Biological Invasions

, Volume 12, Issue 7, pp 2165–2177 | Cite as

Differential reproductive investment, attachment strength and mortality of invasive and indigenous mussels across heterogeneous environments

  • K. R. Nicastro
  • G. I. Zardi
  • C. D. McQuaid
Original Paper


Environmental heterogeneity challenges both indigenous species and invaders and can play a defining role in the dynamics of their interactions. We compare bay and open coast habitats to show how environmental heterogeneity and seasonality affect survival and physiological performances of invasive (Mytilus galloprovincialis) and indigenous (Perna perna) intertidal mussels. P. perna had significantly higher attachment strength than M. galloprovincialis. Attachment was strongly correlated with hydrodynamic stress and was lower for both species in bays. Both species had a major spawning event when wave action was weakest. In bays, there was no correlation between gonad index (GI) and attachment strength for either species, but on the open coast GI was negatively correlated with attachment. In bays, maximum GI of M. galloprovincialis was 64% higher than for P. perna, while on the open coast values did not differ between the two. Thus, on the open coast, both species invest more energy in attachment but P. perna can accommodate energetic demands of increased byssal production without altering gonad production, while M. galloprovincialis cannot. Mortality was significantly correlated to sand stress, while the correlation with wave action was very weak in bays and non-significant on the open coast probably because sand stress peaked during periods of low wave action. The success of the invader and thus the outcomes of its interaction with the indigenous species are governed by habitat-to-habitat variability. In this case the invasive species is likely to prove a weaker competitor on the more stressful and energetically demanding open coast.


Habitat variability Environmental stress Mytilus galloprovincialis Perna perna 



This work is based upon research supported by the South African Research Chairs Initiative of the Department of Science and Technology and National Research Foundation with additional funding from Rhodes University and a Claude Harris Leon postdoctoral research fellowship Foundation awarded to GIZ. We thank Liesl Knott for technical support.

Supplementary material

10530_2009_9619_MOESM1_ESM.doc (31 kb)
Supplementary material 1 (DOC 31 kb)


  1. Babarro JMF, Fernandez-Reiriz MJ, Labarta U (2008) Secretion of byssal threads and attachment strength of Mytilus galloprovincialis: the influence of size and food availability. J Mar Biol Assoc UK 88:783–791CrossRefGoogle Scholar
  2. Baker HG (1986) Patterns of plant invasion in North America. In: Mooney HA, Drake JA (eds) Ecology of biological invasions of North America and Hawaii. Springer, New York, pp 44–57Google Scholar
  3. Bownes S, McQuaid CD (2006) Will the invasive mussel Mytilus galloprovincialis Lamarck replace the indigenous Perna perna L. on the south coast of South Africa? J Exp Mar Biol Ecol 338:140–151CrossRefGoogle Scholar
  4. Broom DM, Johnsen KG (1993) Stress and animal welfare. Chapman & Hall, New YorkGoogle Scholar
  5. Buchanan KL (2000) Stress and the evolution of condition-dependent signals. Trends Ecol Evol 15:156–160CrossRefPubMedGoogle Scholar
  6. Byers JE (2002) Physical habitat attribute mediates biotic resistance to non-indigenous species invasion. Oecologia 130:146–156Google Scholar
  7. Carrington E (2002a) Seasonal variation in the attachment strength of the blue mussel: causes and consequences. Limnol Oceanogr 47:1723–1733CrossRefGoogle Scholar
  8. Carrington E (2002b) The ecomechanics of mussel attachment: from molecules to ecosystems. Integr Comp Biol 42:846–852CrossRefGoogle Scholar
  9. Chesson P (1994) Multispecies competition in variable environment. Theor Popul Biol 45:227–276CrossRefGoogle Scholar
  10. Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366CrossRefGoogle Scholar
  11. Chesson P, Huntly N (1997) The roles of harsh and fluctuating conditions in the dynamics of ecological communities. Am Nat 150:519–553CrossRefPubMedGoogle Scholar
  12. Connell JH, Keough MJ (1985) Disturbance and patch dynamics of subtidal marine animals on hard substrata. In: Pickett STA, White PS (eds) The ecology of natural disturbance and patch dynamics. Academic Press, Orlando, pp 125–151Google Scholar
  13. Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534CrossRefGoogle Scholar
  14. Denny MW (1995) Predicting physical disturbance: mechanistic approaches to the study of survivorship on wave-swept shores. Ecol Monogr 65:371–418CrossRefGoogle Scholar
  15. Denny MW, Wethey D (2000) Physical processes that generate patterns in marine communities. Chapter 1. In: Bertness M, Hay M, Gaines S (eds) Marine community ecology. Sinauer Press, NYGoogle Scholar
  16. Denny MW, Miller LP, Stokes MD, Hunt LJH, Helmuth BST (2003) Extreme water velocities: topographical amplification of wave-induced flow in the surf zone of rocky shores. Limnol Oceanogr 48:1–8Google Scholar
  17. Devinny JS, Volse LA (1978) Effect of sediments on the development of Macrocystis pyrifera gametophytes. Mar Biol 48:343–348CrossRefGoogle Scholar
  18. Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139CrossRefPubMedGoogle Scholar
  19. Erlandsson J, Pal P, McQuaid CD (2006) Re-colonisation rate differs between co-existing indigenous and invasive intertidal mussels following major disturbance. Mar Ecol Prog Ser 320:169–176CrossRefGoogle Scholar
  20. Gaylord B, Blanchette CA, Denny MW (1994) Mechanical consequences of size in wave-swept algae. Ecol Monogr 64:287–813CrossRefGoogle Scholar
  21. Gerlach JD, Rice KJ (2003) Testing life history correlates of invasiveness using congeneric plant species. Ecol Appl 13:167–179CrossRefGoogle Scholar
  22. Griffiths CL, King JA (1979) Energy expended on growth and gonad output in the ribbed mussel Aulacomya ater. Mar Biol 53:217–222CrossRefGoogle Scholar
  23. Griffiths CL, Hockey PAR, Van Erkom Schurink C, Le Roux PJ (1992) Marine invasive aliens on South African shores: Implications for community structure and trophic functioning. S Afr J Mar Sci 12:713–722Google Scholar
  24. Hanekom N (2008) Invasion of an indigenous Perna perna mussel bed on the south coast of South Africa by an alien mussel Mytilus galloprovincialis and its effect on the associated fauna. Biol Inv 10:233–244CrossRefGoogle Scholar
  25. 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 33:1–11Google Scholar
  26. Hastings A, Cuddington K, Davies KF, Dugaw CJ, Elmendorf S, Freestone A et al (2005) The spatial spread of invasions: new developments in theory and evidence. Ecol Lett 8:91–101CrossRefGoogle 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. Hockey PAR, Van Erkom Schurink C (1992) The invasive biology of the mussel Mytilus galloprovincialis on the southern African coast. Trans R Soc S Afr 48:123–139Google Scholar
  29. Hu SS, Tessier AJ (1995) Seasonal succession and the strength of intra- and interspecific competition in a Daphnia assemblage. Ecology 76:2278–2294CrossRefGoogle Scholar
  30. Ishida S, Iwasaki K (2003) Reduced byssal thread production and movement by the intertidal mussel Hormomya mutabilis in response to effluent from predators. J Ethol 21:117–122Google Scholar
  31. Lachance AA, Myrand B, Tremblay R, Koutitonsky V, Carrington E (2008) Biotic and abiotic influences on the attachment strength of blue mussels (Mytilus edulis) from suspended culture. Aquat Biol 2:119–129CrossRefGoogle Scholar
  32. Leicht-Young SA, Silander JA Jr, Latimer AM (2007) Comparative performance of invasive and native Celastrus species across environmental gradients. Oecologia 154:273–282CrossRefPubMedGoogle Scholar
  33. Levins R (1968) Evolution in changing environments. Princeton University Press, PrincetonGoogle Scholar
  34. Lucas JM, Vaccaro E, Waite JH (2002) A molecular, morphometric and mechanical comparison of the structural elements of byssus from Mytilus edulis and Mytilus galloprovincialis. J Exp Biol 205:1807–1817PubMedGoogle Scholar
  35. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  36. Marshall DJ, McQuaid CD (1989) The influence of the respiratory response on the tolerance to sand inundation of the limpets Patella granularis (L) (Prosobranchia) and Siphonaria capensis (Q et G) (Pulmonata). J Exp Mar Biol Ecol 129:191–201CrossRefGoogle Scholar
  37. 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
  38. Melbourne BA, Cornell HA, Davies KF, Dugaw CJ, Elmendorf S, Freestone AL, Hall RJ, Harrison S, Hastings A, Holland M, Holyoak M, Lambrinos J, Moore K, Yokomizo H (2007) Invasion in a heterogeneous world: resistance, coexistence or hostile takeover? Ecol Lett 10:77–94CrossRefPubMedGoogle Scholar
  39. Moeser GM, Carrington E (2006) Seasonal variation in mussel byssal thread mechanics. J Exp Biol 209:1996–2003CrossRefPubMedGoogle Scholar
  40. Moeser GM, Leba H, Carrington E (2006) Seasonal influence of wave action on thread production in Mytilus edulis. J Exp Biol 209:881–890CrossRefPubMedGoogle Scholar
  41. Nicastro KR, Zardi GI, McQuaid CD, Teske PR, Barker NP (2008) Coastal topography drives genetic structure in marine mussels. Mar Ecol Prog Ser 368:189–195CrossRefGoogle Scholar
  42. Paine RT, Levin SA (1981) Intertidal landscapes: disturbance and the dynamics of pattern. Ecol Monogr 51:145–178CrossRefGoogle Scholar
  43. Petes LE, Menge BA, Murphy GD (2007) Environmental stress decreases survival, growth, and reproduction in New Zealand mussels. J Exp Mar Biol Ecol 351:83–91CrossRefGoogle Scholar
  44. Petraitis PS, Latham RE, Niesenbaum RA (1989) The maintenance of species diversity by disturbance. Q Rev Biol 64:393–418CrossRefGoogle Scholar
  45. Pranovi F, Franceschini G, Casale M, Zucchetta M, Torricelli P, Giovanardi O (2006) An ecological imbalance induced by a non-native species: the Manila clam in the Venice Lagoon. Biol Inv 8:595–609CrossRefGoogle Scholar
  46. Robinson TB, Griffiths CL, McQuaid CD, Rius M (2005) Marine alien species of South Africa—status and impacts. S Afr J Mar Sci 27:297–306Google Scholar
  47. Sapolsky RM (1992) Neuroendocrinology of the stress response. In: Becker JB, Breedlove SM, Crews D (eds) Behavioral endocrinology. Massachusetts Institute of Technology Press, Cambridge, pp 287–324Google Scholar
  48. Seed R, Suchanek TH (1992) Population and community ecology of Mytilus. In: Gosling EG (ed) The mussel Mytilus: ecology, physiology, genetics and culture. Elsevier, NewYork, pp 87–169Google Scholar
  49. Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176CrossRefGoogle Scholar
  50. Sheley RL, Olson BE, Larson LL (1997) Effect of weed seed rate and grass defoliation level on diffuse knapweed. J Range Manage 50:39–43CrossRefGoogle Scholar
  51. Sousa WP (2001) Natural disturbance and the dynamics of marine benthic communities. In: Bertness MD, Gaines S, Hay ME (eds) Marine community ecology. Sinauer Assoc., Sunderland, pp 85–130Google Scholar
  52. Steffani CN, Branch GM (2003) Growth rate, condition, and shell shape of Mytilus galloprovincialis: responces to wave exposure. Mar Ecol Prog Ser 246:197–209CrossRefGoogle Scholar
  53. Tolman HL (1999) User manual and system documentation of WAVEWATCH-III version 1.18. NOAA/NWS/NCEO/OMB tecnical note 166, pp 110Google Scholar
  54. 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
  55. von der Meden CEO, Porro F, Erlandsson J, McQuaid CD (2008) Coastline topography affects the distribution of indigenous and invasive mussels. Mar Ecol Prog Ser 372:135–145CrossRefGoogle Scholar
  56. Wilson JB (1984) The intermediate disturbance hypothesis of species coexistence is based on patch dynamics. N Zeal J Ecol 18:176–181Google Scholar
  57. Zardi GI, Nicastro KR, McQuaid CD, Rius M, Porri F (2006a) Hydrodynamic stress and habitat partitioning between indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussels: constraints of an evolutionary strategy. Mar Biol 150:78–88CrossRefGoogle Scholar
  58. Zardi GI, Nicastro KR, Porri F, McQuaid CD (2006b) 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
  59. Zardi GI, McQuaid CD, Nicastro KR (2007) Balancing survival and reproduction: seasonality of wave action, attachment strength and reproductive output in indigenous Perna perna and invasive Mytilus galloprovincialis mussels. Mar Ecol Prog Ser 334:155–163CrossRefGoogle Scholar
  60. Zardi GI, Nicastro KR, McQuaid CD, Erlansson J (2008) Sand and wave induced mortality in invasive (Mytilus galloprovincialis) and indigenous (Perna perna) mussels. Mar Biol 153:853–858CrossRefGoogle Scholar
  61. Zardi GI, Nicastro KR, McQuaid CD, Gektidis M (2009) Effects of endolithic parasitism on invasive and indigenous mussels in a variable physical environment. PloS ONE 4:e6560CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • K. R. Nicastro
    • 1
    • 2
  • G. I. Zardi
    • 1
    • 2
  • C. D. McQuaid
    • 1
  1. 1.Department of Zoology & EntomologyRhodes UniversityGrahamstownSouth Africa
  2. 2.CCMAR-CIMAR, Center of Marine SciencesUniversidade do AlgarveFaroPortugal

Personalised recommendations