Abstract
Mussels often act as ecosystem engineers in rocky intertidal habitats, favoring the occurrence of many small invertebrates by increasing habitat complexity and improving local environmental conditions. This study tests the hypothesis that invertebrate assemblages from intertidal mussel beds differ between wave-sheltered and wave-exposed habitats. To this aim, we surveyed exposed and sheltered sites spanning 350 km of coastline in Nova Scotia, Canada. We identified all invertebrates and measured their abundance in replicate quadrats that were fully covered by mussels. In total, we found 50 invertebrate taxa living in these mussel beds. Multivariate analyses revealed that the composition of invertebrate assemblages differed significantly between both habitat types. Exposed habitats supported a greater species richness, and the species that mainly explained the compositional difference between both environments were more abundant in exposed ones. Assemblages were taxonomically dominated by arthropods, annelids, and molluscs and numerically dominated by tubificid oligochaetes regardless of exposure. Our results suggest that exposed habitats may favor the occurrence of filter-feeders, such as barnacles, and sheltered habitats the occurrence of predators, such as small crabs and sea stars, in intertidal mussel beds from the NW Atlantic coast.
Similar content being viewed by others
References
Alunno-Bruscia M, Petraitis P, Bourget E, Fréchette M (2000) Body-size density relationship for Mytilus edulis in an experimental food-regulated situation. Oikos 90:28–42
Alvarado JL, Castilla JC (1996) Tridimensional matrices of mussels Perumytilus purpuratus on intertidal platforms with varying wave forces in central Chile. Mar Ecol Prog Ser 133:135–141
Arribas LP, Bagur M, Klein E, Penchaszadeh P, Palomo MG (2013) Geographic distribution of mussel species and associated assemblages along the northern Argentinian coast. Aquat Biol 18:91–103
Arroyo MTK, Cavieres LA, Peñaloza A, Arroyo-Kalin MA (2003) Positive associations between the cushion plant Azorella monantha (Apiaceae) and alpine plant species in the Chilean Patagonian Andes. Plant Ecol 169:121–129
Bertness MD (2007) Atlantic shorelines. Natural history and ecology. Princeton University Press, Princeton
Bertness MD, Trussell GC, Ewanchuk PJ, Silliman BR (2004) Do alternate stable community states exist in the Gulf of Maine rocky intertidal zone? Ecology 83:3434–3448
Bertness MD, Crain CM, Reyna MV, Bazterrica MC, Hildago F, Farina JM, Silliman BR (2006) The community structure of western Atlantic Patagonian rocky shores. Ecol Monogr 76:439–460
Borthagaray AI, Carranza A (2007) Mussels as ecosystem engineers: their contribution to species richness in a rocky littoral community. Acta Oecol 31:243–250
Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125
Cardinale BJ, Gross K, Fritschie K, Flombaum P, Fox JW, Rixen C, van Ruijven J, Reich PB, Scherer-Lorenzen M, Wilsey BJ (2013) Biodiversity simultaneously enhances the production and stability of community biomass, but the effects are independent. Ecology 94:1697–1707
Carrington E, Moeser GM, Dimond J, Mello JJ, Boller ML (2009) Seasonal disturbance to mussel beds: field test of a mechanistic model predicting wave dislodgment. Limnol Oceanogr 54:978–986
Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation. PRIMER-E, Plymouth
Coleman FC, Williams SL (2002) Overexploiting marine ecosystem engineers: potential consequences for biodiversity. Trends Ecol Evol 17:40–44
Commito JA, Boncavage EM (1989) Suspension-feeders and coexisting infauna: an enhancement counter example. J Exp Mar Biol Ecol 125:33–42
Commito JA, Rusignuolo BR (2000) Structural complexity in mussel beds: the fractal geometry of surface topography. J Exp Mar Biol Ecol 225:133–152
Crain CM, Bertness MD (2006) Ecosystem engineering across environmental gradients: implications for conservation and management. Bioscience 56:211–218
Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166
Crooks JA, Khim HS (1999) Architectural vs biological effects of a habitat-altering, exotic mussel, Musculista senhousia. J Exp Mar Biol Ecol 240:53–75
Crowe TP, Smith EL, Donkin P, Barnaby DH, Rowland SJ (2004) Measurements of sublethal effects on individual organisms indicate community-level impacts of pollution. J Appl Ecol 41:114–123
Cusson M, Bourget E (2005) Small-scale variations in mussel (Mytilus spp.) dynamics and local production. J Sea Res 53:255–268
Denny M, Wethey D (2001) Physical processes that generate patterns in marine communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer, Sunderland, pp 3–37
Gaines SD, Bertness M (1993) The dynamics of juvenile dispersal: why field ecologists must integrate. Ecology 74:2430–2435
Gibson M (2003) Seashores of the Maritimes. Nimbus Publishing, Halifax
Hammond W, Griffiths CL (2004) Influence of wave exposure on South African mussel beds and their associated infaunal communities. Mar Biol 144:547–552
Harley CDG (2011) Climate change, keystone predation, and biodiversity loss. Science 334:1124–1127
Hastings A, Byers JE, Crooks JA, Cuddington K, Jones CG, Lambrinos JG, Talley TS, Wilson WG (2007) Ecosystem engineering in space and time. Ecol Lett 10:153–164
He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive interactions with increasing environmental stress. Ecol Lett 16:695–706
Heaven CS, Scrosati RA (2008) Benthic community composition across gradients of intertidal elevation, wave exposure, and ice scour in Atlantic Canada. Mar Ecol Prog Ser 369:13–23
Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, Matulich KL, González A, Duffy JE, Gamfeldt L, O’Connor MI (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–108
Hunt HL, Scheibling RE (2001) Predicting wave dislodgment of mussels: variation in attachment strength with body size, habitat, and season. Mar Ecol Prog Ser 213:157–164
Jones CG, Gutiérrez JL, Byers JE, Crooks JA, Lambrinos JG, Talley TS (2010) A framework for understanding physical ecosystem engineering by organisms. Oikos 119:1862–1869
Knopf AA (1981) National Audubon Society field guide to North American seashells. Chanticleer Press, New York
Kozloff EN (1996) Marine invertebrates of the Pacific Northwest. University of Washington Press, Seattle
Krebs CJ (1999) Ecological methodology. Benjamin Cummings, Menlo Park
Lauzon-Guay JS, Hamilton DJ, Barbeau MA (2005) Effect of mussel density and size on the morphology of blue mussels (Mytilus edulis) grown in suspended culture in Prince Edward Island, Canada. Aquaculture 249:265–274
Leonard G, Levine JM, Schmidt P, Bertness MD (1998) Flow-generated bottom-up forcing of intertidal community structure in a Maine estuary. Ecology 79:1395–1411
Menge BA (1978) Predation intensity in a rocky intertidal community. Relation between predator foraging activity and environmental harshness. Oecologia 34:1–16
Menge BA (1995) Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecol Monogr 65:21–74
Menge BA, Branch GM (2001) Rocky intertidal communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer, Sunderland, pp 221–251
Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757
Murray LG, Newell CR, Seed R (2007) Changes in the biodiversity of mussel assemblages induced by two methods of cultivation. J Shellfish Res 26:153–162
O’Connor NE (2010) Shore exposure affects mussel population structure and mediates the effect of epibiotic algae on mussel survival in SW Ireland. Estuar Coast Shelf Sci 87:83–91
O’Connor NE, Crowe TP (2007) Biodiversity among mussels: separating the influence of sizes of mussels from the ages of patches. J Mar Biol Assoc U K 87:551–557
Paine RT, Levin SA (1981) Intertidal landscapes: disturbance and the dynamics of pattern. Ecol Monogr 51:145–178
Palomo MG, People J, Chapman MG, Underwood AJ (2007) Separating the effects of physical and biological aspects of mussel beds on their associated assemblages. Mar Ecol Prog Ser 344:131–142
Pollock LW (1998) A practical guide to the marine animals of northeastern North America. Rutgers University Press, New Brunswick
Prado L, Castilla JC (2006) The bioengineer Perumytilus purpuratus (Mollusca: Bivalvia) in central Chile: biodiversity, habitat structural complexity, and environmental heterogeneity. J Mar Biol Assoc U K 86:417–421
Raffaelli D, Hawkins S (1999) Intertidal ecology. Chapman & Hall, London
Rawson PD, Harper FM (2009) Colonization of the northwest Atlantic by the blue mussel Mytilus trossulus postdates the last glacial maximum. Mar Biol 156:1857–1868
Riisgård HU (2001) On measurement of filtration rates in bivalves—the stony road to reliable data: review and interpretation. Mar Ecol Prog Ser 211:275–291
Scheiner SM, Chiarucci A, Fox GA, Helmus MR, McGlinn DJ, Willig MR (2011) The underpinnings of the relationship of species richness with space and time. Ecol Monogr 81:195–213
Schöb C, Armas C, Guler M, Prieto I, Pugnaire FI (2013) Variability in functional traits mediates plant interactions along stress gradients. J Ecol 101:753–762
Scrosati R, Heaven C (2007) Spatial trends in community richness, diversity, and evenness across rocky intertidal environmental stress gradients in eastern Canada. Mar Ecol Prog Ser 342:1–14
Scrosati RA, van Genne B, Heaven CS, Watt CA (2011) Species richness and diversity in different functional groups across environmental stress gradients: a model for marine rocky shores. Ecography 34:151–161
Seed R (1969) The ecology of Mytilus edulis L. (Lamellibranchiata) on exposed rocky shores. I. Breeding and settlement. Oecologia 3:277–316
Seed R (1996) Patterns of biodiversity in the macro-invertebrate fauna associated with mussel patches on rocky shores. J Mar Biol Assoc U K 76:203–210
Silliman BR, Bertness MD, Altieri AH, Griffin JN, Bazterrica MC, Hidalgo FJ, Crain CM, Reyna MV (2011) Whole-community facilitation regulates biodiversity on Patagonian rocky shores. PLoS One 6:e24502
Suchanek TH (1985) Mussels and their role in structuring rocky shore communities. In: Moore PG, Seed R (eds) The ecology of rocky coasts. Hodder and Stoughton Press, London, pp 70–96
Suchanek TH (1992) Extreme biodiversity in the marine environment: mussel bed communities of Mytilus californianus. Northwest Environ J 8:150–152
Tam JC, Scrosati RA (2011) Mussel and dogwhelk distribution along the northwest Atlantic coast: testing predictions derived from the abundant-centre model. J Biogeogr 38:1536–1545
Tam JC, Scrosati RA (2014) Distribution of cryptic mussel species (Mytilus edulis and M. trossulus) along wave exposure gradients on northwest Atlantic rocky shores. Mar Biol Res 10:51–60
Thiel M, Ullrich N (2002) Hard rock versus 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. Helgol Mar Res 56:21–30
Tsuchiya M, Nishihira M (1986) Islands of Mytilus edulis as a habitat for small intertidal animals: effect of Mytilus age structure on the species composition of the associated fauna and community organization. Mar Ecol Prog Ser 31:171–178
Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge
Valdivia N, Thiel M (2006) Effects of point-source nutrient addition and mussel removal on epibiotic assemblages in Perumytilus purpuratus beds. J Sea Res 56:271–283
Watt CA, Scrosati RA (2013) Bioengineer effects on understory species richness, diversity, and composition change along an environmental stress gradient: experimental and mensurative evidence. Estuar Coast Shelf Sci 123:10–18
Witman JD (1985) Refuges, biological disturbance, and subtidal community organization in New England. Ecol Monogr 55:421–445
Wong MC, Barbeau MA, Hennigar AW, Robinson SMC (2005) Protective refuges for seeded juvenile scallops (Placopecten magellanicus) from sea star (Asterias spp.) and crab (Cancer irroratus and Carcinus maenas) predation. Can J Fish Aquat Sci 62:1766–1781
Wright JP, Jones CG, Boeken B, Shachak M (2006) Predictability of ecosystem engineering effects on species richness across environmental variability and spatial scales. J Ecol 94:815–824
Young IR, Zieger S, Babanin AV (2011) Global trends in wind speed and wave height. Science 332:451–455
Zardi GI, Nicastro KR, McQuaid CD, Rius M, Porri F (2006) Hydrodynamic stress and habitat partitioning between indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussels: constraints of an evolutionary strategy. Mar Biol 150:79–88
Acknowledgments
We are grateful to Julius Ellrich for laboratory assistance, to two anonymous reviewers for helpful comments on an earlier version of this paper, to the Canada Research Chairs (CRC) program, the Canada Foundation for Innovation (CFI), and the Natural Sciences and Engineering Research Council (NSERC, Discovery Grant) for financial support to R.A.S., to the Canadian Bureau for International Education (CBIE) for financial support to L.P.A. through an Emerging Leaders of the Americas Program (ELAP) graduate student scholarship, and to the University of Naples for financial support to L.D. through a graduate student scholarship.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 99 kb)
Rights and permissions
About this article
Cite this article
Arribas, L.P., Donnarumma, L., Palomo, M.G. et al. Intertidal mussels as ecosystem engineers: their associated invertebrate biodiversity under contrasting wave exposures. Mar Biodiv 44, 203–211 (2014). https://doi.org/10.1007/s12526-014-0201-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12526-014-0201-z