Life in sympatry : coexistence of native Eurytemora affinis and invasive Eurytemora carolleeae in the Gulf of Finland (Baltic Sea)

• Autorzy: Sukhikh Natalia , Souissi Anissa , Souissi Sami , Holl Anne-Catherine , Schizas Nikolaos V. , Alekseev Victor

Identyfikatory

DOI

10.1016/j.oceano.2018.11.002

• Języki publikacji: EN

Abstrakty

EN

The invasion of exotic species into native ecosystems is becoming a crucial issue in global biology. Over the last ten years, at least 45 invasions of aquatic species have been reported in the eastern part of the Gulf of Finland; the majority of them were introduced through ballast water. Recently, invasion of the estuarine calanoid copepod Eurytemora carolleeae (Temoridae), originating from North America, has been reported in several European estuaries and particularly in the Gulf of Finland. This species is morphologically very similar to the native Eurytemora affinis, but it is easily discriminated by molecular markers. In this study, we monitored the distribution area of the invasive copepod species in European waters, as well as the population structure of (native) E. affinis and (invasive) E. carolleeae, from 2006 to 2018 in the Gulf of Finland. The population density of E. affinis was significantly higher, compared to E. carolleeae, during most of the study period. The only exception was Neva Bay in 2010, wherein the invasive species dominated possibly due to high temperatures and differences in the levels of fish predation. The reproductive performance of E. carolleeae was also higher than that of E. affinis. These results show different population dynamics between the two species. It was revealed that invasive E. carolleeae develops in some of the very same habitats as native E. affinis, thereby potentially becoming a significant component of the zooplankton in the studied area. Moreover, invader has the potential to displace native E. affinis.

Słowa kluczowe

EN

Eurytemora species; Copepoda; zooplankton; invasive species; native species; Gulf of Finland

• Wydawca: Polish Academy of Sciences, Institute of Oceanology ; Elsevier
• Czasopismo: Oceanologia
• Rocznik: 2019
• Tom: No. 61 (2)
• Strony: 227--238
• Opis fizyczny: Bibliogr. 73 poz., mapa, tab., wykr.

Twórcy

autor

Sukhikh Natalia

• Zoological Institute, Russian Academy of Sciences, Saint Petersburg, Russia

autor

Souissi Anissa

• Lille University, CNRS, ULCO, LOG, Wimereux, France

autor

Souissi Sami

• Lille University, CNRS, ULCO, LOG, Wimereux, France

autor

Holl Anne-Catherine

• Lille University of Science and Technology, CNRS, Villeneuve d'Ascq Cedex, France

autor

Schizas Nikolaos V.

• Department of Marine Sciences, University of Puerto Rico, Mayagüez, Puerto Rico

autor

Alekseev Victor

• Zoological Institute, Russian Academy of Sciences, Saint Petersburg, Russia

Bibliografia

• [1] Alekseev, V., Souissi, A., 2011. 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 2767, 41-56.
• [2] Alekseev, V. R., Abramson, N. I., Sukhikh, N. M., 2009. Introduction of sibling species to the ecosystem of the Baltic Sea. Dokl. Biol. Sci. 429 (5), 694-697.
• [3] Alimov, A. F., Bogutskaya, N. G., et al., 2004. Biological Invasions in Aquatic and Terrestrial Ecosystems. Fellowship of Scientific Publications KMC, Moscow, St. Petersburg, 424 pp., (in Russian).
• [4] Aljanabi, S. M., Martinez, I., 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids. Res. 25-22, 4692-4693.
• [5] Antsulevich, A. E., Ryabova, V. N., Stogov, I. A., 1995. The current state of zooplankton in the Luga Bay of the Gulf of Finland. Bull. St. Petersburg State Univ. 3 (3), 3-9, (in Russian).
• [6] Arnold, J. D., Yue, H. S., 1997. Prevalence, relative abundance, and mean intensity of plerocercoids of Proteocephalus sp. in young striped bass in the Sacramento-San Joaquin estuary. California Fish Game 83 (3), 105-117.
• [7] Basova, S. L., 1983. Survey of the pollution status of the eastern part of the Gulf of Finland by hydrobiological indicators in 1983, Leningrad, 86 pp., (in Russian).
• [8] Beasley, D. E., Bonisoli-Alquati, A., Mousseau, T. A., 2013. The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: a meta-analysis. Ecol. Indic. 30, 218-226.
• [9] Beauchamp, K. A., Kathman, R. D., McDowell, Hedrick, R. P., 2001. Molecular phylogeny of tubificid oligochaetes with special emphasis on Tubifex tubifex (Tubificidae). Mol. Phylogenet. Evol. 19, 216-224.
• [10] Berezina, N. A., Petryashev, V. V., Razinkovas, A., Lesutiene, J., 2011. Alien malacostraca in the eastern Baltic Sea: pathways and consequences. In: Galil, B. S., Clark, P. F., Carlton, J. T. (Eds.), In the Wrong Place — Alien Marine Crustaceans: Distribution, Biology and Impacts Invading Nature, Springer Series, Invasion Ecol., 63, 301-322.
• [11] Beyrend-Dur, D., Souissi, S., Devreker, D., Winkler, D., Hwang, J. S., 2009. Life cycle traits of two transatlantic populations of Eurytemora affinis (Copepoda: Calanoida): salinity effects. J. Plankt. Res. 31 (7), 713-728.
• [12] Brooks, J. L., Dodson, S. I., 1965. Predation, body size, and composition of plankton. The effect of a marine planktivore on lake plankton illustrates theory of size, competition, and predation. Sci. New Ser. 150 (3692), 28-35.
• [13] Cherevichko, A. V., 2017. Zooplankton of water bodies of seaside marches of Malozemelskaya Tundra. Biol. Inl. Waters 2, 88-93, (in Russian).
• [14] Colwell, R. R., 2004. Infectious disease and environement: cholera as a paradigm for waterborne disease. Int Microbiol 7, 285-289.
• [15] Demchuk, A., Uspenskiy, A., Golubkov, S., 2017. Feeding patterns of the abundant coastal fish species in the Eastern Gulf of Finland, Tallinn, Gulf of Finland Science Days, 16 October. , http://dx.doi.org/10.13140/RG.2.2.18238.38724.
• [16] Devreker, D., Souissi, S., Molinero, J. C., Nkubito, F., 2008. Trade-offs of the copepod Eurytemora affinis in mega-tidal estuaries. Insights of high frequency sampling in the Seine estuary. J. Plankton Res. 30, 1329-1342.
• [17] Devreker, D., Souissi, S., Molinero, J. C., Beyrend-Dur, D., Gomez, F., Forget-Leray, J., 2010. Tidal and annual variability of the population structure of Eurytemora affinis in the middle part of the Seine estuary during 2005. Estuar. Coast. Shelf. Sci. 89 (4), 245-255.
• [18] Devreker, D., Pierson, J., Souissi, S., Kimmel, D., Roman, M., 2012. An experimental approach to estimate egg production and development rate of the calanoid copepod Eurytemora affinis in Chesapeake Bay, USA. J. Exp. Mar. Bio. Ecol. 416-417, 72-83.
• [19] Dur, G., Souissi, S., Devreker, D., Ginot, V., Schmitt, F. G., Hwang, J. S., 2009. An individual based model to study the reproduction of egg bearing copepods: application to Eurytemora affinis (Copepoda; Calanoida) from the Seine estuary. Ecol. Model. 8, 1073-1089.
• [20] Fefilova, E. B., 2015. Fauna of the European North-East of Russia. Copepods (Copepoda), 12. 319 pp., (in Russian).
• [21] Folmer, O., Black, M., Hoeh, W., Lutz, R., Vriyenhoek, R., 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294-299.
• [22] Gelembiuk, G. W., May, G. E., Lee, C. E., 2006. Phylogeography and systematics of zebra mussels and related species. Mol. Ecol. 15, 1033-1050.
• [23] Golubkov, S. M., 2009. Changes of biological communities in the eastern Gulf of Finland during the last century. Proc. Zooll. Instit. RAS 313 (4), 406-418.
• [24] Gorokhova, E., Lehtiniemi, M., Motwani, N. H., 2013. Trade-offs between predation risk and growth benefits in the copepod Eurytemora affinis with contrasting pigmentation. PLoS ONE 8 (8), e71385.
• [25] Graham, J. H., Raz, S., Hel-Or, H., Nevo, E., 2010. Fluctuating Asymmetry: Methods, Theory, and Applications, Symmetry, 2, 46-540.
• [26] Gurney, R., 1931. British Fresh-water Copepoda, vol. 1. Ray Society, London, 384 pp.
• [27] Hall, T. A., 1999. Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Res. 41, 95-98.
• [28] Hirche, H.-J., 1992. Egg production of Eurytemora affinis-effect of k-strategy. Estuar. Coast. Shelf Sci. 35, 395-407.
• [29] Hoelzel, A. R., Green, A., 1992. Analysis of population-level variation by sequencing PCR-amplified DNA. In: Hoelzel, A. R. (Ed.), Molecular Genetic Analysis of Populations: A Practical Approach. Oxford Univ. Press, New York, 159-188.
• [30] Katajisto, T., Kotta, J., Lehtiniemi, M., Malavin, S. A., Panov, V. E., 2013. Palaemon elegans Rathke, 1837 (Caridea: Palaemonoidea: Palaemonidae) established in the Gulf of Finland. BioInvas. Rec. 2 (2), 125-132.
• [31] Kimmel, D. G., Miller, W. D., Roman, M. R., 2006. Regional scale climate forcing of mesozooplankton dynamics in Chesapeake Bay. Estuar. Coasts 29 (3), 375-387.
• [32] Knatz, G., 1978. Succession of copepod species in a middle Atlantic estuary. Estuaries 1, 68-71.
• [33] Knowlton, N., 1993. Sibling species in the sea. Annu. Rev. Ecol. Syst. 24, 189-216.
• [34] Lajus, D., Sukhikh, N., Alekseev, V., 2015. 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. 5 (12), 2374-2385.
• [35] Lavrentieva, G. M., Finogenova, N. P., 1999. Hydrobiological characteristics of the Vyborg Gulf, the Bierkesund Strait, the Batareinoy Bay and the Luga Bay (Eastern part of the Gulf of Finland), The Gulf of Finland in the conditions of anthropogenic impact, St. Petersburg, 242 pp., (in Russian).
• [36] Lazareva, V. I., Sabitova, R. Z., Sokolova, E. A., 2018. Features of the structure and distribution of the late summer (august) zooplankton in the Volga reservoirs. Biol. Inl. Waters 82, 28-51, (in Russian).
• [37] Lee, C. E., 2000. Global phylogeography of a cryptic copepod species complex and reproductive isolation between genetically proximate populations. Evolution 54, 2014-2027.
• [38] Lee, C. E., Remfert, J. L., Chang, Y., 2007. Response to selection and evolvability of invasive species. Genetica 129 (2), 179-192.
• [39] Lehtiniemi, M., Antsulevich, A., Kotta, J., Maximov, A., Ojaveer, H., Orlova, M., 2016. Non-indigenous species. In: Raateoja, M., Setälä, O. (Eds.), Reports of the Finnish Environment Institute. The Gulf of Finland Assessment. Finnish Environ. Inst., Helsinki, 264-275.
• [40] Leppäkoski, E., Gollasch, S., Gruszka, P., Ojaveer, H., Olenin, S., Panov, V., 2002a. The Baltic — a sea of invaders. Can. J. Fish Aquat. Sci. 59, 1175-1188.
• [41] Leppäkoski, E., Olenin, S., Gollasch, S., 2002b. The Baltic Sea — a field laboratory for invasion biology. In: Leppäkoski, E., Gollasch, S., Olenin, S. (Eds.), Invasive Aquatic Species of Europe — Distribution, Impacts, Management. Dordrecht, The Netherlands, Kluwer Academic Publ., 253-259.
• [42] Librado, P., Rozas, J., 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451-1452.
• [43] Lloyd, S., Elliott, D., Roman, M., 2013. Egg production by the copepod, Eurytemora affinis, in Chesapeake Bay turbidity maximum regions. J. Plankton. Res. 35 (2), 299-308, http://dx.doi.org/10.1093/plankt/fbt003.
• [44] Makino, W., Tanabe, A. S., 2009. Extreme population genetic differentiation and secondary contact in the freshwater copepod Acanthodiaptomus pacificus in the Japanese Archipelago. Mol. Ecol. 18, 3699-3713.
• [45] Ogorodnikova, V. A., Volkhonskaya, N. I., 2006. Zooplankton of the Luga Bay of the Gulf of Finland (background status before the start of the port facilities operation). Ecological aspects of hydropower construction on the biota of the water area of the eastern part of the Gulf of Finland. St. Petersburg, vol. 331(1). 324-342, (in Russian).
• [46] Ojaveer, H., Kotta, J., 2015. Ecosystem impacts of the widespread non-indigenous species in the Baltic Sea: literature survey evidences major limitations in knowledge. Hydrobiologia 750, 171-185.
• [47] Ostov, I. S., 1971. Characteristic features of the hydrological and hydrochemical regime of the Gulf of Finland as the basis for its fishery development, Biol. Commerc. Resources of the Gulf of Finland. Leningrad 76, 18-45, (in Russian).
• [48] Panov, V. E., Bychenkov, D. E., Berezina, N. A., Maximov, A. M., 2003. Alien species introductions in the eastern Gulf of Finland: current state and possible management options. Proc. Estonian Acad. Sci. Biol. Ecol. 52 (3), 254-267.
• [49] Parent, G. J., Plourde, G. J., Turgeon, S. J., 2012. Natural hybridization between Calanus finmarchicus and C. glacialis (Copepoda) in the Arctic and Northwest Atlantic. Limnol. Oceanogr. 57, 1057-1066.
• [50] Petrusek, A., Seda, J., Machacek, J., Ruthova, S., Smilauer, P., 2008. Daphnia hybridization along ecological gradients in pelagic environments: the potential for the presence of hybrid zones in plankton. Proc. R. Soc. B. Biol. Sci. 363, 2931-2941.
• [51] Piasecki, W., Goodwin, A. E., Eiras, J. C., Nowak, B. F., 2004. Importance of copepod in freshwater aquaculture. Zool. Stud. 43 (2), 193-205.
• [52] Pierson, J. J., Kimmel, D. G., Roman, M. R., 2016. Temperature impacts on Eurytemora carolleeae size and vital rates in the upper Chesapeake Bay in winter. Estuar. Coasts 39 (4), 1122-1132.
• [53] Pollumae, A., Kotta, J., 2007. Factors describing the distribution of the zooplankton community in the Gulf of Finland in the context of interactions between native and introduced predatory cladocerans. Oceanologia 49 (2), 277-290.
• [54] Pollumaea, A., Valjataga, K., 2004. Cercopagis pengoi (Cladocera) in the Gulf of Finland: environmental variables affecting its distribution and interaction with Bosmina coregoni maritima. Proc. Estonian Acad. Sci. Biol. Ecol. 53 (4), 276-282.
• [55] Pritchard, V. L., Knutson, V. L., Lee, M., Zieba, J., Edmands, S., 2012. Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus. J. Evol. Biol. 26, 416-433.
• [56] Raupach, M. J., Mayer, C., Malyutina, M., Wägele, J.-W., 2009. Multiple origins of deep-sea Asellota (Crustacea: Isopoda) from shallow waters revealed by molecular data. Proc R Soc Lond Ser B 276, 799-808.
• [57] Ryabova, V. N., Pogrebov, V. B., 1991. Biological seasonality in the zooplankton of the Gulf of Finland. Hydrobiol. J. 27 (1), 19-24, (in Russian).
• [58] Sergeev, V. N., Ryabova, V. N., Belogolovaya, L. A., 1971. Features of the dynamics and distribution of zooplankton in the eastern part of the Gulf of Finland in 1969. Izvestiya GosNIORH 123, 52-64, (in Russian).
• [59] Spiridonov, M., Ryabchuk, D., Zhamoida, V., Sergeev, A., Sivkov, V., Boldyrev, V., 2011. Geological hazard potential at the baltic sea and its coastal zone: examples from the Eastern Gulf of Finland and the Kaliningrad Area. In: Harff, J., Björck, S., Hoth, P. (Eds.), The Baltic Sea Basin. Springer-Verlag, Berlin, Heidelberg, 337-364.
• [60] Sturmbauer, C., Opadiya, G. B., Niederstätter, H., Riedmann, A., Dallinger, R., 1999. Mitochondrial DNA reveals cryptic oligochaete species differing in cadmium resistance. Mol. Biol. Evol. 16, 967-974.
• [61] Sukhikh, N. M., Alekseev, V. R., 2013. Eurytemora caspica sp.nov. from the Caspian sea — one more new species within the E. affinis complex (Copepoda: Calanoida). Proc. Zool. Inst. RAS 317 (1), 85-100.
• [62] Sukhikh, N. M., Souissi, A., Souissi, S., Alekseev, V. R., 2013. Invasion of Eurytemora sibling species (Copepoda: Temoridae) from North America into the Baltic Sea and European Atlantic coast estuaries. J. Nat. Hist. 47 (5-12), 753-767.
• [63] Sukhikh, N. M., Castric, V., Polyakova, N. V., Souissi, S., Alekseev, V. R., 2016a. Isolated Populations of Eurytemora americana Williams (Crustacea, Copepoda) in the White Sea Rock Pools-Postglacial Relicts or Anthropogenic Invasion? Rus. J. Biol. Invas. 7 (4), 396-404.
• [64] Sukhikh, N. M., Souissi, A., Souissi, S., Winkler, G., Castric, V., Holl, A. C., Alekseev, V. R., 2016b. Genetic and morphological heterogeneity among populations of Eurytemora affinis (Crustacea: Copepoda: Temoridae) in European waters. C.R. Biol. 339, 197-206.
• [65] Sukhikh, N. M., Lazareva, V. I., Alekseev, V. R., 2018. Eurytemora caspica Sukhikh et alekseev in the Volga river basin. In: Abstract Book, All-Russian Scientific Conference: “Volga and its life”. 22-26 October 2018, Borok, Russia p. 127, (in Russian).
• [66] Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729.
• [67] Taylor, D. J., Hebert, P. D. N., 1993. Habitat-dependent hybrid parentage and differential introgression between neighboringly sympatric Daphnia species. Proc. Natl. Acad. Sci. USA 90, 7079-7083, http://dx.doi.org/10.1073/pnas.90.15.7079.
• [68] Thompson, J. D., Higgins, D. J., Gibson, T. J., 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
• [69] Uitto, A., Gorokhova, E., Valipakka, P., 1999. Distribution of the non-indigenous Cercopagis pengoi in the coastal waters of the eastern Gulf of Finland. ICES J. Mar. Sci. 56 (Suppl.), 49-57, http://dx.doi.org/10.1006/jmsc.1999.0613.
• [70] Wasmund, N., Augustin, C., Pollehne, F., Siegel, H., Zettler, M., 2013. Biologische ustandseinschätzung der Ostsee im Jahre 2012. Meereswiss Ber, Warnemünde, p. 92.
• [71] White, T. J., Burns, T., Lee, S., Taylor, J., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M. A., Gelfand, D. H., Shinsky, J. J., White, T. J. (Eds.), PCR Protocols: A Guide to Methods and Applications. Acad. Press, San Diego, California, 315-322.
• [72] Winkler, G., Souissi, S., Poux, C., Castric, V., 2011. Genetic heterogeneity among Eurytemora affinis populations in Western Europe. Mar. Biol. 158, 1841-1856.
• [73] Zakharov, V. M., 1989. Future prospects for population phenogenetics. Sov. Sci. Rev. Sect. F: Physiol. Gen. Biol. Rev. 4, 1-79, (in Russian).

Uwagi

Opracowanie rekordu w ramach umowy 509/P-DUN/2018 ze środków MNiSW przeznaczonych na działalność upowszechniającą naukę (2019).