Euxinian relict amphipods of the Eastern Paratethys in the subterranean fauna of coastal habitats of the Northern Black Sea region

CHERTOPRUD E.M., PALATOV D.M., VINARSKI M.V.

A taxonomic revision of the stygobiont microsnails from north-western Transcaucasia (Krasnodar Krai, Russia) is presented. Two new genera—Schapsugia gen. n. and Tachira gen. n. are established. It is shown that the genus Paladilhiopsis does not occur in this area, and the snails previously assigned to this genus belong to Schapsugia gen. n. Two nominal species Paladilhiopsis orientalis Starobogatov, 1962, and P. subovata Starobogatov, 1962 are considered junior synonyms of Sch. pulcherrima (Starobogatov, 1962), based on a re-examination of their conchological variation. In addition, two more species of Schapsugia are described: Sch. kudepsta sp. nov. and Sch. occultata sp. nov. The anatomical structure of another species, Geyeria valvataeformis Starobogatov, 1962 was studied for the first time. It is revealed that it should be placed in a separate genus (Tachira gen. n.). Thus, the previously proposed placement of the microsnails from north-western Transcaucasia in hydrobiid genera from the Balkan Peninsula (Geyeria, Paladilhiopsis) is rejected.

Palatov D.M., Marin I.N.

Marin I., Palatov D.

An endemic subterranean species of the genus Niphargus Schiödte, 1849 (Crustacea: Amphipoda: Niphargidae) belonging to the cave-dwelling “ carpathicus ” species group is discovered inside an abandoned mine in the Republic of North Ossetia–Alania, Russian Federation. This is the first record of the genus Niphargus from the central mountainous part of on the northern slope of the Greater Caucasian Ridge. Integrative taxonomy revealed that new species is closely related to European Niphargus ambulator than any of the Caucasian species, and has survived in cryptic refugia since the Miocene for more than 5.5Mya. It can also be assumed that the genus Niphargus was also previously distributed in the territory beyond the Caucasian Ridge to the North Caucasus and probably throughout the pre-Caucasian plain (Ciscaucasia). It is likely that most of the species from the Ciscaucasia became extinct presumably during the Pleistocene (Quaternary) glacial episodes or earlier, although we still expect the new relict species in cryptic refugia. Our study also suggests that subterranean species are narrowly localized and require strict protection and attention to their habitats, since the destruction of population leads to the loss of a unique genetic lineage and it is unlike to recover.

MARIN I., KRYLENKO S., PALATOV D.

A new species of the genus Niphargus is described from the Gelendzhik–Tuapse area of the Russian southwestern Caucasus. It belongs to the “puteanus” species group and phylogenetically related to Caucasian N. ciscaucasicus and N. talikadzei, separating from other Caucasian species of the genus by the presence of 2 hooks in retinacules on pleopods, different rami of uropod I both in males and females, and relatively large inner ramus of uropod III. Molecular study has revealed that Niphargus bzhidik sp. nov. and related N. ciscaucasicus are relicts of the Late Miocene speciation, associated with the Messinian crisis (5.96–5.33Mya) separated widespread Paratethys species, which survived in long-term genetic isolation for a long time. The new species is blind and epigean, and probably unable to spread over long distances, but this way of life probably allowed surviving in refugee during the Quaternary period with a colder climate. Analysis of stable isotopes (δ13C/δ15N) revealed that the new species is carnivorous, in contrast to another studied stygobiotic herbivorous Niphargus species (e.g., Niphargus cf. tauricus). The key to the Caucasian and Eastern Asian species of the genus Niphargus, known from the territory of the former USSR, is presented in the article. [http://zoobank.org/urn:lsid:zoobank.org:act:E0019189-2432-4B64-B153-94C43FDD93E3]

Bargrizaneh Z., Fišer C., Esmaeili-Rineh S.

Chertoprud E.M., Palatov D.M., Vinarski M.V.

A new genus of stygobiont hydrobiid snails, endemic to Georgia, is described. Sitnikovia gen. nov. includes two species: S. megruli sp. nov. and S. ratschuli sp. nov., known only from their type localities (Garakha and Sakishore caves). The data of shell characters, penial morphology, and radula of the new genus are provided.

Marin I.N.

Stoch F., Christian E., Flot J.

The Niphargus tatrensis species complex, entirely subterranean, has a wide distribution range extending from Southern Poland to Austria and Slovenia. Because of its large and confusing morphological variability, it was subdivided into several ‘forms’, four of which described from Austrian caves. To shed light on this chaotic situation, we sampled the type localities of all described species and forms in the complex, as well as additional sites in Austria, and used nuclear (28S, ITS) and mtDNA (COI) sequences to revise its taxonomy. Phylogenetic analysis confirmed that the Niphargus tatrensis species complex is monophyletic. Applying four species delimitation methods to the COI dataset converged on the presence of four species in Austria; by contrast, the same methods applied to ITS concurred with a haploweb analysis of this marker in distinguishing only three species in the country. Reconstruction of ancestral ranges suggested that the Austrian clade originated in Eastern Europe. Bayesian biogeographical analyses revealed a complex history of lineage divergence and secondary contact during the Pleistocene climatic fluctuations, possibly responsible for the higher variability of COI in comparison with ITS. Based on the above, we conclude that only three valid species are present in Austria: considering all described forms as subspecies, two of them are elevated to species rank whereas one new species is formally described and illustrated.

Antić D.Ž., Reip H.S.

The Caucasian leucogeorgiinine genera Archileucogeorgia Lohmander, 1936 and Leucogeorgia Verhoeff, 1930 are revised, with Leucogeorgia being considered as a senior subjective synonym of Archileucogeorgia, syn. nov. The following new combinations are thus warranted: Leucogeorgia abchasica (Lohmander, 1936) and L. satunini (Lohmander, 1936), both comb. nov. ex Archileucogeorgia. All four previously described species, viz., L. longipes Verhoeff, 1930, L. abchasica, L. satunini and L. rediviva Golovatch, 1983, are redescribed based on new material, partly also on the type series, with a lectotype being designated for L. longipes. In addition, eleven new species of Leucogeorgia are described, both with normal (L. borealis sp. nov., L. gioi sp. nov., L. golovatchi sp. nov., L. lobata sp. nov., L. oculata sp. nov. and L. prometheus sp. nov.) and modified mouthparts (L. caudata sp. nov., L. mystax sp. nov., L. profunda sp. nov., L. redivivoides sp. nov. and L. turbanovi sp. nov., all clearly troglobionts). Additionally, a new monotypic genus, Martvilia gen. nov., is erected, with M. parva gen. et sp. nov. as the type species, another presumed troglobiont. An identification key to both genera and all 16 species of Caucasian Leucogeorgiini is presented. Several other members of this tribe are also re-examined, including a syntype male of Telsonius nycteridonis Strasser, 1976, from Greece, herewith designated as the lectotype. Troglomorphisms and mouthpart modifications, as well as the distributions and relationships within both Leucogeorgia and Leucogeorgiini, and a Leucogeorgiini species richness estimate for the western Caucasus are discussed.

Grego J., Mumladze L., Falniowski A., Osikowski A., Rysiewska A., Palatov D.M., Hofman S.

Marin I.N.

MARIN I., PALATOV D.

The precopulatory mate guarding (amplexus) was observed in epigean Niphargus cf. magnus Birštein, 1940 collected near Tuapse in the Western Caucasus of Russia. The records of amplexing representatives of the subterranean genus Niphargus Schiödte, 1849 (Crustacea: Amphipoda: Niphargidae) are extremely rare, and there are no publications describing the amplexus in this amphipod genus. The presented report shows that Niphargus have a chemically stimulated short-time amplexus immediately after the molt of the female, similar to the representatives of relative epigean and subterranean gammaridean amphipods. It is relatively short in time, possibly, because of adaptation to inhabit narrows spaces in underground habitats. 

Marin I., Palatov D.

A new endemic species of the genus Niphargus is described from the vicinity of Apsheronsk, Krasnodar region, North Caucasus. Genetic and morphological studies show that the new species is related t...

Vinarski M.V., Palatov D.M.

Fišer C., Delić T., Luštrik R., Zagmajster M., Altermatt F.

Species that successfully colonized subterranean environments are subject to two opposing selection processes. Stringent abiotic factors select for convergent adaptations, such as loss of eyes and pigments, while interspecific competition drives between-species divergence. Subterranean species can resolve opposing selection by adaptation to physically different microhabitats. Yet, species frequently co-occur in physically homogeneous subterranean habitats, like interstitial. These co-occurrences in such a narrow ecological context can be explained either by equalizing mechanisms, in which neither of the co-occurring species has a competitive advantage, or by more complex niche models that include species’ differentiation along a trophic niche axis. We tested these hypotheses using the amphipod genus Niphargus. We analysed Europe-wide co-occurrence records of Niphargus species from interstitial habitats, split into six independent large-scale regions. Firstly, we addressed whether species’ pairwise co-occurrences are random using a probabilistic model. Secondly, we tested whether species cluster into distinct functional–morphological groups and whether ecologically or phylogenetically distinct species are more likely to co-occur. We found that 68% of species co-occurrences were not different from random expectation, indicating that most species had access to most sites within each region. The remaining 32% co-occurred either significantly more or less often than expected by chance. Cluster analysis of functional morphological characters showed that interstitial species belong to two feeding types, micro- and macrofeeders, likely representing two peaks of the interstitial adaptive landscape, and hinting that niche divergence, as a mechanism allowing coexistence, is favoured. Finally, we found that the number of co-occurrences increases with increasing differentiation of functional morphology, but not phylogenetic differences. We conclude that ecological differentiation may be important in shaping such interstitial communities.

Palatov D.M., Chertoprud E.M.

Marin I.N., Palatov D.M.

Marin I.N., Palatov D.M.

A review and partial revision of the diversity of freshwater stygobiotic crustaceans in the territory of the Republic of North Ossetia–Alania, in the North Caucasus, is presented here. Previously, two species of the genus Proasellus Dudich, 1925 (Isopoda, Asellidae), P. uallagirus Palatov & Sokolova, 2020 and P. irystonicus Palatov & Sokolova, 2020, and one species of the genus Niphargus Schiödte, 1849 (Amphipoda, Niphargidae), N. alanicus Marin & Palatov, 2021, were described from the hyporhean/underground habitats (hyporhea) in the area. However, further research using an integrative approach has revealed that only a single species of the genus Proasellus (P. uallagirus) is actually widely distributed in the hyporhean riverbed habitats in the area, while the diversity of the genus Niphargus is higher than previously known. Six more new Niphargus species— namely, N. ardonicus sp. nov., N. sadonicus sp. nov., N. fiagdonicus sp. nov., N. tschertschesovae sp. nov., N. osseticus sp. nov. and N. zeyensis sp. nov., were discovered from the various hypogean underground water sources (i.e., springs and seeps) and are described in this article. Their phylogenetic relationships with their congeners, as well as their ecology and known distribution, are discussed. Furthermore, molecular genetic analysis, with an interpretation of the estimated divergence time, suggests that the studied hyporheic/stygobiotic crustaceans started to diverge from related European and Balkan sister species during the Late Miocene, approximately 8–5.8 Mya, with the reduction in the Paratethys and the uplifting of the Caucasus Mountains. Local speciation was led by local geological processes and karst fragmentation during the Late Pliocene and Early Pleistocene periods, starting around 5.3 Mya. The obtained data suggest that the mountainous area of the North Ossetia–Alania could be considered as a post-Pliocene glacial refugium for subterranean and stygobiotic fauna—the first known for the North Caucasus region.

MARIN I., BARJADZE S., MAGHRADZE E., PALATOV D.

Two new Caucasian species of the genus Niphargus Schiödte, 1849 (Crustacea: Amphipoda: Niphargidae), N. rachalechkhumensis sp. nov. and N. tvishiensis sp. nov., are described from the stygobiotic habitats of the Racha-Lechkhumi and Kvemo Svaneti karst systems in Western Georgia. Both newly described species belong to the southwestern Caucasian “Niphargus borutzkyi” ingroup related to the European “carphaticus” species complex and can be clearly separated from the congeners by morphological features, mostly in uropod III and epimeral plates, and genetically. Identification key for all known species to the “Niphargus borutzkyi” ingroup is provided, as well as their phylogenetic relationships, the estimated time of the origin and the current distribution of the ingroup in the Colchis lowland of the southwestern Caucasus are also discussed.  

MARIN I., PALATOV D., COPILAȘ-CIOCIANU D.

The first insight into the unexpectedly diverse amphipod assemblage of the Durso River (Novorossiysk area) in the SW mountainous pre-Caucasian area is presented. The presence of six species is revealed, including three new records for the area and one species new to science. The phylogenetic relationships of all studied species and their relatives were examined based on the divergence of the COI mtDNA gene marker (barcoding). The conducted research clearly showed that the coastal part of the Black Sea and the adjacent pre-Caucasian river/land areas harbors a significant undescribed diversity, and that the transitional sea/river brackish biotopes are important reservoirs of the endemicity. A new genus, Litorogammarus gen. nov. is proposed for native pebble-dwelling species, namely Echinogammarus karadagiensis Grintsov, 2009, Echinogammarus mazestiensis Marin & Palatov, 2021 and the newly discovered Litorogammarus dursi sp. nov., from the lower (estuarine) part of the Durso River and adjacent coastal areas. These three species form a strongly supported molecular clade and share a number of characters such as smooth body without carinae and setae, antenna II armed with dense curled setae, lacking calceoli, pereopods III–VII with sparse, short setation, epimeral plates armed with spines only, telson lobes longer than broad, gradually tapering, bearing only spines. Pectenogammarus oliviiformis (Greze, 1985) comb. nov. is also discovered in the area and is re-described herein. Although this is probably one of the most abundant and common coastal pebble-dwelling species along the northeastern coasts of the Black Sea, it was previously poorly described and thus overlooked by researchers.  

Marin I.N., Palatov D.M.

A new species of the genus Niphargus Schiödte, 1849 (Crustacea: Amphipoda: Niphargidae), co-existing with other stygobiotic amphipods, Diasynurella kiwi Marin and Palatov, 2023 and Pontonyx donensis (Martynov, 1919) (Crangonyctidae), is described from a small spring on a shore of Kiziterinka River in Rostov-on-Don City in the mouth of the Don River. Two of the three species in the studied spring, D. kiwi and the discovered Niphargus, belong to microcrustaceans not exceeding the total body size of 3 mm. The new species, Niphargus rostovi sp. nov., represents one of the smallest species within the genus and is mostly related to the Greek Niphargus karkabounasi Ntakis, Anastasiadou, Zakšek and Fišer, 2015, which is also not reaching the body size of 3 mm. One more related undescribed species is found on the Crete Island by the molecular genetic data. These species represent a separate phylogenetic lineage within the “carpathicus” species complex, which diverged from the congeners in the Late Miocene for more than 10 Mya. At the same time, the speciation within the ingroup started about 5–6 Mya, obviously correlating with the drainage of the Euxinian basin of the Eastern Paratethys, connecting the lower Don and southern Greece areas. Niphargus potamophilus Birštein, 1954 is also first recorded from the mouth of the Belbek River in the Crimean Peninsula, closing the known area from the Kuban River delta to Rostov-on-Don area and further along the western coast of the Black Sea to Bulgaria. Analysis of the recent records of long-time lineages of endemic/subterranean/stygobiotic animals unable to disperse for long distances assumed that glacial refugium existed at the mouth of the Don River, along with the South Caucasus (Colchis) and the southern Caspian (Hyrcania), where many species have survived several periods of glaciation since the late Miocene.

Copilaș-Ciocianu D., Palatov D., Rewicz T., Sands A.F., Arbačiauskas K., van Haaren T., Hebert P.D., Grabowski M., Marin I.

Abstract Amphipods have diversified greatly in the Ponto-Caspian region. Although many of these species are prominent invaders their systematics remains unclear. Taking an integrative approach, we investigate the taxonomy of Trichogammarus trichiatus, a widespread invader in European inland waters. It was initially described from the north-eastern Black Sea coast as Chaetogammarus trichiatus by Martynov in 1932. A similar taxon, Chaetogammarus tenellus major, was described by Cărăușu from the western Black Sea in 1943 but later synonymized with C. trichiatus. Chaetogammarus trichiatus was itself shuffled between Chaetogammarus and the Atlanto-Mediterranean Echinogammarus, currently being assigned to Trichogammarus. Our analyses (six DNA markers, 60 measurements and scanning electron microscopic imaging) reveal that T. trichiatus and C. tenellus major are distinct species; the former is a Caucasian endemic, whereas the latter invaded Europe. Unexpectedly, T. trichiatus is an incipient species molecularly nested in Chaetogammarus ischnus, despite pronounced morphological and geographical differentiation. We also recover Chaetogammarus as polyphyletic, yet its member species are nested in the Ponto-Caspian radiation, thus distinct from Echinogammarus. Consequently, we reassign T. trichiatus to Chaetogammarus (Chaetogammarus trichiatus), synonymize Trichogammarus with Chaetogammarus and place C. tenellus major in the new genus Spirogammarus gen. nov. (Spirogammarus major comb. & stat. nov.). Chaetogammarus necessitates further systematic refinement.

Chertoprud E., Grego J., Mumladze L., Hofman S., Palatov D., Osikowski A., Jaszczyńska A., Falniowski A.

Since 2020, the south-western Caucasus has been recognized as a hotspot of stygobiotic Mollusca diversity after revealing a large number of new, range-restricted species within the spring snail family Hydrobiidae, subfamily Sadlerianinae sensu Szarowska. Meantime, based on extensive material collected in the south-western Caucasus during the last decades, we studied members of another spring snail subfamily Belgrandiellinae Radoman, 1983. Modern integrative taxonomic work revealed hitherto unknown diversity within this subfamily in the region and further proved the importance of the south-western Caucasus as a hotspot of stygobiotic life. In particular, the subterranean environment and springs of Georgia were known to be inhabited by the genus Tschernomorica Vinarski and Palatov, 2019 with four nominal species. Our research, based on a morpho-anatomical study and genetic investigation of COI/H3 mitochondrial/nuclear markers, revealed additionally seven species and three genera new to science—Colchiella lugella gen. et sp. nov., C. nazodelavo gen. et sp. nov., C. shiksa gen. et sp. nov., C. dadiani gen. et sp. nov., Sataplia cavernicola gen. et sp. nov., Aetis starobogatovi gen. et sp. nov., and Tschernomorica kopidophora sp. nov. —to inhabit the Georgian part of south-western Caucasus. The full taxonomic description of each new taxa, along with the review of habitat characteristics and conservation status, is provided. Molecular genetics suggests that the ancestors of Caucasian Belgrandiellinae have migrated from south-western Europe, probably more than once during the late Messinian and early Pliocene periods. Later, Plio-Pleistocene climate oscillations, particularly the repeated rise and fall of the Black Sea water level, resulted in the isolation and radiation of various lineages within the Caucasus and Crimea.

Marin I.N., Palatov D.M.

Marin I.N., Turbanov I.S., Prokopov G.A., Palatov D.M.

A new species of the genus Niphargus Schiödte, 1849 (Crustacea: Amphipoda), co-occurring with water louse Asellus cf. aquaticus (Linnaeus, 1758) (Crustacea: Isopoda) in deep wells, is described from the Tarkhankut Upland, located in the northwestern part of the Crimean Peninsula. Niphargus tarkhankuticus sp. nov. corresponds to a separate phylogenetic lineage (the “tarkhankuticus” ingroup), also including several undescribed species from the coastal habitats of the Black Sea (the Crimean Peninsula, the southern Caucasus and the northern coast of Turkey), which is related to the paraphyletic European “stygius-longicaudatus” group. The divergence of the “tarkhankuticus” ingroup from the related European species probably appeared in the Late Miocene age, about 11–10 Mya, related to the separation of the Eastern Paratethys for different basins (Euxinian, Alpine and Pannopian). At the same time, the speciation within the ingroup started in Pliocene, about 5.76–3.6 Mya, and correlated with the Black Sea leveling and the drainage of coastal marine carbonate accumulations, including the Tarkhankut Upland. Intraspecific values of COI mtDNA gene markers (p-distances) for N. tarkhankuticus sp. nov. are about 2%, showing that the division into a number of isolated subpopulations, probably associated with local tectonic movements, the active formation of the river network, and further karst processes in the Tarkhankut Upland occurred during the Pleistocene (since 2.58 Mya). Analysis of stable isotopes (δ13C/δ15N) revealed that only discovered macrocrustaceans in the studied wells of the Tarkhankut Upland have non-overlapping trophic niches, with A. cf. aquaticus possibly feeding on algae/periphyton, while the trophic position of N. tarkhankuticus sp. nov. is close to predators.