Abstract
Bivalve mollusk Anadara kagoshimensis is classified among the top 100 dangerous invasive species of the Mediterranean and Black seas. Using as an example the colonization by Anadara of the Kazachya (Cossack) Bay (Crimea, the Black Sea), the article identifies and discusses biocenotic relations of the mollusk with sea bottom substrates, epibionts, potential environmental competitors, and predator Rapana venosa. Relations of A. kagoshimensis to the complex of phytoepibionts and zooepibionts are presented for the first time. It is shown that Anadara can be an edificator and form a specific complex of algoconsorts and zooconsorts, while playing a positive role in increasing and preserving the species diversity in certain areas of the Black Sea. The increase in biomass and diversity of filter feeders following the occurrence of Anadara in the study region argues in favor of its positive effect on the biocenosis.
Similar content being viewed by others
REFERENCES
Anistratenko, V.V. and Khaliman, I.A., Bivalve mollusk Anadara inaequivalvis (Bivalvia, Arcidae) in the northern part of the Sea of Azov: completion of the colonization of the Azov-Black Sea basin, Vestn. Zool., 2006, vol. 40, no. 6, pp. 505–511.
Anistratenko, V.V., Anistratenko, O.Yu., and Khaliman, I.A., Conchological variability of Anadara inaequivalvis (Bivalvia, Arcidae) in the Black–Azov Sea Basin, Vestn. Zool., 2014, vol. 48, no. 5, pp. 457–466.
Baranov, A.Yu., Levenets, I.R., Sabitova, L.I., and Lebedev, E.B., Macroepibiosis of three scallop species in the waters of southern Primorye, Izv. Tikhookean. Inst. Rybov. Okeanogr., 2017, vol. 191, pp. 196–209.
Bondarev, I.P. and Bondarenko, L.V., Consorts of gastropod mollusk Rapana venosa (Valenciennes, 1846) in the northern Black Sea. Part IV: Arthropoda, Morsk. Biol. Zh., 2019, vol. 4, no. 2, pp. 11–22. https://doi.org/10.21072/mbj.2019.04.2.02
Bondarev, I.P. and Milchakova, N.A., Macroalgal fouling of shells of Rapana venosa (Valenciennes, 1846) (Gastropoda, Muricidae) in the Northern Black Sea, Int. J. Mar. Sci., 2018, vol. 8, no. 15, pp. 127–137. https://doi.org/10.5376/ijms.2018.08.0015
Bondarev, I.P. and Revkov, N.K., Consorts of gastropod mollusk Rapana venosa (Valenciennes, 1846) in the northern Black Sea. Part I: Porifera, Cnidaria, Bryozoa, Chordata, Morsk. Biol. Zh., 2017a, vol. 2, no. 2, pp. 21–34. https://doi.org/10.21072/mbj.2017.02.2.02
Bondarev, I.P. and Revkov, N.K., Consorts of gastropod mollusk Rapana venosa (Valenciennes, 1846) in the northern Black Sea. Part II: Mollusca (Polyplacophora, Bivalvia), Morsk. Biol. Zh., 2017b, vol. 2, no. 3, pp. 12–22. https://doi.org/10.21072/mbj.2017.02.3.02
Bondarev, I.P. and Revkov, N.K., Consorts of gastropod mollusk Rapana venosa (Valenciennes, 1846) in the northern Black Sea. Part III: Mollusca (Gastropoda), Morsk. Biol. Zh., 2018, vol. 3, no. 1, pp. 3–14. https://doi.org/10.21072/mbj.2018.03.1.02
ondarev, I.P., Biological foundations of facies structuring of the Black Sea shelf, Geol. Polezn. Iskop. Mirovogo Okeana, 2014, no. 4, pp. 72–90
Bondarev, I.P., Dynamics of the leading species of modern facies of the Black Sea, Geol. Polezn. Iskop. Mirovogo Okeana, 2013, no. 3, pp. 78–93.
Bondarev, I.P., Features of nutrition and development prospects of Rapana venosa (Valenciennes, 1846) in the Black Sea, Voprosy sokhraneniya bioraznoobraziya vodnykh ob”ektov: Materialy Mezhdunar. konf. (Rostov-na-Donu, 27 noyabrya 2015 g.) (Problems of Conservation of Biodiversity of Water Bodies: Proc. Int. Conf. (Rostov-on-Don, November 27, 2015)), Rostov-on-Don, 2015, pp. 44–48.
Bondarev, I.P., New data on biology and ecology of Flexopecten glaber (Linnaeus, 1758) (Bivalvia, Pectinidae) in the Black Sea, Vodn. Bioresur. Sreda Obitaniya, 2019, vol. 2, no. 2, pp. 36–44. https://celestra.ru/uploads/ files/N2_2019_36_44.pdf. Accessed January 20, 2020.
Bondarev, I.P., Taxonomic status of Flexopecten glaber ponticus (Bucquoy, Dautzenberg & Dollfus, 1898)—the Black Sea Flexopecten glaber (Linnaeus, 1758) (Bivalvia: Pectinidae), Morsk. Biol. Zh., 2018, vol. 3, no. 4, pp. 29–35. https://doi.org/10.21072/mbj.2018.03.4.03
Bondarev, I.P., The structure of Rapana venosa (Gastropoda, Muricidae) populations of the Sevastopol bays (Black Sea), Morsk. Biol. Zh., 2016, vol. 1, no. 3, pp. 14–21.
Cerrano, C., Calcinai, B., Bertolino, M., Valisano, L., and Bavestrello, G., Epibionts of the scallop Adamussium colbecki (Smith, 1902) in the Ross Sea, Antarctica, Chem. Ecol., 2006, vol. 22, suppl. 1, pp. 235–244.
Denisenko, S.G. and Savinov, V.M., Fouling of the Icelandic scallop in the area of the Seven Islands of East Murman, in Bentos Barentseva morya (Bentos of the Barents Sea), Apatity: Kol’sk. Fil. Akad. Nauk SSSR, 1984, pp. 102–112.
Dittman, D. and Robles, C., Effect of algal epiphytes on the mussel Mytilus californianus,Ecology, 1991, no. 72, pp. 286–296.
Emrić, V., Macroinvertebrate fauna associated with natural populations of Mediterranean mussel (Mytilus galloprovincialis Lamarck, 1819) in Lim channel, Istra, Ann.,Ser. Hist. Nat., 1996, vol. 6, no. 9, pp. 67–72.
Evstigneeva, I.K., Tankovskaya, I.N., Grintsov, V.V., Lisitskaya, E.V., and Makarov, M.V., Biodiversity of macrophyte communities of Cossack Bay (Sevastopol, Black Sea)), Byull. Mosk. O-va Ispyt. Prir.,Otd. Biol., 2015, vol. 120, no. 6, pp. 51–64.
Gosling, E.M., Bivalve Molluscs. Biology, Ecology and Culture, Cornwall: Fishing News Books, 2004.
Kalugina-Gutnik, A.A., Fitobentos Chernogo morya (Phytobenthos of the Black Sea), Kiev: Nauk. Dumka, 1975.
Kolyuchkina, G.A., Chikina, V.L., Biryukova, S.V., Bulysheva, N.I., Basin, A.B., Lyubimov, I.V., and Kovalenko, V.P., Long-term changes in the populations of the bivalve mollusc-invader Anadara kagoshimensis on the northeastern coast of the Black Sea, Tr. Vseross. Nauchno-Issled.Inst. Rybn. Khoz. Okeanogr., 2018, vol. 170, pp. 3–15.
Krapal, A.-M., Popa, O.P., Levarda, A.F., Iorgu, E.I., Costache, M., Crocetta, F., and Popa, L.O., Molecular confirmation on the presence of Anadara kagoshimensis (Tokunaga, 1906) (Mollusca: Bivalvia: Arcidae) in the Black Sea, Trav. Mus. Natl. Hist. Nat. Grigore Antipa, 2014, vol. 57, no. 1, pp. 9–12.
Levenets, I.R., Makrovodorosli soobshchestv obrastaniya na melkovod’e yuzhnogo Primor’ya (Macroalgae of Fouling Communities in the Shallow Water of Southern Primorye), Vladivostok: Dal’nauka, 2011.
Levenets, I.R., Ovsyannikova, I.I., and Lebedev, E.B., The composition of the macroepibiosis of the scallop Mizuhopecten yessoensis in the Peter the Great Gulf, Sea of Japan, Byull. Dal’nevost. Malakol. O-va, 2005, no. 9, pp. 155–168.
Lutaenko, K.A. and Levenets, I.R., Observations on seaweed attachment to bivalve shells in Peter the Great Bay (East Sea) and their taphonomic implications, Korean J. Malacol., 2015, no. 31, pp. 221–232.
Lutaenko, K.A., The arcid collection (Bivalvia: Arcidae) of Carl Emil Lischke in the Zoological Institute, St. Petersburg, Arch. Molluskenkd., 2015, vol. 144, no. 2, pp. 125–138.
Lutaenko, K.A., To the fauna of bivalves of the subfamily Anadarinae (Arcidae) of southern India, Byull. Dal’nevost. Malakol. O-va, 2006, no. 10, pp. 102–121.
Minicheva, G., Maximova, O.V., Moruchkova, N.A., Simakova, U.V., Sburlea, A., Dencheva, K., Aktan, Y., and Sezgin, M., The State of Macrophytobenthos, in State of the Environment of the Black Sea (2001–2006/7), Oguz, T., Ed., Istanbul, 2008. http://www.blacksea-commission.org/_publ-SOE2009.asp. Accessed April 8, 2020.
Mityaseva, N.A., Maksimova, O.V., and Georgiev, A.A., Macroalgae flora of the northern part of the Russian Black Sea coast, Ekol. Morya, 2003, no. 64, pp. 24–28.
Naumov, A.D., Dvustvorchatye mollyuski Belogo morya. Opyt ekologo-faunisticheskogo analiza (Bivalves of the White Sea. Ecological-Faunistic Analysis), St. Petersburg, 2006.
Perrings, C., Williamson, M., Barbier, E.B., Delfino, D., Dalmazzone, S., Shogren, J., Simmons, P., and Watkinson, A., Biological invasion risks and the public good: an economic perspective, Conserv. Ecol., 2002, no. 6, pp. 1–7.
Revkov, N.K. and Shcherban’, S.A., Biology features of the bivalve mollusk Anadara kagoshimensis in the Black Sea, Ekosistemy, 2017, vol. 9, pp. 47–56.
Revkov, N.K., Boltacheva, N.A., Bondarev, I.P., Bondarenko, L.V., and Timofeev, V.A., The state of zoological resources of the benthal of the deep-sea zone of the Crimean shelf after the crisis of the Black Sea ecosystem of the second half of the 20th century (according to expeditionary research of 2010 aboard the R/V ProfessorVodyanitsky), in 100 let Karadagskoi nauchnoi stantsii im. T.I. Vyazemskogo: Sbornik nauchnykh trudov (100th Anniversary of the Vyazemsky Karadag Scientific Station: Collection of Scientific Papers), Gaevskaya, A.V. and Morozova, A.L., Eds., Simferopol: N. Orianda, pp. 549–571.
Revkov, N.K., Features of Black Sea colonization by a recent invader, bivalve mollusk Anadara kagoshimensis (Bivalvia, Arcidae), Morsk. Biol. Zh., 2016, vol. 1, no. 2, pp. 3–17. https://doi.org/10.21072/mbj.2016.01.2.01
Sahin, C., Emiral, H., Okumus, I., and Mutlu Gozler, A., The benthic exotic species of the Black Sea: blood cockle (Anadara inaequivalvis, Bruguiere, 1789: Bivalve) and rapa whelk (Rapana thomasiana, Crosse, 1861: Mollusc), J. Anim. Vet. Adv., 2009, vol. 8, no. 2, pp. 240–245.
Savini, D. and Occhipinti-Ambrogi, A., Consumption rates and prey preference of the invasive gastropod Rapana venosa in the Northern Adriatic Sea, Helgol. Mar. Res., 2006, no. 60, pp. 153–159. https://doi.org/10.1007/s10152-006-0029-4
Schejter, L. and Bremec, C.S., Epibionts on Flexopecten felipponei (Dall, 1922), an uncommon scallop from Argentina, Am. Malacol. Bull., 2007, vol. 22, no. 1, pp. 75–82.
Soldatov, A.A., Revkov, N.K., and Petrosyan, V.G., Anadara kagoshimensis (Tokunaga, 1906), in Samye opasnye invazionnye vidy Rossii (TOP-100) (The Most Dangerous Invasive Species of Russia (TOP-100)), Dgebuadze, Yu.Yu., Petrosyan, V.G., and Khlyap, L.A., Eds., Moscow: Tovarishchestvo Nauchn. Izd. KMK, 2018.
Strafella, P., Ferrari, A., Fabi, G., Salvalaggio, V., Punzo, E., Cuicchi, C., Santelli, A., Cariani, A., Tinti, F., Tassetti, A., and Scarcella, G., Anadara kagoshimensis (Mollusca: Bivalvia: Arcidae) in Adriatic Sea: morphological analysis, molecular taxonomy, spatial distribution, and prediction, Mediterr. Mar. Sci., 2018, vol. 18, no. 3, pp. 443–453. https://doi.org/10.12681/mms.1933
Streftaris, N. and Zenetos, A., Alien marine species in the Mediterranean – the 100 ‘worst invasives’ and their impact, Mediterr. Mar. Sci., 2006, no. 7, pp. 87–118.
Tikhonova, E.A. and Alemov, S.V., Characteristics of bottom sediments and macrobenthos of the Cossack Bay in the first decade of the 21st century, Ekol. Bezop. Pribrezhn. Shel’fovoi Zon Kompleksn. Ispol’z. Resur. Shel’fa, 2012, no. 26, pp. 88–94.
Witman, J.D. and Suchanek, T.H., Mussels inflow: drag and dislodgement by epizoans, Mar. Ecol. Prog. Ser., 1984, no. 16, pp. 259–268.
Zaika, V.E., Valovaya, N.A., Povchun, A.S., and Revkov, N.K., Mitilidy Chernogo morya (Mytilids of the Black Sea), Kiev: Nauk. Dumka, 1990.
Zenkevich, L.A., Biologiya morei SSSR (Biology of the Seas of the USSR), Moscow: Akad. Nauk SSSR, 1986.
ACKNOWLEDGMENTS
The author thanks the anonymous reviewers for the constructive remarks and recommendations, following which improved the quality of the study.
Funding
This work was carried out in accordance with the topic of the state task of the Kovalevsky Institute of Biology of the Southern Seas “Patterns of Formation and Anthropogenic Transformation of Biodiversity and Bioresources of the Azov-Black Sea Basin and Other Regions of the World Ocean”; state registration no. АААА-А18-118020890074-2.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares that has no conflicts of interest.
Statement on the Welfare of Animals
This article does not contain any studies involving animals performed by the author.
Additional information
Translated by E. Kuznetsova
Rights and permissions
About this article
Cite this article
Bondarev, I.P. Features of Biocenotic Relations of Anadara kagoshimensis (Bivalvia, Arcidae) in the Kazachya Bay of the Black Sea. Russ J Biol Invasions 11, 198–207 (2020). https://doi.org/10.1134/S2075111720030030
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S2075111720030030