Article

Stygobiotic atyid shrimps (Crustacea, Decapoda, Atyidae) from the Amtkel karst system, Western Abkhazia, Caucasus, with a redescription of Xiphocaridinella osterloffi and the description of two new co-occurring species

Authors:
  • A. N. Severtsov Institute of Ecology and Evolution
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Abstract

A morphogenetic revision of Caucasian stygobiotic shrimps from the Amtkel karst system in western Abkha-zia is presented. The neotype of Xiphocaridinella osterloffi (Juzbaš'jan 1941) comb. n. is designated and carefully re-described based on material from the type locality, the Lower Shakuran (= Nizhnya-Shakuranskya) Cave, Gulripshi District. Two new Xiphocaridinella species are described from several different caves, showing a connection between them within the Amtkel karst system. Xiphocaridinella falcirostris Marin sp. n. is described from underground streams of both Lower Shakuran and Besletka caves, Sukhumi District, and Xipho-caridinella smirnovi Marin sp. n. from the Besletka Cave. These records also represent additional cases of stygobiotic shrimp co-occurrence in the western Caucasus, simultaneously revealing the historical fragmentation of a formerly single underground karst habitat and speciation in the ancestral population. Both new species can be separated from congeners by morphological features, mainly the shape and armature of the rostrum, as well as genetically. Thus, the diversity of Caucasian Xiphocaridinella known from the Kolkh-ida coastal lowland (Colchis) of the eastern Black Sea region is increased to twelve species.

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... The stygobiotic atyid shrimp genus Xiphocaridinella Sadowsky, 1930 (Crustacea: Decapoda: Atyidae) currently includes 13 valid species described from the subterranean water habitats of the northern and northwestern part of Kolkhida coastal lowland plain of the eastern Black Sea (Colchis), SW Caucasus (e.g. Sadowsky, 1930;Birštein, 1939Birštein, , 1948Juzbaš'jan, 1940Juzbaš'jan, , 1941Marin, Sokolova, 2014;Marin, 2017aMarin, , b, 2018aMarin, , b, 2019Marin, , 2020. Sadowsky (1930) proposed a new genus Xiphocaridinella for the Caucasian representatives of the subterranean Troglocaris-like shrimps, which was once placed in the subgenus Troglocaris Dormitzer, 1853(e.g., De Grave, Fransen, 2011, but recently again restored to the full generic status (Marin, 2017b;WoRMS, 2021). ...
... n. (n=2) collected in the Verdzistava II Cave (Racha-Lechkhumi and Kvemo Svaneti, Georgia) is very low, 0.005±0.0003 substitutions per 100 nucleotide positions (about 0.5%), indicating that the two specimens belong to the same species, and being similar to other known species of the genus Xiphocaridinella (see Marin, 2017aMarin, , 2018aMarin, , b, 2019Marin, , 2020Marin, Turbanov, 2021). The interspecific K2P-distances between Xiphocaridinella lechkhumensis sp.n. ...
... DNA EXTRACTION. Partial fragment of the cytochrome c oxidase subunit I gene (COI) of the mitochondrial DNA is used as one of the most informative markers for assessing species status within Xiphocaridinella (Avise, 1993;Sket, Zakšek, 2009;Marin, 2017aMarin, , b, 2018aMarin, , b, 2019Marin, , 2020. Total genomic DNA was extracted from muscle tissue of the pleon using the innu-PREP DNA Micro Kit (AnalitikJena, Germany). ...
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An integrative approach resulted in a description of a new species of stygobiotic shrimps of the genus Xiphocaridinella Sadowsky, 1930 (Crustacea: Decapoda: Atyidae) from the southern part of the Racha-Lechkhumi and Kvemo Svaneti Region of the Western Georgia (SW Caucasus). The area and caves, from which this species is recorded will be flooded during the construction of the Tvishi hydroelectric power plant and it is unknown whether it will be possible to find the species again. Xiphocaridinella lechkhumensis sp.n. is easily separated from the other species of the genus both morphologically and genetically, as evidenced by barcoding segments of the mitochondrial COI gene marker (barcoding). In addition, we discovered a new population of X. kumistavi Marin, 2017 in the Satevzia Cave from Imereti Region. This population genetically diverged from the type series from the Prometheus Cave by the barcoding gap of 2.4%. The genus Xiphocaridinella in the Colchis Valley of the SW Caucasus now encompasses 15 species.
... The stygobiotic atyid shrimp genus Xiphocaridinella Sadowsky, 1930 (Crustacea: Decapoda: Atyidae) currently includes 13 valid species described in the subterranean water habitats of the southwestern Caucasus, from the northern and northwestern part of Kolkhida coastal lowland plain (Colchis) of the southwestern Caucasus [Sadowsky, 1930;Birštein, 1939Birštein, , 1948Juzbaš'jan, 1940Juzbaš'jan, , 1941Marin, Sokolova, 2014;Marin, Sinelnikov, 2017;Marin, 2017aMarin, , b, 2018aMarin, , b, 2019Marin, , 2020Marin, Turbanov, 2021]. The knowledge about these stygobiotic shrimps living in underground (stygobiotic) habitats is still incomplete, and new species have been discovered to date. ...
... DNA EXTRACTION. The cytochrome c oxidase subunit I (COI) mtDNA gene marker is used as one of the most informative markers for genetic studies at population and species level for marking species within Xiphocaridinella species complex [Avise, 1993;Sket, Zakšek, 2009;Marin, 2020]. Total genomic DNA was extracted from muscle tissue using the innuPREP DNA Micro Kit (AnalitikJena, Germany). ...
... (n=1) and other Caucasian Xiphocaridinella species are more 0.06 substitutions per 100 nucleotide positions (more than 6%); the phylogenetically closest species is X. dbari, which is known also from Verevkina Cave (-2130 m) and the Gegskaya (Gega) Cave (43°23′43.7″N 40°27′28.4″E) of the same Gagra Ridge (see Marin [2020] Sadowsky, 1930 Xiphocaridinella demidovi sp.n. Рис. 1. Xiphocaridinella demidovi sp.n., $, голотип, pcl. ...
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A new species of the genus Xiphocaridinella Sadowsky, 1930 (Crustacea: Decapoda: Atyidae), Xiphocaridinella demidovi sp.n., and two specimens of X. dbari Marin, 2019 are described from the bottom section (–2212 m) of the world’s deepest Verevkina Cave, located in the Arabika karst massif of the Gagra Ridge, southwestern Caucasus. Consequently, these species are the most deep living troglobionts/stygobionts in the world, whose taxonomic status is officially confirmed. Based on morphology and DNA analysis, both species are closely related representing sister clade separated for 6% by COI mtDNA gene marker. From the latter species and related congeners, the new species can be easily separated by a relatively long rostrum, pointed distally and reaching the distal margin of basal antennular segment, slender carpus of pereiopod II, the presence of 3 ischial spines and reduced exopods on pereiopods III–IV as well as stouter/wider telson. Due to the discovery of Xiphocaridinella demidovi sp.n., 14 species of the genus Xiphocaridinella are currently known from the Colchis Lowland of the southwestern Caucasus.
... whose waters passing through the valley drained over 1-1.5 km away, absorbed into the channel ponor caves -Pakchuchaya, Kholodnaya (=Kamnepadnaya), Vodopadnaya (=Bolshaya Medveditsa) and others. Significant fluctuations in the water level in the lake the Besletka Cave during a powerful flood in May 2017 (Marin, 2020). This species is described herewith as a new to science. ...
... 41°20'02.0"E) (Juzbaš'jan 1940(Juzbaš'jan , 1941, X. falcirostris Marin, 2020 from the Nizhne-Shakuranskaya and Besletka caves (Marin, 2020) and X. smirnovi Marin, 2020 from the Besletka Cave (Marin, 2020). ...
... 41°20'02.0"E) (Juzbaš'jan 1940(Juzbaš'jan , 1941, X. falcirostris Marin, 2020 from the Nizhne-Shakuranskaya and Besletka caves (Marin, 2020) and X. smirnovi Marin, 2020 from the Besletka Cave (Marin, 2020). ...
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Based on the morpho-genetic study of stygobiotic shrimps from the genus Xiphocaridinella Sadowsky, 1930 (Crustacea: Decapoda: Atyidae), a hydrogeological connection of a number of distant caves in Central Abkhazia of the southwestern Caucasus is satisfied, which indicates the possibility of using biospeleological studies in some cases to identify karst hydrosystems together with traditional hydrogeological methods. Moreover, a new stygobiotic atyid shrimp from the genus Xiphocaridinella , X. kelasuri sp. n., is described based on morphology and analysis of mitochondrial cytochrome oxidase I DNA sequences from three distant caves. The new species is genetically divergent from relatives and phylogenetically related to Xiphocaridinella smirnovi Marin, 2020, described from the Besletka (=Tskaro) Cave. Recently, the number of described speciesof the genus Xiphocaridinella from Caucasus has increased to 13 species, while the diversity of Xiphocaridinella found in the Besletka (=Tskaro) Cave is increasing to 3 species, which is higher than in any other known cave where Troglocaris -like shrimps have been discovered.
... Our records suggest that the hydrological systems of the Lethe caves (Bou-Atni area), El-Khadim and Al-Jebah caves (Al-Coeffiah area) are somehow interconnected, as both habitats harbor the same species of stygobiotic shrimp, T. lethaea, which is commonly observed. Furthermore, some biospeleological methods that study the DNA of subterranean stygobiotic animals and enable the establishment of biogeographic connections between underground watercourses should be used in conjunction with traditional hydrogeological methods to connect caves (Marin 2020;Marin and Turbanov 2021). This method can be applied in future research based on our findings, as well as other stygobiotic animals that may be prevalent in subterranean watercourses. ...
Article
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This study confirms the existence of the blind cave shrimp Typhlocaris lethaea Parisi, 1920, in Lethe Cave, Benghazi, Libya, nearly a century after its initial discovery, and documents its new distribution in the Al-Coeffiah caves. Field surveys conducted in 2023 and 2024 revealed its presence in the El-Khadim and Al-Jebah caves, extending its known range by 9 km. Specimens were found in subterranean lakes characterized by complete darkness, with water parameters including an average temperature of 22 °C, pH of 7.67, and salinity of 4.72 ppt. Two specimens were used for further analysis. These findings suggest that the species is more widespread than previously thought and highlight the potential hydrological connections within the karstic system. Additionally, the discovery of a depigmented isopod in El-Khadim cave suggests further hidden biodiversity. Given its IUCN data-deficient status, our findings emphasize the need for conservation efforts to protect these fragile ecosystems from human impacts, ensuring the preservation of Libya’s unique subterranean biodiversity.
... Xiphocaridinella shrimps from the order Decapoda are the second most important genus of the aquatic fauna of the Caucasian caves; species of this genus also dominate some communities, often in large numbers of individuals. Today, the genus is being closely examined and new species are being described (Marin, 2020). ...
Chapter
Invertebrates which are native to the caves of the Caucasus Mountains are still poorly studied. Many of them are endemics with narrow ecological tolerances, and new species are frequently discovered. Regrettably, none of the Caucasian cave invertebrate species is included in the IUCN Red List, and very few are protected on the national level by inclusion in national Red Books and Red Lists. The restricted range area, increasing pressure on the habitats from tourism development, and lack of protection measures make cave invertebrates vulnerable. For the purpose of effective protection, it is advisable to assess Caucasian cave invertebrates using the IUCN categories and criteria. The official inclusion in the Red List would facilitate setting up protected areas in the caves where they live and thereby ensure the conservation of species.
... At the same time, the Caucasus is the second region of the Western Palearctic (after the Balkan Peninsula) in term of karst area size, variety of landscapes and climatic conditions (e.g., Myers et al., 2000;Krever et al., 2001). Since 2010, recent biospeleological studies in the Crimean Peninsula, the Russian Caucasus and the adjacent regions of Abkhazia have focused mainly on the diversity and ecology of the diplopods (Golovatch, 2011;Golovatch, Chumachenko, 2013;Golovatch et al., 2016;Antić, Makarov, 2016;Antić et al., 2018;Antić, Reip, 2020), cave carabid beetles (Belousov, Koval, 2009Giachino, 2011;Reboleira, Ortuno, 2014) and arachnids (Tchemeris, 2013), cave shrimps (Marin, Sokolova, 2014;Marin, 2017Marin, , 2018Marin, , 2019Marin, , 2020Marin, Turbanov, 2021), crangonyctid (Sidorov, 2015) and gammarid amphipods (Sidorov et al., 2015a(Sidorov et al., , b, 2018Sidorov, 2016;Sidorov, Samokhin, 2016), woodlice (Gongalsky, Taiti, 2014;Turbanov, Gongalsky, 2016), springtails (Collembola) (Jordana et al., 2012;Vargovitsh, 2012Vargovitsh, , 2013, false scorpions (Kolesnikov, Turbanov, 2020), stygobiotic gastropods (Vinarski et al., 2014;Grego et al., 2017Grego et al., , 2020Vinarski, Palatov, 2019;Chertoprud et al., 2020Chertoprud et al., , 2021 and some other subterranean animals (e.g., Golovatch et al., 2018). These data are mostly taxonomic, without any conclusions about the origin and phylogeny of these subterranean animals. ...
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The article presents a morphogenetic revision of the relatively small Niphargus “tauricus” ingroup of the “stygius” species group (Crustacea: Amphipoda: Niphargidae), that lives in the coastal caves/springs of Dobrogea in Romania, the Crimean Peninsula and the south-western foothills of the Caucasus Mountains. Six species, namely Niphargus utrishensis Marin et Palatov sp.n., Niphargus novorossicus Marin et Palatov sp.n., Niphargus alisae Marin, Krylenko et Palatov sp.n., Niphargus ashamba Marin, Krylenko et Palatov sp.n., Niphargus malakhovi Marin et Palatov sp.n. and Niphargus dederkoyi Marin et Palatov sp.n. are described from the Black Sea coastal foothills of the south-western part of the Caucasus Mountains. Crimean Niphargus tauricus Birštein 1964 is re-described based on topotypic material. Morphological diagnoses, key for species identification, as well as molecular sequence data (COI mtDNA gene marker) are represented for all species of the “tauricus” ingroup. It is assumed that these species are Euxinian relicts of the Eastern Paratethys and were settled in their current habitats at the end of the Miocene at least 5 Mya. According to the data obtained, the related species of the ingroup are confined to the same mountain ridge, which suggests that the settlement occurred by several "waves". At the same time, we suppose that the modern species distribution is shaped rather by the uplift of Caucasian coastal mountain ridges and karst fragmentation occurred during the the last 2–3 Mya (since Late Pliocene–Early Pleistocene) than the fluctuation of the sea level. Because these animals are not able to disperse actively, we believe that these unique ancient genetic lineages (species) and their biotopes (underground water habitats) are in need of especial protection.
... How to cite this article : Marin I.N. 2020. The Quaternary speciation in the Caucasus: a new cryptic species of stygobiotic amphipod of the genus Niphargus ...
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A new cryptic species of stygobiotic amphipod of the genus Niphargus Schiödte, 1849 (Amphipoda: Niphargidae) is described from underground stream and lakes in the Kumistavi (Prometheus) Cave, Tskaltubo–Kumistavi, Imereti region of the Western Georgia, Caucasus, based on morphology and DNA analysis. The new species belongs to the “carpathicus“ species complex with the representatives in Europe, Caucasus and Iran, but clearly differs from all Caucasian congeners by stout telson, which is about as long as wide (vs. about not less than 1.5 times in other relative species); relatively stout basal part of dactyli of pereopods V–VII, which is about as long as wide (vs. usually more than 1.5 times as long as wide in other related species); and almost rectangular palm of gnathopods I and II with straight distal margin (vs. usually sloped distal margin in other relative species). The sister species N. borutzkyi Birštein, 1933, inhabiting the neighboring, but isolated underground karst system, including of the Sataplia, Sapichkhia and Tskaltsitela caves, differs from the new species in some minor morphological features and genetically (about 10% or 0.1 substitutions per 100 nucleotides by COI gene marker). The phylogenetic analysis of available genetic data (COI mtDNA) shows that karsts regions in the vicinity of Kutaisi are currently inhabited by closely related Niphargus species descended from the ancestral taxon in the Quaternary as a result of geological processes that caused fragmentation of the ancestral range.
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The complete re-description of Caucasian local endemic stygobitic atyid shrimp Troglocaris (Xiphocaridinella) jusbaschjani Birštein, 1948 is firstly presented after its original description given by Dr. Ya. A. Birštein (1948) under the name Troglocaris schmidti jusbaschjani. The species is still known exclusively from the type locality, hydrogen sulfide bathes of the small Agura River, Sochi area, Russian Federation. Remarks on morphology, coloration of both females and males and data on ecology of Troglocaris (Xiphocaridinella) jusbaschjani Birštein, 1948 as well as remarks on morphology of relative congeneric species from Caucassus, Troglocaris (Xiphocaridinella) kutaissiana (Sadowsky, 1930) (type species of the subgenus) and Troglocaris (Xiphocaridinella) fagei Birštein, 1939, are provided. Discussion on the validity of some subgenera within the genus Troglocaris s. str. Dormitzer, 1853 are also presented.
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A selection of the most representative distribution patterns of stygobiont animals is presented. The range of a genus may extend beyond the Dinaride karst, while some species exhibit a holo-Dinaric distribution. The mero-Dinaric distribution is organised in two vicarious centres (in the NW and SE) as well as an epilittoral and a paralittoral belt. The paralittoral distribution is a result of paleogeographic rather than present-day ecological conditions. Important differences between the interstitial faunas of Slovenia (and NE Italy) and Macedonia are probably the result of their different sources. Some other distribution patterns are discussed or summarized from the existing literature. The distribution patterns of this stygobiont fauna are extremely diverse, and are influenced by the geological complexity of the territory as well as by the richness of the fauna concerned. New distribution data for some Copepoda, Thermosbaenacea, and Amphipoda are appended.Predstavljen je izbor najznailnejih vzorcev razirjenosti stigobiontskih ivali. Areal rodu lahko vkljuuje ve kot le Dinarski kras, holodinarsko razirjenost pa e kaejo posamezne vrste. Merodinarska razirjenost izhaja iz dveh centrov (na SZ in na JV) ali pa je epilitoralna ali paralitoralna. Paralitoralna razirjenost je vezana na paleogeografske in ne na dananje ekoloke razmere. Pomembne razlike med intersticialnima favnama Slovenije (in SV Italije) in Makedonije so verjetno posledica njunega razlinega izvora. Obravnavani ali pa povzeti iz obstojeih razprav so e nekateri vzorci razirjenosti. Vzorci razirjenosti tukajnje stigobiontske favne so izredno raznoliki, kar je posledica geoloke pestrosti ozemlja, kot tudi izrednega bogastva favne. Dodani so novi podatki o razirjenosti nekaterih kopepodov, termosbenacejev in amfipodov.
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The remarkably discontinuous distribution of the cave shrimp genus Troglocaris in South France, West Balkans, and West Caucasus has long been considered a biogeographic enigma. To solve it, its phylogeny was reconstructed by analyzing sequences from two mitochondrial (cytochrome oxidase I and 16S rRNA) and one nuclear gene (28S rRNA) using maximum likelihood, parsimony and Bayesian inference. The genus was found to be polyphyletic because the French taxon T. inermis had no direct common ancestry with other Troglocaris taxa but was sister to the epigean freshwater atyid Dugastella valentina. All other Troglocaris species constituted a well-supported monophylum, the second cave shrimp genus Spelaeocaris nested within. The monophylum had a well-defined structure: (1) a clade restricted to the Dinaric area of the Western Balkans containing the type species T. anophthalmus along with some unnamed species, and (2) a geographically mixed clade split between the Caucasian T. kutaissiana species complex on one, and T. hercegovinensis, S. pretneri, plus an unnamed taxon on the other side. It was surprising to find the dichotomy between the Caucasian and one of the West-Balkan lineages so low in the phylogenetic hierarchy of the genus. Taking into account molecular rates of other decapods, we tentatively dated this split at 6-11 Myr. This time is in agreement with the brackish and freshwater phase of the Paratethys thus allowing for a freshwater common ancestor of Caucasian and Dinaric cave shrimps. This would weaken the marine relicts hypothesis that has often been invoked to explain the distribution of freshwater cave species with close marine relatives.
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Secondary sympatric occurrence of sibling species of subterranean shrimps in the Karst
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