and their consequent sensitivity to the changing climate. In this study, we investigated the invertebrate diversity of two ice caves in Northeastern Italy (Bus delle Taccole and Caverna del Sieson, Veneto Region). During 2022 and 2023, we sampled, using pitfall traps, the invertebrates dwelling at different locations in each cave: the shaft base, an intermediate hall, and the cave bottom. At each cave location, we also collected ice samples, on which we measured the stable isotopes of oxygen and hydrogen (δ18O, δ2H), and monitored the air temperature with data-loggers. The two caves had different invertebrate communities, both dominated by a combination of troglobiotic and cryophilic taxa. Despite a low taxonomic richness, which was higher at Taccole (15 taxa) than at Sieson (11 taxa), both caves hosted rare/endemic species, four of which are not described yet. At each cave, the ice water isotopic signatures differed among cave locations, suggesting the ice had formed under different climatic conditions, and/or resulted from different frequencies of thawing/freezing events. The occurrence of summer melt at both caves suggests that these unique ecosystems will quickly disappear, along with their specialized and unique biodiversity. Full article
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25 pages, 11154 KiB  
Article
The Diversity of Subterranean Terrestrial Arthropods in Resava Cave (Eastern Serbia)
by Nikola Vesović, Christo Deltshev, Plamen Mitov, Dragan Antić, Dalibor Z. Stojanović, Dejan V. Stojanović, Katarina Stojanović, Milenka Božanić, Aleksandra Ignjatović-Ćupina and Srećko Ćurčić
Diversity 2024, 16(4), 234; https://doi.org/10.3390/d16040234 - 16 Apr 2024
Viewed by 3709
Abstract
The Balkan region is rich in limestone deposits, which have created one of the largest hotspots of subterranean biodiversity. This paper gives an overview of the diversity of subterranean terrestrial arthropods in Resava Cave in eastern Serbia. This cave is protected and has [...] Read more.
The Balkan region is rich in limestone deposits, which have created one of the largest hotspots of subterranean biodiversity. This paper gives an overview of the diversity of subterranean terrestrial arthropods in Resava Cave in eastern Serbia. This cave is protected and has the status of a natural monument. At the same time, it is one of the most visited caves in Serbia and its surroundings. Our study comprises the results of three years of biospeleological investigations of the famous Serbian cave in combination with data from the few available literature sources on the arthropod fauna of the cave. The arthropod samples were collected both manually and with pitfall traps. A total of 107 arthropod species from the four major subphyla were registered in the cave: 66 species of Hexapoda, 27 species of Chelicerata, 11 species of Myriapoda and three species of Crustacea. For four troglobitic, 16 troglophilic and 87 trogloxenic species recorded in the cave, descriptions of their microhabitats and information on their distribution in the cave are given. Considering the medium size of Resava Cave and the lack of permanent water flow in the two main levels on the one hand, and the large number of arthropod species recorded on the other, the cave is relatively rich in hypogean terrestrial arthropod fauna compared to other caves in Serbia that have been biospeleologically studied so far. Full article
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12 pages, 11493 KiB  
Article
Groundwater Amphipods of the Hyporheic Interstitial: A Case Study from Luxembourg and The Greater Region
by Dieter Weber and Alexander M. Weigand
Diversity 2023, 15(3), 411; https://doi.org/10.3390/d15030411 - 11 Mar 2023
Cited by 2 | Viewed by 1765
Abstract
Hyporheic interstitials are ecologically dynamic and often neglected aquatic environments. In this study, groundwater amphipods (Niphargidae, Pseudoniphargidae and Crangonyctidae) were sampled in hyporheic interstitials throughout Luxembourg and The Greater Region and specimens were analyzed by DNA barcoding. Sites characterized by gravel or coarse [...] Read more.
Hyporheic interstitials are ecologically dynamic and often neglected aquatic environments. In this study, groundwater amphipods (Niphargidae, Pseudoniphargidae and Crangonyctidae) were sampled in hyporheic interstitials throughout Luxembourg and The Greater Region and specimens were analyzed by DNA barcoding. Sites characterized by gravel or coarse sand and high flow velocities of incoming water were the most species- and specimen-rich. A total of 11 species were detected, of which the Niphargus aquilex lineage EF of the N. aquilex cryptic species complex and juveniles of N. schellenbergi dominated the data set, but an unknown lineage of the N. aquilex-complex was also found. Some regions appeared to be devoid of groundwater amphipods. We hypothesize that underlying sandstone formations resulting in low sediment porosity may prevent physical colonization, but also that historical water pollution may have a long-lasting effect, either through the persistence of contaminants in the sediment or low recolonization rates of affected populations. In summary, our approach expanded regional species inventories, confirmed known occurrences, and validated previously questionable or historical morphology-based detections. In addition, the collection of absence data provided valuable insights into local extinctions. Finally, DNA-based distribution data are needed to gather information on the ecological affinities of groundwater amphipods to understudied hyporheic interstitial environments. Full article
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12 pages, 5030 KiB  
Article
Not the Last Piece of the Puzzle: Niphargus Phylogeny in Hungary
by Gergely Balázs, Špela Borko, Dorottya Angyal, Valerija Zakšek, Anna Biró, Cene Fišer and Gábor Herczeg
Diversity 2023, 15(2), 223; https://doi.org/10.3390/d15020223 - 3 Feb 2023
Cited by 2 | Viewed by 1878
Abstract
The Palaearctic genus Niphargus is a promising model system to understand subterranean fauna genesis in Europe. The Pannonian Plain (mainly covered by Hungary) in Central Europe, once being the area of the Paratethys, is a key area for Niphargus diversification. However, our knowledge [...] Read more.
The Palaearctic genus Niphargus is a promising model system to understand subterranean fauna genesis in Europe. The Pannonian Plain (mainly covered by Hungary) in Central Europe, once being the area of the Paratethys, is a key area for Niphargus diversification. However, our knowledge on Hungarian species of Niphargus is primarily based on sporadic taxonomical works from the pre-molecular era. Here, we studied 14 localities, covering the eight valid Hungarian species of Niphargus and including nine previously unstudied populations. Based on sequences of three gene fragments, we reconstructed their phylogeny using maximum likelihood and Bayesian approaches. We found that not all Hungarian species of Niphargus are closely related, and even species sampled at the same localities can belong to different clades. Some Hungarian species form monophyletic clades, while others are nested in various non-Hungarian lineages. The new populations are all genetically distinct from the known species. Our results suggest that the Hungarian Niphargus fauna has originated from seven unrelated clades and its diversity is underestimated due to unknown populations and cryptic species. The detection of genetically distinct species of Niphargus from non-carbonate regions calls for further research efforts. The high diversity and the number of putative new species in the N. tatrensis clade warrants further, high-resolution phylogenetic studies. Full article
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10 pages, 1160 KiB  
Article
On the Diversity of Semiochemicals of the Pygidial Gland Secretions of Subterranean Ground Beetles (Coleoptera: Carabidae)
by Sofija Vranić, Ljubodrag Vujisić, Nikola Vesović, Marina Todosijević, Miloš Pavićević, Dejan Radović and Srećko Ćurčić
Diversity 2023, 15(2), 136; https://doi.org/10.3390/d15020136 - 19 Jan 2023
Cited by 1 | Viewed by 2015
Abstract
Pygidial glands are of great importance to ground beetles for defense against predators, especially for the species that live in subterranean habitats. The purpose of our study is to better understand the chemistry of the pygidial gland secretions of subterranean ground beetles, as [...] Read more.
Pygidial glands are of great importance to ground beetles for defense against predators, especially for the species that live in subterranean habitats. The purpose of our study is to better understand the chemistry of the pygidial gland secretions of subterranean ground beetles, as well as the function and structure of the glands. We studied both the chemical composition of the pygidial gland secretion and morphology of the glands in adults of the troglophilic ground beetle species Laemostenus (Antisphodrus) cavicola (Schaum, 1858). The chemical composition of its defensive secretion was revealed using gas chromatography-mass spectrometry (GC-MS), while pygidial gland morphology of the beetle was investigated using bright-field microcopy. In total, seven chemical compounds were detected in the secretion mixture. Formic acid was the most dominant compound, followed by dodecyl acetate and undecane. Other chemicals were present in minor amounts. The morphological structure of the pygidial glands of L. (A.) cavicola was compared with the structure of the glands of the related congeneric troglophilic species Laemostenus (Pristonychus) punctatus (Dejean, 1828). Summary data on the semiochemicals that have been recorded so far in subterranean ground beetle species are presented, and the differences in the chemical composition of the secretions between and among troglobitic and troglophilic species are discussed. So far, forty-four compounds have been detected in four subterranean ground beetle species (two troglobites belonging to the tribe Trechini and two troglophiles belonging to the tribe Sphodrini). The results of this study indicate the great diversity of chemicals in the pygidial gland secretions of subterranean ground beetles. Full article
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24 pages, 2664 KiB  
Article
Contrasting Phylogeographic Patterns of Mitochondrial and Genome-Wide Variation in the Groundwater Amphipod Crangonyx islandicus That Survived the Ice Age in Iceland
by David Eme, Kristen M. Westfall, Brynja Matthíasardóttir, Bjarni Kristófer Kristjánsson and Snæbjörn Pálsson
Diversity 2023, 15(1), 88; https://doi.org/10.3390/d15010088 - 10 Jan 2023
Cited by 1 | Viewed by 2044
Abstract
The analysis of phylogeographic patterns has often been based on mitochondrial DNA variation, but recent analyses dealing with nuclear DNA have in some instances revealed mito-nuclear discordances and complex evolutionary histories. These enigmatic scenarios, which may involve stochastic lineage sorting, ancestral hybridization, past [...] Read more.
The analysis of phylogeographic patterns has often been based on mitochondrial DNA variation, but recent analyses dealing with nuclear DNA have in some instances revealed mito-nuclear discordances and complex evolutionary histories. These enigmatic scenarios, which may involve stochastic lineage sorting, ancestral hybridization, past dispersal and secondary contacts, are increasingly scrutinized with a new generation of genomic tools such as RADseq, which also poses additional analytical challenges. Here, we revisited the previously inconclusive phylogeographic history, showing the mito-nuclear discordance of an endemic groundwater amphipod from Iceland, Crangonyx islandicus, which is the only metazoan known to have survived the Pleistocene beneath the glaciers. Previous studies based on three DNA markers documented a mitochondrial scenario with the main divergence occurring between populations in northern Iceland and an ITS scenario with the main divergence between the south and north. We used double digest restriction-site-associated DNA sequencing (ddRADseq) to clarify this mito-nuclear discordance by applying several statistical methods while estimating the sensitivity to different analytical approaches (data-type, differentiation indices and base call uncertainty). A majority of nuclear markers and methods support the ITS divergence. Nevertheless, a more complex scenario emerges, possibly involving introgression led by male-biased dispersal among northern locations or mitochondrial capture, which may have been further strengthened by natural selection. Full article
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28 pages, 6070 KiB  
Article
Deep Troglomorphy: New Arrhopalitidae (Collembola: Symphypleona) of Different Life Forms from the Snezhnaya Cave System in the Caucasus
by Robert S. Vargovitsh
Diversity 2022, 14(8), 678; https://doi.org/10.3390/d14080678 - 19 Aug 2022
Cited by 3 | Viewed by 2117
Abstract
The Snezhnaya (=Snow) Cave System (depth −1760 m; total length 40.8 km), located in the West Caucasus, is inhabited by distinctly troglomorphic collembolan species from several families. Two new species of the family Arrhopalitidae occur in the deep parts of the system. Both [...] Read more.
The Snezhnaya (=Snow) Cave System (depth −1760 m; total length 40.8 km), located in the West Caucasus, is inhabited by distinctly troglomorphic collembolan species from several families. Two new species of the family Arrhopalitidae occur in the deep parts of the system. Both are highly morphologically specialized; however, they evolved into different troglobiont life forms. Arrhopalites profundus sp. nov. with extremely long claws, lamellate mucro, and an enlarged sensory organ of third antennal segment lives exclusively in hygropetric and epineustonic habitats, whereas Pygmarrhopalites rystsovi sp. nov., with greatly elongated and multi-subsegmentated antennae and long legs, prefers open terrestrial spaces. The troglomorphy, as well as ecological life forms of the obligate cave-dwelling Arrhopalitidae, in general, are discussed and classified as neustonic-hygropetric, atmobiont, intrasubstrate, and intermediate troglomorphs. Full article
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12 pages, 1939 KiB  
Hypothesis
A Subsurface Stepping Stone Hypothesis for the Conquest of Land by Arthropods
by Amos Frumkin and Ariel D. Chipman
Diversity 2024, 16(1), 6; https://doi.org/10.3390/d16010006 - 22 Dec 2023
Cited by 1 | Viewed by 2031
Abstract
The conquest of land by arthropods is commonly believed to be a surface phenomenon associated with the arrival of photosynthetic plants, atmospheric oxygenation, and an ozone shield in the mid-Paleozoic Era. However, recent molecular and fossil evidence suggests terrestrial fauna may have first [...] Read more.
The conquest of land by arthropods is commonly believed to be a surface phenomenon associated with the arrival of photosynthetic plants, atmospheric oxygenation, and an ozone shield in the mid-Paleozoic Era. However, recent molecular and fossil evidence suggests terrestrial fauna may have first appeared in the Cambrian, before the proliferation of plants and ozone, which are thought to be essential for survival. This raises the question—how could arthropods survive on land without established plants and an ozone shield? We propose a hypothesis that chemolithoautotrophic cave ecosystems, independent of photosynthesis, may have served as a subsurface stepping stone, providing a possible explanation for the land invasion enigma. Chemolithoautrophic caves have offered abundant food and radiation protection, enabling ancient arthropods to evolve strategies to adapt to new frontiers through gradual dispersion from the sea to shielded cave waters, then to cave hygropetric margins of cave waters, and, finally, to the surface. Full article
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