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Trends and drivers of Macoma balthica L. dynamics in Kandalaksha Bay, the White Sea

Published online by Cambridge University Press:  22 August 2017

Evgeny A. Genelt-Yanovskiy Open the ORCID record for Evgeny A. Genelt-Yanovskiy [Opens in a new window] ,
Dmitriy A. Aristov ,
Alexey V. Poloskin  and
Sophia A. Nazarova Open the ORCID record for Sophia A. Nazarova [Opens in a new window]
Evgeny A. Genelt-Yanovskiy
Affiliation:
Department of Ichthyology and Hydrobiology, Saint-Petersburg State University, Saint-Petersburg, Russia Zoological Institute of Russian Academy of Sciences, Saint-Petersburg, Russia
Dmitriy A. Aristov
Affiliation:
Zoological Institute of Russian Academy of Sciences, Saint-Petersburg, Russia Laboratory of Marine Benthic Ecology and Hydrobiology, Saint-Petersburg, Russia
Alexey V. Poloskin
Affiliation:
Laboratory of Marine Benthic Ecology and Hydrobiology, Saint-Petersburg, Russia Department of Invertebrate Zoology, Saint-Petersburg State University, Saint-Petersburg, Russia
Sophia A. Nazarova*
Affiliation:
Department of Ichthyology and Hydrobiology, Saint-Petersburg State University, Saint-Petersburg, Russia Zoological Institute of Russian Academy of Sciences, Saint-Petersburg, Russia
*
Correspondence should be addressed to: S.A. Nazarova, Marine Research Lab, Zoological Institute, Russian Academy of Science, Universitetskaya emb., 1, Saint-Petersburg, 199034, Russia email: [email protected]
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Abstract

Long-term population dynamics of marine invertebrates can be shaped by environmental conditions as well as biotic factors, including predation, diseases, interspecific or intraspecific competition. Towards the northern edge of species ranges the role of biotic interactions gradually decreases while the impact of climate oscillations becomes more important. This study examined the long-term changes in abundance, individual growth rates and shell shape characteristics of Macoma balthica, one of the dominant species in White Sea soft-bottom intertidal communities. To test the role of predators in changes in clam abundance, we examined the number of moonsnails Amauropsis islandica. Macoma balthica exhibited spatially synchronous population dynamics at six sites in Kandalaksha Bay, where densities of clams varied between 140 and 8500 ind. m−2 during the 21-year period of observations. Statistical modelling using generalized additive models (GAM) shows that a combination of mild winter and warm summer led to an increase in M. balthica density the following year. Predation by A. islandica had no impact on changes in M. balthica density. Growth rates of M. balthica were higher during a cool decade, but clams that lived in a warmer period were characterized by more globose shells. Our results suggest that the climate oscillations can be regarded as the key factor causing the shift in abundance of M. balthica in the White Sea during the last two decades via recruitment and survival.

Keywords

Macoma balthicaLimecola balthicaWhite Seapopulation dynamicslinear growthAmauropsis islandicaNaticidaepredator-prey interactionsclimate change
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Special Issue 1: Special Section: European Marine Biology Symposium Papers 2016 , February 2018 , pp. 13 - 24
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Ambrose, W.G., Carroll, M.L., Greenacre, M., Thorrold, S.R. and McMahon, K.W. (2006) Variation in Serripes groenlandicus (Bivalvia) growth in a Norwegian high-Arctic fjord: evidence for local-and large-scale climatic forcing. Global Change Biology 12, 1595–1607.CrossRefGoogle Scholar
Appeldoorn, R.S. (1983) Variation in the growth rate of Mya arenaria and its relationship to the environment as analyzed through principal components analysis and the omega parameter of the von Bertalanffy equation [Soft shell clam populations]. Fishery Bulletin United States, National Marine Fisheries Service 81, 75–84.Google Scholar
Aristov, D., Varfolomeeva, M. and Puzachenko, G. (2015) All's good in a famine? Hydrobia ulvae as a secondary prey for juveniles of Iceland moonsnails Amauropsis islandica at the White Sea sandflats. Journal of the Marine Biological Association of the United Kingdom 95, 1601–1606.CrossRefGoogle Scholar
Aristov, D.A. (2013) The dynamic of predatory gastropod mollusk Amauropsis islandica (Gmelin, 1791) (Naticidae: Caenogastropoda) at the Kandalaksha Bay conservation area (White Sea). In Nemova, N.N., Murzina, S.A. and Mescheryakova, O.V. (eds) Proceedings of the XII Conference on Exploration, Sustainable Use and Protection of Natural Resources of the White Sea. Petrozavodsk: Kola Research Center, pp. 21–23. [In Russian]Google Scholar
Austin, G.E. and Rehfisch, M.M. (2005) Shifting nonbreeding distributions of migratory fauna in relation to climatic change. Global Change Biology 11, 31–38.CrossRefGoogle Scholar
Azarov, V.V. (1963) Fishes feeding at the intertidal zone of Ryashkov and Lodeyniy islands in the White Sea (Kandalaksha Bay). Proceedings of Kandalaksha Reserve 4, 35–53. [In Russian]Google Scholar
Babkov, A.I. and Golikov, A.N. (1984) Hydrobiocomplexes of the White Sea. Leningrad: Zoological Institute AS USSR Publishers. [In Russian]Google Scholar
Becquet, V., Lasota, R., Pante, E., Sokolowski, A., Wolowicz, M. and Garcia, P. (2013) Effects of fine-scale environmental heterogeneity on local genetic structure in Macoma balthica from the Gulf of Gdañsk (southern Baltic Sea). Hydrobiologia 714, 61–70.CrossRefGoogle Scholar
Berge, J., Johnsen, G., Nilsen, F., Gulliksen, B. and Slagstad, D. (2005) Ocean temperature oscillations enable reappearance of blue mussels Mytilus edulis in Svalbard after a 1000 year absence. Marine Ecology Progress Series 303, 167–175.CrossRefGoogle Scholar
Beukema, J.J. and Dekker, R. (2005) Decline of recruitment success in cockles and other bivalves in the Wadden Sea: possible role of climate change, predation on postlarvae and fisheries. Marine Ecology Progress Series 287, 149–167.CrossRefGoogle Scholar
Beukema, J.J. and Dekker, R. (2014) Variability in predator abundance links winter temperatures and bivalve recruitment: correlative evidence from long-term data in a tidal flat. Marine Ecology Progress Series 513, 1–15.CrossRefGoogle Scholar
Beukema, J.J., Dekker, R., Essink, K. and Michaelis, H. (2001) Synchronized reproductive success of the main bivalve species in the Wadden Sea: causes and consequences. Marine Ecology. Progress Series 211, 143–155.CrossRefGoogle Scholar
Beukema, J.J., Dekker, R. and Jansen, J.M. (2009) Some like it cold: populations of the tellinid bivalve Macoma balthica (L.) suffer in various ways from a warming climate. Marine Ecology Progress Series 384, 135–145.CrossRefGoogle Scholar
Beukema, J.J., Dekker, R., van Stralen, M.R. and de Vlas, J. (2015) Large-scale synchronization of annual recruitment success and stock size in Wadden Sea populations of the mussel Mytilus edulis L. Helgoland Marine Research 69, 327–333.CrossRefGoogle Scholar
Beukema, J.J., Essink, K., Michaelis, H. and Zwarts, L. (1993) Year-to-year variability in the biomass of macrobenthic animals on tidal flats of the Wadden Sea: how predictable is this food source for birds? Netherlands Journal of Sea Research 31, 319–330.CrossRefGoogle Scholar
Beukema, J.J. and Meehan, B.W. (1985) Latitudinal variation in linear growth and other shell characteristics of Macoma balthica . Marine Biology 90, 27–33.CrossRefGoogle Scholar
Caddy, J.F. (1967) Maturation of gametes and spawning in Macoma balthica (L.). Canadian Journal of Zoology 45, 955–965.CrossRefGoogle ScholarPubMed
Caddy, J.F. (2010) Hydrodynamic sorting in the life history dynamics of Macoma balthica in a nursery area in the Thames estuary, England. Ciencia Pesquera 18, 14.Google Scholar
Carroll, M.L., Ambrose, W.G., Levin, B.S., Henkes, G.A., Hop, H. and Renaud, P.E. (2011) Pan-Svalbard growth rate variability and environmental regulation in the Arctic bivalve Serripes groenlandicus . Journal of Marine Systems 88, 239–251.CrossRefGoogle Scholar
Clements, J.C. and Rawlings, T.A. (2014) Ontogenetic shifts in the predatory habits of the northern moonsnail (Lunatia heros) on the Northwestern Atlantic Coast. Journal of Shellfish Research 33, 755–768.CrossRefGoogle Scholar
Compton, T.J., Bodnar, W., Koolhaas, A., Dekinga, A., Holthuijsen, S., ten Horn, J., McSweeney, N., van Gils, J.A. and Piersma, T. (2016) Burrowing behavior of a deposit feeding bivalve predicts change in intertidal ecosystem state. Frontiers in Ecology and Evolution 4, 1–9.CrossRefGoogle Scholar
de Wilde, P.A.W.J. (1975) Influence of temperature on behaviour, energy metabolism and growth of Macoma balthica (L.). In Barnes, H. (ed.) Proceeding of 9th European Marine Biology Symposium. Aberdeen: Aberdeen University Press, pp. 239–256.Google Scholar
Egorova, E.N. (2007) New data against the bipolar status of the genus Amauropsis (Naticidae, Mollusca) with a description of the new genus Pseudoamauropsis from Antarctic region. Zoological Journal 86, 16–29. [In Russian]Google Scholar
Filatov, N., Tolstikov, A. and Zdorovennov, R. (2007) Features of variability in hydrophysical processes and fields. In Filatov, N. and Terzhevik, A. (eds) The White Sea and their watershed under influences of climate and anthropogenic impact. Petrozavodsk: Karelian Research Center RAS, pp. 189–257. [In Russian]Google Scholar
Gerasimova, A.V. and Maximovich, N.V. (2013) Age–size structure of common bivalve mollusc populations in the White Sea: the causes of instability. Hydrobiologia 706, 119–137.CrossRefGoogle Scholar
Gillmor, R.B. (1980) Intertidal growth in suspension-feeding bivalves. PhD thesis. University of Maine, Maine, USA.Google Scholar
Golikov, A.N. (1987) Class Gastropoda. In Starobogatov, Y.I. and Naumov, A.D. (eds) Mollusks of the White Sea. Leningrad: Nauka, pp. 41–204. [In Russian]Google Scholar
Hamilton, L.C., Brown, B.C. and Rasmussen, R.O. (2003) West Greenland's cod-to-shrimp transition: local dimensions of climatic change. Arctic 56, 271–282.CrossRefGoogle Scholar
Helmuth, B., Mieszkowska, N., Moore, P. and Hawkins, S.J. (2006) Living on the edge of two changing worlds: forecasting the responses of rocky intertidal ecosystems to climate change. Annual Review of Ecology, Evolution, and Systematics 37, 373–404.CrossRefGoogle Scholar
Honkoop, P.J.C. and Van der Meer, J. (1997) Reproductive output of Macoma balthica populations in relation to winter-temperature and intertidal-height mediated changes of body mass. Marine Ecology Progress Series 149, 155–162.CrossRefGoogle Scholar
Honkoop, P.J.C., Van der Meer, J., Beukema, J.J. and Kwast, D. (1998) Does temperature-influenced egg production predict the recruitment in the bivalve Macoma balthica? Marine Ecology Progress Series 164, 229–235.CrossRefGoogle Scholar
Hulscher, J.B. (1982) The oystercatcher Haematopus ostralegus as a predator of the bivalve Macoma balthica in the Dutch Wadden Sea. Ardea 70, 89–152.Google Scholar
Hummel, H. (1985) Food intake of Macoma balthica (Mollusca) in relation to seasonal changes in its potential food on a tidal flat in the Dutch Wadden Sea. Netherlands Journal of Sea Research 19, 52–76.CrossRefGoogle Scholar
Ivanova, T.S., Ivanov, M.V., Golovin, P.V., Polyakova, N.V. and Lajus, D.L. (2016) The White Sea threespine stickleback population: spawning habitats, mortality, and abundance. Evolutionary Ecology Research 17, 301–315.Google Scholar
Jueterbock, A., Tyberghein, L., Verbruggen, H., Coyer, J.A., Olsen, J.L. and Hoarau, G. (2013) Climate change impact on seaweed meadow distribution in the North Atlantic rocky intertidal. Ecology and Evolution 3, 1356–1373.CrossRefGoogle ScholarPubMed
Kabat, A.R. (1990) Predatory ecology of naticid gastropods with a review of shell boring predation. Malacologia 32, 155–193.Google Scholar
Khaitov, V. (2013) Life in an unstable house: community dynamics in changing mussel beds. Hydrobiologia 706, 139–158.CrossRefGoogle Scholar
Khaitov, V.M. and Lentsman, N.V. (2016) The cycle of mussels: long-term dynamics of mussel beds on intertidal soft bottoms at the White Sea. Hydrobiologia 781, 161–180.CrossRefGoogle Scholar
Khalaman, V.V. (2013) Regular and irregular events in fouling communities in the White Sea. Hydrobiologia 706, 205–219.CrossRefGoogle Scholar
Khalaman, V.V. and Naumov, A.D. (2009) Long-term dynamics of common species of polychaetes in fouling communities of the White Sea. Russian Journal of Marine Biology 35, 463–473.CrossRefGoogle Scholar
Koryakin, A.S. (2012) Sea birds monitoring in Kandalaksha Bay of the White Sea (1967–2010 years). Zoological Journal 91, 800–808. [In Russian]Google Scholar
Kuznetsov, V.V. (1960) The White Sea and biological peculiarities of its flora and fauna. Moscow-Leningrad: Academy of Sciences Publishers. [In Russian]Google Scholar
Legendre, P. and Legendre, L.F. (2012) Numerical ecology. Amsterdam: Elsevier.Google Scholar
Luttikhuizen, P.C., Drent, J., Peijnenburg, K., Van Der Veer, H.W. and Johannesson, K. (2012) Genetic architecture in a marine hybrid zone: comparing outlier detection and genomic clines analysis in the bivalve Macoma balthica . Molecular Ecology 21, 3048–3061.CrossRefGoogle Scholar
Luttikhuizen, P.C., Drent, J., Van Delden, W. and Piersma, T. (2003) Spatially structured genetic variation in a broadcast spawning bivalve: quantitative vs molecular traits. Journal of Evolutionary Biology 16, 260–272.CrossRefGoogle Scholar
MacKenzie, B.R., Payne, M.R., Boje, J., Høyer, J.L. and Siegstad, H. (2014) A cascade of warming impacts brings bluefin tuna to Greenland waters. Global Change Biology 20, 2484–2491.CrossRefGoogle ScholarPubMed
Malham, S.K., Hutchinson, T.H. and Longshaw, M. (2012) A review of the biology of European cockles (Cerastoderma spp.). Journal of the Marine Biological Association of the United Kingdom 92, 1563–1577.CrossRefGoogle Scholar
Marfenin, N.N., Bolshakov, F. and Mardashova, M. (2013) Fluctuations in settlement and survival of a barnacle Semibalanus balanoides in the White Sea intertidal. Hydrobiologia 706, 51–68.CrossRefGoogle Scholar
Marshall, G.J., Vignols, R.M. and Rees, W.G. (2016) Climate change in the Kola Peninsula, Arctic Russia, during the last 50 years from meteorological observations. Journal of Climate 29, 6823–6840.CrossRefGoogle Scholar
Maximovich, N.V. (1985) Peculiarities of ecology and reproduction cycle of Macoma balthica L. in the Chupa inlet. In Khlebovich, V.V. and Skarlato, O.A. (eds) Biocoenosis of Chupa Bay at the White Sea and its seasonal dynamics. The investigations of marine fauna. Leningrad: Nauka Publishers, pp. 230–243. [In Russian]Google Scholar
Maximovich, N.V., Gerasimova, A.V. and Kunina, T.A. (1991) Dynamics of structural characteristics in littoral beds of Macoma balthica L. in the Chupa Inlet (the White Sea). Vestnik Leningradskogo Universiteta, Series 3 Biology 2, 23–31. [In Russian]Google Scholar
Maximovich, N.V., Gerasimova, A.V. and Kunina, T.A. (1992) Production of Macoma balthica population in the Chupa Bay (the White Sea). I. Linear growth. Vestnik Leningradskogo Universiteta, Series 3 Biology 4, 12–19. [In Russian]Google Scholar
Mokievskiy, V.O., Popovkina, A.B., Poyarkov, N.D., Tzetlin, A.B., Zhadan, A.E. and Isachenko, A.Yu (2012) Foraging of common eider (Somateria molissima) wintering in Velikaya Salma strait (Kandalaksha Bay, the White Sea). Zoological Journal 91, 881–896. [In Russian]Google Scholar
Naumov, A.D. (2013) Long-term fluctuations of soft-bottom intertidal community structure affected by ice cover at two small sea bights in the Chupa Inlet (Kandalaksha Bay) of the White Sea. Hydrobiologia 706, 159–173.CrossRefGoogle Scholar
Naumov, A.D., Savchenko, O.N., Aristov, D.A. and Biyagov, K.L. (2014) Twenty-seven-years-long dynamics of biomass in fourteen benthic species from two sites at the White Sea intertidal. In Naumov, A.D. (ed.) 49 European Marine Biology Symposium, St-Petersburg. Abstracts. St-Petersburg: ZIN RAS, p. 54.Google Scholar
Nehls, G., Hertzler, I. and Scheiffarth, G. (1997) Stable mussel Mytilus edulis beds in the Wadden Sea – they're just for the birds. Helgoland Marine Research 51, 361–372.Google Scholar
Newell, C.R. and Hidu, H. (1982) The effects of sediment type on growth rate and shell allometry in the soft shelled clam Mya arenaria L. Journal of Experimental Marine Biology and Ecology 65, 285–295.CrossRefGoogle Scholar
Nikula, R., Strelkov, P. and Väinölä, R. (2007) Diversity and Trans-Arctic invasion history of mitochondrial lineages in the North Atlantic Macoma balthica complex (Bivalvia: Tellinidae). Evolution 61, 928–941.CrossRefGoogle ScholarPubMed
Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Szoecs, E. and Wagner, H. (2016) vegan: community ecology package. https://CRAN.R-project.org/package=vegan.Google Scholar
Olafsson, E.B. (1986) Density dependence in suspension-feeding and deposit-feeding populations of the bivalve Macoma balthica: a field experiment. Journal of Animal Ecology 55, 517–526.CrossRefGoogle Scholar
Parkinson, C.L. (2014) Spatially mapped reductions in the length of the Arctic sea ice season. Geophysical Research Letters 41, 4316–4322.CrossRefGoogle ScholarPubMed
Pertsov, N.A. (1963) Some new data on feeding of birds during breeding season at Northern Archipelago, Kandalaksha State Reserve. Proceedings of Kandalaksha Reserve 4, 29–34. [In Russian]Google Scholar
Philippart, C.J., van Aken, H.M., Beukema, J.J., Bos, O.G., Cadée, G.C. and Dekker, R. (2003) Climate-related changes in recruitment of the bivalve Macoma balthica . Limnology and Oceanography 48, 2171–2185.CrossRefGoogle Scholar
Pinheiro, J. and Bates, D. (2006) Mixed-effects models in S and S-PLUS. New York, NY: Springer Science & Business Media.Google Scholar
R Core Team (2016) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Sarà, G., Palmeri, V., Montalto, V., Rinaldi, A. and Widdows, J. (2013) Parameterisation of bivalve functional traits for mechanistic eco-physiological dynamic energy budget (DEB) models. Marine Ecology Progress Series 480, 99–117.CrossRefGoogle Scholar
Sartori, A.F. (2016) Limecola balthica (Linnaeus, 1758). In MolluscaBase. Accessed through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=880017 on 2017-01-19.Google Scholar
Seed, R. (1968) Factors influencing shell shape in the mussel Mytilus edulis . Journal of the Marine Biological Association of the United Kingdom 48, 561–584.CrossRefGoogle Scholar
Seitz, R.D. and Lipcius, R.N. (2001) Variation in top-down and bottom-up control of marine bivalves at differing spatial scales. ICES Journal of Marine Science: Journal du Conseil 58, 689–699.CrossRefGoogle Scholar
Sejr, M.K., Blicher, M.E. and Rysgaard, S. (2009) Sea ice cover affects inter-annual and geographic variation in growth of the Arctic cockle Clinocardium ciliatum (Bivalvia) in Greenland. Marine Ecology Progress Series 389, 149–158.CrossRefGoogle Scholar
Selin, N.I. (2008) Feeding behavior, ration and size structure of a population of the predatory gastropod Cryptonatica janthostoma in Vostok Bay, Sea of Japan. Russian Journal of Marine Biology 34, 186–190.CrossRefGoogle Scholar
Semenova, N.L. (1974) Distribution of bivalve mollusk Macoma balthica (L.) in some inlets of Kandalaksha Bay at the White Sea. Proceedings of the White Sea Biological Station of Moscow State University 4, 87–102.Google Scholar
Sergievsky, S.O., Granovitch, A.I. and Sokolova, I.M. (1997) Long-term studies of Littorina obtusata and Littorina saxatilis populations in the White Sea. Oceanolica Acta 20, 259–265.Google Scholar
Strasser, M., Dekker, R., Essink, K., Günther, C.-P., Jaklin, S., Kröncke, I., Madsen, P.B., Michaelis, H. and Vedel, G. (2003) How predictable is high bivalve recruitment in the Wadden Sea after a severe winter? Journal of Sea Research 49, 47–57.CrossRefGoogle Scholar
Strelkov, P., Nikula, R. and Väinölä, R. (2007) Macoma balthica in the White and Barents Seas: properties of a widespread marine hybrid swarm (Mollusca: Bivalvia). Molecular Ecology 16, 4110–4127.CrossRefGoogle ScholarPubMed
Sukhotin, A. and Berger, V. (2013) Long-term monitoring studies as a powerful tool in marine ecosystem research. Hydrobiologia 706, 1–9.CrossRefGoogle Scholar
Sveshnikov, V.A. (1963) Biocenotic relations and environmental conditions of some food invertebrates of intertidal infauna in the Kandalaksha Bay of the White Sea. Proceedings of Kandalaksha Reserve 4, 114–134. [In Russian].Google Scholar
Tolmacheva, E.L. (2013) Ecology of common species of suborder Lari of the White Sea. PhD thesis. Petrozavodsk State University, Petrozavodsk, Russia.Google Scholar
Usov, N., Kutcheva, I., Primakov, I. and Martynova, D. (2013) Every species is good in its season: do the shifts in the annual temperature dynamics affect the phenology of the zooplankton species in the White Sea? Hydrobiologia 706, 11–33.CrossRefGoogle Scholar
Varfolomeeva, M. and Naumov, A. (2013) Long-term temporal and spatial variation of macrobenthos in the intertidal soft-bottom flats of two small bights (Chupa Inlet, Kandalaksha Bay, White Sea). Hydrobiologia 706, 175–189.CrossRefGoogle Scholar
Vignali, R. and Galleni, L. (1986) Naticid predation on soft bottom bivalves: a study on a beach shell assemblage. Oebalia 13, 157–178.Google Scholar
Visser, G.H., Dekinga, A., Achterkamp, B. and Piersma, T. (2000) Ingested water equilibrates isotopically with the body water pool of a shorebird with unrivaled water fluxes. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 279, R1795–R1804.CrossRefGoogle ScholarPubMed
von Bertalanffy, L. (1938) A quantitative theory of organic growth (inquiries on growth laws. II). Human Biology 10, 181–213.Google Scholar
Wassmann, P., Duarte, C.M., Agusti, S. and Sejr, M.K. (2011) Footprints of climate change in the Arctic marine ecosystem. Global Change Biology 17, 1235–1249.CrossRefGoogle Scholar
Wethey, D.S., Woodin, S.A., Hilbish, T.J., Jones, S.J., Lima, F.P. and Brannock, P.M. (2011) Response of intertidal populations to climate: effects of extreme events vs long term change. Journal of Experimental Marine Biology and Ecology 400, 132–144.CrossRefGoogle Scholar
Wiltse, W.I. (1980) Effects of Polinices duplicatus (Gastropoda: Naticidae) on infaunal community structure at Barnstable Harbor, Massachusetts, USA. Marine Biology 56, 301–310.CrossRefGoogle Scholar
Wood, S. (2006) Generalized additive models: an introduction with R. Boca Raton, FL: CRC Press.CrossRefGoogle Scholar
Zubakha, M.A., Poloskin, A.V. and Goltsev, N.A. (2000) Peculiarities in reproduction and recruitment of Macoma balthica L. population at the White Sea. Vestnik Sankt-Peterburgskogo Universiteta. Series 3: Biology 2, 108–115. [In Russian].Google Scholar
Zuur, A., Ieno, E.N., Walker, N., Saveliev, A.A. and Smith, G.M. (2009) Mixed effects models and extensions in ecology with R. New York, NY: Springer Science & Business Media.CrossRefGoogle Scholar
Zwarts, L. and Blomert, A.-M. (1992) Why knot Calidris canutus take medium-sized Macoma balthica when six prey species are available. Marine Ecology Progress Series 83, 113–128.CrossRefGoogle Scholar
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