Marine Biology

, Volume 156, Issue 10, pp 1993–2000 | Cite as

Patterns of shell repair in articulate brachiopods indicate size constitutes a refuge from predation

  • Elizabeth M. Harper
  • Lloyd S. Peck
  • Katharine R. Hendry
Original Paper

Abstract

The cost of overcoming prey defenses relative to the value of internal tissues is a key criterion in predator/prey interactions. Optimal foraging theory predicts: (1) specific sizes of prey will result in the best returns to predators, and (2) there will often be a size at which the cost/benefit balance is low enough to effectively exclude predation. Data presented here on styles of repaired shell damage and size at which injury had been sustained was collected from samples of terebratulide brachiopods from the Antarctic Peninisula (Liothyrella uva), Falkland Islands (Magellania venosa and Terebratella dorsata) and Chile (M. venosa). The predominant form of damage on shells was indicative of predators attacking the valve margins. The modal size for repaired damage was more than 10 mm smaller than the modal size for the overall size distribution in each species and there were no repaired attacks in the largest size classes of any species. These data suggest that size forms a refuge from predation, as would be predicted by optimal foraging theory. The optimal sizes that predators appeared to attack vary between species, as do the sizes that provided a refuge from predation. High levels of multiple repairs (19% of the M. venosa population from the Falkland Islands sampled had 2 or more repairs) suggest that the mortality following attack is low, suggesting that many predators abandon their attacks.

References

  1. Abrams PA (2000) The evolution of predator-prey interactions: theory and evidence. Annu Rev Eco Evol Syst 31:79–105CrossRefGoogle Scholar
  2. Alexander RR (1981) Predation scars preserved in Chesterian brachiopods: probable culprits and evolutionary consequences for the articulates. J Paleontol 55:192–203Google Scholar
  3. Alexander RR (1986a) Resistance to and repair of shell breakage induced by durophages in Late Ordovician brachiopods. J Paleontol 60:273–285Google Scholar
  4. Alexander RR (1986b) Frequency of sublethal shell-breakage in articulate brachiopod assemblages through geologic time. Biostratigraphie du Paléozoique 4:150–166Google Scholar
  5. Alexander RR, Dietl GP (2001) Shell repair frequency in New Jersey bivalves: a recent baseline for tests of escalation with Tertiary Mid-Atlantic congeners. Palaios 16:354–371Google Scholar
  6. Alexander RR, Dietl GP (2003) The fossil record of shell-breaking predation on marine bivalves and gastropods. In: Kelley PH, Kowalewski M, Hansen TA (eds) Predator–prey interactions in the fossil record. Kluwer, New York, pp 141–176Google Scholar
  7. Aronson RB, Thatje S, Clarke A, Peck LS, Blake DB, Wilga CD, Seibel BA (2007) Climate change and invisibility of the Antarctic benthos. Annu Rev Ecol Evol Syst 38:129–154CrossRefGoogle Scholar
  8. Brey T, Peck LS, Gutt T, Hain S, Arntz W (1995) Population dynamics of Magellania fragilis, a brachiopod dominating a mixed-bottom macrobenthic assemblage on the Antarctic shelf. J Mar Biol Assoc UK 75:857–870CrossRefGoogle Scholar
  9. Brown KM, Fraser KPP, Barnes DKA, Peck LS (2004) Ice scour frequency dictates Antarctic shallow-water community structure. Oecologia 141:121–129PubMedCrossRefGoogle Scholar
  10. Cadée GC (1999) Shell damage and shell repair in the Antarctic limpet Nacella concinna from King George Island. J Sea Res 41:149–161CrossRefGoogle Scholar
  11. Checa A (1993) Non-predatory shell damage in recent deep endobenthic bivalves from Spain. Palaeogeogr Palaeoclimatol Palaeoecol 100:309–331CrossRefGoogle Scholar
  12. Cintra-Buenrostro CE (2007) Trampling, peeling and nibbling mussels: an experimental assessment of mechanical and predatory damage to shells of Mytilus trossulus (Mollusca: Mytilidae). J Shellfish Res 26:221–231CrossRefGoogle Scholar
  13. Clarke A, Aronson RB, Crame JA, Gili J, Blake DB (2004) Evolution and diversity of the benthic fauna of the Southern Ocean continental shelf. Antarct Sci 16:559–568CrossRefGoogle Scholar
  14. Delance JH, Emig CC (2004) Drilling predation on Gryphus vitreus (Brachiopoda) off the French Mediterranean coasts. Palaeogeogr Palaeoclimatol Palaeoecol 208:23–30CrossRefGoogle Scholar
  15. Dietl GP, Alexander RR (2005) High frequency and severity of breakage-induced shell repair in western Atlantic Pinnidae (Bivalvia). J Molluscan Stud 71:307–311CrossRefGoogle Scholar
  16. Dietl GP, Alexander RR, Bien WF (2000) Escalation in late Cretaceous-early Paleocene oysters (Gryphaeidae) from the Atlantic Coastal Plain. Paleobiology 26:215–237CrossRefGoogle Scholar
  17. Elner RW, Hughes RN (1978) Energy maximisation in the diet of the shore crab Carcinus maenas. J Anim Ecol 47:103–116CrossRefGoogle Scholar
  18. Elner RW, Lavoie RE (1983) Predation on American oysters (Crassostrea virginica [Gmelin]) by American lobsters (Homarus americanus Milne Edwards), Rock crabs (Cancer irroratus Say) and Mud crabs (Neopanope sayi [Smith]). J Shellfish Res 3:129–134Google Scholar
  19. Gaspar MB, Richardson CA, Monteiro CC (1994) The effects of dredging on the shell formation of the razor clam Ensis siliqua from Barrina, southern Portugal. J Mar Biol Assoc UK 74:927–938Google Scholar
  20. Geary DW, Allmon WD, Reakokudk MJ (1991) Stomatopod predation on fossil gastropods from the Plio-Pleistocene of Florida. J Paleontol 65:355–360Google Scholar
  21. Griffiths AM, Gosselin LA (2008) Ontogenetic shift in susceptibility to predators in juvenile northern abalone, Haliotis kamtschatkana. J Exp Mar Biol Ecol 360:85–93CrossRefGoogle Scholar
  22. Harper EM (2005) Evidence of predation damage in Pliocene Apletosia maxima (Brachiopoda). Palaeontology 48:197–208CrossRefGoogle Scholar
  23. Harper EM, Peck LS (2003) Predatory behaviour and metabolic costs in the Antarctic muricid gastropod Trophon longstaffi. Polar Biol 26:208–217Google Scholar
  24. Hughes RN (1980) Optimal foraging theory in the marine context. Oceanogr Mar Biol Annu Rev 18:423–481Google Scholar
  25. Hughes RN, Seed R (1995) Behavioural mechanisms of prey selection in crabs. J Exp Mar Biol Ecol 193:225–238CrossRefGoogle Scholar
  26. James MA, Ansell AD, Collins MJ, Curry GB, Peck LS, Rhodes MC (1992) Recent advances in the study of living brachiopods. Adv Mar Biol Rev 28:175–387CrossRefGoogle Scholar
  27. Kowalewski M (2002) The fossil record of predation: an overview of analytical methods. Paleontol Soc Paper 8:3–42Google Scholar
  28. Kowalewski M, Flessa KW, Marcot JD (1997) Predatory scars in the shells of a recent lingulid brachiopod: paleontological and ecological implications. Acta Pal Pol 42:497–532Google Scholar
  29. Kowalewski M, Hoffmeister AP, Baumiller TK, Bambach RK (2005) Secondary evolutionary escalation between brachiopods and enemies of other prey. Science 308:1774–1777PubMedCrossRefGoogle Scholar
  30. Lau CJ (1987) Feeding behaviour of the Hawaiian slipper lobster (Scyllarides squammosus) with a review of decapod crustacean feeding tactics on molluscan prey. Bull Mar Sci 41:378–391Google Scholar
  31. Lee DE (1978) Aspects of the ecology and paleoecology of the brachiopod Notosaria nigricans (Sowerby). J Roy Soc NZ 8:395–417Google Scholar
  32. Leighton LR (2002) Inferring predation intensity in the marine fossil record. Paleobiology 28:328–342CrossRefGoogle Scholar
  33. Mahon AR, Amsler CD, McClintock JB, Amsler AO, Baker BJ (2003) Tissue-specific palatability and chemical defenses against macropredators and pathogens in the common articulate brachiopod Liothyrella uva from the Antarctic Peninsula. J Exp Mar Biol Ecol 290:197–210CrossRefGoogle Scholar
  34. McClintock JB, Slattery M, Thayer CW (1993) Energy content and chemical defence of the articulate brachiopod Liothyrella uva (Jackson, 1912) from the Antarctic Peninsula. J Exp Mar Biol Ecol 169:103–116CrossRefGoogle Scholar
  35. Morton B, Harper EM (2008) Predation upon Mytilus galloprovincialis (Bivalvia: Mytilidae) by juvenile Carcinus maenas (Crustacea: Decapoda) using mandibular chipping. J Mar Biol Assoc UK 88:563–568CrossRefGoogle Scholar
  36. Norton SF (1988) Role of the gastropod shell and operculum in inhibiting predation by fishes. Science 241:92–94PubMedCrossRefGoogle Scholar
  37. Paine RT (1969) Growth and size distribution of the brachiopod Terebratalia transversa Sowerby. Pacific Sci 13:337–343Google Scholar
  38. Paine RT (1976) Size-limited predation: an observational and experimental approach with the Mytilus: Pisaster interaction. Ecology 57:858–873CrossRefGoogle Scholar
  39. Palmer AR (1992) Calcification in marine molluscs: how costly is it? Proc Nat Acad Sci USA 89:1379–1382PubMedCrossRefGoogle Scholar
  40. Peck LS (1993) The tissues of articulate brachiopods and their value to predators. Phil Trans Roy Soc Lond B 339:17–32CrossRefGoogle Scholar
  41. Peck LS (2001) Ecology of articulates In Carlson S, Sandy M (eds) Short course on brachiopods. Geol Soc of the USA, University of Kansas, pp 171–184Google Scholar
  42. Peck LS, Brey T (1996) Radiocarbon bomb signals verify biennial growth bands in the shells of 50 year old brachiopods from Antarctica. Nature 380:206–207CrossRefGoogle Scholar
  43. Peck LS, Clarke A, Holmes LJ (1987) Size, shape and the distribution of organic matter in the Antarctic brachiopod Liothyrella uva. Lethaia 20:33–40CrossRefGoogle Scholar
  44. Peck LS, Brockington S, Brey T (1997) Growth and metabolism in the Antarctic brachiopod Liothyrella uva. Philos Trans Roy Soc B 352:851–858CrossRefGoogle Scholar
  45. Peck LS, Brockington S, Van Hove S, Beghyn M (1999) Community recovery following catastrophic iceberg impacts in Antarctica. Mar Ecol Prog Ser 186:1–8CrossRefGoogle Scholar
  46. Pennings SC (1990) Predator-prey interactions in opisthobranch gastropods—effects of prey body size and habitat complexity. Mar Ecol Prog Ser 82:95–101CrossRefGoogle Scholar
  47. Raffaelli DG (1978) The relationship between shell injuries, shell thickness and habitat characteristics of the intertidal snail Littorina rudis Maton. J Molluscan Stud 44:166–170Google Scholar
  48. Ramsay K, Richardson CA, Kaiser MJ (2001) Causes of shell scarring in dog cockles Glycymeris glycymeris L. J Sea Res 45:131–139CrossRefGoogle Scholar
  49. Seed R (1990) Predator–prey relationships between the swimming crab Thalamita danae Stimpson (Deacpoda: Portunidae) and the mussels Perna viridis (L.) and Brachidontes variabilis (Krauss). In: Morton B (ed) The marine flora and fauna of Hong Kong and Southern China III. Proceedings of the third international workshop on the marine flora and fauna of Hong Kong and Southern China, Hong Kong 1986. Hong Kong University Press, Hong Kong, pp 993–1013Google Scholar
  50. Shanks AL, Wright WG (1986) Adding teeth to wave action: the destructive effects of wave-borne rocks on intertidal organisms. Oecologia 69:420–428CrossRefGoogle Scholar
  51. Sommer U, Meusel B, Stielau C (1999) An experimental analysis of the importance of body-size in the seastar–mussel predator–prey relationship. Acta Oecologia 20:81–86CrossRefGoogle Scholar
  52. Stanley SM (1974) What has happened to the articulate brachiopods? Geol Soc Amer Abstr Prog 6:966–967Google Scholar
  53. Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, PrincetonGoogle Scholar
  54. Taylor DL (2003) Size-dependent predation on post-settlement winter flounder Pseudopleuronectes americanus by the sand shrimp Crangon septemspinosa. Mar Ecol Prog Ser 263:197–215CrossRefGoogle Scholar
  55. Thayer CW (1985) Brachiopods versus mussels: competition, predation and palatability. Science 228:1527–1528PubMedCrossRefGoogle Scholar
  56. Thayer CW, Allmon R (1990) Unpalatable thecideid brachiopods from Palau: ecological and evolutionary implications. In: MacKinnon DL, Lee DE (eds) Campbell JD Brachiopods through time. Balkema, Rotterdam, pp 253–260Google Scholar
  57. Vermeij GJ (1983) Traces and trends in predation, with special reference to bivalved animals. Palaeontology 26:455–465Google Scholar
  58. Witman JD, Cooper RA (1983) Disturbance and contrasting patterns of population structure in the brachiopod Terebratulina septentrionalis (Couthouy) from two subtidal habitats. J Exp Mar Biol Ecol 73:57–79CrossRefGoogle Scholar
  59. Yamada SB, Boulding EG (1998) Claw morphology, prey size selection and foraging efficiency in generalist and specialist shell-breaking crabs. J Exp Mar Biol Ecol 220:191–211CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Elizabeth M. Harper
    • 1
  • Lloyd S. Peck
    • 2
  • Katharine R. Hendry
    • 1
    • 3
  1. 1.Department of Earth SciencesUniversity of CambridgeCambridgeUK
  2. 2.British Antarctic SurveyNatural Environment Research CouncilCambridgeUK
  3. 3.Department of Earth SciencesUniversity of OxfordOxfordUK

Personalised recommendations