Abstract
Among invasive species there is a special group so named cryptic species for which morphological identification is very difficult. This review is devoted to analysis of the dispersal routes of two copepod cryptic species complexes into aquatic ecosystems. Eurytemora carolleeae introduction was revealed in 2007 with bar-code. The species was described as a new taxon; its distribution was also studied using morphology. Biological invasions of two other Copepod species Acanthocyclops americanus and Eurytemora caspica were mainly studied using morphological methods since the species have already been described. At the same time, to confirm their distinctions from local forms molecular genetic tools were also used. Two scenarios resulting from cryptic species’ invasions and their competitions with native species were the partly (E. carrolleeae) or full displacement (A. americanus). When assessing the possible negative impact of invasive species on competitors, the most attention should be paid to predator species. Identification of cryptic species significantly complicates the situation with the assessment of bioinvasion and needs the use of molecular methods.
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REFERENCES
Abramova, E., Vishnyakova, I., Boike, J., Abramova, A., Solovyev, G., and Martynov, F., Structure of freshwater zooplankton communities from tundra waterbodies in the Lena River Delta, Russian Arctic, with a discussion on new records of glacial relict copepods, Polar Biol., 2017, vol. 40, no. 8, pp. 1629–1643. https://doi.org/10.1007/s00300-017-2087-2
Ackerman, J.D., Sim, B., Nichols, S.J., and Claudi, R.M., A review of the early life history of zebra mussels (Dreissena polymorpha): Comparisons with marine bivalves, Can. J. Zool., 1994, vol. 72, pp. 1169–1179.
Alekseev, V., and Souissi, A., A new species within the Eurytemora affinis complex (Copepoda: Calanoida) from the Atlantic Coast of USA, with observations on eight morphologically different European populations, Zootaxa, 2011, vol. 2767, pp. 41–56.
Alekseev, V., Makrushin, A., and Jiang-Shiou, H., Survivorship of activated resting stages in toxic environments: Provide treatment cues for ballast water, Mar. Pollut. Bull., 2010, vol. 61, pp. 254–258.
Alekseev, V.R., Growth, development and production of mass species of cyclops in the hollow system of the Volga delta, Cand. Sci. (Biol.) Dissertation, Leningrad, 1981.
Alekseev, V.R., Opredelitel’ presnovodnykh bespozvonochnykh Rossii i sopredel’nykh territorii (Key to Freshwater Invertebrates of Russia and Adjacent Lands), vol. 2: Rakoobraznye (Crustacea, Suborder Cyclopoida; Suborder Harpacticoida), St. Petersburg: Zool. Instit. Ross. Akad. Nauk, 1995, pp. 75–128.
Alekseev, V.R., Key to freshwater Cyclopidae of Russia and adjacent lands (Crustacea), Zoosystematica Rossica, 1998, vol. 7, pp. 25–43.
Alekseev, V. R., Confusing invader: Acanthocyclops americanus (Copepoda: Cyclopoida) and its biological, anthropogenic and climate-dependent mechanisms of rapid distribution in Eurasia, Water, 2021, vol. 13, no. 10, p. 1423. https://doi.org/10.3390/w13101423
Alekseev, V. R., and Kossova, A. A., Finding of Acanthocyclops americanus (Copepoda) in the delta of the Volga River, J. Zool., 1976, vol. 5511, pp. 1726–1728.
Alekseev, V.R. and Pugachev, V.A., Some peculiarities of food relationships between Acanthocyclops americanus (March.) and phyllopod nauplii, in Izuchenie povedeniya vodnykh bespozvonochnykh v estestvennykh usloviyakh: tezisy dokladov III Vsesoyuznogo simpoziuma po povedeniyu vodnykh bespozvonochnykh (Study of Aquatic Invertebrates’ Behaviour in Natural Conditions, Proc. III All-Union Symp. on the Behaviour of Aquatic Invertebrates), Borok, 1978, pp. 3–4.
Alekseev, V.R., and Sukhikh, N.M., Ust-Luga seaport of Russia: Biological invasions and resting stages accumulation, Life, 2023, vol. 13, no. 1, p. 117. https://doi.org/10.3390/life13010117
Alekseev, V.R., Fefilova, E. and Dumont, H.J., Some noteworthy free-living copepods from surface freshwater in Belgium, Belgian Journal of Zoology, 2002, vol. 132, pp. 133–139.
Alekseev, V.R., Abramson, N.I., and Sukhikh, N.M., Introduction of sibling species to the ecosystem of the Baltic Sea, Dokl. Biol. Sci., 2009, vol. 429, no. 5, pp. 694—697.
Alekseev, V.R., Miracle, M.R., Sahuquillo, M., and Vicente, E., Redescription of Acanthocyclops vernalis (Fischer, 1853) and Acanthocyclops robustus (Sars, 1863) from neotypes, with special reference to their distinction from Acanthocyclops americanus (Marsh, 1892) and its invasion of Eurasia, Limnetica, 2020, vol. 40, pp. 57–78.
Anufriieva E., Hołyńska M., and Shadrin N., Current invasions of Asian Cyclopid species (Copepoda: Cyclopidae) in Crimea, with taxonomical and zoogeographical remarks on the hypersaline and freshwater fauna, Ann. Zool., 2014, vol. 64, no. 1, pp. 109–130. https://doi.org/10.3161/000345414X680636
Arnold, J.D. and Yue, H.S., Prevalence, relative abundance, and mean intensity of plerocercoids of Proteocephalus sp. in young striped bass in the Sacramento-San Joaquin estuary, Calif. Fish Game, 1997, vol. 83, no. 3, pp. 105—117.
Beasley, D.E., Bonisoli-Alquati A., and Mousseau T.A., The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: A meta-analysis, Ecol. Indic., 2013, vol. 30, pp. 218–226. https://doi.org/10.1016/j.ecolind.2013.02.024
Beyrend-Dur, D., Souissi, S., Devreker, D., Winkler, G., and Hwang, J.S., Life cycle traits of two transatlantic populations of Eurytemora affinis (Copepoda: Calanoida): Salinity effects, J. Plankton Res., 2009, vol. 31, no. 7, pp. 713–728. https://doi.org/10.1093/plankt/fbp020
Carlton, J.T., Biological invasions and cryptogenic species, Ecology, 1996, vol. 77, pp. 1653–1655. https://doi.org/10.2307/2265767
Chuykov, Y.S., Fauna of planktonic invertebrate reservoirs of the Northern Caspian and Caspian Seas, in Gidrobiologicheskie issledovaniya estuariev (Hydrobiological Studies of Estuaries), St. Petersburg: Zool. Inst. Ross. Akad. Nauk, 1986, pp. 58–74.
Colwell, R.R., Infectious disease and environement: Cholera as a paradigm for waterborne disease, Int. Microbiol., 2004, vol. 7, pp. 285–289.
Declerck, S.A., Malo, A.R., Diehl, S., et al., Rapid adaptation of herbivore consumers to nutrient limitation: Eco-evolutionary feedbacks to population demography and resource control, Ecol. Lett., 2015, vol. 18, pp. 553–562. https://doi.org/10.1111/ele.12436
Devreker, D., Souissi, S., Molinero, J.C., and Nkubito, F., Trade-offs of the copepod Eurytemora affinis in mega-tidal estuaries. Insights of high frequency sampling in the Seine estuary, J. Plankton Res., 2008, vol. 30, no. 12, pp. 1329–1342. https://doi.org/10.1093/plankt/fbn086
Devreker, D., Souissi, S., Molinero, J.C., Beyrend-Dur, D., Gomez, F., and Forget-Leray, J., Tidal and annual variability of the population structure of Eurytemora affinis in the middle part of the Seine estuary during 2005, Estuarine, Coastal Shelf Sci., 2010, vol. 89, no.4, pp. 245–255. https://doi.org/10.1016/j.ecss.2010.07.010
Devreker, D., Pierson, J., Souissi, S., Kimmel, D., and Roman, M., An experimental approach to estimate egg production and development rate of the Calanoid copepod Eurytemora affinis in Chesapeake Bay, USA, J. Exp. Mar. Biol. Ecol., 2012, vol. 416–417, pp. 72–83. https://doi.org/10.1016/j.jembe.2012.02.010
Dodson S.I., Skelly D.A., and Lee C.E., Out of Alaska: Morphological evolution and diversity within the genus Eurytemora from its ancestral range (Crustacea, Copepoda), Hydrobiologia, 2010, vol. 653, pp. 131–148.
Dur, G., Souissi, S., Devreker, D., Ginot, V., Schmitt, F.G., and Hwang, J.S., An individual based model to study the reproduction of egg bearing copepods: application to Eurytemora affinis (Copepoda; Calanoida) from the Seine estuary, Ecol. Model., 2009, vol. 8, pp. 1073–1089. https://doi.org/10.1016/j.ecolmodel.2008.12.013
Dussart, B.H., Contribution à l'étude des Copépodes d’Espagne, Publicaciones del Instituto de Biologia Aplicada (Barcelona), 1967, vol. 42, pp. 87–105.
Dussart, B.H. Acanthocyclops americanus en France, Bulletin du Muséum National d’Histoire Naturelle, 1971, vol. 42, pp. 725–729.
Gelembiuk, G.W., May, G.E., and Lee, C.E., Phylogeography and systematics of zebra mussels and related species, Mol. Ecol., 2006, vol. 15, pp. 1033–1050. https://doi.org/10.1111/j.1365-294X.2006.02816.x
Geller, J.B., Darling, J.A., and Carlton, J.T., Genetic perspectives on marine biological invasions, Annual Review of Marine Science, 2010, vol. 2, pp. 401–427. https://doi.org/10.1146/annurev.marine.010908.163745
Goedknegt, M.A., Thieltges, D.W., van der Meer, J., Wegner, K.M., and Luttikhuizen, P.C., Cryptic invasion of a parasitic copepod: Compromised identification when morphologically similar invaders co-occur in invaded ecosystems, PLoS One, 2018, vol. 13, no. 3, p. e0193354. https://doi.org/10.1371/journal.pone.0193354
Gollasch, S., MacDonald, E., Belson, S., Botnen, H., Christensen, J.T., Hamer, J.P., Houvenaghel, G., Jermert, A., Lucas, I., Masson, D., et al., Distribution, impacts and management. Life in ballast tanks, in Invasive Aquatic Species of Europe, Leppäkoski, E., Olenin, S., and Gollasch, S., Eds., Dordrecht: Springer, 2002, pp. 217–231.
Grabowski, M., Rewicz, T., Bacela-Spychalska, K., et al., Cryptic invasion of Baltic lowlands by freshwater amphipod of Pontic origin, Aquatic Invasions, 2012, vol. 7, no. 3, pp. 337–346. https://doi.org/10.3391/ai.2012.7.3.005
Gurney, R., British Fresh-Water Copepod, London: Ray Society, 1931, vol. 1, p. 238
Hirche, H.-J., Egg production of Eurytemora affinis—Effect of k-strategy, Estuarine, Coastal Shelf Sci., 1992, vol. 35, pp. 395–407. https://doi.org/10.1016/S0272-7714(05)80035-6
Hutchinson, G. E., The paradox of the plankton, The American Naturalist, 1961, vol. 95, pp. 137–145.
Ishida, S., and Taylor D.J., Quaternary diversification in a sexual Holarctic zooplankter, Daphnia galeata, Mol. Ecol., 2007, vol. 16, pp. 569–582. https://doi.org/10.1111/j.1365-294X.2006.03160.x
Jarić, I., Heger, T., Castro Monzon, F., Jeschke, J.M., Kowarik, I., McConkey, K.R., Pyšek, P., Sagouis, A., and Essl, F., Crypticity in biological invasions, Trends Ecol. Evol., 2019, vol. 34, no. 4, pp. 291–302. https://doi.org/10.1016/j.tree.2018.12.008
Kamburska, L., Schrimpf, W., Djavidnia, S., Shiganova, T., and Stefanova, K., Addressing the Ecological Issue of the Invasive Species: Special Focus on the Ctenophore Mnemiopsis leidyi (Agassiz, 1865) in the Black Sea, EUR 22310 EN, EC JRC Institute of Environment and Sustainability, 2006, p. 59.
Kiefer, F., Freilebende, Copepoda, in Die Binnengewässer Einzeldarstellungen aus del Limnologie und ihren Nachbargebietien. Das Zooplankton der Binnengewässer, 2. Teil, Elster, H.J. and Ohle, W., Eds., Stuttgart: Schweizerbart’sche Verlagsbuchhandlung, 1978.
Kimmel, D.G., Miller, W.D., and Roman, M.R. Regional scale climate forcing of mesozooplankton dynamics in Chesapeake Bay, Estuaries and Coasts, 2006, vol. 29, no. 3, pp. 375–387. https://doi.org/10.1007/BF02784987
Knatz, G., Succession of copepod species in a middle Atlantic estuary, Estuaries, 1978, vol. 1, pp. 68–71.
Knowlton, N., Sibling species in the sea, Annu. Rev. Ecol. Syst., 1993, vol. 24, pp. 189–216. https://doi.org/10.1146/annurev.es.24.110193.001201
Kotov, A.A, Garibian, P.G., Bekker, E.I., Taylor, D.J., and Karabanov, D.P., A new species group from the Daphnia curvirostris species complex (Cladocera: Anomopoda) from the eastern Palaearctic: Taxonomy, phylogeny and phylogeography, Zool. J. Lin. Soc., 2020. https://doi.org/10.1093/zoolinnean/zlaa046
Kruppa, E.G., On the morphological deviations of Acanthocyclops americanus Marsh and Cyclops vicinus Uljanin (Crustacea,Copepoda) from the polluted water bodies of Almaty Region (Southeastern Kazakhstan), Russian Journal of Aquatic Ecology, 1998, vol. 7, pp. 11–16.
Kruppa, E. G., The ecological preferences of Eurytemora affinis (Poppe, 1880) in the water bodies of Kazakhstan (Central Asia) and some notes about Eurytemora caspica Sukhikh & Alekseev, 2013, Crustaceana, 2020, vol. 93, nos. 3–5, pp. 405–428. https://doi.org/10.1163/15685403-00003967
Lajus, D., Sukhikh, N., and Alekseev, V., Cryptic or pseudocryptic: Can morphological methods inform copepod taxonomy? An analysis of publications and a case study of the Eurytemora affinis species complex, Ecol. Evol., 2015, vol. 5, no. 12, pp. 2374–2385. https://doi.org/10.1002/ece3.1521
Lajus, D., Sukhikh, N., and Alekseev, V., Stochastic phenotypic variation: Empirical results and potential use in Eurytemora research (Copepoda, Calanoida), Crustaceana, 2020, vol. 93, pp. 317–336. https://doi.org/10.1163/15685403-00003983
Lazareva, V. I., Distribution of Eurytemora caspica Sukhikh & Alekseev, 2013 (Copepoda, Calanoida) in the water reservoirs of the Volga and Don River basins, Crustaceana, 2020, vol. 93 (3–5), pp. 261–273. https://doi.org/10.1163/15685403-00003982
Lazareva, V.I., Current state and long-term dynamics of zooplankton of the Tsimlyansk Reservoir (Don River, Russia), Arid Ecosyst., 2021, vol. 11, no. 2, pp. 213–219. https://doi.org/10.1134/S2079096121020098
Lazareva, V.I., Sabitova, R.Z., and Sokolova, E.A., Features of structure and distribution of late summer (August) zooplankton in the Volga reservoirs, Tr. Inst. Biol. Vnutr. Vod Ross. Akad. Nauk, 2018, no. 82 (85), pp. 28–51. https://doi.org/10.24411/0320-3557-2018-1-0011
Lee, C.E., Rapid and repeated invasions of fresh water by the copepod Eurytemora affinis, Evolution, 1999, vol. 53, 1423–1434. https://doi.org/10.2307/2640889
Lee, C.E., Global phylogeography of a cryptic copepod species complex and reproductive isolation between genetically proximate populations, Evolution, 2000, vol. 54, pp. 2014–2027. https://doi.org/10.1111/j.0014-3820.2000.tb01245.x
Lee, C.E. and Frost, B.W., Morphological stasis in the Eurytemora affinis species complex (Copepoda: Temoridae), Hydrobiologia 2002, vol. 480, pp. 111–128.
Lee, C.E., Remfert, J.L., and Chang, Y., Response to selection and evolvability of invasive species, Genetica, 2007, vol. 129, no. 2, pp. 179—192. https://doi.org/10.1007/s10709-006-9013-9
Lloyd, S., Elliott, D., and Roman, M., Egg production by the copepod, Eurytemora affinis, in Chesapeake Bay turbidity maximum regions, J. Plankton. Res., 2013, vol. 35, no. 2, p. 299. https://doi.org/10.1093/plankt/fbt003
Lowndes, A.G., On Cyclops americanus, Marsh, Annals and Magazine of Natural History, 1926, vol. 17, pp. 616–619. https://doi.org/10.1080/00222932608633452
Lowndes, A.G., Cyclops americanus Marsh. A discussion and description of its specific characteristics and its occurrence in Europe, Int. Rev. Gesamten Hydrobiol., 1928, vol. 19, pp. 12–20. https://doi.org/10.1002/iroh.19280190103
Lowndes, A.G. Eurytemora thompsoni, A. Willey, a new European record, Annals and Magazine of Natural History, 1931, vol. 8, pp. 501–507.
Mergeay, J., Verschuren D., and de Meester L., Cryptic invasion and dispersal of an American Daphnia in East Africa, Limnol. Oceanogr., 2005, vol. 50, pp. 1278–1283. https://doi.org/10.4319/lo.2005.50.4.1278
Mirabdullayev, I.M., and Defaye, D., On the taxonomy of the Acanthocyclops robustus species complex (Copepoda, Cyclopidae), Acanthocyclops robustus (G.O. Sars, 1863) and Acanthocyclops trajani n. sp., Selevinia, 2002, vols. 1–4, pp. 7–20.
Mirabdullayev, I.M. and Defaye, D., On the taxonomy of the Acanthocyclops robustus species complex (Copepoda, Cyclopidae): Acanthocyclops brevispinosus and A. einslei sp. n., Vestn. Zool., 2004, pp. 38, 27–37.
Miracle, M.R., Alekseev, V., Monchenko, V., Sentandreu, V., and Vicente, E., Molecular-geneticbased contribution to the taxonomy of the Acanthocyclops robustus group, J. Nat. Hist., 2013, vol. 47, рр. 863–888. https://doi.org/10.1080/00222933.2012.744432
Miura, O., Molecular genetic approaches to elucidate the ecological and evolutionary issues associated with biological invasions, Ecol. Res., 2007, vol. 22, pp. 876–883. https://doi.org/10.1007/s11284-007-0389-5
Monakov, A.V., Feeding of Freshwater Invertebrates, Ghent: Kenobi Publications, 2003.
Monchenko, V. I., On species independence of Acanthocyclops americanus (Marsh) and on its finding in the Soviet Union, Zool. Zh., 1961, vol. 40, pp. 13–19.
Monchenko, V.I., Shchelepnoroti tsyklopopodibni, tsyklopy (Cyclopidae) (Gnathostome Cyclopoids (Cyclopidae)), Kyiv, Ukraine: Naukova Dumka, 1974.
Morais, P., and Reichard, M., Cryptic invasions: A review, Sci. Total Environ., 2017, vol. 613, pp. 1438–1448. https://doi.org/10.1016/j.scitotenv.2017.06.133
Novak, S.J., Geographic origins and introduction dynamics, in Encyclopedia of Biological Invasions, Simberloff, D. and Rejmánek, M., Eds., Berkeley and Los Angeles: University of California Press, 2011, pp. 273–280.
Panov, V., and Caceres, C., Role of diapause in dispersal of aquatic invertebrates, in Diapause in Aquatic Invertebrates: Theory and Human Use, Dordrecht: Springer, 2007, pp. 187–195. https://doi.org/10.1007/978-1-4020-5680-2_12
Papakostas, S., Michaloudi, E., Proios, K., et al., Integrative taxonomy recognises evolutionary units despite widespread mitonuclear discordance: Evidence from a rotifer cryptic species complex, Syst. Biol., 2016, vol. 65, pp. 508–524. https://doi.org/10.1093/sysbio/syw016
Piasecki, W., Goodwin, A.E., Eiras, J.C., and Nowak, B.F., Importance of copepod in freshwater aquaculture, Zool. Stud., 2004, vol. 43, no. 2, pp. 193–205.
Pierson, J.J., Kimmel, D.G., and Roman, M.R., Temperature impacts on Eurytemora carolleeae size and vital rates in the upper Chesapeake Bay in winter, Estuaries and Coasts, 2016, vol. 39, no. 4, pp. 1122–1132. https://doi.org/10.1007/s12237-015-0063-z
Roman, J., Diluting the founder effect: Cryptic invasions expand a marine invader’s range, Proc. R. Soc. B, 2006, vol. 273, pp. 2453–2459. https://doi.org/10.1098/rspb.2006.3597
Samchishina, L.V., Ecological–faunistic and morphological aspects of the study of freshwater and brackish-water Calanoida (Crustacea, Copepoda) of Ukraine, Cand Sci. (Biol.) Dissertation, Kyiv: I. I. Shmal’gauzen Inst. Zool. Natl. Acad. Sci. Ukraine, 2005.
Sharma, P. and Kotov, A.A., Establishment of Chydorus sphaericus (O.F. Muller, 1785) (Crustacea: Cladocera) in Australia: Consequences of mass fish stocking from Northern Europe?, J. Limnol., 2015, vol. 74, pp. 225–233. https://doi.org/10.4081/jlimnol.2014.1037
Sługocki, Ł., Rymaszewska, A., and Kirczuk, L., To fit or to belong: Characterization of the non-native invader Eurytemora carolleeae (Copepoda: Calanoida) in the Oder River system (Central Europe), Aquatic Invasions, 2021, vol. 16, no. 3, pp. 443–460. https://doi.org/10.3391/ai.2021.16.3.04
Sukhikh, N.M., and Alekseev, V.R., Eurytemora caspica sp. nov. from the Caspian Sea—One more new species within the E. affinis complex (Copepoda: Calanoida), Proc. Zool. Inst. Russ. Acad. Sci., 2013a, vol. 317, no. 1, pp. 85—100. https://doi.org/10.31610/trudyzin/2013.317.1.85
Sukhikh, N.M., Souissi, A., Souissi, S., and Alekseev, V.R., Invasion of Eurytemora sibling species (Copepoda: Temoridae) from North America into the Baltic Sea and European Atlantic coast estuaries, J. Nat. Hist., 2013b, vol. 47, nos. 5–12, pp. 753–767. https://doi.org/10.1080/00222933.2012.716865
Sukhikh, N.M., Souissi, A., Souissi, S., Winkler, G., Castric, V., Holl, A.C., and Alekseev, V.R., Genetic and morphological heterogeneity among populations of Eurytemora affinis (Crustacea: Copepoda: Temoridae) in European waters, C.R. Biol., 2016, vol. 339, pp. 197–206. https://doi.org/10.1016/j.crvi.2016.03.004
Sukhikh, N.M., Souissi, A., Souissi, S., Holl, A.C., Schizas, N.V., and Alekseev V., Life in sympatry: Coexistence of native Eurytemora affinis and invasive Eurytemora carolleeae in the Gulf of Finland (Baltic Sea), Oceanologia, 2019, vol. 61, pp. 227–238. https://doi.org/10.1016/j.oceano.2018.11.002
Sukhikh, N., Abramova, E., Holl, A.C., Souissi, S., and Alekseev, V., A comparative analysis of genetic differentiation of the E. affinis species complex and some other Eurytemora species, using CO1, ITSn and 18SrRNA genes (Copepoda, Calanoida), Crustaceana, 2020a, vol. 93, pp. 931–955. https://doi.org/10.1163/15685403-bja10074
Sukhikh, N.M., Lazareva, V.I., and Alekseev, V.R., Copepod Eurytemora caspica Sukhikh et Alekseev, 2013 (Crustacea, Calanoida) in Volga and Kama River Reservoirs, Inland Water Biol., 2020b, vol. 13, pp. 198–205. https://doi.org/10.1134/S1995082920020145
Taylor, D.J., Connelly, S.J., and Kotov, A.A., The Intercontinental phylogeography of neustonic daphniids, Sci. Rep., 2020, vol. 10, p. 1818. https://doi.org/10.1038/s41598-020-58743-8
Uitto, A., Gorokhova, E., and Valipakka, P., Distribution of the nonindigenous Cercopagis pengoi in the coastal waters of the eastern Gulf of Finland, ICES J. Mar. Sci., 1999, vol. 56 (suppl.), pp. 49–57. https://doi.org/10.1006/jmsc.1999.0613
Vasquez, A.A., Hudson, P.L., Fujimoto, M., Keeler, K., Armenio, P.M., and Ram, J.L., Eurytemora carolleeae in the Laurentian Great Lakes revealed by phylogenetic and morphological analysis, J. Great Lakes Res., 2016, vol. 42, no. 4, pp. 802–811. https://doi.org/10.1016/j.jglr.2016.04.001
Vijushkova, V.P., and Kuznetsova, V.P., Distribution of Acanthocyclops americanus (Marsh.) Copepoda in USSR, Zool. Zh., 1974, vol. 53, pp. 1873–1875.
Wasmund, N., Augustin, C., Pollehne, F., Siegel, H., and Zettler, M., Biologische standseinschätzung der Ostsee im Jahre, 2012, Warnemünde, Germany: Meereswiss Ber, 2013, p. 92.
weatherarchive.ru/Sea/Ust-luga/July. Accessed February 27, 2023.
https://en.wikipedia.org/wiki/2010_Northern_Hemisphe-re_heat_waves. Accessed February 27, 2023
Winkler, G., Dodson, J.J., and Lee, C.E., Heterogeneity within the native range: population genetic analyses of sympatric invasive and noninvasive clades of the freshwater invading copepod Eurytemora affinis, Mol. Ecol., 2008, vol. 17, pp. 415–430. https://doi.org/10.1111/j.1365-294X.2007.03480.x
Winkler, G., Souissi, S., Poux, C., and Castric, V. Genetic hetero-geneity among Eurytemora affinis populations in Western Europe, Mar. Biol., 2011, vol. 158, pp. 1841–1856. https://doi.org/10.1007/s00227-011-1696-5
Zakharov, V. M., Future Prospects for Population Phenogenetics, Soviet Scientific Reviews Series, Section F, 1989, vol. 4, pp. 1–79.
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We are very grateful to O. Chaban for her help preparing this manuscript. For this study, the Federal Collection of the Zoological Institute of the Russian Academy of Sciences (St. Petersburg, Russia) was used.
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Sukhikh, N., Alekseev, V. Two Life Strategies in Copepod Cryptic Species: Coexistence and Displacement. Russ J Biol Invasions 14, 666–676 (2023). https://doi.org/10.1134/S2075111723040161
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DOI: https://doi.org/10.1134/S2075111723040161