Phenotypic plasticity at fine-grained spatial scales: the scorched mussel Perumytilus purpuratus growing on Patagonian rocky salt-marshes
Keywords:little mussels, ecomorph, geometric morphometrics, shape variation, rocky intertidal, Patagonia
Understanding phenotypic plasticity of species at different spatial scales is vital in the current context of an increasing pace of environmental changes. Through this knowledge, it is possible to predict their potential to adapt and/or evolve in face of new environmental conditions such as climate change, and/or to understand their ecological range expansion. In Patagonian rocky salt-marshes, one of the most abundant invertebrate species is the scorched mussel Perumytilus purpuratus. In this system, this mussel can be found inhabiting both vegetated and non-vegetated patches, which differ in critical environmental conditions. We performed a field study evaluating whether mussels growing in vegetated patches differ in shell shape from those growing in adjacent non-vegetated patches. We sampled individuals from both patch types and assessed their shell shape and size using geometric morphometrics. The results showed that mussels from vegetated patches had shells that were more dorsoventrally expanded, anterodorsally restricted and globose in shape than those from non-vegetated patches, which showed the opposite traits resulting in a more elongated shell. The differences found could be driven by the different conditions of temperature, desiccation rate, wave action and population density to which mussels are exposed in each patch type. These results revealed the striking phenotypic plasticity of shell form of this native species at a fine-grained scale, which could be one of the explanations for its success in its ecological range expansion.
Adami M., Pastorino G., Orensanz J.M. 2013. Phenotypic differentiation of ecologically significant Brachidontes species co-occurring in intertidal mussel beds from the southwestern Atlantic. Malacologia 56: 1-9.
Addison B. 2009. Shell traits of a marine mussel mediate predation selectivity by crabs and sea stars. J. Shellfish Res. 28: 299-303.
Alunno-Bruscia M., Bourget E., Fréchette M. 2001. Shell allometry and length-mass-density relationship for Mytilus edulis in an experimental food-regulated situation. Mar. Ecol. Prog. Ser. 219: 177-188.
Barbariol V., Razouls S. 2000. Experimental studies on the respiratory metabolism of Mytilus galloprovincialis (Mollusca Bivalvia) from the Mediterranean Sea (Gulf of Lion). Vie Milieu 50: 87-92.
Baythavong B.S. 2011. Linking the Spatial Scale of Environmental Variation and the Evolution of Phenotypic Plasticity: Selection Favors Adaptive Plasticity in Fine-Grained Environments. Amm. Nat. 178: 75-87.
Beadman H., Caldow R., Kaiser M., et al. 2003. How to toughen up your mussels: using mussel shell morphological plasticity to reduce predation losses. Mar. Biol. 142: 487-494.
Bergström P., Lindegarth M. 2016. Environmental influence on mussel (Mytilus edulis) growth - A quantile regression approach. Estuar. Coast. Shelf. Sci. 171: 123-132.
Bertness M.D., Gaines S.D., Yeh S.M. 1998. Making mountains out of barnacles: the dynamics of acorn barnacle hummocking. Ecology 79: 1382-1394.
Bertness M.D., Mullan C., Silliman B.R., et al. 2006. The community structure of western Atlantic Patagonian rocky shores. Ecol. Mon. 76: 429-460.
Bookstein F. 1991. Morphometric Tools for Landmark Data: Geometric and Biology. Cambridge University Press, New York, 435 pp.
Bourdeau P.E, Butlin R.K, Brönmark C, et al. 2015. What can aquatic gastropods tell us about phenotypic plasticity? A review and meta-analysis. Heredity 115: 312-321.
Bortolus A. 2010. Marismas Patagónicas: las últimas de Sudamérica. Ciencia Hoy 19: 10-15.
Briggs J.C., Bowen B.W. 2013. Marine shelf habitat: biogeography and evolution. J. Biogeogr. 40: 1023-1035.
Brönmark C., Lakowitz T., Hollander J. 2011. Predator-Induced Morphological Plasticity Across Local Populations of a Freshwater Snail. PLoS ONE 6: e21773.
Brown R.A., Seed R., O’Connor J. 1976. A comparison of relative growth in Cerastoderma (=Cardium) edule, Modiolus modiolus, and Mytilus edulis (Mollusca: Bivalvia). J. Zool. (Lond). 179: 297-315.
Chinzei K., Savazzi E., Seilacher A. 1982. Adaptional strategies of bivalves living as infaunal secondary soft bottom dwellers. Neues. Jahrb. Geol. Paleaontol. Abh. 164: 229-244.
Cigarria J., Fernandez J. 1998. Manila clam (Ruditapes philippinarum) culture in oyster bag: influence of density on survival, growth and biometric relationships. J. Mar. Biol. Assoc. UK 78: 551-560.
Covich A.P. 2010. Winning the biodiversity arms race among freshwater gastropods: competition and coexistence through shell variability and predator avoidance. Hydrobiologia 653: 191-215.
Cubillo A.M., Peteiro L.G., Fernández-Reiriz M.J., et al. 2012. Influence of stocking density on growth of mussels (Mytilus galloprovincialis) in suspended culture. Aquaculture 342: 103-111.
DeWitt T.J., Scheiner S.M. 2004. Phenotypic Plasticity: Functional and Conceptual Approaches, Oxford University Press, 272 pp.
Fitzer S.C., Vittert L., Bowman A., et al. 2015. Ocean acidification and temperature increase impact mussel shell shape and thickness: problematic for protection? Ecol. Evol. 5: 4875-4884.
Fox R.J., Donelson J.M., Schunter C., et al. 2019. Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Phil. Trans. R. Soc. B 374: 20180174.
Gao S.B., Mo L.D., Zhang L.H., et al. 2018. Phenotypic plasticity vs. local adaptation in quantitative traits differences of Stipa grandis in semi-arid steppe, China. Sci. Rep. 8: 3148.
Helmuth B.S. 1998. Intertidal mussel microclimates: predicting the body temperature of a sessile invertebrate. Ecol. Mon. 68: 51-74.
Hidalgo F.J., Silliman B.R., Bazterrica M.C., et al. 2007. Predation on the rocky shores of Patagonia, Argentina. Estuar. Coast. 30: 886-894.
Kirby R.R., Bayne B.L. 1994. Phenotypic variation along a cline in allozyme and karyotype frequencies, and its relationship with habitat, in the dog-whelk Nucella lapillus L. Biol J. Linn. Soc. 53: 255-275.
Kirk M., Esler D., Boyd W.S. 2007. Morphology and density of mussels on natural and aquaculture structure habitats: implications for sea duck predators. Mar. Ecol. Prog. Ser. 346: 179-187.
Klingenberg C.P. 2011. MorphoJ: an integrated software package for geometric morphometrics. Mol. Ecol. Res. 11: 353-357.
Kroeker K.J., Kordas R.L., Crim R., et al. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biol. 19: 1884-1896.
Levinton J.S. 2001. Marine Biology: Function, Biodiversity, Ecology, Oxford University Press, New York, 515 pp.
Márquez F., Frizzera A.C., Vázquez N. 2017. Environment-specific shell shape variation in the boring mytilid Leiosolenus patagonicus (d’Orbigny, 1842). Mar. Biol. Res. 13: 246-252.
Márquez F., Adami M., Trovant B., et al. 2018. Allometric differences on the shell shape of two scorched mussel species along the Atlantic South America coast. Evol. Ecol. 32: 43-56.
McDonald J.H., Seed R., Koehn R.K. 1991. Allozymes and morphometric characters of three species of Mytilus in the Northern and Southern Hemispheres. Mar. Biol. 111: 323-333.
Melatunan S., Calosi P., Rundle S.D., et al. 2013. Effects of ocean acidification and elevated temperature on shell plasticity and its energetic basis in an intertidal gastropod. Mar. Ecol. Prog. Ser. 472: 155-168.
Mestre N.C., Thatje S., Tyler P.A. 2009. The ocean is not deep enough: pressure tolerances during early ontogeny of the blue mussel Mytilus edulis. Proc. R. Soc. Lond. B. Biol. Sci. 276: 717-726.
Miner B.G., Sultan S.E., Morgan S.G., et al. 2005. Ecological consequences of phenotypic plasticity. Trends Ecol. Evol. 20: 685-692.
Mitteroecker P., Gunz P. 2009. Advances in Geometric morphometrics. Evol. Biol. 36: 235-247.
Monteiro L. 1999. Multivariate regression models and geometric morphometrics: The search for causal factors in the analysis of shape. Syst. Biol. 48: 192-199.
Ohba S. 1956. Effects of population density on mortality and growth in an experimental culture of bivalve, Venerupis semidecussata. Biol. J. Okayama. Univ. 2: 169-173.
Orr J.C., Fabry V.J., Aumont O., et al. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681-686.
Padilla D.K., Savedo M.M. 2013. A systematic review of phenotypic plasticity in marine invertebrate and plant systems. Adv. Mar. Biol. 65: 67-94.
Paine R.T., Suchanek T.H. 1983. Convergence of ecological processes between independently evolved competitive dominants: a tunicate-mussel comparison. Evolution 37: 821-831.
Peyer S.M., Hermanson J.C., Lee C.E. 2016. Developmental plasticity of shell morphology of quagga mussels from shallow and deep-water habitats of the Great Lakes. J. Exp. Biol. 213: 2602-2609.
Piersma T., Van Gils J.A. 2011. The flexible phenotype: a body-centred integration of ecology, physiology, and behaviour. Oxford University Press, New York, 222 pp.
Rohlf F.J. 2004. TPS Shareware Series. Department of Ecology and Evolution, State University of New York, Stony Brook, New York.
Rohlf F.J. 2016a. TpsUtil. version 1.70. Department of Ecology and Evolution, State University of New York Stony Brook, New York.
Rohlf F.J. 2016b. TpsRelw. version 1.64. Department of Ecology and Evolution, State University of New York Stony Brook, NY New York.
Rohlf F.J., Slice D. 1990. Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks. Syst. Biol. 39: 40-59.
Scheiner S.M.1993. Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24: 35-68.
Scherer A.E., Lunt J., Draper A.M., et al. 2016. Phenotypic plasticity in oysters (Crassostrea virginica) mediated by chemical signals from predators and injured prey. Invert. Biol. 135: 97-107.
Schwenk K., Padilla D.K., Bakken G.S., et al. 2009. Grand challenges in organismal biology. Integr. Comp. Biol. 49: 7-14.
Seed R. 1968. Factors influencing shell shape in Mytilus edulis. J. Mar. Biol. Assoc. UK 48: 561-584.
Seed R. 1969. The ecology of Mytilus edulis L. (Lamellibranchiata) on exposed rocky shores. II. Growth and mortality. Oecologia 3: 317-335.
Seed R. 1973. Absolute and allometric growth in the mussel, Mytilus edulis L. (Mollusca Bivalvia). Proc. Malacol. Soc. Lond. 40: 343-357.
Silliman B.R., Bertness M.D., Altieri A.H., et al. 2011. Whole-community facilitation regulates biodiversity on Patagonian rocky shores. PloS ONE 6: e24502.
Soot-Ryen T. 1955. A report on the family Mytilidae (Pelecypoda). Allan Hancock Pacific Expeditions (series) 20. Univ. South California, Los Angeles. 174 pp.
Steffani C.N., Branch G.M. 2003. Growth rate, condition, and shell shape of Mytilus galloprovincialis: responses to wave exposure. Mar. Ecol. Prog. Ser. 246: 197-209.
Stoeckmann A. 2003. Physiological energetics of Lake Erie dreissenid mussels: a basis for the displacement of Dreissena polymorpha by Dreissena bugensis. Can. J.Fish. Aquat. Sci. 60: 126-134.
Sueiro M.C. 2012. Plantas vasculares como agentes modificadores de ecosistemas en la costa Patagónica. Universidad de Buenos Aires, PhD thesis 131 pp.
Sueiro M.C., Bortolus A., Schwindt E. 2011. Habitat complexity and community composition: relationships between different ecosystem engineers and the associated macroinvertebrate assemblages. Helgol. Mar. Res. 65: 467-477.
Sueiro M.C., Bortolus A., Schwindt E. 2012. The role of the physical structure of Spartina densiflora Brong. in structuring macroinvertebrate assemblages. Aquatic. Ecol. 46: 25-36.
Tanita S., Kikuchi S. 1957. On the density effect of the raft cultured oysters. I. The density effect within one plate. Bull. Tohoku. Reg. Fish. Lab. Res. 9: 133-142.
Telesca L., Michalek K., Sanders T., et al. 2018. Blue mussel shell shape plasticity and natural environments: a quantitative approach. Sci. Rep. 8: 2865.
Trivellini M.M., Van der Molen S., Márquez F. 2018. Fluctuating asymmetry in the shell shape of the Atlantic Patagonian mussel, Mytilus platensis, generated by habitat-specific constraints. Hydrobiologia 822: 189-201.
Trovant B., Orensanz J.M., Ruzzante D.E., et al. 2015. Scorched mussels (Bivalvia: Mytilidae: Brachidontinae) from the temperate coasts of South America: Phylogenetic relationships, trans-Pacific connections and the footprints of Quaternary glaciations. Mol. Phylogenetics. Evol. 82: 60-74.
Wilbur K.M., Saleuddin A.S.M. 1983. Shell formation. In: Wilbur K.M., Saleuddin A.S.M. (eds), The Mollusca, Academic Press, New York, pp. 235-287.
Zelditch M.L., Swiderski D.L., Sheets H.D., et al. 2004. Geometric Morphometrics for Biologists. Ed. Elsevier, London, 443 pp.
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