Advertisement

Marine Biology

, Volume 159, Issue 4, pp 863–872 | Cite as

Shell ecophenotype in the blue mussel (Mytilus edulis) determines the spatial pattern in foraging behaviour of an oystercatcher (Haematopus ostralegus) population

  • Alexandra ZieritzEmail author
  • Gemma Clucas
  • Lauren Axtmann
  • David C. Aldridge
Original Paper

Abstract

When feeding on blue mussels (Mytilus edulis), oystercatchers (Haematopus ostralegus) either stab into the mollusc’s gaping valves or hammer through its dorsal or ventral shell. Whilst the selectivity of hammering and stabbing oystercatchers for specific prey morphologies has been well studied, the way in which the effects of environment on M. edulis morphology can in turn affect feeding methods of H. ostralegus is very poorly understood. Based on morphological analyses on randomly selected shells from three intertidal zones, this study failed to detect differences in morphology or distribution of dorsally and ventrally hammered shells but confirms the finding of previous authors that hammering oystercatchers select thinner mussels than stabbing birds. Additionally, we show that this difference in optimal prey morphology can lead to spatial patterns in oystercatcher feeding behaviour. Whilst at the low intertidal and higher mid intertidal zones, characterised by comparatively thick shells, most empty shells had apparently been stabbed, hammering was the dominant feeding behaviour at the lower mid intertidal zone, where shells were thinner. Preference of hammering birds for smaller mussels was not ubiquitous. Sagittal shell shape was predominantly influenced by allometric growth effects and had only minor effect on prey selection. All oystercatchers preferred less inflated mussels, with the degree of shell inflation gradually increasing with higher intertidal elevation. Our results illustrate the importance of small-scale patterns in prey ecophenotypes in determining the distribution and feeding dynamics of wading birds.

Keywords

Shell Thickness Intertidal Zone Allometric Growth Feeding Type Optimal Forage Theory 
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.

Notes

Acknowledgments

We would like to thank two anonymous reviewers for their helpful comments that greatly improved the manuscript. The recently closed Wells Field Study Centre provided a much valued base and resource for this study. Its closure represents the loss of an important facility for the study of marine biology.

References

  1. 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 219:177–188CrossRefGoogle Scholar
  2. Beadman HA, Caldow RWG, Kaiser MJ, Willows RI (2003) How to toughen up your mussels: using mussel shell morphological plasticity to reduce predation losses. Mar Biol 142:487–494Google Scholar
  3. Buschbaum C, Saier B (2001) Growth of the mussel Mytilus edulis L. in the Wadden sea affected by tidal emergence and barnacle epibionts. J Sea Res 45:27–36CrossRefGoogle Scholar
  4. Crampton JS, Haines AJ (1996) Users’ manual for programs HANGLE, HMATCH and HCURVE for the Fourier shape analysis of two-dimensional outlines. Inst Geol Nucl Sci Sci Rep 96(37):1–28Google Scholar
  5. Crawley MJ (2002) Statistical computing, an introduction to data analysis using S-plus. John Wiley and Sons Ltd, ChichesterGoogle Scholar
  6. Durell SEA Le V Dit, Goss-Custard JD (1984) Prey selection within a size-class of mussels, Mytilus edulis, by oystercatchers, Haematopus ostralegus. Anim Behav 32:1197–1203CrossRefGoogle Scholar
  7. Ens BJ (1982) Size selection in mussel-feeding oystercatchers. Wader Study Group Bull 34:16–20Google Scholar
  8. Goss-Custard JD, Sutherland WJ (1984) Feeding specializations in oystercatchers Haematopus ostralegus. Anim Behav 32:299–301CrossRefGoogle Scholar
  9. Goss-Custard JD, Durell SEA Le V Dit, Mc Grorty S, Reading CJ, Clarke RT (1981) Factors affecting the occupation of mussel (Mytilus edulis) beds by oystercatchers (Haematopus ostralegus) on the Exe estuary, Devon. In: Jones NV, Wolff WJ (eds) Feeding and survival strategies of estuarine organisms. Plenum Press, London, pp 217–230CrossRefGoogle Scholar
  10. Goss-Custard JD, West AD, Durell SEA Le V Dit (1993) The availability and quality of the mussel prey (Mytilus edulis) of oystercatchers (Haematopus ostralegus). Neth J Sea Res 31:419–439CrossRefGoogle Scholar
  11. Goss-Custard JD, West AD, Sutherland WJ (1996) Where to feed. In: Goss-Custard JD (ed) The oystercatcher: from individuals to populations. Oxford Ornithology Series. Oxford University Press, Oxford, pp 105–132Google Scholar
  12. Goss-Custard JD, Clarke RT, McGrorty S, Nagarajan R, Sitters HP, West AD (2002) Beware of these errors when measuring intake rates in waders. Wader Study Group Bull 98:30–37Google Scholar
  13. Griffiths RJ (1981) Aerial exposure and energy balance in littoral and sublittoral Choromytilus meridionalis (Kr.) (Bivalvia). J Exp Mar Biol Ecol 52:231–241CrossRefGoogle Scholar
  14. Hammer Ø, Harper DAT (2006) PAST version 1.57. Natural History Museum, University of Oslo, Norway. http://folk.uio.no/ohammer/past/. Accessed 1 Dec 2010
  15. Heppleston PB (1971) Feeding techniques of the oystercatcher. Bird Study 18:15–20CrossRefGoogle Scholar
  16. Hoffman JI, Peck LS, Hillyard G, Zieritz A, Clark MS (2010) No evidence for genetic differentiation between Antarctic limpet Nacella concinna morphotypes. Mar Biol 157:765–778CrossRefGoogle Scholar
  17. Hulscher JB (1988) Mussel Mytilus edulis kills oystercatcher Haematopus ostralegus. Limosa 61:42–45Google Scholar
  18. Hulscher JB (1996) Food and feeding behaviour. In: Goss-Custard JD (ed) The oystercatcher: from individuals to populations. Oxford Ornithology Series. Oxford University Press, Oxford, pp 7–29Google Scholar
  19. Innes DJ, Bates JA (1999) Morphological variation of Mytilus edulis and Mytilus trossulus in eastern Newfoundland. Mar Biol 133:691–699CrossRefGoogle Scholar
  20. Krapivka S, Toro JE, Alcapan AC, Astorga M, Presa P, Perez M, Guinez R (2007) Shell-shape variation along the latitudinal range of the Chilean blue mussel Mytilus chilensis (Hupe 1854). Aquac Res 38:1770–1777CrossRefGoogle Scholar
  21. Krebs JR (1978) Optimal foraging: decision rules for predators. In: Krebs JR, Davies NB (eds) Behavioural ecology, an evolutionary approach. Blackwell Scientific Publications, Oxford, pp 23–63Google Scholar
  22. MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609CrossRefGoogle Scholar
  23. Meire PM (1996) Using optimal foraging theory to determine the density of mussels Mytilus edulis that can be harvested by hammering oystercatchers Haematopus ostralegus. Ardea 84A:141–152Google Scholar
  24. Mitton JB, Koehn RK (1985) Shell shape variation in the Blue Mussel, Mytilus edulis L., and its association with enzyme heterozygosity. J Exp Mar Biol Ecol 90:73–80CrossRefGoogle Scholar
  25. Nagarajan R, Goss-Custard JD, Lea SEG (2002a) Oystercatchers use colour preference to achieve longer-term optimality. Proc R Soc Lond B Biol Sci 269:523–528CrossRefGoogle Scholar
  26. Nagarajan R, Lea SEG, Goss-Custard JD (2002b) Reevaluation of patterns of mussel (Mytilus edulis) selection by European oystercatchers (Haematopus ostralegus). Can J Zool 80:846–853CrossRefGoogle Scholar
  27. Norton-Griffiths M (1967) Some ecological aspects of the feeding behaviour of the oystercatcher Haematopus ostralegus on the edible mussel Mytilus edulis. Ibis 109:412–424CrossRefGoogle Scholar
  28. Reimer O, Tedengren M (1996) Phenotypical improvement of morphological defences in the mussel Mytilus edulis induced by exposure to the predator Asterias rubens. Oikos 75:383–390CrossRefGoogle Scholar
  29. Rutten AL, Oosterbeek K, Ens BJ, Verhulst S (2006) Optimal foraging on perilous prey: risk of bill damage reduces optimal prey size in oystercatchers. Behav Ecol 17:297–302CrossRefGoogle Scholar
  30. Seed R (1968) Factors influencing shell shape in the mussel Mytilus edulis. J Mar Biol Assoc UK 48:561–584CrossRefGoogle Scholar
  31. Seed R (1976) Ecology. In: Bayne BL (ed) Marine mussels: their ecology and physiology. Cambridge University Press, London, pp 13–65Google Scholar
  32. Smith LD, Jennings JA (2000) Induced defensive responses by the bivalve Mytilus edulis to predators with different attack modes. Mar Biol 136:461–469CrossRefGoogle Scholar
  33. Stanley SM (1970) Relation of shell form to life habits in the Bivalvia (Mollusca). Mem Geol Soc Am 125:1–296Google Scholar
  34. Stanley SM (1972) Functional morphology and evolution of byssally attached bivalve mollusks. J Paleontol 46:165–212Google Scholar
  35. Stanley SM (1975) Adaptive themes in the evolution of the Bivalvia (Mollusca). Annu Rev Earth Planet Sci 3:361–385CrossRefGoogle Scholar
  36. Stirling HP, Okumus I (1994) Growth, mortality and shell morphology of cultivated mussel (Mytilus edulis) stocks cross-planted between two Scottish sea lochs. Mar Biol 119:115–123CrossRefGoogle Scholar
  37. Sutherland WJ, Ens BJ (1987) The criteria determining the selection of mussels Mytilus edulis by oystercatchers Haematopus ostralegus. Behaviour 103:187–202CrossRefGoogle Scholar
  38. Sutherland WJ, Ens BJ, Goss-Custard JD, Hulscher JB (1996) Specialization. In: Goss-Custard JD (ed) The oystercatcher: from individuals to populations. Oxford Ornithology Series. Oxford University Press, Oxford, pp 56–76Google Scholar
  39. Wanink JH, Zwarts L (1993) Environmental effects on the growth rate of intertidal invertebrates and some implications for foraging waders. Neth J Sea Res 31:407–418CrossRefGoogle Scholar
  40. Wilson AM, Vickery JA, Brown A, Langston RHW, Smallshire D, Wotton S, Vanhinsbergh D (2005) Changes in the numbers of breeding waders on lowland wet grasslands in England and Wales between 1982 and 2002. Bird Study 52:55–69CrossRefGoogle Scholar
  41. Zieritz A, Aldridge DC (2009) Identification of ecophenotypic trends within three European freshwater mussel species (Bivalvia: Unionoida) using traditional and modern morphometric techniques. Biol J Linn Soc 98:814–825CrossRefGoogle Scholar
  42. Zieritz A, Hoffman JI, Amos W, Aldridge DC (2010) Phenotypic plasticity and genetic isolation-by-distance in the freshwater mussel Unio pictorum (Mollusca: Unionoida). Evol Ecol 24:923–938CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Alexandra Zieritz
    • 1
    • 2
    Email author
  • Gemma Clucas
    • 1
  • Lauren Axtmann
    • 1
  • David C. Aldridge
    • 1
  1. 1.Department of ZoologyUniversity of CambridgeCambridgeUK
  2. 2.Unit of Aquatic Systems BiologyTechnische Universität MünchenFreisingGermany

Personalised recommendations