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Comparative efficiency of Mytilus edulis as engineering species for shallow-water fouling communities on artificial structures in the White Sea

Published online by Cambridge University Press:  23 June 2021

Vyacheslav V. Khalaman Open the ORCID record for Vyacheslav V. Khalaman [Opens in a new window] ,
Alexander Yu. Komendantov ,
Nina S. Golubovskaya  and
Polina A. Manoylina
Vyacheslav V. Khalaman*
Affiliation:
Zoological Institute RAS, Saint-Petersburg199034, Russia
Alexander Yu. Komendantov
Affiliation:
Zoological Institute RAS, Saint-Petersburg199034, Russia
Nina S. Golubovskaya
Affiliation:
Murmansk State Technical University, Murmansk183010, Russia
Polina A. Manoylina
Affiliation:
Saint-Petersburg State University, Saint-Petersburg199034, Russia
*
Author for correspondence: Vyacheslav V. Khalaman, E-mail: VKhalaman@gmail.com
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Abstract

Currently, there is little comparative data on ‘efficiency’ of different engineering species, i.e. species richness, density and biomass of the associated organisms that have been supported by engineering species. The use of fouling communities makes it possible to compare the efficiency of different engineering species under the same conditions, which is necessary to obtain correct estimates and difficult to do when studying natural bottom communities. In this study, we have analysed the fouling communities in four different mussel culture farms in the White Sea to test the following hypotheses. (1) Different engineering species (mussel Mytilus edulis, solitary ascidian Styela rustica, sponge Halichondria panicea) have different assemblages of the associated vagile fauna. (2) Mytilus edulis is the most efficient engineering species, i.e. species richness, species diversity, density and biomass of the associated vagile fauna is higher in the mussel communities than in those dominated by Styela rustica or Halichondria panicea. The first hypothesis was confirmed, while the second was rejected. In all the culture farms studied, all parameters of the mussel-associated vagile fauna were not higher and in most cases were even lower than those of the fauna associated with ascidians or sponges. The reason for this seems to be the very dense packing of mussels in patches. Therefore, Mytilus edulis is not the most efficient engineering species among fouling organisms, at least in the conditions of the subarctic White Sea. The data obtained are particularly important in view of the ever-increasing volume of anthropogenic substrate and fouling communities in coastal marine ecosystems.

Keywords

Associated faunaecosystem engineerfouling communityMytilus edulisStyela rusticaWhite Sea
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 101 , Issue 3 , May 2021 , pp. 511 - 525
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Abdo, DA (2007) Endofauna differences between two temperate marine sponges (Demospongiae; Haplosclerida; Chalinidae) from southwest Australia. Marine Biology 152, 845–854.CrossRefGoogle Scholar
Adami, ML, Tablado, A and López Gappa, J (2004) Spatial and temporal variability in intertidal assemblages dominated by the mussel Brachidontes rodriguezii (d'Orbigny, 1846). Hydrobiologia 520, 49–59.CrossRefGoogle Scholar
Airoldi, L, Turon, X, Perkol-Finkel, Sh and Rius, M (2015) Corridors for aliens but not for natives: effects of marine urban sprawl at a regional scale. Diversity and Distributions 21, 755–768.CrossRefGoogle Scholar
Albano, MJ and Obenat, SM (2009) Assemblage of benthic macrofauna in the aggregates of the tubiculous worm Phyllochaetopterus socialis in the Mar del Plata harbour, Argentina. Journal of the Marine Biological Association of the United Kingdom 89, 1099–1108.CrossRefGoogle Scholar
Anderson, MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.Google Scholar
Anderson, MJ (2005) Permutational Multivariate Analysis of Variance. Auckland: Department of Statistics, University of Auckland.Google Scholar
Arribas, LP, Donnarumma, L, Palomo, MG and Scrosati, RA (2014) Intertidal mussels as ecosystem engineers: their associated invertebrate biodiversity under contrasting wave exposures. Marine Biodiversity 44, 203–211.CrossRefGoogle Scholar
Berger, V, Dahle, S, Galaktionov, K, Kosobokova, X, Naumov, A, Rat'kova, T, Savinov, V and Savinova, T (2001) White Sea: Ecology and Environment. St. Petersburg – Tromsø: Derzavets Publisher.Google Scholar
Borthagaray, AI and Carranza, A (2007). Mussels as ecosystem engineers: their contribution to species richness in a rocky littoral community. Acta Oecologica 31, 243–250.CrossRefGoogle Scholar
Bouma, TJ, Olenin, S, Reise, K and Ysebaert, T (2009) Ecosystem engineering and biodiversity in coastal sediments: posing hypotheses. Helgoland Marine Research 63, 95–106.CrossRefGoogle Scholar
Buschbaum, C, Dittmann, S, Hong, J-S, Hwang, I-S, Strasser, M, Thiel, M, Valdivia, N, Yoon, S-P and Reise, K (2009) Mytilid mussels: global habitat engineers in coastal sediments. Helgoland Marine Research 63, 47–58.CrossRefGoogle Scholar
Büttger, H, Asmus, H, Asmus, R, Buschbaum, C, Dittmann, S and Nehls, G (2008) Community dynamics of intertidal soft-bottom mussel beds over two decades. Helgoland Marine Research 62, 23–36.CrossRefGoogle Scholar
Carvalho, S, Curdia, J, Pereira, F, Guerra-Garcia, JM, Santos, MN and Cunha, MR (2014) Biodiversity patterns of epifaunal assemblages associated with the gorgonians Eunicella gazella and Leptogorgia lusitanica in response to host, space and time. Journal of Sea Research 85, 37–47.CrossRefGoogle Scholar
Castilla, JC, Lagos, NA and Cerda, M (2004) Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a mid-intertidal rocky shore. Marine Ecology Progress Series 268, 119–130.CrossRefGoogle Scholar
Chapman, MG, People, J and Blockley, D (2005) Intertidal assemblages associated with natural corallina turf and invasive mussel beds. Biodiversity and Conservation 14, 1761–1776.CrossRefGoogle Scholar
Çinar, ME, Katagan, T, Ergen, Z and Sezgin, M (2002) Zoobenthos-inhabiting Sarcotragus muscarum (Porifera: Demospongiae) from the Aegean Sea. Hydrobiologia 482, 107–117.CrossRefGoogle Scholar
Commito, JA and Rusignuolo, BR (2000) Structural complexity in mussel beds: the fractal geometry of surface topography. Journal of Experimental Marine Biology and Ecology 225, 133–152.CrossRefGoogle Scholar
Costa, MFB, Mansur, KFR and Leite, FPP (2015) Temporal variation of the gammaridean fauna (Crustacea, Amphipoda) associated with the sponge Mycale angulosa (Porifera, Demospongiae) in south-eastern Brazil. Nauplius 23, 79–87.CrossRefGoogle Scholar
Costello, MJ and Myers, AA (1987) Amphipod fauna of the sponges Halichondria panicea and Hymeniacidon perleve in Lough Hyne, Ireland. Marine Ecology Progress Series 4, 115–121.CrossRefGoogle Scholar
Crain, CM and Bertness, MD (2006) Ecosystem engineering across environmental gradients: implications for conservation and management. BioScience 56, 211–218.CrossRefGoogle Scholar
Crooks, JA and Khim, HS (1999) Architectural vs biological effects of a habitat-altering, exotic mussel, Musculista senhousia. Journal of Experimental Marine Biology and Ecology 240, 53–75.CrossRefGoogle Scholar
Crowe, TP, Cusson, M, Bulleri, F, Davoult, D, Arenas, F, Aspden, R, Benedetti-Cecchi, L, Bevilacqua, S, Davidson, I, Defew, E, Fraschetti, S, Golléty, C, Griffin, JN, Herkül, K, Kotta, J, Migné, A, Molis, M, Nicol, SK, Noël, LM-LJ, Pinto, IS, Valdivia, N, Vaselli, S and Jenkins, SR (2013) Large-scale variation in combined impacts of canopy loss and disturbance on community structure and ecosystem functioning. PLoS ONE 8, e66238.CrossRefGoogle ScholarPubMed
Curdia, J, Carvalho, S, Pereira, F, Guerra-Garcia, JM, Santos, MN and Cunha, MR (2015) Diversity and abundance of invertebrate epifaunal assemblages associated with gorgonians are driven by colony attributes. Coral Reefs 34, 611–624.CrossRefGoogle Scholar
Dean, TA (1981) Structural aspects of sessile invertebrates as organizing forces in an estuarine fouling community. Journal of Experimental Marine Biology and Ecology 53, 163–180.CrossRefGoogle Scholar
Dias, IM, Curdia, J, Cunha, MR, Santos, MN and Carvalho, S (2015). Temporal variability in epifaunal assemblages associated with temperate gorgonian gardens. Marine Environmental Research 112, 140–151.CrossRefGoogle ScholarPubMed
Dittmann, S (1990). Mussel beds – amensalism or amelioration for intertidal fauna? Helgoländer Meeresuntersuchungen 44, 335–352.CrossRefGoogle Scholar
Drolet, D, Himmelman, JH and Rochette, R (2004) Use of refuges by the ophiuroid Ophiopholis aculeata: contrasting effects of substratum complexity on predation risk from two predators. Marine Ecology Progress Series 284, 173–183.CrossRefGoogle Scholar
Duarte, LFL and Nalesso, RC (1996) The sponge Zygomycale parishii (Bowerbank) and its endobiotic fauna. Estuarine, Coastal and Shelf Science 42, 139–151.CrossRefGoogle Scholar
Emrić, V (1996) Macroinvertebrate fauna associated with natural populations of Mediterranean mussel (Mytilus galloprovincialis Lamarc, 1819) in Lim channel, Istra. Annales. Series Historia Naturalis 6, 67–72.Google Scholar
Gerovasileiou, V, Chintiroglou, CC, Konstantinou, D and Voultsiadou, E (2016) Sponges as “living hotels” in Mediterranean marine caves. Scientia Marina 80, 279–289.CrossRefGoogle Scholar
Golikov, AN, Scarlato, OA, Galtsova, VV and Menshutkina, TV (1985) Ecosystems of the Chupa Inlet of the White Sea and their seasonal dynamic. Exploration of the Fauna of the Seas 31, 5–83. [In Russian.]Google Scholar
Gravina, MF, Cardone, F, Bonifazi, A, Bertrandino, MS, Chimienti, G, Longo, C, Marzano, CN, Moretti, M, Lisco, S, Moretti, V, Corriero, G and Giangrande, A (2018) Sabellaria spinulosa (Polychaeta, Annelida) reefs in the Mediterranean Sea: habitat mapping, dynamics and associated fauna for conservation management. Estuarine, Coastal and Shelf Science 200, 248–257.CrossRefGoogle Scholar
Günther, C-P (1996) Development of small Mytilus beds and its effects on resident intertidal macrofauna. Marine Ecology 17, 117–130.CrossRefGoogle Scholar
Gutiérrez, JI, Jones, CG, Strayer, DL and Iribarne, O (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101, 79–90.CrossRefGoogle Scholar
Gutiérrez, JI, Jones, CG, Byers, J and Arkema, K (2011) Physical ecosystem engineers and the functioning of estuaries and coasts. In Wolanski, E and McLusky, DS (eds), Treatise on Estuarine and Coastal Science. Functioning of Ecosystems at the Land-Ocean Interface, vol. 7. Waltham, MA: Elsevier, Academic Press, pp. 53–81.CrossRefGoogle Scholar
Ivanov, MV, Smagina, DS, Chivilev, SM and Kruglikov, OE (2013) Degradation and recovery of an Arctic benthic community under organic enrichment. Hydrobiologia 706, 191–204.CrossRefGoogle Scholar
Jones, CG, Lawton, JH and Shachak, M (1994) Organisms as ecosystem engineers. Oikos 69, 373–386.CrossRefGoogle Scholar
Jones, CG, Gutiérres, JL, Byers, JE, Crooks, JA, Lambrinos, JG and Talley, TS (2010) A framework for understanding physical ecosystem engineering by organisms. Oikos 119, 1862–1869.CrossRefGoogle Scholar
Khaitov, VM and Brovkina, JB (2014) Mechanisms used by the inhabitants of a sand flat in the White Sea to colonize aggregates of Mytilus edulis Linnaeus, 1758 (Bivalvia: Mytilidae). Russian Journal of Marine Biology 40, 295–302.CrossRefGoogle Scholar
Khaitov, VM, Artemyeva, AV, Gornykh, AE, Zhizhina, OG and Yakovis, EL (2007) The role of mussel patches in structuring of soft-bottom intertidal communities. 1. Structure of community associated with mussel patches on the White Sea littoral. Vestnik of Saint Petersburg University. Series 3. Biology. Vyp. 4, 3–12. [In Russian.]Google Scholar
Khalaman, VV (1989) The investigation of fouling community succession in the White Sea using the information index of species diversity. Proceeding of the Zoological Institute AS USSR 203, 34–45. [In Russian.]Google Scholar
Khalaman, VV (1998) Correlations of spatial distribution of organisms in fouling communities of the White Sea. Zhurnal obschey biologii 59, 58–73. [In Russian.]Google Scholar
Khalaman, VV (2001 a) Fouling communities of mussel aquaculture installations in the White Sea. Russian Journal of Marine Biology 27, 227–237.CrossRefGoogle Scholar
Khalaman, VV (2001 b) Succession of fouling communities on an artificial substrate of a mussel culture in the White Sea. Russian Journal of Marine Biology 27, 345–352.CrossRefGoogle Scholar
Khalaman, VV (2005) Long-term changes in shallow-water fouling communities of the White Sea. Russian Journal of Marine Biology 31, 344–351.CrossRefGoogle Scholar
Khalaman, VV (2013) Regular and irregular events in fouling communities in the White Sea. Hydrobiologia 706, 205–219.CrossRefGoogle Scholar
Khalaman, VV and Komendantov, AYu (2011) Structure of fouling communities formed by Halichondria panicea (Porifera: Demospongiae) in the White Sea. Russian Journal of Ecology 42, 493–501.CrossRefGoogle Scholar
Khalaman, VV and Naumov, AD (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
Khalaman, VV, Komendantov, AYu, Malavenda, SS and Mikhaylova, TA (2016) Algae vs animals in early fouling communities of the White Sea. Marine Ecology Progress Series 553, 13–32.CrossRefGoogle Scholar
Koivisto, ME and Westerbom, M (2010) Habitat structure and complexity as determinants of biodiversity in blue mussel beds on sublittoral rocky shores. Marine Biology 157, 1436–1474.CrossRefGoogle Scholar
Lee, SY, Fong, CW and Wu, RSS (2001) The effects of seagrass (Zostera japonica) canopy structure on associated fauna: a study using artificial seagrass units and sampling of natural beds. Journal of Experimental Marine Biology and Ecology 259, 23–50.CrossRefGoogle ScholarPubMed
Lezin, PA (2007) The spatial structure of the White Sea mussel (Mytilus edulis) aggregations. Zoologicheskii zhurnal 86, 163–166. [In Russian.]Google Scholar
Lezin, PA, Agat'eva, NA and Khalaman, VV (2006) A comparative study of the pumping activity of some fouling animals from the White Sea. Russian Journal of Marine Biology 32, 245–249.CrossRefGoogle Scholar
Lintas, C and Seed, R (1994) Spatial variation in the fauna associated with Mytilus edulis on a wave-exposed rocky shore. Journal of Molluscan Studies 60, 165–174.CrossRefGoogle Scholar
McCloskey, RM and Unsworth, RKF (2015) Decreasing seagrass density negatively influences associated fauna. PeerJ 3, e1053.CrossRefGoogle ScholarPubMed
McLeod, IM, Parsons, DM, Morrison, MA, Van Dijken, SG and Taylor, RB (2014) Mussel reefs on soft sediments: a severely reduced but important habitat for macroinvertebrates and fishes in New Zealand. New Zealand Journal of Marine and Freshwater Research 48, 48–59.CrossRefGoogle Scholar
Monteiro, SM, Chapman, MG and Underwood, AJ (2002) Patches of the ascidian Pyura stolonifera (Heller, 1878): structure of habitat and associated intertidal assemblages. Journal of Experimental Marine Biology and Ecology 270, 171–189.CrossRefGoogle Scholar
Murray, LG, Newell, CR and Seed, R (2007) Changes in the biodiversity of mussel assemblages induced by two methods of cultivation. Journal of Shellfish Research 26, 153–162.CrossRefGoogle Scholar
Myers, AA and Southgate, T (1980) Artificial substrates as a means of monitoring rocky shore cryptofauna. Journal of the Marine Biological Association of the United Kingdom 60, 963–975.CrossRefGoogle Scholar
Naumov, AD (2006) Clams of the White Sea: ecological and faunistic analysis. Exploration of Fauna of the Seas 59(67). St. Petersburg: Zoological Institute RAS. [In Russian.]Google Scholar
Naumov, AD, Khalaman, VV and Fokin, MV (2009) Long-term dynamics of the abundance of several intertidal polychaetes in two inlets of Kandalaksha Bay (White Sea). Russian Journal of Marine Biology 35, 381–387.CrossRefGoogle Scholar
Neves, G and Omena, E (2003) Influence of sponge morphology on the composition of the polychaete associated fauna from Rocas Atoll, northeast Brazil. Coral Reefs 22, 123–129.CrossRefGoogle Scholar
Norling, P and Kautsky, N (2007) Structural and functional effects of Mytilus edulis on diversity of associated species and ecosystem functioning. Marine Ecology Progress Series 351, 163–175.CrossRefGoogle Scholar
Oshurkov, VV (1985) Dynamics and structure of some fouling and benthos communities of the White Sea. In Scarlato, OA (ed.), Ecology of the Fouling in the White Sea. Leningrad: Zoological Institute AN USSR, pp. 44–59. [In Russian.]Google Scholar
Oshurkov, VV (1992) Succession and climax in some fouling communities. Biofouling 6, 1–12.CrossRefGoogle Scholar
Palomo, MC, People, J, Chapman, MG and Underwood, AJ (2007) Separating the effects of physical and biological aspects of mussel beds on their associated assemblages. Marine Ecology Progress Series 344, 131–142.CrossRefGoogle Scholar
Plotkin, AS, Railkin, AI, Gerasimova, EI, Pimenov, AYu and Sipenkova, TM (2005) Subtidal underwater rock communities of the White Sea: structure and interaction with bottom flow. Russian Journal of Marine Biology 31, 335–343.CrossRefGoogle Scholar
Ponti, M, Grech, D, Mori, M, Perlini, RA, Ventra, V, Penzalis, PA and Cerrano, C (2016) The role of gorgonians on the diversity of vagile benthic fauna in Mediterranean rocky habitats. Marine Biology 163, 1–14.CrossRefGoogle Scholar
Prado, L and Castilla, JC (2006) The bioengineer Perumytilus purpuratus (Mollusca: Bivalvia) in central Chile: biodiversity, habitat structural complexity, and environmental heterogeneity. Journal of the Marine Biological Association of the United Kingdom 86, 417–421.CrossRefGoogle Scholar
Reznichenko, OG (1978) Classification and spatial-scale characteristics of fouling biotopes. Russian Journal of Marine Biology 4, 3–15. [In Russian.]Google Scholar
Sardiña, P, Cataldo, DH and Boltovskoy, D (2008) The effects of the invasive mussel, Limnoperna fortunei, on associated fauna in South American freshwaters: importance of physical structure and food supply. Fundamental and Applied Limnology/Archiv für Hydrobiologie 173, 135–144.CrossRefGoogle Scholar
Seed, R (1996) Patterns of biodiversity in the macro-invertebrate fauna associated with mussel patches on rocky shore. Journal of the Marine Biological Association of the United Kingdom 76, 203–210.CrossRefGoogle Scholar
Sepúlveda, RD, Camus, PA and Moreno, CA (2016) Diversity of faunal assemblages associated with ribbed mussel beds along the South American coast: relative roles of biogeography and bioengineering. Marine Ecology 37, 943–956.CrossRefGoogle Scholar
Serejo, CS (1998) Gammaridean and Caprellidean fauna (Crustacea) associated with the sponge Dysidea fragilis Johnston at Arraial do Cabo, Rio de Janeiro, Brazil. Bulletin of Marine Science 63, 363–385.Google Scholar
Simpson, TJS, Smale, DA, McDonald, JI and Wernberg, T (2017) Large scale variability in the structure of sessile invertebrate assemblages in artificial habitats reveals the importance of local-scale processes. Journal of Experimental Marine Biology and Ecology 494, 10–19.CrossRefGoogle Scholar
Suchanek, TH (1992) Extreme biodiversity in the marine environment: mussel bed communities of Mytilus californianus. Northwest Environmetal Journal 8, 150–152.Google Scholar
Sukhotin, AA (1992) Respiration and energetics in mussel (Mytilus edulis L.) cultured in the White Sea. Aquaculture 101, 41–57.CrossRefGoogle Scholar
Svane, I and Petersen, JK (2001) On the problems of epibioses, fouling and artificial reefs, a review. Marine Ecology 22, 169–188.CrossRefGoogle Scholar
Svane, I and Setyobudiandi, I (1996) Diversity of associated fauna in beds of the blue mussel Mytilus edulis L.: effects of location, patch size, and position within a patch. Ophelia 45, 39–53.CrossRefGoogle Scholar
Thiel, M and Ullrich, N (2002) Hard rock vs soft bottom: the fauna associated with intertidal mussel beds on hard bottoms along the coast of Chile, and considerations on the functional role of mussel beds. Helgoland Marine Research 56, 21–30.CrossRefGoogle Scholar
Tokeshi, M (1995) Polychaete abundance and dispersion patterns in mussel beds: a non-trivial ‘infaunal’ assemblage on a Pacific south American rocky shore. Marine Ecology Progress Series 125, 137–147.CrossRefGoogle Scholar
Tokeshi, M and Romero, L (1995) Filling a gap: dynamics of space occupancy on a mussel-dominated subtropical rocky shore. Marine Ecology Progress Series 119, 167–176.CrossRefGoogle Scholar
Tsuchiya, M and Nishihira, M (1985) Islands of Mytilus edulis as a habitat for small intertidal animals: effect of island size on community structure. Marine Ecology Progress Series 25, 71–81.CrossRefGoogle Scholar
Tsuchiya, M and Nishihira, M (1986) Islands of Mytilus edulis as a habitat for small intertidal animals: effect of Mytilus age structure on the special composition of the associated fauna and community organisation. Marine Ecology Progress Series 31, 171–178.CrossRefGoogle Scholar
Uryupova, EF, Spiridonov, VA and Zhadan, DG (2012). Amphipods (Crustacea: Amphipoda) associated with red algae (Rhodophyta) in Kandalaksha Bay (the White Sea, Russia). Journal of the Marine Biological Association of the United Kingdom 92, 265–273.CrossRefGoogle Scholar
Yakovis, EL, Artemieva, AV, Fokin, MV, Varfolomeeva, MA and Shunatova, NN (2007) Effect of habitat architecture on mobile benthic macrofauna associated with patches of barnacles and ascidians. Marine Ecology Progress Series 348, 117–124.CrossRefGoogle Scholar