Abstract
Predation risk has strong effects on organismal physiology that can cascade to impact ecosystem structure and function. Physiological processes in general are sensitive to temperature. Thus, the temperature at which predators and prey interact may shape physiological response to predation risk. We measured and evaluated how temperature and predation risk affected growth rates of predaceous damselfly nymphs (Enallagma vesperum, Odonata: Coenagrionidae). First, we conducted growth trials at five temperatures crossed with two levels of predation risk (fish predator present versus absent) and measured growth rates, consumption rates, assimilation efficiencies, and production efficiencies of 107 individual damselflies. Second, we used a model to evaluate if and how component physiological responses to predation risk affected growth rates across temperatures. In the absence of mortality threat, growth rates of damselflies increased with warming until about 23.5 °C and then began to decline, a typical unimodal response to changes in temperature. Under predation risk, growth rates were lower and the shape of the thermal response was less apparent. Higher metabolic and survival costs induced by predation risk were only partially offset by changes in consumption rates and assimilation efficiencies and the magnitude of non-consumptive effects varied as a function of temperature. Furthermore, we documented that thermal physiology was mediated by predation risk, a known driver of organismal physiology that occurs in the context of species interactions. A general understanding of climatic impacts on ectothermic populations requires consideration of the community context of thermal physiology, including non-consumptive effects of predators.
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References
Anderson DR (2008) Model based inference in the life sciences: a primer on evidence. Springer, New York
Ayres MP, Scriber JM (1994) Local adaptation to regional climates in Papilio canadensis (Lepidoptera: Papilionidae). Ecol Monogr 64:465–482
Barton BT (2010) Climate warming and predation risk during herbivore ontogeny. Ecology 10:2811–2818
Barton BT, Beckerman AP, Schmitz OJ (2009) Climate warming strengthens indirect interactions in an old-field food web. Ecology 90:2346–2351
Beckerman AP, Wieski K, Baird DJ (2007) Behavioural versus physiological mediation of life history under predation risk. Oecologia 152:335–343
Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–673
Chen XJ, Xu FX, Ji X (2003) Influence of body temperature on food assimilation and locomotor performance in whitestriped grass lizards Takydromus wolteri (Lacertidae). J Therm Biol 28:385–391
Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201
Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. PNAS 105:6668–6672
Englund G, Öhlund G, Hein CL, Diehl S (2011) Temperature dependence of the functional response. Ecol Lett 14:914–921
Gillooly JE, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251
Gordon GT (1968) Quantitative aspects of insect nutrition. Am Zool 8:131–138
Harwood RH (1979) The effect of temperature on the digestive efficiency of three species of lizard, Cnemidophorus tigris, Gerrhonotus multicarinatu and Sceloporus occidentalis. Comp Biochem Physiol 63A:417–433
Hawlena D, Schmitz OJ (2010a) Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am Nat 176:537–556
Hawlena D, Schmitz OJ (2010b) Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. PNAS 107:15503–15507
Hawlena D, Strickland MS, Bradford MA, Schmitz OJ (2012) Fear of predation slows litter decomposition. Science 336:1434–1438
Higginson AD, Ruxton GD (2010) Adaptive changes in size and age at metamorphosis can qualitatively vary with predator type and available defenses. Ecology 91:2756–2768
Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York
Johansson F, Andersson J (2009) Scared fish get lazy, and lazy fish get fat. J Anim Ecol 78:772–777
Johnson DM, Akre BG, Crowley PH (1975) Modeling arthropod predation: wasteful killing by damselfly naiads. Ecology 56:1081–1093
Kingsolver JG (2009) The well-temperatured biologist. Am Nat 174:755–768
Kingsolver JG, Woods HA (1997) Thermal sensitivity of feeding and digestion in Manduca caterpillars. Physiol Zool 70:631–638
Kingsolver JG, Woods HA (1998) Interactions of temperature and dietary protein concentration in growth and feeding of Manduca sexta caterpillars. Physiol Entomol 23:354–359
Kollberg I, Bylund H, Schmidt A, Gershenzon J, Björkman C (2013) Multiple effects of temperature, photoperiod and food quality on the performance of a pine sawfly. Ecol Entomol 38:201–208
Lawton JH (1970) Feeding and food energy assimilation in larvae of the damselfly Pyrrhosoma nymphula. J Anim Ecol 39:669–689
Lemoine NP, Burkepile DE (2012) Temperature-induced mismatches between consumption and metabolism reduce consumer fitness. Ecology 93:2483–2489
Lima S (1998) Non-lethal effects in the ecology of predator–prey interactions. Bioscience 48:25–34
Lima S, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
McPeek MA (1998) The consequences of changing the top predator in a food web: a comparative experimental approach. Ecol Monogr 68:1–23
McPeek MA (2004) The growth/predation-risk trade-off: so what is the mechanism? Am Nat 163:E88–E111
McPeek MA, Peckarsky BL (1998) Life histories and the strength of species interactions: combining mortality, growth, and fecundity effects. Ecology 79:867–879
McPeek MA, Grace M, Richardson JML (2001) Physiological and behavioral responses to predators shape the growth/predation risk trade-off in damselflies. Ecology 82:1535–1545
Niven JE, Scharlemann JPW (2005) Do insect metabolic rates at rest and during flight scale with body mass? Biol Lett 1:346–349
O’Connor MI, Gilbert B, Brown CJ (2011) Theoretical predictions for how temperature affects the dynamics of interacting herbivores and plants. Am Nat 178:626–638
Pangle K, Peacor S, Johannsson O (2007) Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88:402–412
Preisser EL, Bolnick DI (2008) The many faces of fear: comparing the pathways and impacts of nonconsumptive predator effects on prey populations. PloS ONE 3:e2465
Rall BC, Vucic-Pestic O, Ehnes RB, Emmerson M, Brose U (2010) Temperature, predator–prey interaction strength and population stability. Glob Change Biol 16:2145–2157
Schmitz OJ (2008) Effect of predator hunting mode on grassland ecosystem function. Science 319:952–954
Slos S, Stoks R (2008) Predation risk induces stress proteins and reduces antioxidant defense. Funct Ecol 22:637–642
Slos S, Meester LD, Stoks R (2009) Behavioural activity levels and expression of stress proteins under predation risk in two damselfly species. Ecol Entomol 34:297–303
Stoks R, McPeek MA (2003) Antipredator behavior and physiology determine Lestes species turnover along the pond-permanence gradient. Ecology 84:3327–3338
Stoks R, Swillen I, De Block M (2012) Behaviour and physiology shape the growth accelerations associated with predation risk, high temperatures and southern latitudes in Ischnura damselfly larvae. J Anim Ecol 81:1034–1040
Sunardi Asaeda T, Manatunge J (2007) Physiological responses of topmouth gudgeon, Pseudorasbora parva, to predator cues and variation of current velocity. Aquat Ecol 41:111–118
Thaler JS, Contreras J, Davidowitz G (2014) Effects of predation risk and plant resistance on Manduca sexta caterpillar feeding behaviour and physiology. Ecol Entomol 39:210–216
Thompson DJ (1978) Towards a realistic predator-prey model: the effect of temperature on the functional response and life history of larvae of the damselfly, Ischnura elegans. J Anim Ecol 47:757–767
Vasseur DA, McCann KS (2005) A mechanistic approach for modeling temperature-dependent consumer-resource dynamics. Am Nat 166:184–198
Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone–behavior interactions: the “emergency life history stage”. Am Zool 38:191–206
Woodley CM (2003) Peterson MS (2003) Measuring responses to simulated predation threat using behavioral and physiological metrics: the role of aquatic vegetation. Oecologia 136:155–160
Acknowledgments
This project was made possible with funding from Dartmouth’s Biology Department (the R. Melville Cramer Fund). Thanks to Laurel Symes for help with damselfly identification; Danny O’Donnell, Zach Wood, Lauren Bonvini, Kathy Culler, and Bret Manning for help with lab and field work; and Craig Layne and Sam Fey for help with Daphnia rearing. Kathy Cottingham, Alex Huryn, Ross Virginia, Sam Fey, Mike Logan, and three anonymous reviewers provided valuable feedback on the manuscript.
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Communicated by Jennifer Thaler.
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Culler, L.E., McPeek, M.A. & Ayres, M.P. Predation risk shapes thermal physiology of a predaceous damselfly. Oecologia 176, 653–660 (2014). https://doi.org/10.1007/s00442-014-3058-8
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DOI: https://doi.org/10.1007/s00442-014-3058-8