Adaptive strategy of Rapana venosa (Gastropoda, Muricidae) in the invasive population of the Black Sea


Keywords: rapa whelk; COI gene; invasions; morpho-ecological forms; distribution.

Abstract

We conducted molecular-genetic and morphological studies on the veined rapa whelk Rapana venosa (Valenciennes, 1846) in the Crimean waters of the Black Sea in order to determine possible reasons of the invasive success of this mollusk. Molecular-genetic tests were performed using COI gene; the surveyed samples reliably identified to R. venosa species. We compared the data on initial (from the Far-Eastern seas) and some invasive populations. In the natural conditions of the Yellow, East China Seas, and the Sea of Japan, the genetic diversity of rapa whelk is high (Hd = 0.933, π = 0.002). In all the invasive populations of rapa whelk (Black Sea, European and North American), an extremely low level of haplotypic and nucleotide diversity was determined (Hd = 0.0, π = 0.0). Despite low values of genetic diversity, the invasive populations of rapa whelk are characterized by ecological success. We noted stable growth of populations, tolerance to diseases and parasites, effective reproduction, high fertility. This contradicts the main provisions of the population genetics theory of formation of edge of range populations, because usually only a small number of specimens of rapa whelk were introduced. The explanations of the unique condition of the invasive populations of rapa whelk, both from an ecological perspective (high resistance to fluctuations of hydrological factors and chemical pollution, absence of enemies, high fertility) and genetic perspective (high selective value of separate haplotypes settled in the new water areas) have not been confirmed. We determined that a very important factor for the naturalization of the rapa whelk at low genetic diversity is the intra-species morpho-ecological divergence. In the Crimean water area of the Black Sea, R. venosa was found to have two morpho-ecological forms associated with the peculiarities of the development of the proportions of the shell. Study of successful invasive species would allow timely and adequate reaction to new cases of introduction.

References

Aguilar, R., Ogburn, M. B., Driskell, A. C., Weigt, L. A., Groves, M. C., & Hines, A. H. (2016). Gutsy genetics: Identification of digested piscine prey items in the stomach contents of sympatric native and introduced warmwater catfishes via DNA barcoding. Environmental Biology of Fishes, 100, 325–336.


Berner, D., Stutz, W. E., & Bolnick, D. I. (2010). Foraging trait (co)variances in stickleback evolve deterministically and do not predict trajectories of adaptive diversification. Evolution, 64, 2265–2277.


Bondarev, I. P. (2016). Struktura populyacij Rapana venosa (Gastropoda, Muricidae) sevastopol’skih buht (Chyornoe more) [Population structure of Rapana venosa (Gastropoda, Muricidae) of Sevastopol bays (Black Sea)]. Morskoj Biologicheskij Zhurnal, 1(3), 14–21 (in Russian).


Carranza, A., de Mello, C., Ligrone, A., Gonzalez, S., Piriz, P., & Scarabino, F. (2010). Observations on the invading gastropod Rapana venosa in Punta del Este, Maldonado Bay, Uruguay. Biological Invasions, 9534, 27–31.


Chandler, E. A., McDowell, J. R., & Graves, J. E. (2008). Genetically monomorphic invasive populations of the rapa whelk, Rapana venosa. Molecular Ecology, 17, 4079–4091.


Dae-Won, K., Yoo, W. G., Park, H. C., Yoo, H. S., Kang, D. W., Jin, S. D., Min, H. K., Paek, W. K., & Lim, J. (2012). DNA barcoding of fish, insects, and shellfish in Korea. Genomics and Informatics, 10(3), 206–211.


Elton, C. (1960). Ekologiya nashestvij zhivotnyh i rastenij [Ecology of invasions of animals and plants]. Inostrannaya Literatura, Moscow (in Russian).


Giberto, D. A., Bremec, C. S., Schejter, L., Schiariti, A., Mianzan, H., & Acha, E. M. (2006). The invasive rapa whelk Rapana venosa (Valenciennes, 1846): Status and potential ecological impacts in the Río de la Plata estuary, Argentina-Uruguay. Journal of Shellfish Research, 25(3), 919–924.


Goulletquer, P., Bachelet, G., Sauriau, P. G., & Noel, P. (2002). Open Atlantic coast of Europe – a century of introduced species into French waters. In: Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer Academic Publishers, Dordrecht.


Harding, J. M., Kingsley-Smith, P., Savini, D., & Mann, R. (2007). Comparison of predation signatures by Atlantic oyster drills (Urosalpinx cinerea Say, Muricidae) and veined rapa whelks (Rapana venosa Valenciennes, Muricidae) in bivalve prey. Journal of Experimental Marine Biology and Ecology, 352, 1–11.


Kerckhof, F., Vink, R. J., Nieweg, D. C., & Post, J. N. J. (2006). The veined whelk Rapana venosa has reached the North Sea. Aquatic Invasions, 1(1), 35–37.


Koutsoubas, D., & Voultsiadou-Koukoura, E. (1991). The occurrence of Rapana venosa (Valenciennes, 1846) (Gastropoda, Thaididae) in the Aegean Sea. Bolletino Malacogico, 26(10–12), 201–204.


Lanfranconi, A., Hutton, M., Brugnoli, E., & Muniz, P. (2009). New record of the alien mollusc Rapana venosa (Valenciennes 1846) in the Uruguayan coastal zone of Rio de la Plata. Pan-American Journal of Aquatic Sciences, 4(2), 216–221.


Librado, P., & Rozas, J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25(11), 1451–1452.


Mann, R., & Harding, J. M. (2000). Invasion of the North American Atlantic coast by a large predatory Asian mollusk. Biological Invasions, 2, 7–22.


Mann, R., & Harding, J. M. (2003). Salinity tolerance of larval Rapana venosa: Implications for dispersal and establishment of an invading predatory gastropod on the North American Atlantic coast. Biological Bulletin, 204, 96–103.


Mina, M. V. (2001). Morphological diversification of fish as a consequence of the divergence of ontogenetic trajectories. Russian Journal of Developmental Biology, 32, 397–402.


Odum, E. P. (1985). Trends expected in stressed ecosystems. Bio-Science, 35, 419–422.


Pereladov, M. V. (2013). Sovremennoe sostoyanie populyacii i osobennosti biologii rapany (Rapana venosa) v severo-vostochnoj chasti Chyornogo moray [The current state of the population and the biology of the Rapana venosa in the northeastern Black Sea]. Trudy VNIRO, 150, 8–20 (in Russian).


Revkov, N. K. (2009). Nekotorye zamechaniya po sostavu i mnogoletnej dinamike fauny mollyuskov ryhlyh gruntov yugo-vostochnogo Kryma (Chernoe more) [Some comments on the composition and long-term dynamics of the mollusk fauna of loose soils if the south-eastern Crimea (Black Sea)]. Karadag-2009. Ekosi-Gidrofizika, Sevastopol. Pp. 251–261 (in Ukrainian). https://doi.org/10.13140/RG.2.1.1962.2881


Roman, J., & Darling, J. A. (2007). Paradox lost: Genetic diversity and the success of aquatic invasions. Trends in Ecology and Evolution, 22, 454–464.


Saitou, N., & Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4), 406–425.


Sakai, A. K., Allendorf, F. W., Holt, J. S., Lodge, D. M., Molofsky, J., With, K. A., Baughman, S., Cabin, R. J., Cohen, J. E., Ellstrand, N. C., McCauley, D. E., O’Neil, P., Parker, I. M., Thompson, J. N., & Weller, S. G. (2001). The population biology of invasive species. Annual Review of Ecology and Systematics, 32, 305–332.


Savini, D., & Occhipinti-Ambrogi, A. (2006). Consumption rates and prey preference of the invasive gastropod Rapana venosa in the Northern Adriatic Sea. Helgoland Marine Research, 60, 153–159.


Savini, D., Castellazzi, M., Favruzza, M., & Occhipinti-Ambrogi, A. (2004). The alien mollusc Rapana venosa (Valenciennes, 1846; Gastropoda, Muricidae) in the Northern Adriatic Sea: Population structure and shell morphology. Chemistry and Ecology, 20(Suppl. 1), 411–424.


Seyhan, K., Mazlum, E. R., Emiral, H., Engin, S., & Demirhan, S. (2003). Diel feeding periodicity, gastric emptying, and estimated daily food consumption of whelk (Rapana venosa) in the south eastern Black Sea (Turkey) marine ecosystem. Indian Journal of Marine Science, 32(3), 249–251.


Shen, Y., Kang, J., & He, S. (2016). DNA barcoding for the identification of common economic aquatic products in Central China and its application for the supervision of the marked trade. Food Control, 61, 79–91.


Shmalgauzen, I. I. (1982). Organizm kak celoe v individual’nom i istoricheskom razvitii [The organism as a whole in individual and historical development]. Nauka, Moscow (in Russian).


Slynko, Y. V., Slynko, E. E., Pirkova, A. V., & Ryabushko, V. I. (2018). Mitochondrial DNA barcoding of the pacific oyster Crassostrea gigas (Thunberg, 1793) (Mollusca: Bivalvia: Ostreidae), cultivated in the Black Sea. Russian Journal of Genetics, 54, 1445–1451.


Sun, X., & Yang, A. (2016). The complete mitochondrial genome of Rapana venosa (Gastropoda, Muricidae). Mitochondrial DNA Part A: DNA Mapping, Sequencing, and Analysis, 27(2), 1471–1472.


Ward, J. L., & McLennan, D. A. (2009). Historical and ecological correlates of body shape in the brook stickleback, Culaea inconstans. Biological Journal of the Linnean Society, 96(4), 769–783.


Westphal, M. I., Browne, M., MacKinnon, K., & Noble, I. (2008). The link between international trade and the global distribution of invasive alien species. Biological Invasions, 10, 391–398.


Wilson, J. R. U., Dormontt, E. E., Prentis, P. J., Lowe, A. J., & Richardson, D. M. (2009). Something in the way you move: Dispersal pathways affect invasion success. Trends in Ecology and Evolution, 24(3), 136–144.


Xue, D.-X., Graves, J., Carranza, A., Sylantyev, S., Snigirov, S., Zhang, T., & Liu, J.-X. (2018). Successful worldwide invasion of the veined rapa whelk, Rapana venosa, despite a dramatic genetic bottleneck. Biological Invasions, 20(11), 3297–3314.


Yang, J., Li, Q., Kong, L., Zheng, X., & Wang, R. (2008). Genetic structure of the veined rapa whelk (Rapana venosa) populations along the coast of China. Biochemical Genetics, 46, 539–548.


Zou, S., Li, Q., & Kong, L. (2012). Multigene barcoding and phylogeny of geographically widespread muricids (Gastropoda: Neogastropoda) along the coast of China. Marine Biotechnology, 14(1), 21–34.

Published
2020-02-10
Section
Articles