Marine Biology

, Volume 150, Issue 1, pp 79–88 | Cite as

Hydrodynamic stress and habitat partitioning between indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussels: constraints of an evolutionary strategy

  • G. I. ZardiEmail author
  • K. R. Nicastro
  • C. D. McQuaid
  • M. Rius
  • F. Porri
Research Article


The ability of a mussel to withstand wave-generated hydrodynamic stress depends mainly on its byssal attachment strength. This study investigated causes and consequences of different attachment strengths of the two dominant mussels species on the South African south coast, the invasive Mytilus galloprovincialis and the indigenous Perna perna, which dominate the upper and the lower areas of the lower balanoid zone, respectively and co-exist in the middle area. Attachment strength of P. perna was significantly higher than that of M. galloprovincialis. Likewise solitary mussels were more strongly attached than mussels living within mussel beds (bed mussels), and in both cases this can be explained by more and thicker byssal threads. Having a wider shell, M. galloprovincialis is also subjected to higher hydrodynamic loads than P. perna. Attachment strength of both species increased from higher to lower shore, in response to a gradient of stronger wave action. The morphological features of the invasive species and its higher mortality rates during winter storms help to explain the exclusion of M. galloprovincialis from the low shore. The results are discussed in the context of the evolutionary strategy of the alien mussel, which directs most of its energy to fast growth and high reproductive output, apparently at the cost of reduced attachment strength. This raises the prediction that its invasive impact will be more pronounced at sites subject to strong but not extreme wave action.


Shell Length Hydrodynamic Force Perna Mussel Species Byssal Thread 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This research was funded by Rhodes University and the National Research Foundation of South Africa.


  1. Apte S, Holland BS, Godwin LS, Gardner JPA (2000) Jumping ships: a stepping stone event mediating transfer of a non-indigenous species via a potentially unsuitable environment. Biol Invasions 2:75–79CrossRefGoogle Scholar
  2. Bairati A, Vitellaro-Zuccarello L (1976) The ultrastructure of the byssal apparatus of Mytilus galloprovincialis. IV. Observation by transmission electron microscopy. Cell Tissue Res 166:219–234CrossRefGoogle Scholar
  3. Bell CM, Gosline JM (1996) Mechanical design of mussel byssus: material yield enhances attachment strength. J Exp Biol 199:1005–1017PubMedGoogle Scholar
  4. Bell CM, Gosline JM (1997) Strategies for life in flow: tenacity, morphometry, and probability of dislodgement of two Mytilus species. Mar Ecol Prog Ser 159:197–208CrossRefGoogle Scholar
  5. Benedict CV, Waite JH (1986) Composition and ultrastructure of the byssus of Mytilus edulis. J Morphol 189:261–270CrossRefGoogle Scholar
  6. Branch GM, Steffani CN (2004) Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck). J Exp Mar Biol Ecol 300:189–215CrossRefGoogle Scholar
  7. Brown CH (1952) Some structural proteins of Mytilus edulis L. Q J Microsc Sci 93:487–502Google Scholar
  8. Brundrit GB, Shannon LV (1989) Cape storms and the Agulhas current: a glimpse of the future? S Afr J Mar Sci 85:619–620Google Scholar
  9. Bustamante RH, Branch GM (1996) The dependence of intertidal consumers on kelp-derived organic matter on the west coast of South Africa. J Exp Mar Biol Ecol 196:1–28CrossRefGoogle Scholar
  10. Butman CA, Frechette M, Geyer WR (1994) Flume experiments on food supply to the blue mussel Mytilus edulis L. as a function of boundary layer flow. Limnol Oceanogr 39:1755–1768CrossRefGoogle Scholar
  11. Calvo-Ugarteburu G, McQuaid CD (1998) Parasitism and invasive species: effects of digenetic trematodes on mussels. Mar Ecol Prog Ser 169:149–163CrossRefGoogle Scholar
  12. Carrington E (2002) Seasonal variation in the attachment strength of the blue mussel: causes and consequences. Limnol Oceanogr 47:1723–1733CrossRefGoogle Scholar
  13. Denny MV (1985) Wave forces on intertidal organisms: a case study. Limnol Oceanogr 30:1171–1187CrossRefGoogle Scholar
  14. Denny MW (1987) Lift as a mechanism of patch initiation in mussel beds. J Exp Mar Biol Ecol 113:231–245CrossRefGoogle Scholar
  15. Denny MW (1988) Biology and mechanism of the wave swept environment. Princeton University Press, Princeton, NJGoogle Scholar
  16. Denny MW (1995) Predicting physical disturbance: mechanistic approaches to the study of survivorship on wave-swept shores. Ecol Monogr 65:371–418CrossRefGoogle Scholar
  17. Denny MW, Daniel TL, Koehl MAR (1985) Mechanical limits to size in wave-swept organisms. Ecol Monogr 55:69–102CrossRefGoogle Scholar
  18. Denny MW, Gaines SD (1990) On the prediction of maximal intertidal wave forces. Limnol Oceanogr 35:1–15CrossRefGoogle Scholar
  19. De Moor IJ, Bruton MN (1988) Atlas of alien and translocated indigenous aquatic animals in southern Africa. South African National Scientific Programmes Report, vol 144. Pretoria, South AfricaGoogle Scholar
  20. Dolmer P, Svane I (1994) Attachment and orientation of Mytilus edulis L. In flowing water. Ophelia 40:63–74CrossRefGoogle Scholar
  21. Erlandsson J, Pal P, McQuaid CD (2006) Re-colonization rate differs between co-existing indigenous and invasive intertidal mussels following major disturbance. Mar Ecol Prog Ser (in press)Google Scholar
  22. Frechette M, Butman CA, Geyer WR (1989) The importance of boundary-layer flow in suppling phytoplankton to the benthic suspension feeder, Mytilus edulis L. Limnol Oceanogr 34:19–36CrossRefGoogle Scholar
  23. Gaylord B (2000) Biological implications of surf-zone complexity. Limnol Oceanogr 45:174–188CrossRefGoogle Scholar
  24. Gaylord B, Blanchette CA, Denny MW (1994) Mechanical consequences of size in wave-swept algae. Ecol Monogr 64:287–813CrossRefGoogle Scholar
  25. Griffiths CL, King JA (1979) Energy expended on growth and gonad output in the ribbed mussel Aulacomya ater. Mar Biol 53:217–222CrossRefGoogle Scholar
  26. Griffiths CL, Hockey PAR, Van Erkom Shurink C, Le Roux PJ (1992) Marine invasive aliens on South African shores: implications for community structure and trophic functioning. S Afr J Mar Sci 12:713–722CrossRefGoogle Scholar
  27. Hawkins AJS, Bayne BL (1985) Seasonal variation in the relative utilization of carbon and nitrogen by the mussel Mytilus edulis: budgets, conversion efficiencies and maintenance requirements. Mar Ecol Prog Ser 25:181–188CrossRefGoogle Scholar
  28. Harger JRE (1970) The effect of wave impact on some aspects of the biology of sea mussels. Veliger 12:401–414Google Scholar
  29. Harris JM, Branch GM, Elliott BL, Currie B, Dye AH, McQuaid CD, Tomalin BJ, Velasquez C (1998) Spatial an temporal variability in recruitment of intertidal mussels around the coast of southern Africa. S Afr J Zool 33:1–11CrossRefGoogle Scholar
  30. Hilbish TJ, Mullinax A, Dolven SI, Meyer A, Koehn RH, Rawson PD (2000) Origin of the antitropical distribution pattern in marine mussels (Mytilus spp.): routes and timing of transequatorial migration. Mar Biol 136:69–77CrossRefGoogle Scholar
  31. Hockey CL, van Erkom Schurink C (1992) The invasive biology of the mussel Mytilus galloprovincialis on the southern African coast. Trans R Soc S Afr 48:123–139CrossRefGoogle Scholar
  32. Hunt HL, Scheibling RE (2001) Predicting wave dislodgement of mussels: variation in attachment strength with body size, habitat, and season. Mar Ecol Prog Ser 213:157–164CrossRefGoogle Scholar
  33. Lee CY, Lim SS, Owen MD (1990) The rate and strength of the byssal reattachment by the blue mussels (Mytilus edulis L.). Can J Zool 68:2005–2009CrossRefGoogle Scholar
  34. Lee SY, Morton BS (1985) The introduction of the Mediterranean mussel Mytilus galloprovincialis into Hong Kong. Malacol Rev 18:107–109Google Scholar
  35. Lubchenco J, Menge BA (1978) Community development and persistence in a low rocky intertidal zone. Ecol Monogr 48:67–94CrossRefGoogle Scholar
  36. McDonald JH, Seed R, Koehn RK (1991) Allozymes and morphometric characters of three specie of Mytilus in the Northern and Southern Hemispheres. Mar Biol 111:323–333CrossRefGoogle Scholar
  37. McQuaid CD, Branch GM (1984) Influence of sea temperature, substratum and wave exposure on rocky intertidal communities: an analysis of faunal and floral biomass. Mar Ecol Prog Ser 19:145–151CrossRefGoogle Scholar
  38. McQuaid CD, Branch GM (1985) Trophic structure of rocky intertidal communities: response to wave action and implications for energy flow. Mar Ecol Prog Ser 22:153–161CrossRefGoogle Scholar
  39. McQuaid CD, Lindsay TL (2000) Effect of wave exposure on growth and mortality rates of the mussel Perna perna: bottom-up regulation of intertidal populations. Mar Ecol Prog Ser 206:147–154CrossRefGoogle Scholar
  40. Menge BA (1976) Organization of the New England rocky intertidal community: role of predation, competition, and environmental heterogeneity. Ecol Monogr 46:355–393CrossRefGoogle Scholar
  41. Okamura B (1986) Group living and the effects of spatial position in aggregations of Mytilus edulis. Oecologia 69:341–347CrossRefGoogle Scholar
  42. O’Riordan CA, Monismith SG, Koseff JR (1993) A study of concentration boundary-layer formation over a bed of model bivalves. Limnol Oceanogr 38:1712–1729CrossRefGoogle Scholar
  43. Paine RT, Levin SA (1981) Intertidal landscapes: disturbance and the dynamics of pattern. Ecol Monogr 51:145–178CrossRefGoogle Scholar
  44. Palumbi SR (1984) Measuring intertidal wave force. J Exp Mar Biol Ecol 81:171–179CrossRefGoogle Scholar
  45. Price HA (1982) An analysis of factors determining seasonal variation in the byssal attachment strength of Mytilus edulis L. J Mar Biol Assoc UK 62:147–155CrossRefGoogle Scholar
  46. Rius M, McQuaid CD (2006) Wave action and competitive interaction between the invasive mussel Mytilus galloprovincialis and the indigenous Perna perna in South Africa. Mar Biol (in press)Google Scholar
  47. Robinson TB, Griffiths CL, McQuaid CD, Rius M (2005) Marine alien species of South Africa—status and impacts. Afr J Mar Sci 27:297–306CrossRefGoogle Scholar
  48. Schneider KR, Wethey DS, Helmuth BST, Hilbish TJ (2005) Implications of movement behaviour on mussels dislodgment: exogenous selection in a Mytilus spp. hybrid zone. Mar Biol 146:333–343CrossRefGoogle Scholar
  49. Seed R, Suchanek TH (1992) Population and community ecology of Mytilus. In: Gosling EG (ed) The mussel Mytilus: ecology, physiology, genetics and culture. Elsevier, New York, pp 87–169Google Scholar
  50. Sousa WP (1985) The role of disturbance in natural communities. Annu Rev Ecol Sys 15:353–391CrossRefGoogle Scholar
  51. Steffani CN, Branch GM (2003a) Growth rate, condition, and shell shape of Mytilus galloprovincialis: responses to wave exposure. Mar Ecol Prog Ser 246:197–209CrossRefGoogle Scholar
  52. Steffani CN, Branch GM (2003b) Spatial comparisons of populations of an indigenous limpet Scutellastra argenvillei and an alien mussel Mytilus galloprovincialis: along a gradient of wave action. Afr J Mar Sci 25:195–212CrossRefGoogle Scholar
  53. Van Erkom Schurink C, Griffiths CL (1991) A comparison of reproductive cycles and reproductive output in four southern African mussel species. Mar Ecol Prog Ser 76:123–134CrossRefGoogle Scholar
  54. Van Erkom Schurink C, Griffiths CL (1993) Factors affecting relative rates of growth in four South African mussel species. Aquaculture 109:253–273Google Scholar
  55. Waite JH (1992) The formation of mussel byssus: anatomy of a natural manufacturing process. In: Case ST (ed) Results and problems in cell differentiation, vol 19. Biopolymers, Springer, Berlin Heidelberg New York, pp 27–54Google Scholar
  56. Wilkins NP, Fujino K, Gosling EM (1983) The Mediterranean mussel Mytilus galloprovincialis Lmk. In Japan. Biol J Linn Soc 20:365–374CrossRefGoogle Scholar
  57. Willis GL, Skibinski DO (1992) Variation in strength of attachment to the substrate explains differential mortality in hybrid mussel (Mytilus galloprovincialis and Mytilus edulis) populations. Mar Biol 112:403–408CrossRefGoogle Scholar
  58. Witman JD, Suchanek TH (1984) Mussels in flow: drag and dislodgement by epizoans. Mar Ecol Prog Ser 16:259–268CrossRefGoogle Scholar
  59. Young GA (1985) Byssus-thread formation by the mussel Mytilus edulis: effects of environmental factors. Mar Ecol Prog Ser 24:261–271CrossRefGoogle Scholar
  60. Zardi GI, Nicastro KR, Porri F, McQuaid CD (2006) Sand stress as a non-determinant of habitat segregation of indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussels in South Africa. Mar Biol 148:1031–1038CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • G. I. Zardi
    • 1
    Email author
  • K. R. Nicastro
    • 1
  • C. D. McQuaid
    • 1
  • M. Rius
    • 1
  • F. Porri
    • 1
  1. 1.Department of Zoology and EntomologyRhodes UniversityGrahamstownSouth Africa

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