Хищники регулируют структуру смешанных поселений Mytilus edulis L. и M. trossulus Gould на мелководьях Белого моря

В.М. Хайтов, А.Ю. Макарычева, Р.Б. Нематова и А.И. Евдокимова

Труды Зоологического института РАН, 2023, 327(1): 8–24 · https://doi.org/10.31610/trudyzin/2023.327.1.8

Резюме

Криптические виды мидий Mytilus edulis (Me) и M. trossulus (Mt) образуют смешанные поселения на мелководье Белого моря. Соотношение Mt и Me в локальных поселениях варьирует в широких пределах, но факторы, регулирующие таксономический состав смешанных популяций, изучены слабо. Настоящее исследование посвящено оценке влияния морских звезд (Asterias rubens), как ключевого хищника, на соотношение Mt-Me в естественных местообитаниях. Для исследования мы провели серию полевых экспериментов, в которых моллюсков двух видов помещали на керамические пластины в разных соотношениях Mt и Me. Пластины были помещены на дно в участках, где наблюдалось скопление звезд. После экспозиции мы оценили для мидий вероятность быть съеденными. Мы построили линейную модель, включающую несколько предикторов, потенциально влияющих на вероятность быть съеденным (биомасса морских звезд, размер мидии, вид мидии, численность мидий на пластинах, соотношение Mt-Me на экспериментальных блоках и численность особей того же вида). Анализ показал, что вероятность быть съеденным возрастает с увеличением биомассы морских звезд. Вероятность быть съеденной была выше для Mt по сравнению с Me. Это указывает на то, что Mt является более предпочтительной добычей. Также были выявлены отрицательные корреляции между вероятностью быть съеденным и размером раковины, количеством конспецификов и численностью мидий. Значимой зависимости от соотношения Mt-Me обнаружено не было. Кроме того, мы провели сборы проб в естественных биотопах, в которых было отмечено массовое нашествие морских звезд. Было показано значительное снижение доли Mt в мидиевых друзах после атаки хищников, звезды выедали Mt. Эти результаты показывают, что хищники могут вносить вклад в регулирование состава смешанных поселений Mt-Me в Белом море.

Ключевые слова

выбор жертвы хищником, межвидовые взаимоотношения, Asterias, Mytilus edulis, Mytilus trossulus

Поступила в редакцию 4 декабря 2022 г. · Принята в печать 14 февраля 2023 г. · Опубликована 25 марта 2023 г.

Литература

Agüera A., Jansen J.M. and Smaal A.C. 2020. Blue mussel (Mytilus edulis L.) association with conspecifics affects mussel size selection by the common seastar (Asterias rubens L.). Journal of Sea Research, 164: 101935. https://doi.org/10.1016/j.seares.2020.101935

Barton K. 2020. MuM In: Multi-Model Inference. https://CRAN.R-project.org/package=MuMIn

Bates D., Mächler M., Bolker B. and Walker S. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1): 1–48. https://doi.org/10.18637/jss.v067.i01

Beaumont A.R., Hawkins M.P., Doig F.L., Davies I.M. and Snow M. 2008. Three species of Mytilus and their hybrids identified in a Scottish Loch: natives, relicts and invaders? Journal of Experimental Marine Biology and Ecology, 367(2): 100–110. https://doi.org/10.1016/j.jembe.2008.08.021

Comesaña A.S., Toro J.E., Innes D.J. and Thompson R.J. 1999. A molecular approach to the ecology of a mussel (Mytilus edulis – M. trossulus) hybrid zone on the east coast of Newfoundland, Canada. Marine Biology, 133(2): 213–221. https://doi.org/10.1007/s002270050460

Commito J.A., Dow W.E. and Grupe B.M. 2006. Hierarchical spatial structure in soft-bottom mussel beds. Journal of Experimental Marine Biology and Ecology, 330(1): 27–37. https://doi.org/10.1016/j.jembe.2005.12.015

Dare P.J. 1982. Notes on the swarming behaviour and population density of Asterias rubens L. (Echinodermata: Asteroidea) feeding on the mussel, Mytilus edulis L. ICES Journal of Marine Science, 40(2): 112–118. https://doi.org/10.1093/icesjms/40.2.112

Dias P.J., Dordor A., Tulett D., Piertney S., Davies I.M. and Snow M. 2009. Survey of mussel (Mytilus) species at scottish shellfish farms. Aquaculture Research, 40(15): 1715–1722. https://doi.org/10.1111/j.1365-2109.2009.02274.x

Dickey J.W.E., Cuthbert R.N., Morón Lugo S.C., Casties I., Dick J.T.A., Steffen G.T. and Briski E. 2021. The stars are out: Predicting the effect of seawater freshening on the ecological impact of a sea star keystone predator. Ecological Indicators, 132: 108293. https://doi.org/10.1016/j.ecolind.2021.108293

Dolmer P. 1998. The interactions between bed structure of Mytilus edulis L. and the predator Asterias rubens L. Journal of Experimental Marine Biology and Ecology, 228(1): 137–150. https://doi.org/10.1016/S0022-0981(98)00024-0

Galstoff P. and Loosanoff V. 1939. Natural history and method of controlling the starfish (Asterias forbesi). Bulletin of the United States Bureau of Fisheries, 49: 73–132.

Garcı́a A.A. 2015. The role of the starfish (Asterias rubens L.) predation in blue mussel (Mytilus edulis L.) seedbed stability. PhD thesis. Wageningen University. Wageningen, 170 p.

Gardner J.P. and Thompson R.J. 2009. Influence of genotype and geography on shell shape and morphometric trait variation among north atlantic blue mussel (Mytilus spp.) populations. Biological Journal of the Linnean Society, 96(4): 875–897. https://doi.org/10.1111/j.1095-8312.2008.01166.x

Holling C.S. 1959. The components of predation as revealed by a study of small-mammal predation of the european Pine Sawfly. The Canadian Entomologist, 91(5): 293–320. https://doi.org/10.4039/Ent91293-5

Hothorn T., Bretz F. and Westfall P. 2008. Simultaneous inference in general parametric models. Biometrical Journal, 50(3): 346–363. https://doi.org/10.1002/bimj.200810425

Hummel C., Honkoop P. and Van der Meer J. 2011. Small is profitable: No support for the optimal foraging theory in sea stars Asterias rubens foraging on the blue edible mussel Mytilus edulis. Estuarine, Coastal and Shelf Science, 94(1): 89–92. https://doi.org/10.1016/j.ecss.2011.05.028

Innes D. and Bates J. 1999. Morphological variation of Mytilus edulis and Mytilus trossulus in eastern Newfoundland. Marine Biology, 133(4): 691–699. https://doi.org/10.1007/s002270050510

Kamermans P., Blankendaal M. and Perdon J. 2009. Predation of shore crabs (Carcinus maenas (L.)) and starfish (Asterias rubens L.) on blue mussel (Mytilus edulis L.) seed from wild sources and spat collectors. Aquaculture, 290(3–4): 256–262. https://doi.org/10.1016/j.aquaculture.2009.02.031

Katolikova M., Khaitov V., Väinölä R., Gantsevich M. and Strelkov P. 2016. Genetic, ecological and morphological distinctness of the blue mussels Mytilus trossulus Gould and M. edulis L. in the White Sea. PLoS ONE, 11(4). https://doi.org/10.1371/journal.pone.0152963

Kautsky N., Johannesson K. and Tedengren M. 1990. Genotypic and phenotypic differences between Baltic and North Sea populations of Mytilus edulis evaluated through reciprocal transplantations. I. Growth and morphology. Marine Ecology Progress Series, 59: 203–210. https://doi.org/10.3354/meps059203

Khaitov V., Makarycheva A., Gantsevich M., Lentsman N., Skazina M., Gagarina A., Katolikova M. and Strelkov P. 2018. Discriminating eaters: Sea stars Asterias rubens L. feed preferably on Mytilus trossulus Gould in mixed stocks of Mytilus trossulus and Mytilus edulis L. Biological Bulletin, 234(2): 85–95. https://doi.org/10.1086/697944

Khaitov V., Marchenko J., Katolikova M., Väinölä R., Kingston S.E., Carlon D.B., Gantsevich M. and Strelkov P. 2021. Species identification based on a semi-diagnostic marker: Evaluation of a simple conchological test for distinguishing blue mussels Mytilus edulis L. and M. trossulus Gould. PLoS ONE, 16(7): 1–27. https://doi.org/10.1371/journal.pone.0249587

Kijewski T., Zbawicka M., Strand J., Kautsky H., Kotta J., Rätsep M. and Wenne R. 2019. Random forest assessment of correlation between environmental factors and genetic differentiation of populations: Case of marine mussels Mytilus. Oceanologia, 61(1): 131–142. https://doi.org/10.1016/j.oceano.2018.08.002

Liu G., Stapleton E., Innes D. and Thompson R. 2011. Aggregational behavior of the blue mussels Mytilus edulis and Mytilus trossulus: A potential pre-zygotic reproductive isolation mechanism. Marine Ecology, 32(4): 480–487. https://doi.org/10.1111/j.1439-0485.2011.00446.x

Lowen J.B., Innes D.J. and Thompson R.J. 2013. Predator-induced defenses differ between sympatric Mytilus edulis and M. trossulus. Marine Ecology Progress Series, 475: 135–143. https://doi.org/10.3354/meps10106

McDonald J., Seed R. and Koehn R. 1991. Allozymes and morphometric characters of three species of Mytilus in the Northern and Southern Hemispheres. Marine Biology, 111(3): 323–333. https://doi.org/10.1007/BF01319403

Michalek K., Vendrami D.L., Bekaert M., Green D.H., Last K.S., Telesca L., Wilding T.A. and Hoffman J.I. 2021. Mytilus trossulus introgression and consequences for shell traits in longline cultivated mussels. Evolutionary applications, 14(7): 1830–1843. https://doi.org/10.1111/eva.13245

Michalek K., Ventura A. and Sanders T. 2016. Mytilus hybridisation and impact on aquaculture: A minireview. Marine Genomics, 27: 3–7. https://doi.org/10.1016/j.margen.2016.04.008

Nakagawa S. and Schielzeth H. 2013. A general and simple method for obtaining R² from generalized linear mixed-effects models. Methods in Ecology and Evolution, 4(2): 133–142. https://doi.org/10.1111/j.2041-210x.2012.00261.x

Naumov A.D. 2011. Anomalous ejection of sea stars in the Dvinsky Bay in spring 1990: according to documents from the archives of the White Sea Biological Station of the Zoological Institute of the Russian Academy of Sciences. Zoological Institute of the Russian Academy of Sciences, Saint Petertsburg, 411 p. [In Russian].

O’Neill S.M., Sutterlin A. and Aggett D. 1983. The effects of size-selective feeding by starfish (Asterias vulgaris) on the production of mussels (Mytilus edulis) cultured on nets. Aquaculture, 35: 211–220. https://doi.org/10.1016/0044-8486(83)90092-3

Okamura B. 1986. Group living and the effects of spatial position in aggregations of Mytilus edulis. Oecologia, 69(3): 341–347. https://doi.org/10.1007/BF00377054

Pedersen E.J., Miller D.L., Simpson G.L. and Ross N. 2019. Hierarchical generalized additive models in ecology: An introduction with mgcv. PeerJ, 7: e6876. https://doi.org/10.7717/peerj.6876

Penney R.W., Hart M.J. and Templeman N.D. 2008. Genotype-dependent variability in somatic tissue and shell weights and its effect on meat yield in mixed species [Mytilus edulis L., M. trossulus (Gould) and their hybrids] cultured mussel populations. Journal of Shellfish Research, 27(4): 827–834. https://doi.org/10.2983/0730-8000(2008)27[827:GVISTA]2.0.CO;2

Popovic I. and Riginos C. 2020. Comparative genomics reveals divergent thermal selection in warm- and cold-tolerant marine mussels. Molecular Ecology, 29(3): 519–535. https://doi.org/10.1111/mec.15339

R Core Team. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

Reimer O. and Tedengren M. 1997. Predator-induced changes in byssal attachment, aggregation and migration in the blue mussel, Mytilus edulis. Marine and Freshwater Behaviour and Phy, 30(4): 251–266. https://doi.org/10.1080/10236249709379029

Ridgway G. and Nævdal G. 2004. Genotypes of Mytilus from waters of different salinity around Bergen, Norway. Helgoland Marine Research, 58(2): 104. https://doi.org/10.1007/s10152-004-0175-5

Riginos C. and Cunningham C.W. 2005. Invited review: local adaptation and species segregation in two mussel (Mytilus edulis x Mytilus trossulus) hybrid zones. Molecular ecology, 14(2): 381–400. https://doi.org/10.1111/j.1365-294X.2004.02379.x

Sarantchova O.L. 2001. Research into tolerance for the environment salinity in sea starfish Asterias rubens L. from populations of the White Sea and Barentz Sea. Journal of experimental marine biology and ecology, 264(1): 15–28. https://doi.org/10.1016/S0022-0981(01)00298-2

Seed R. 1969. The ecology of Mytilus edulis l. (Lamellibranchiata) on exposed rocky shores. II. Growth and mortality. Oecologia, 3: 317–350. https://doi.org/10.1007/BF00390381

Smith T.M. and Smith R.L. 2012. Predation. In: B. Wilbur, ed. Elements of ecology. 8th Edition, Pearson Benjamin Cummings, San Francisco: 273–297.

Stuckas H., Knöbel L., Schade H., Breusing C., Hinrichsen H.H., Bartel M., Langguth K. and Melzner F. 2017. Combining hydrodynamic modelling with genetics: can passive larval drift shape the genetic structure of Baltic Mytilus populations? Molecular Ecology, 26(10): 2765–2782. https://doi.org/10.1111/mec.14075

Tam J.C. and Scrosati R.A. 2014. Distribution of cryptic mussel species (Mytilus edulis and M. trossulus) along wave exposure gradients on northwest Atlantic rocky shores. Marine Biology Research, 10(1): 51–60. https://doi.org/10.1080/17451000.2013.793809

Telesca L., Michalek K., Sanders T., Peck L.S., Thyrring J. and Harper E.M. 2018. Blue mussel shell shape plasticity and natural environments: A quantitative approach. Scientific Reports, 8(1): 1–15. https://doi.org/10.1038/s41598-018-20122-9

Väinölä R. and Strelkov P. 2011. Mytilus trossulus in Northern Europe. Marine Biology, 158(4): 817–833. https://doi.org/10.1007/s00227-010-1609-z

Wenne R., Zbawicka M., Bach L., Strelkov P., Gantsevich M., Kukliński P., Kijewski T., McDonald J.H., Sundsaasen K.K., Árnyasi M., Lien S., Kaasik A., Herkul K. and Kotta J. 2020. Trans-atlantic distribution and introgression as inferred from single nucleotide polymorphism: Mussels Mytilus and environmental factors. Genes, 11(5): 530. https://doi.org/10.3390/genes11050530

Wickham H. and Stryjewski L. 2011. 40 years of boxplots. Am. Statistician: 2011, 17 p.

Witman J.D., Genovese S.J., Bruno J.F., McLaughlin J.W. and Pavlin B.I. 2003. Massive prey recruitment and the control of rocky subtidal communities on large spatial scales. Ecological Monographs, 73(3): 441–462. https://doi.org/10.1890/01-4073

Wood S.N. 2006. Generalized additive models: An introduction with R. Chapman and Hall/CRC, New York, 416 p. https://doi.org/10.1201/9781420010404

Zimmer R.K., Ferrier G.A., Kim S.J., Ogorzalek Loo R.R., Zimmer C.A. and Loo J.A. 2017. Keystone predation and molecules of keystone significance. Ecology, 98(6): 1710–1721. https://doi.org/10.1002/ecy.1849

Zimmer R.K., Ferrier G.A. and Zimmer C.A. 2016. KEYSTONEin: A glycoprotein cue drives predation on mussels and structures rocky intertidal communities. Marine Ecology Progress Series, 560: 199–206. https://doi.org/10.3354/meps11939

Zolotarev V. and Shurova N. 1997. Relations of prismatic and nacreous layers in the shells of the mussel Mytilus trossulus. Russian Journal of Marine Biology, 23(1): 26–31.