Abstract
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.
References
- Adamowicz, S.J., Marinone, M.C., Menu-Marque, S., Martin, J.W., Allen, D.C., Pyle, M.N., De los Ríos, P., Sobel, C.N., Ibañez, C., Pinto, J. & Witt, J.D.S (2018) The Hyalella (Crustacea: Amphipoda) species cloud of the ancient Lake Titicaca originated from multiple colonizations. Molecular Phylogenetics and Evolution, 125, 232–242. https://doi.org/10.1016/j.ympev.2018.03.004 DOI: https://doi.org/10.1016/j.ympev.2018.03.004
- Astrin, J.J. & Stuben, P.E. (2008) Phylogeny in cryptic weevils: molecules, morphology and new genera of western Palaearctic Cryptorhynchinae (Coleoptera: Curculionidae). Invertebrate Systematics, 22, 503–522. https://doi.org/10.1071/IS07057 DOI: https://doi.org/10.1071/IS07057
- Bij De Vaate, A., Jazdzewski, K., Ketelaars, H.A.M., Gollasch, S. & Van Der Velde, G. (2002) Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Canadian Journal of Fisheries and Aquatic Sciences, 59, 1159–1174. https://doi.org/10.1139/f02-098 DOI: https://doi.org/10.1139/f02-098
- Chevreux, E. (1894) Gammarus simoni, nov. sp., Amphipode des eaux douces d’AIgerie et de Tunisie. Bulletin de la Société zoologique de France, 19, 171–176. https://doi.org/10.5962/bhl.title.15972 DOI: https://doi.org/10.5962/bhl.title.15972
- Copilaș‑Ciocianu, D. & Sidorov, D. (2022) Taxonomic, ecological and morphological diversity of Ponto‑Caspian gammaroidean amphipods: a review. Organisms Diversity & Evolution, 22, 285–315. https://doi.org/10.1007/s13127-021-00536-6 DOI: https://doi.org/10.1007/s13127-021-00536-6
- Copilaș-Ciocianu, D., Sidorov, D., & Šidagytė-Copilas, E. (2023) Global distribution and diversity of alien Ponto-Caspian amphipods. Biological Invasions, 25, 179–195. https://doi.org/10.1007/s10530-022-02908-1 DOI: https://doi.org/10.1007/s10530-022-02908-1
- Copilaş-Ciocianu, D., Rewicz, T., Sands, A.F., Palatov, D., Marin, I., Arbačiauskas, K., Hebert, P.D.N., Grabowski, M. & Audzijonyte, A. (2022) A DNA barcode reference library for endemic Ponto-Caspian amphipods. Scientific Report, 12 (1), 11332. https://doi.org/10.1038/s41598-022-15442-w DOI: https://doi.org/10.1038/s41598-022-15442-w
- Copilaş-Ciocianu, D., Palatov, D., Rewicz, T., Sands, A.F., Arbačiauskas, K., Ton van Haaren, Hebert, P.D.N., Grabowski, M. & Marin, I. (2023) A widespread Ponto-Caspian invader with a mistaken identity: integrative taxonomy elucidates the confusing taxonomy of Trichogammarus trichiatus (Crustacea, Amphipoda). Zoological Journal of the Linnean Society, XX, 1–26. https://doi.org/10.1093/zoolinnean/zlad010 DOI: https://doi.org/10.1093/zoolinnean/zlad010
- Cristescu, M.E.A. & Hebert, P.D.N. (2005) The “Crustacean Seas” – an evolutionary perspective on the Ponto-Caspian peracarids. Canadian Journal of Fisheries and Aquatic Sciences, 62, 505–517. https://doi.org/10.1139/F04-210 DOI: https://doi.org/10.1139/f04-210
- Cristescu, M.E., Adamowicz, S.J., Vaillant, J.J. & Hafner, D.G. (2010) Ancient lakes revisited: From the ecology to the genetics of speciation. Molecular Ecology, 19 (22), 4837–4851. https://doi.org/10.1111/j.1365-294X.2010.04832.x DOI: https://doi.org/10.1111/j.1365-294X.2010.04832.x
- Edgar, R.C. (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Researches, 32, 1792–1797. https://doi.org/10.1093/nar/gkh340 DOI: https://doi.org/10.1093/nar/gkh340
- Greze, I.I. (1985) Bokoplavy. Fauna Ukrainy. Vol. 26. Vyschije rakoobraznyje. Vypysk 5. Naukova Dumka, Kiev, 176 pp.
- García-París, M., Jurado-Angulo, P., Rodríguez-Flores, P.C. & Rosas-Ramos, N. (2023) Nomenclatural changes in a taxonomically complex group (Amphipoda: Gammaridae). Zootaxa, 5230 (5), 595–600. https://doi.org/10.11646/zootaxa.5230.5.7 DOI: https://doi.org/10.11646/zootaxa.5230.5.7
- Grintsov, V.A. (2009) A new amphipod species Echinogammarus karadagiensis sp. n. (Amphipoda, Gammaridae) from Crimean Coasts (Black Sea). Vestnik Zoologii, 43 (2), e23-e26. https://doi.org/10.2478/v10058-009-0007-9 DOI: https://doi.org/10.2478/v10058-009-0007-9
- Grintsov, V.A. (2016) Dynamics of population structure of two species of the genus Echinogammarus (Gammaridae, Amphipoda) from Laspi Bay (Crimea, Black Sea). Marine Biological Journal, 1 (3), 22–26. https://doi.org/10.21072/mbj.2016.01.3.03 DOI: https://doi.org/10.21072/mbj.2016.01.3.03
- Grintsov, V.A. (2022) Amphipods of the Black Sea: An Illustrated Guide Atlas. A.O. Kovalevsky Institute of Biology of the Southern Seas of RAS, IBSS, Sevastopol, 476 pp.
- Hou, Z. & Sket, B. (2016) A review of Gammaridae (Crustacea: Amphipoda): the family extent, its evolutionary history, and taxonomic redefinition of genera. Zoological Journal of the Linnean Society, 176 (2), 323–348. https://doi.org/10.1111/zoj.12318 DOI: https://doi.org/10.1111/zoj.12318
- Sket, B. & Hou, Z. (2018) Family Gammaridae (Crustacea: Amphipoda), mainly its Echinogammarus clade in SW Europe. Further elucidation of its phylogeny and taxonomy. Acta Biologica Slovenica, 61 (1), 93–102.
- Hou, Z., Sket, B. & Li, S. (2014) Phylogenetic analyses of Gammaridae crustacean reveal different diversification patterns among sister lineages in the Tethyan region. Cladistics, 30, 352–365. https://doi.org/10.1111/cla.12055 DOI: https://doi.org/10.1111/cla.12055
- Jurado-Rivera, J.A., Zapelloni, F., Pons, J., Juan, C. & Jaume, D. (2020) Morphological and molecular species boundaries in the Hyalella species flock of Lake Titicaca (Crustacea: Amphipoda). Contributions to Zoology, 89 (4), 353–372. https://doi.org/10.1163/18759866-bja10004 DOI: https://doi.org/10.1163/18759866-bja10004
- Latreille, P.A. (1802) Histoire Naturelle, Générale et Particulière des Crustacés et des Insectes. Ouvrage Faisant suite à l’Histoire Naturelle Générale et Particulière, Composée par LeClerc de Buffon, et Rédigée par C.S. Sonnini, Membre de Plusieurs Sociétés Savantes. Vol. 3. Dufart, Paris, 468 pp. DOI: https://doi.org/10.5962/bhl.title.15764
- Latreille, P.A. (1816) Nouveau Dictionnaire d’histoire naturelle, appliquée aux arts, à l’Agriculture, à l’Economic rurale et domestique, à la Médecine, etc. Par une Société de Naturalistes et d’Agriculteurs, Nouvelle Édition, Paris, 1, 467–469.
- Leach, W.E. (1813-1815) Crustaceology. In: Brewster, D. (Ed.), The Edinburgh Encyclopaedia. 7 (1), 7 (2) & 9 (1). Balfour, Edinburgh, pp. 383–384 (1813), 385–437 + 765–766 (1814) & pl. CCXXI [1815].
- Marin, I. & Palatov, D. (2021) New and non-alien: Echinogammarus mazestiensis sp. n. from the southwestern Caucasus (Amphipoda: Gammaridae). Zoology in the Middle East, 67 (4), 309–320. https://doi.org/10.1080/09397140.2021.1949139 DOI: https://doi.org/10.1080/09397140.2021.1949139
- Marin, I. & Palatov, D. (2022) Dursogammarus dromaderus gen. et sp. nov., a new Ponto-Caspian gammarid (Amphipoda: Gammaridae) from the coastal pebble habitats of the foothills of the Caucasus. Zoology in the Middle East, 68 (3), 237–246. https://doi.org/10.1080/09397140.2022.2116171 DOI: https://doi.org/10.1080/09397140.2022.2116171
- Marin, I., Krylenko, S. & Palatov, D. (2021) Euxinian relict amphipods of the Eastern Paratethys in the subterranean fauna of coastal habitats of the Northern Black Sea region. Invertebrate Zoology, 18 (3), 247–320. https://doi.org/10.15298/invertzool.18.3.05 DOI: https://doi.org/10.15298/invertzool.18.3.05
- Martynov, A. (1924) On some interesting Malacostraca from fresh-waters of European Russia. Russische Hydrobiologische Zeitschrift, 3, 210–216. [in Russian with English summary]
- Martynov, A.V. (1932) A contribution to the knowledge of the fresh-water fauna of the Black Sea coast of Caucasus. I. Amphipoda. Trudy Zoologicheskogo Instituta Akademii Nauk SSSR, 1, 73–98. [in Russian]
- Martens, K. (1997) Speciation in ancient lakes. Trends in Ecology and Evolution, 12 (5), 177–182. https://doi.org/10.1016/S0169-5347(97)01039-2 DOI: https://doi.org/10.1016/S0169-5347(97)01039-2
- Messiaen, M., Lock, K., Gabriels, W., Vercauteren, T., Wouters, K., Boets, P. & Goethals, P.L.M. (2010) Alien macrocrustaceans in freshwater ecosystems in the eastern part of Flanders (Belgium). Belgian Journal of Zoology, 140, 30–39.
- Milne Edwards, H. (1830). Extrait de recherches pour servir à l’histoire naturelle des crustacés amphipodes. Annales des Sciences Naturelles, 20, 353–399. https://doi.org/10.5962/bhl.part.12300 DOI: https://doi.org/10.5962/bhl.part.12300
- Morduhaj-Boltovskoj, F.D. (1960) Kaspiyskaya fauna v Azovo-Chernomorskom bassejne. Izdatelstvo Akademii Nauk SSSR, 56 (4), 1–288. [in Russian]
- Morduhaj-Boltovskoj, F.D., Geze, I.I. & Vasilenko, S.V. (1969) s.n. In: Otryad Amfipody, ili Raznonogie, Amphipoda/Opredelitel’ fauny Chernogo i Azovskogo morej. T.2. Svobodnozhivushchie bespozvonochnye. Rakoobraznye, Kiev, pp. 440–524 [in Russian]
- Nahavandi, N., Ketmaier, V., Plath, M. & Tiedemann, R. (2013) Diversification of Ponto-Caspian aquatic fauna: Morphology and molecules retrieve congruent evolutionary relationships in Pontogammarus maeoticus (Amphipoda: Pontogammaridae). Molecular Phylogenetics and Evolution, 69 (3), 1063–1076. https://doi.org/10.1016/j.ympev.2013.05.021 DOI: https://doi.org/10.1016/j.ympev.2013.05.021
- Pallas, P.S. (1766) Miscellanea zoologica. Quibus novae imprimis atque obscurae animalium species describuntur et observationibus iconibusque illustrantur. Petrum van Cleef, Hagí Comitum, 224 pp. https://doi.org/10.5962/bhl.title.69851 DOI: https://doi.org/10.5962/bhl.title.69851
- Pinkster, S. (1973) The Echinogammarus berilloni-group, a number of predominantly iberian amphipod species (Crustacea). Bijdragen tot de Dierkunde, 43 (1), 1–38. https://doi.org/10.1163/26660644-04301001 DOI: https://doi.org/10.1163/26660644-04301001
- Pinkster, S. & Stock, J.H. (1972) Members of the Echinogammarus simoni-group and the genus Eulimnogammarus (Crustacea, Amphipoda) from the Iberian Peninsula and North Africa, with description of a new species. Bulletin Zoologisch Museum Universiteit van Amsterdam, 2 (10), 85–115.
- Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 901–904. https://doi.org/10.1093/sysbio/syy032 DOI: https://doi.org/10.1093/sysbio/syy032
- Reid, D.M. (1940) Three species of Amphipoda (Crustacea) new to Britain. Annals and Magazine of Natural History, Series 11, 6, 335–337. https://doi.org/10.1080/03745481.1940.9723687 DOI: https://doi.org/10.1080/03745481.1940.9723687
- Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) Mrbayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61 (3), 539–542. https://doi.org/10.1093/sysbio/sys029 DOI: https://doi.org/10.1093/sysbio/sys029
- Sars, G.O. (1894) Crustacea caspia. Contributions to the knowledge of the Carcinological Fauna of the Caspian Sea. Part III. Amphipoda. Gammarida. Bulletin de l’Academie Imperiale des Sciences de St.-Petersbourg, Series 5, 1, 179–223, 343–378.
- Schäferna, K. (1923) Amphipoda balcanica, spolu s poznámkami o jiných sladkovodních Amphipodech. Mémoires de la Société Royale des Sciences de Bohème Prague,Clasee des Sciences, Annee 1921–1922, 12, 1–111.
- Schellenberg, A. (1928) Report on Amphipoda. Zoological results of the Cambridge Expedition to the Suez Canal. Transactions of the Zoological Society of London, 22, 633–692. https://doi.org/10.1111/j.1096-3642.1928.tb00209.x DOI: https://doi.org/10.1111/j.1096-3642.1928.tb00209.x
- Schellenberg, A. (1937) Schlussel und Diagnosen der dem Susswasser-Gammarus nahestehenden Einheiten ausschlisslich der Arten des Baikalsees und Australiens. Zoologischer Anzeiger, 117, 267–280.
- Sowinskij, V.K. (1904) Vvedenie v izuchenie fauny Ponto-Caspiyskogo-Aralskogo mosrskogo basseaina. Zapiski Kievskoho obshestva estestvoispytateley, 18, 1–497. [in Russian]
- Stebbing, T.R.R. (1899) Amphipoda from the Copenhagen Museum and other sources, part II. The Transactions of the Linnean Society of London, Zoology, Series 2, 7 (8), 395–432. https://doi.org/10.1111/j.1096-3642.1899.tb00202.x DOI: https://doi.org/10.1111/j.1096-3642.1899.tb00202.x
- Takhteev, V.V. (2000) [Esseyes on the amphipods of Lake Baikal (systematic, comparative ecology, evolution)]. Irkutsk University Press, Irkutsk, 350 pp. [in Russian]
- Takhteev, V.V. (2019) On the current state of taxonomy of the Baikal Lake amphipods (Crustacea: Amphipoda) and the typological ways of constructing their system. Arthropoda Selecta, 28 (3), 374–402. https://doi.org/10.15298/arthsel.28.3.03 DOI: https://doi.org/10.15298/arthsel.28.3.03
- Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729. https://doi.org/10.1093/molbev/mst197 DOI: https://doi.org/10.1093/molbev/mst197
- Trifinopoulos, J., Nguyen, L.-T., von Haeseler, A. & Minh, B.Q. (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 44, 232–235. https://doi.org/10.1093/nar/gkw256 DOI: https://doi.org/10.1093/nar/gkw256
- Väinölä, R., Witt, J.D.S., Grabowski, M., Bradbury, J.H., Jazdzewski, K. & Sket, B. (2008) Global diversity of amphipods (Amphipoda; Crustacea) in freshwater. Hydrobiologia, 595 (1), 241–255. https://doi.org/10.1007/s10750-007-9020-6 DOI: https://doi.org/10.1007/s10750-007-9020-6