Article

Alexey A. Zotin, Dr. Sc., Leading Researcher of the Laboratory of evolutional biology of development of the Koltsov Institute of Developmental Biology of RAS (119334, Russia, Moscow, Vavilov Street, 26); e-mail: aazotin@mail.ru
Svetlana A. Murzina, Dr. Sc., Head of environmental biochemistry laboratory of the Institute of Biology of the Karelian Research Centre of RAS (185910, Russia, Republic of Karelia, Petrozavodsk, Pushkinskaya Street, 11); iD ORCID: https://orcid.org/0000-0002-9705-2741; e-mail: murzina.svetlana@gmail.com
Denis A. Efremov, PhD, Researcher of the Laboratory of ecology of fish and water invertebrates of the Institute of Biology of the Karelian Research Centre of RAS (185910, Russia, Republic of Karelia, Petrozavodsk, Pushkinskaya Street, 11); e-mail: denisefremov@list.ru
Panu Oulasvirta, Chairman of the Board, Owner/Senior Consultant, Alleco Ltd. (Veneentekijantie, 4, FI-00210, Helsinki, Finland); e-mail: panu.oulasvirta@alleco.fi
Evgeny P. Ieshko, Dr. Sc., Chief Researcher of the Laboratory of parasitology of animals and plants of the Institute of Biology of the Karelian Research Centre of RAS (185910, Russia, Republic of Karelia, Petrozavodsk, Pushkinskaya Street, 11); iD ORCID: https://orcid.org/0000-0002-3133-4383; e-mail: ieshkoep@gmail.com

Zotin A.A., Murzina S.A., Efremov D.A., Oulasvirta P., Ieshko E.P. 2021. Ecology of Margaritifera margaritifera (Bivalvia, Margaritiferidae) in the River Kamennaya, White Sea Basin, Russia. Nature Conservation Research 6(Suppl.1): 61–75. https://dx.doi.org/10.24189/ncr.2021.005

The conditions for cohabitation of juvenile Salmo salar and Margaritifera margaritifera in the River Kamennaya (River Kem catchment, White Sea drainage basin, Russia) were studied. The M. margaritifera population in the River Kamennaya contains about 1000 specimens. The only intermediate host capable of sustaining the existence of this rare North European mussel is the juvenile S. salar. In this study, we investigated a set of parameters and processes to get a more comprehensive insight into the ecology of the M. margaritifera. One of such parameters is the individual linear growth, which was investigated in freshwater mussels from the River Kamennaya. Growth deceleration coefficients varied widely and differed significantly among specimens. The population-averaged coefficient of growth deceleration was 0.076. The growth of mussels in the River Kamennaya involves three regular biorhythms with the following periods: 11.5, 6.4 and 4.0 years. The biorhythm periods were roughly constant both through an individual's ontogeny and among different individuals. A comparison of our results with data on other M. margaritifera populations in the Republic of Karelia and the Murmansk Region reveals a reliable (p < 0.01) negative correlation between growth deceleration coefficients and mean annual temperature in the M. margaritifera habitat. The abundance, spatial distribution and age structure of juvenile S. salar and M. margaritifera are presented. The rates of glochidial infection in S. salar juveniles at different ages were estimated. The developmental stages and the status of glochidia encysted on juvenile S. salar gills were observed and described using histological methods. The results of this study will be used to suggest activities and measures aimed to preserve populations of M. margaritifera and S. salar in the River Kamennaya, primarily to promote juvenile S. salar numbers and M. margaritifera settlement in rapids with a high density of young individuals.

Atlantic salmon, endangered species conservation, freshwater pearl mussel, glochidia, growth, infection, Salmo salar

Received: 16.05.2020. Revised: 11.10.2020. Accepted: 25.10.2020.

Alimov A.F. 1981. Functional Ecology of Freshwater Bivalves. Leningrad: Nauka. 248 p. [In Russian]
Arendt A., Heinen P., Molitor M., Mullet T., Thielen F. 2010. Restauration des populations de moules perlières en Ardennes. Rapport d'activité annuel (Période du 1er août au 31 juillet 2010). Fondation Hëllef fir d'Natur. 118 p.
Artemyev A.V. 2007. Red Data Book of the Republic of Karelia. Petrozavodsk: Petrozavodsk State University. 364 p. [In Russian]
Bauer G. 1986. The status of the freshwater pearl mussel Margaritifera margaritifera L. in the south of its European range. Biological Conservation 38(1): 1–9. DOI: 10.1016/0006-3207(86)90015-7
Bauer G. 1988. Threats to the freshwater pearl mussel Margaritifera margaritifera L. in Central Europe. Biological Conservation 45(4): 239–253. DOI: 10.1016/0006-3207(88)90056-0
Bauer G. 1992. Variation in the Life Span and Size of the Freshwater Pearl Mussel. Journal of Animal Ecology 61(2): 425–436. DOI: 10.2307/5333
von Bertalanffy L. 1960. Principles and theory of growth. In: Fundamental Aspects of Normal and Malignant Growth. Amsterdam: Elsevier. P. 137–259.
Bohlin T. 1984. Quantitative electrofishing for salmon and trout – views and recommendations. Information från Sötvattenslaboratoriet 4: 1–33.
Bruno D.W., McVicar A.H., Waddell I.F. 1988. Natural infection of farmed Atlantic salmon, Salmo salar L., parr by glochidia of the freshwater pearl mussel, Margaritifera margaritifera L. Bulletin of the European Association of Fish Pathologists 8(2): 23–26.
Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W. 1997. Parasitology meets ecology on its own terms: Margolis et al. Revisited. Journal of Parasitology 83(4): 575–583. DOI: 10.2307/3284227
Bykhovskaya-Pavlovskaya I.E. 1985. Fish Parasites. Study Manual. Leningrad: Nauka. 123 p. [In Russian]
CLIMATE-DATA.ORG. 2020. Climate data of cities worldwide. Available from: https://ru.climate-data.org/
Cochet G. 2004. La moule perlière et les nayades de France. Histoire d'une sauvegarde. Nohanent: Catiche production. 32 p.
Council of Europe. 1979. Convention on the conservation of European wildlife and natural heritage. Bern: Switzerland. Available from: http://conventions.coe.int/Treaty/EN/Treaties/Html/104.htm
Denic M., Geist J. 2017. The freshwater pearl mussel Margaritifera margaritifera in Bavaria, Germany – Population status, conservation efforts and challenges. Biology Bulletin 44(1): 61–66. DOI: 10.1134/S1062359017010034
Dolmen D., Kleiven E. 2008. Distribution, status and threats of the freshwater pearl mussel Margaritifera margaritifera (Linnaeus) (Bivalvia, Margaritiferidae) in Norway. Fauna Norvegica 26/27: 3–14. DOI: 10.5324/fn.v26i0.569
Dunca E., Mutvei H. 2009. Åldersbestämning av unga flodpärlmusslor i Sverige. Sweden: WWF. 24 p.
Dunca E., Söderberg H., Norrgrann O. 2011. Shell growth and age determination in the freshwater pearl mussel Margaritifera margaritifera in Sweden: natural versus limed streams. Ferrantia 64: 48–58.
Dyduch-Falniowska A., Zając K. 2005. Margaritifera margaritifera (Linneaus, 1758) eastern pearlshell: freshwater pearl mussel. Polska czerwona księga zwierząt. bezkręgowce Vol. 1. 447 p.
Geist J. 2010. Strategies for the conservation of endangered freshwater pearl mussels (Margaritifera margaritifera L.): a synthesis of Conservation Genetics and Ecology. Hydrobiologia 644(1): 69–88. DOI: 10.1007/s10750-010-0190-2
Gumpinger C., Pichler-Scheder C., Huemer D. 2016. Das oberösterreichische Artenschutzprojekt «Vision Flussperlmuschel». Österreichs Fischerei 69: 259–273.
Hastie L.C., Young M.R., Boon P.J. 2000. Growth characteristics of freshwater pearl mussels, Margaritifera margaritifera (L.). Freshwater Biology 43(2): 243–256. DOI: 10.1046/j.1365-2427.2000.00544.x
Ieshko E.P., Geist J., Murzina S.A., Veselov A.E., Lebedeva D.I., Ziuganov V.V. 2016. The characteristics of the infection of juvenile Atlantic salmon with glochidia of the freshwater pearl mussel in rivers of Northwest Russia. Knowledge and Management of Aquatic Ecosystems 417: 6. DOI: 10.1051/kmae/2015039
Inha I.K. 1999. Kalevalan laulumailta. Toim. Pekka Laaksonen. Suomalaisen Kirjallisuuden Seuran Toimituksia 739. Helsinki: SKS. 437 p.
IUCN. 2020. The IUCN Red List of Threatened Species. Version 2020-2. Available from: https://www.iucnredlist.org
Ivanter E.V., Korosov A.V. 2010. Elementary Biometrics. Petrozavodsk: Petrozavosk State University. 104 p. [In Russian]
Karna D.W., Millemann R.E. 1978. Glochidiosis of salmonid fishes. III. Comparative susceptibility to natural infection with Margaritifera margaritifera (L.) (Pelecypoda: Margaritanidae) and associated histopathology. Journal of Parasitology 64(3): 528–537. DOI: 10.2307/3279799
Kennedy M.K., Van Guelpen L., Pohle G., Bajona L. (Eds.). 2020. Canadian Register of Marine Species. Available from: http://www.marinespecies.org/carms on 2020-06-08
Kotiranta H., Uotila P., Sulkava S., Peltonen S.L. (Eds.) 1998. Red Data Book of East Fennoscandia. Helsinki: Ministry Environ. 344 p.
Lavictoire L., Ramsey A.D., Moorkens E.A., Souch G., Barnhart M.C. 2018. Ontogeny of juvenile freshwater pearl mussels, Margaritifera margaritifera (Bivalvia: Margaritiferidae). PLoS ONE 13(3): e0193637. DOI: 10.1371/journal.pone.0193637
Makhrov A., Bespalaya J., Bolotov I., Vikhrev I., Gofarov M., Alekseeva Y., Zotin A. 2014. Historical geography of pearl harvesting and current status of populations of freshwater pearl mussel Margaritifera margaritifera (L.) in the western part of Northern European Russia. Hydrobiologia 735(1): 149–159. DOI: 10.1007/s10750-013-1546-1
Malek-Mansour M., Nicolis G., Prigogine I. 1980. Nonequilibrium phase transitions in chemical systems. In: A.I. Zotin (Ed.): Termodynamics and kinetics of biological processes. Moscow: Nauka. P. 59–83. [In Russian]
Meyers T.R., Millemann R.E. 1977. Glochidiosis of salmonid fishes. I. Comparative susceptibility to experimental infection with Margaritifera margaritifera (L.) (Pelecypoda: Margaritanidae). Journal of Parasitology 63(4): 728–733. DOI: 10.2307/3279583
Mikodina E.V., Sedova M.A., Chmilevsky D.A., Mikulin A.E., Pyanova S.V., Poluektova O.G. 2009. Histology for ichthyologists: experience and advices. Moscow: VNIRO. 111 p. [In Russian]
Moorkens E. 2010. Addressing the conservation and rehabilitation of Margaritifera margaritifera populations in the republic of Ireland within the framework of the habitats and species directive. Journal of Conchology 40(3): 339–350.
Motte G., Terren S., Bocca S., Collas P. 2013. Conservation of habitats of freshwater pearl mussel (Margaritifera margaritifera). In: International Meeting on Improving the environment for the Freshwater Pearl Mussel. Kerfermarkt, Austria.
Murzina S.A., Ieshko E.P., Zotin A.A. 2017. The freshwater pearl mussel Margaritifera margaritifera L.: metamorphosis, growth, and development dynamics of encysted glochidia. Biology Bulletin 44(1): 6–13. DOI: 10.1134/S106235901701006X
Nezlin L.P., Cunjak R.A., Zotin A.A., Ziuganov V.V. 1994. Glochidium morphology of the freshwater pearl mussel (Margaritifera margaritifera) and glochidiosis of Atlantic salmon (Salmo salar): a study by scanning electron microscopy. Canadian Journal of Zoology 72(1): 15–21. DOI: 10.1139/z94-003
Olofsson P. 2017. Regional monitoring of freshwater pearl mussel Margaritifera margaritifera in the County of Norrbotten, Sweden. Biology Bulletin 44(1): 74–80. DOI: 10.1134/S1062359017010095
Oulasvirta P. 2010. Freshwater pearl mussel in Kamennaya River – expedition to the Kostamuksha State Nature Reserve, NW Russia. In: E.P. Ieshko, T. Lindholm (Eds.): Conservation of the freshwater pearl mussel Margaritifera margaritifera populations in Northern Europe. Petrozavodsk: Karelian Research Centre of RAS. P. 64–68.
Oulasvirta P., Leinikki J., Syväranta J. 2017. Freshwater pearl mussel in Finland – current status and future prospects. Biology Bulletin 44(1): 81–91. DOI: 10.1134/S1062359017010101
Outeiro A., Ondina P., Fernández C., Amaro R., San Miguel E. 2007. Population density and age structure of the freshwater pearl mussel, Margaritifera margaritifera, in two Iberian rivers. Freshwater Biology 53(3): 485–496. DOI: 10.1111/j.1365-2427.2007.01913.x
Prigogine I. 1972. La thermodynamique de la vie. La Recherche 3(24): 547–562.
Rozsa L., Reiczigel J., Majoros G. 2000. Quantifying parasites in samples of hosts. Journal of Parasitology 86(2): 228–232. DOI: 10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2
Rudzīte M., Rudzītis M., Birzaks J. 2017. The populations of the freshwater pearl mussel, Margaritifera margaritifera (Linnaeus, 1758), and the thick shelled river mussel, Unio crassus Philipsson, 1788, in Latvia. Biology Bulletin 44(1): 99–107. DOI: 10.1134/S1062359017010125
San Miguel E., Monserrat S., Fernández C., Amaro R., Hermida M., Ondina P., Altaba C.R. 2004. Growth models and longevity of freshwater pearl mussels (Margaritifera margaritifera) in Spain. Canadian Journal of Zoology 82(8): 1370–1379. DOI: 10.1139/z04-113
Shapiro S.S., Wilk M.B. 1965. An analysis of variance test for normality. Biometrika 52(3): 591–611.
Simon O.P., Vaníčková I., Bílỳ M., Douda K., Patzenhauerová H., Hruška J., Peltánová A. 2015. The status of freshwater pearl mussel in the Czech Republic: several successfully rejuvenated populations but the absence of natural reproduction. Limnologica 50: 11–20. DOI: 10.1016/j.limno.2014.11.004
Sousa R., Amorim A., Sobral C., Froufe E., Varandas S., Teixeira A., Lopes-Lima M. 2013. Ecological Status of a Margaritifera margaritifera (Linnaeus, 1758) Population at the Southern Edge of its Distribution (River Paiva, Portugal). Environmental Management 52(5): 1230–1238. DOI: 10.1007/s00267-013-0117-6
Studenov I.I. 2000. Review of methods for assessing the production of salmon rivers. Arkhangelsk. 47 p. [In Russian]
Van Valen L. 1973. A new evolutionary law. Evolutionary Theory 1: 1–30.
Young M., Williams J. 1984. The reproductive biology of the freshwater pearl mussel Margaritifera margaritifera (Linn.) in Scotland I. Field studies. Archiv für Hydrobiologie 99(4): 405–422.
Young M.R., Cosgrove P.J., Hastie L.C. 2001. The extent of, and causes for, the decline of a highly threatened naiad: Margaritifera margaritifera. In: G. Bauer, K. Wächtler (Eds.): Ecology and Evolution of the Freshwater Mussels Unionoida. Vol. 145. Berlin: Springer-Verlag. P. 337–357. DOI: 10.1007/978-3-642-56869-5_19
Zippin C. 1956. An Evaluation of the Removal Method of Estimating Animal Populations. Biometrics 12(2): 163–189. DOI: 10.2307/3001759
Ziuganov V.V., Zotin A.A. 2001. Freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758). In: Red Data Book of the Russian Federation (Animals). Moscow: Astrel'. P. 61–62. [In Russian]
Ziuganov V., Zotin A., Nezlin L., Tretiakov V. 1994. The freshwater pearl mussels and their relationships with salmonid fish. Moscow: VNIRO. 104 p.
Zolotarev V.N. 1974. Multiannual rhythms of growth of mussel L. grayana shell. Ekologiya 3: 76–80. [In Russian]
Zotin A.A. 2000. Statistical estimation of allometric coefficients. Biology Bulletin 27(5): 431–437. [In Russian]
Zotin A.A. 2009. Patterns of growth and energy metabolism in the ontogeny of mollusks. Dr.Sc. Thesis Abstract. Moscow. 30 p. [In Russian]
Zotin A.A. 2014. Why linear thermodynamics does describe change of entropy production in living systems? Natural Science 6(7): 495–502. DOI: 10.4236/ns.2014.67048
Zotin A.A. 2020. Growth biorhythms of the European pearl mussel Margaritifera margaritifera (Bivalvia, Margaritiferidae). Varzuga River Population (Murmansk Region). Biology Bulletin 47(4): 368–375.
Zotin A.A., Ieshko E.P. 2017. Comparative analysis of the growth of Margaritifera margaritifera (Bivalvia) from different populations of Karelia and Kola Peninsula. Biology Bulletin 44(1): 1–5. DOI: 10.1134/S1062359017010186
Zotin A.A., Ieshko E.P. 2018. Biorhythms of Margaritifera margaritifera (Bivalvia, Margaritiferidae) freshwater pearl mussel growth: population of Syuskyuyanioki River (Karelia). Russian Journal of Developmental Biology 49(4): 206–213. DOI: 10.1134/S1062360418040082
Zotin A.A., Ieshko E.P. 2020. Biorhythms of Margaritifera margaritifera (Bivalvia, Margaritiferidae) freshwater pearl mussel growth: population of Nemina River (Karelia). Biology Bulletin. [In press]
Zotin A.A., Kleimenov S.Yu. 2013. Endogenous biorhythms of the specific growth rate in individual development of Lymnaea stagnalis (Lymnaeidae, Gastropoda). Biology Bulletin 40(1): 1–10. DOI: 10.1134/S1062359013010147
Zotin A.A., Murzina S.A., Ieshko E.P. 2018. Growth biorhythms in the freshwater pearl mussel Margaritifera margaritifera (Bivalvia, Margaritiferidae). Livojoki river population (Karelia). Knowledge and management of aquatic ecosystems 419: 44. DOI: 10.1051/kmae/2018033
Zotin A.A., Murzina S.A., Bystrova K.A., Ieshko E.P. 2020. Growth Parameters of the Freshwater Pearl Mussel Margaritifera margaritifera (Bivalvia, Margaritiferidae), Vuokinjoki River Population (Karelia). Malacologia 63(1): 67–75. DOI: 10.4002/040.063.0107