Marine Biology

, Volume 160, Issue 6, pp 1489–1496 | Cite as

The effect of water temperature on drilling and ingestion rates of the dogwhelk Nucella lapillus feeding on Mytilus edulis mussels in the laboratory

Original Paper

Abstract

In highly seasonal intertidal habitats, changes in temperature through the year may drive substantial shifts in feeding and growth rates of organisms. For the dogwhelk Nucella lapillus, attacking and consuming Mytilus edulis mussels can take hours or days, depending on temperature. Handling time of dogwhelks feeding on mussels is therefore greatly affected by ocean temperature. I recorded attack time in the laboratory, partitioned into drilling and consumption time, for juvenile dogwhelks across a range of seawater temperatures representative of field seawater temperatures during the main growing seasons of summer and autumn. The combined length of a drilling attack and subsequent ingestion time tripled across the 10 °C decline in water temperatures from July through November, driven primarily by an increase in ingestion time. The observed reduction in handling time, coupled with projected sea surface warming in New England by the end of the twenty-first century, could extend the length of the growing season for Nucella and subsequently have cascading effects on the prey community.

Supplementary material

227_2013_2202_MOESM1_ESM.pdf (267 kb)
Supplementary material 1 (PDF 266 kb)
227_2013_2202_MOESM2_ESM.docx (22 kb)
Supplementary material 2 (DOCX 22 kb)

References

  1. Audacity Development Team (2010) Audacity 1.3beta. http://audacity.sourceforge.net/
  2. Bayne BL, Scullard C (1978) Rates of feeding by Thais (Nucella) lapillus (L.). J Exp Mar Biol Ecol 32:113–129CrossRefGoogle Scholar
  3. Brown KM, Stickle WB (2002) Physical constraints on the foraging ecology of a predatory snail. Mar Freshw Behav Physiol 35(3):157–166CrossRefGoogle Scholar
  4. Burrows MT, Hughes RN (1989) Natural foraging of the dogwhelk, Nucella lapillus (Linnaeus)—the weather and whether to feed. J Molluscan Stud 55(2):285–295CrossRefGoogle Scholar
  5. Burrows MT, Hughes RN (1990) Variation in growth and consumption among individuals and populations of dogwhelks, Nucella lapillus—a link between foraging behavior and fitness. J Anim Ecol 59(2):723–742CrossRefGoogle Scholar
  6. Burrows MT, Hughes RN (1991) Variation in foraging behavior among individuals and populations of dogwhelks, Nucella lapillus—natural constraints on energy intake. J Anim Ecol 60(2):497–514CrossRefGoogle Scholar
  7. Carriker MR (1981) Shell penetration and feeding by naticacean and muricacean predatory gastropods: a synthesis. Malacologia 20:403–422Google Scholar
  8. Chétail M, Fournié J (1969) Shell-boring mechanism of the gastropod, Purpura (Thais) lapillus: a physiological demonstration of the role of carbonic anhydrase in the dissolution of CaCO3. Am Zool 9(3):983–990. doi:10.1093/icb/9.3.983 Google Scholar
  9. Connell JH (1961) Effects of competition, predation by Thais lapillus, and other factors on natural populations of the barnacle Balanus balanoides. Ecol Monogr 31(1):61–104CrossRefGoogle Scholar
  10. Denny MW, Hunt LJH, Miller LP, Harley CDG (2009) On the prediction of extreme ecological events. Ecol Monogr 79(3):397–421. doi:10.1890/08-0579.1 CrossRefGoogle Scholar
  11. Etter RJ (1989) Life history variation in the intertidal snail Nucella lapillus across a wave-exposure gradient. Ecology 70(6):1857–1876CrossRefGoogle Scholar
  12. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65(3):414–432CrossRefGoogle Scholar
  13. Feare CJ (1970) Aspects of the ecology of an exposed shore population of dogwhelks Nucella lapillus (L.). Oecologia 5:1–18CrossRefGoogle Scholar
  14. Fisher JAD, Rhile EC, Liu H, Petraitis PS (2009) An intertidal snail shows a dramatic size increase over the past century. Proc Natl Acad Sci USA 106(13):5209–5212. doi:10.1073/pnas.0812137106 CrossRefGoogle Scholar
  15. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. SAGE Publications, Thousand OaksGoogle Scholar
  16. Freeman AS, Byers JE (2006) Divergent induced responses to an invasive predator in marine mussel populations. Science 313:831–833CrossRefGoogle Scholar
  17. Gooding RA, Harley CDG, Tang E (2009) Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. Proc Natl Acad Sci USA 106(23):9316–9321. doi:10.1073/pnas.0811143106 CrossRefGoogle Scholar
  18. Hughes RN, Drewett D (1985) A comparison of the foraging behavior of dogwhelks, Nucella lapillus (L.), feeding on barnacles or mussels on the shore. J Molluscan Stud 51(1):73–77Google Scholar
  19. Hughes RN, Dunkin SB (1984) Behavioural components of prey selection by dogwhelks, Nucella lapillus (L.), feeding on mussels, Mytilus edulis L., in the laboratory. J Exp Mar Biol Ecol 77(1–2):45–68. doi:10.1016/0022-0981(84)90050-9 CrossRefGoogle Scholar
  20. IPCC (2007) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Cambridge University Press, CambridgeGoogle Scholar
  21. IPCC Working Group III (2000) IPCC Special report emissions scenarios. summary for policymakers. intergovernmental panel on climate change. 20 pgsGoogle Scholar
  22. Jones SJ, Mieszkowska N, Wethey DS (2009) Linking thermal tolerances and biogeography: Mytilus edulis (L.) at its southern limit on the east coast of the United States. Biol Bull 217(1):73Google Scholar
  23. Largen MJ (1967) The influence of water temperature upon the life of the dog-whelk Thais lapillus (Gastropoda: Prosobranchia). J Anim Ecol 36(1):207–214CrossRefGoogle Scholar
  24. Lemoine NP, Burkepile DE (2012) Temperature-induced mismatches between consumption and metabolism reduce consumer fitness. Ecology 93(11):2483–2489. doi:10.1890/12-0375.1 CrossRefGoogle Scholar
  25. Matassa CM, Trussell GC (2011) Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects. Ecology 92(12):2258–2266. doi:10.1890/11-0424.1 CrossRefGoogle Scholar
  26. Meehl GA, Covey C, Delworth TL, Latif M, McAvaney B, Mitchell JFB, Stouffer RJ, Taylor KE (2007) The WCRP CMIP3 multimodel dataset. Bull Am Meteorol Soc 88:1383–1394. doi:10.1175/BAMS-88-9-1383 CrossRefGoogle Scholar
  27. Menge BA (1978) Predation intensity in a rocky intertidal community. Effect of an algal canopy, wave action, and desiccation on predator feeding rates. Oecologia 34(4):17–35CrossRefGoogle Scholar
  28. Palmer AR (1990) Effect of crab effluent and scent of damaged conspecifics on feeding, growth, and shell morphology of the Atlantic dogwhelk Nucella lapillus (L.). Hydrobiologia 193:155–182CrossRefGoogle Scholar
  29. Petraitis PS (1992) Effects of body size and water temperature on grazing rates of four intertidal gastropods. Aust J Ecology 17(4):409–414CrossRefGoogle Scholar
  30. Pincebourde S, Sanford E, Helmuth B (2008) Body temperature during low tide alters the feeding performance of a top intertidal predator. Limnol Oceanogr 53(4):1562–1573CrossRefGoogle Scholar
  31. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org/
  32. Rall BC, Vucic-Pestic O, Ehnes RB, Emmerson M, Brose U (2010) Temperature, predator–prey interaction strength and population stability. Glob Change Biol 16(8):2145–2157. doi:10.1111/j.1365-2486.2009.02124.x CrossRefGoogle Scholar
  33. Rasband WS (1997-2013) ImageJ. US National Institutes of Health, Bethesda, Maryland http://rsb.info.nih.gov/ij/
  34. Rovero F, Hughes RN, Chelazzi G (1999a) Effect of experience on predatory behaviour of dogwhelks. Anim Behav 57:1241–1249CrossRefGoogle Scholar
  35. Rovero F, Hughes RN, Chelazzi G (1999b) Automatic recording of the radular activity of dogwhelks (Nucella lapillus) drilling mussels (Mytilus edulis). J Mar Biol Assoc U K 79(6):1079–1083. doi:10.1017/S0025315499001320 CrossRefGoogle Scholar
  36. Sandison EE (1967) Respiratory response to temperature and temperature tolerance of some intertidal gastropods. J Exp Mar Biol Ecol 1:271–281CrossRefGoogle Scholar
  37. Sanford E (2002a) The feeding, growth, and energetics of two rocky intertidal predators (Pisaster ochraceus and Nucella canaliculata) under water temperatures simulating episodic upwelling. J Exp Mar Biol Ecol 273:199–218. doi:10.1016/S0022-0981(02)00164-8 CrossRefGoogle Scholar
  38. Sanford E (2002b) Water temperature, predation, and the neglected role of physiological rate effects in rocky intertidal communities. Integr Comp Biol 42:881–891CrossRefGoogle Scholar
  39. Stickle WB, Bayne BL (1987) Energetics of the muricid gastropod Thais (Nucella) lapillus (L.). J Exp Mar Biol Ecol 107(3):263–278. doi:10.1016/0022-0981(87)90043-8 CrossRefGoogle Scholar
  40. Stickle WB, Moore MN, Bayne BL (1985) Effects of temperature, salinity and aerial exposure on predation and lysosomal stability of the dogwhelk Thais (Nucella) lapillus (L.). J Exp Mar Biol Ecol 93(3):235–258. doi:10.1016/0022-0981(85)90242-4 CrossRefGoogle Scholar
  41. Trussell GC, Ewanchuk PJ, Matassa CM (2006a) Habitat effects on the relative importance of trait-and density-mediated indirect interactions. Ecol Lett 9(11):1245–1252CrossRefGoogle Scholar
  42. Trussell GC, Ewanchuk PJ, Matassa CM (2006b) The fear of being eaten reduces energy transfer in a simple food chain. Ecology 87(12):2979–2984CrossRefGoogle Scholar
  43. Vadas RL, Burrows MT, Hughes RN (1994) Foraging strategies of dogwhelks, Nucella lapillus (L.): interacting effects of age, diet and chemical cues to the threat of predation. Oecologia 100(4):439–450. doi:10.1007/bf00317866 CrossRefGoogle Scholar
  44. Welch WR (1968) Changes in abundance of the green crab, Carcinus maenas (L.), in relation to recent temperature changes. Fish Bull 67(2):337–345Google Scholar
  45. Widdows J, Bayne BL (1971) Temperature acclimation of Mytilus edulis with reference to its energy budget. J Mar Biol Assoc UK 51:827–843CrossRefGoogle Scholar
  46. Yamane L, Gilman SE (2009) Opposite responses by an intertidal predator to increasing aquatic and aerial temperatures. Mar Ecol Prog Ser 393:27–36. doi:10.3354/meps08276 CrossRefGoogle Scholar
  47. Yee EH, Murray SN (2004) Effects of temperature on activity, food consumption rates, and gut passage times of seaweed-eating Tegula species (Trochidae) from California. Mar Biol 145:895–903. doi:10.1007/s00227-004-1379-6 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Marine Science CenterNortheastern UniversityNahantUSA
  2. 2.Hopkins Marine StationStanford UniversityPacific GroveUSA

Personalised recommendations