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Effects of predation risk across a latitudinal temperature gradient

  • Community ecology - Original research
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Abstract

The nonconsumptive effects (NCEs) of predators on prey behavior and physiology can influence the structure and function of ecological communities. However, the strength of NCEs should depend on the physiological and environmental contexts in which prey must choose between food and safety. For ectotherms, temperature effects on metabolism and foraging rates may shape these choices, thereby altering NCE strength. We examined NCEs in a rocky intertidal food chain across a latitudinal sea surface temperature gradient within the Gulf of Maine. The NCEs of green crabs (Carcinus maenas) on the foraging, growth, and growth efficiency of prey snails (Nucella lapillus) were consistent across a broad (~8.5 °C) temperature range, even though snails that were transplanted south consumed twice as many mussels (Mytilus edulis) and grew twice as much as snails that were transplanted north. The positive effects of warmer temperatures in the south allowed snails under high risk to perform similarly to or better than snails under low risk at cooler temperatures. Our results suggest that for prey populations residing at temperatures below their thermal optimum, the positive effects of future warming may offset the negative effects of predation risk. Such effects may be favorable to prey populations facing increased predation rates due to warmer temperatures associated with climate change. Attention to the direct and indirect effects of temperature on species interactions should improve our ability to predict the effects of climate change on ecological communities.

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References

  • Abrams PA, Menge BA, Mittelbach GG, Spiller D, Yodzis P (1996) The role of indirect effects in food webs. In: Polis GA, Winemiller K (eds) Food webs: dynamics and structure. Chapman and Hall, New York, pp 371–395

    Chapter  Google Scholar 

  • Angilletta MJ, Dunham AE (2003) The temperature size rule in ectotherms: simple evolutionary explanations may not be general. Am Nat 162:332–342. doi:10.1086/377187

    Article  PubMed  Google Scholar 

  • Angilletta MJ, Wilson RS, Navas CA, James RS (2003) Tradeoffs and the evolution of thermal reaction norms. Trends Ecol Evol 18:234–240. doi:10.1016/S0169-5347(03)00087-9

    Article  Google Scholar 

  • Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509. doi:10.1093/icb/44.6.498

    Article  PubMed  Google Scholar 

  • Bayne BL (1976) Marine mussels, their ecology and physiology. Cambridge University Press, New York

    Google Scholar 

  • Bayne B, Scullard C (1978) Rates of feeding by Thais (Nucella) lapillus (L.). J Exp Mar Biol Ecol 32:113–129. doi:10.1016/0022-0981(78)90110-7

    Article  Google Scholar 

  • Bertness MD, Leonard GH (1997) The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78:1976–1989. doi:10.2307/2265938

    Article  Google Scholar 

  • Bertness M, Trussell G, Ewanchuk PJ, Silliman BR, Crain CM (2004) Consumer-controlled community states on Gulf of Maine rocky shores. Ecology 85:1321–1331. doi:10.1890/02-0636

    Article  Google Scholar 

  • Bolnick D, Preisser EL (2005) Resource competition modifies the strength of trait-mediated predator-prey interactions: a meta-analysis. Ecology 86:2771–2779

    Article  Google Scholar 

  • Boonstra R, Hik D, Singleton GR, Tinnikov A (1998) The impact of predator-induced stress on the snowshoe hare cycle. Ecol Monogr 68:371–394. doi:10.1890/0012-9615(1998)068[0371:TIOPIS]2.0.CO;2

    Article  Google Scholar 

  • Bryson ES, Trussell GC, Ewanchuk PJ (2014) Broad-scale geographic variation in the organization of rocky intertidal communities in the Gulf of Maine. Ecol Monogr. doi:10.1890/13-1106.110.1890/13-1106.1

    Google Scholar 

  • Burrows MT, Hughes RN (1989) Natural foraging of the dogwhelk, Nucella lapillus (Linnaeus); the weather and whether to feed. J Molluscan Stud 55:285–295. doi:10.1093/mollus/55.2.285

    Article  Google Scholar 

  • Burrows MT, Hughes RN (1990) Variation in growth and consumption among individuals and populations of dogwhelks, Nucella lapillus: a link between foraging behaviour and fitness. J Anim Ecol 59:723–742. doi:10.2307/4891

    Article  Google Scholar 

  • Cossins AR, Bowler K (1987) Temperature biology of animals. Chapman and Hall, London

    Book  Google Scholar 

  • Creel S, Christianson D, Liley S, Winnie JA (2007) Predation risk affects reproductive physiology and demography of elk. Science 315:960. doi:10.1126/science.1135918

    Article  CAS  PubMed  Google Scholar 

  • Dahlhoff EP, Buckley BA, Menge BA (2001) Physiology of the rocky intertidal predator Nucella ostrina along an environmental stress gradient. Ecology 82:2816–2829. doi:10.2307/2679963

    Article  Google Scholar 

  • Dell AI, Pawar S, Savage VM (2013) Temperature dependence of trophic interactions are driven by asymmetry of species responses and foraging strategy. J Anim Ecol 83:70–84. doi:10.1111/1365-2656.12081

    Article  PubMed  Google Scholar 

  • Elner RW, Hughes RN (1978) Energy maximization in the diet of the shore crab, Carcinus maenas. J Anim Ecol 47:103–116. doi:10.2307/3925

    Article  Google Scholar 

  • Freeman AS, Hamer CE (2009) The persistent effect of wave exposure on TMIIs and crab predation in Nucella lapillus. J Exp Mar Biol Ecol 372:58–63. doi:10.1016/j.jembe.2009.02.002

    Article  Google Scholar 

  • Frumhoff PC, McCarthy JJ, Melillo JM, Moser SC, Wuebbles DJ (2007) Confronting climate change in the US Northeast. Synthesis Report of the Northeast Climate Impacts Assessment (NECIA). Union of Concerned Scientists, Cambridge, Massachusetts

  • Grosholz ED, Ruiz GM (1996) Predicting the impact of introduced marine species: lessons from the multiple invasions of the European green crab Carcinus maenas. Biol Conserv 78:59–66. doi:10.1016/0006-3207(94)00018-2

    Article  Google Scholar 

  • Hiebenthal C, Philipp EE, Eisenhauer A, Wahl M (2013) Effects of seawater pCO2 and temperature on shell growth, shell stability, condition and cellular stress of Western Baltic Sea Mytilus edulis (L.) and Arctica islandica (L.). Mar Biol 160:2073–2087. doi:10.1007/s00227-012-2080-9

    Article  CAS  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York

    Google Scholar 

  • Houston AI, McNamara JM, Hutchinson JM (1993) General results concerning the trade-off between gaining energy and avoiding predation. Philos Trans R Soc B 341:375–397. doi:10.1098/rstb.1993.0123

    Article  Google Scholar 

  • Hughes RN (1972) Annual production of two Nova Scotian populations of Nucella lapillus (L.). Oecologia 8:356–370. doi:10.1007/BF00367538

    Article  Google Scholar 

  • Iles AC (2014) Towards predicting community level effects of climate: Relative temperature scaling of metabolic and ingestion rates. Ecology 95:2657–2668. doi:10.1890/13-1342.1

    Article  Google Scholar 

  • IPCC Working Group III (2000) IPCC Special Report Emissions Scenarios: Summary for Policymakers IPCC Special Report Emissions Scenarios. Switzerland, Geneva, p 20

    Google Scholar 

  • Jones SJ, Lima FP, Wethey DS (2010) Rising environmental temperatures and biogeography: poleward range contraction of the blue mussel, Mytilus edulis L., in the western Atlantic. J Biogeogr 37:2243–2259. doi:10.1111/j.1365-2699.2010.02386.x

    Article  Google Scholar 

  • Klassen GJ, Locke A (2007) A biological synopsis of the European green crab, Carcinus maenas. Can Manuscr Rep Fish Aquat Sci 2818: vii-75. http://www.dfo-mpo.gc.ca/library/330845.pdf

  • Kordas RL, Harley CD, O’Connor MI (2011) Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. J Exp Mar Biol Ecol 400:218–226. doi:10.1016/j.jembe.2011.02.029

    Article  Google Scholar 

  • Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso JP (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol 19:1884–1896. doi:10.1111/gcb.12179

    Article  Google Scholar 

  • Landes A, Zimmer M (2012) Acidification and warming affect both a calcifying predator and prey, but not their interaction. Mar Ecol Prog Ser 450:1–10. doi:10.3354/meps09666

    Article  Google Scholar 

  • Largen MJ (1967) The influence of water temperature upon the life of the dog-whelk Thais lapillus (Gastropoda: Prosobranchia). J Anim Ecol 36:207–214. doi:10.2307/3022

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640. doi:10.1139/z90-092

    Article  Google Scholar 

  • Luttbeg B, Rowe L, Mangel M (2003) Prey state and experimental design affect relative size of trait- and density-mediated indirect effects. Ecology 84:1140–1150. doi:10.1890/0012-9658(2003)084[1140:PSAEDA]2.0.CO;2

    Article  Google Scholar 

  • Matassa CM (2014) Ecological context shapes the response of consumers to predation risk. PhD Dissertation, Department of Marine and Environmental Sciences, Northeastern University, Boston, Massachusetts, USA. http://hdl.handle.net/2047/d20004941

  • Matassa CM, Trussell GC (2011) Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects. Ecology 92:2258–2266. doi:10.1890/11-0424.1

    Article  PubMed  Google Scholar 

  • Matzelle AJ, Sará G, Montalto V, Zippay M, Trussell GC, Helmuth B (2014) ​A bioenergetics framework for integrating the effects of multiple stressors: opening a ‘black box’ in climate change research. Am Malacol Bull (in press)

  • McNamara JM, Houston AI (1987) Starvation and predation as factors limiting population size. Ecology 68:1515–1519. doi:10.2307/1938669

    Article  Google Scholar 

  • Menge BA (1976) Organization of the New England rocky intertidal community: role of predation, competition, and environmental heterogeneity. Ecol Monogr 46:355–393. doi:10.2307/1942563

    Article  Google Scholar 

  • Menge BA (1978a) Predation intensity in a rocky intertidal community. Effect of an algal canopy, wave action and desiccation on predator feeding rates. Oecologia 34:17–35. doi:10.1007/BF00346238

    Article  Google Scholar 

  • Menge BA (1978b) Predation intensity in a rocky intertidal community. Relation between predator foraging activity and environmental harshness. Oecologia 34:1–16. doi:10.1007/BF00346237

    Article  Google Scholar 

  • Miller LP (2013) The effect of water temperature on drilling and ingestion rates of the dogwhelk Nucella lapillus feeding on Mytilus edulis mussels in the laboratory. Mar Biol 160:1489–1496. doi:10.1007/s00227-013-2202-z

    Article  Google Scholar 

  • Miller LP, Matassa CM, Trussell GC (2014) Climate change enhances the negative effects of predation risk on an intermediate consumer. Glob Change Biol. doi:10.1111/gcb.12639

    Google Scholar 

  • Monaco CJ, Helmuth B (2011) Tipping points, thresholds and the keystone role of physiology in marine climate change research. Adv Mar Biol 60:123–160. doi:10.1016/B978-0-12-385529-9.00003-2

    Article  PubMed  Google Scholar 

  • O’Connor MI (2009) Warming strengthens an herbivore-plant interaction. Ecology 90:388–398. doi:10.1890/08-0034.1

    Article  PubMed  Google Scholar 

  • Palmer AR (1982) Growth in marine gastropods: a non-destructive technique for independently measuring shell and body weight. Malacologia 23:63–74

    Google Scholar 

  • Palmer AR (1992) Calcification in marine molluscs: how costly is it? Proc Natl Acad Sci USA 89:1379–1382

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pauwels K, Stoks R, De Meester L (2005) Coping with predator stress: interclonal differences in induction of heat-shock proteins in the water flea Daphnia magna. J Evol Biol 18:867–872. doi:10.1111/j.1420-9101.2005.00890.x

    Article  CAS  PubMed  Google Scholar 

  • Perrin N (1995) About Berrigan and Charnov’s life-history puzzle. Oikos 73:137–139. doi:10.2307/3545737

    Article  Google Scholar 

  • Pincebourde S, Sanford E, Helmuth B (2008) Body temperature during low tide alters the feeding performance of a top intertidal predator. Limnol Oceanogr 53:1562–1573. doi:10.4319/lo.2008.53.4.1562

    Article  Google Scholar 

  • Queirós AM, Fernandes JA, Faulwetter S, Nunes J, Rastrick SP, Mieszkowska N, Artioli Y, Yool A, Calosi P, Arvanitidis C (2014) Scaling up experimental ocean acidification and warming research: from individuals to the ecosystem. Glob Change Biol. doi:10.1111/gcb.12675

    Google Scholar 

  • R Core Team (2013) R: A language and environment for statistical computing (v. 3.0.2). R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Rall BC et al (2012) Universal temperature and body-mass scaling of feeding rates. Philos Trans R Soc B 367:2923–2934. doi:10.2307/41740019

    Article  Google Scholar 

  • Ripple WJ, Beschta RL (2004) Wolves and the ecology of fear: can predation risk structure ecosystems? Bioscience 54:755–766. doi:10.1641/0006-3568(2004)054[0755:WATEOF]2.0.CO;2

    Article  Google Scholar 

  • Rovero F, Hughes RN, Chelazzi G (1999) Cardiac and behavioural responses of mussels to risk of predation by dogwhelks. Anim Behav 58:707–714. doi:10.1006/anbe.1999.1176

    Article  PubMed  Google Scholar 

  • Sanford E (1999) Regulation of keystone predation by small changes in ocean temperature. Science 283:2095–2097. doi:10.1126/science.283.5410.2095

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sanford E (2002b) Water temperature, predation, and the neglected role of physiological rate effects in rocky intertidal communities. Integr Comp Biol 42:881–891. doi:10.1093/icb/42.4.881

    Article  PubMed  Google Scholar 

  • Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163. doi:10.1111/j.1461-0248.2003.00560.x

    Article  Google Scholar 

  • Schmitz OJ, Hawlena D, Trussell GC (2010) Predator control of ecosystem nutrient dynamics. Ecol Lett 13:1199–1209. doi:10.1111/j.1461-0248.2010.01511.x

    Article  PubMed  Google Scholar 

  • Sih A (1980) Optimal behavior: can foragers balance two conflicting demands? Science 210:1041–1043. doi:10.1126/science.210.4473.1041

    Article  CAS  PubMed  Google Scholar 

  • Slos S, Stoks R (2008) Predation risk induces stress proteins and reduces antioxidant defense. Funct Ecol 22:637–642. doi:10.1111/j.1365-2435.2008.01424.x

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (2012) Biometry: the principles and practice of statistics in biological research, 4th edn. W.H. Freeman, New York

    Google Scholar 

  • Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integr Comp Biol 42:780–789. doi:10.1093/icb/42.4.780

    Article  PubMed  Google Scholar 

  • Stickle WB, Bayne BL (1982) Effects of temperature and salinity on oxygen consumption and nitrogen excretion in Thais (Nucella) lapillus (L.). J Exp Mar Biol Ecol 58:1–17. doi:10.1016/0022-0981(82)90093-4

    Article  CAS  Google Scholar 

  • Stickle WB, Bayne BL (1987) Energetics of the muricid gastropod Thais (Nucella) lapillus (L.). J Exp Mar Biol Ecol 107:263–278. doi:10.1016/0022-0981(87)90043-8

    Article  Google Scholar 

  • 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 93:235–258. doi:10.1016/0022-0981(85)90242-4

    Article  Google Scholar 

  • Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65. doi:10.1126/science.1083073

    Article  CAS  PubMed  Google Scholar 

  • Tepolt CK, Somero GN (2014) Master of all trades: thermal acclimation and adaptation of cardiac function in a broadly distributed marine invasive species, the European green crab, Carcinus maenas. J Exp Biol 217:1129–1138. doi:10.1242/jeb.093849

    Article  PubMed  Google Scholar 

  • Tewksbury JJ, Huey RB, Deutsch CA (2008) Putting the heat on tropical animals. Science 320:1296–1297. doi:10.1126/science.1159328

    Article  CAS  PubMed  Google Scholar 

  • Trussell GC, Smith LD (2000) Induced defenses in response to an invading crab predator: an explanation of historical and geographic phenotypic change. Proc Natl Acad Sci USA 97:2123–2127. doi:10.1073/pnas.040423397

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Trussell GC, Ewanchuk PJ, Bertness MD (2002) Field evidence of trait-mediated indirect interactions in a rocky intertidal food web. Ecol Lett 5:241–245. doi:10.1046/j.1461-0248.2002.00304.x

    Article  Google Scholar 

  • Trussell GC, Ewanchuk PJ, Bertness MD (2003) Trait-mediated effects in rocky intertidal food chains: predator risk cues alter prey feeding rates. Ecology 84: 629–640.http://www.jstor.org/stable/3107858

  • Trussell GC, Ewanchuk PJ, Matassa CM (2006a) The fear of being eaten reduces energy transfer in a simple food chain. Ecology 87:2979–2984. doi:10.1890/0012-9658(2006)87[2979:TFOBER]2.0.CO;2

    Article  PubMed  Google Scholar 

  • Trussell GC, Ewanchuk PJ, Matassa CM (2006b) Habitat effects on the relative importance of trait- and density-mediated indirect interactions. Ecol Lett 9:1245–1252. doi:10.1111/j.1461-0248.2006.00981.x

    Article  PubMed  Google Scholar 

  • Vucic-Pestic O, Ehnes RB, Rall BC, Brose U (2011) Warming up the system: higher predator feeding rates but lower energetic efficiencies. Glob Change Biol 17:1301–1310. doi:10.1111/j.1365-2486.2010.02329.x

    Article  Google Scholar 

  • Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. Am Nat 142:242–272. doi:10.1086/285537

    Article  CAS  PubMed  Google Scholar 

  • Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100. doi:10.1890/0012-9658(2003)084[1083:AROTII]2.0.CO;2

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

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Acknowledgments

We thank S. June, S. Donelan, E. Forbes, K. McClure, and A. Milanese for assistance with the experiment and K. Jans for access to the field site in Lubec, Maine. This study is part of the PhD dissertation of CMM and was generously supported by the National Science Foundation through a Doctoral Dissertation Improvement Grant (IOS-1110675), grants OCE-0648525 and 0727628 to GCT, and OCE-0963010 to GCT et al. as part of the Academic Research Infrastructure Recovery and Reinvestment Program. This is contribution #320 from the Marine Science Center. The authors have no conflicts of interest to declare.

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  1. Marine Science Center, Northeastern University, East Point, Nahant, MA, 01908, USA

    Catherine M. Matassa & Geoffrey C. Trussell

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  1. Catherine M. Matassa
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  2. Geoffrey C. Trussell
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Correspondence to Catherine M. Matassa.

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Communicated by Pete Peterson.

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Matassa, C.M., Trussell, G.C. Effects of predation risk across a latitudinal temperature gradient. Oecologia 177, 775–784 (2015). https://doi.org/10.1007/s00442-014-3156-7

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