, Volume 191, Issue 3, pp 709–719 | Cite as

Phenotypically plastic responses to predation risk are temperature dependent

  • Thomas M. LuhringEmail author
  • Janna M. Vavra
  • Clayton E. Cressler
  • John P. DeLong
Global change ecology – original research


Predicting how organisms respond to climate change requires that we understand the temperature dependence of fitness in relevant ecological contexts (e.g., with or without predation risk). Predation risk often induces changes to life history traits that are themselves temperature dependent. We explore how perceived predation risk and temperature interact to determine fitness (indicated by the intrinsic rate of increase, r) through changes to its underlying components (net reproductive rate, generation time, and survival) in Daphnia magna. We exposed Daphnia to predation cues from dragonfly naiads early, late, or throughout their ontogeny. Predation risk increased r differentially across temperatures and depending on the timing of exposure to predation cues. The timing of predation risk likewise altered the temperature-dependent response of T and R0. Daphnia at hotter temperatures responded to predation risk by increasing r through a combination of increased R0 and decreased T that together countered an increase in mortality rate. However, only D. magna that experienced predation cues early in ontogeny showed elevated r at colder temperatures. These results highlight the fact that phenotypically plastic responses of life history traits to predation risk can be strongly temperature dependent.


Climate change Fecundity Life history Mortality Reproduction Survivorship 



We thank J. Hite for experimental design suggestions, and J. Hotovy, K. Sullivan, S. Tjards, M. Pinto, S. French, B. Bathke, B. Harmon, C. Urbauer, S. Uiterwaal, and R. Vetter for transferring, and counting over 2000 daphnia neonates. We thank AE Scott Peacor, C. Streid, and two anonymous reviewers for their helpful comments on the manuscript. TML thanks the University of Nebraska’s Program of Excellence in Population Biology.

Author contributions statement

TML conceived the study; TML, JMV, CEC, and JPD designed the study; TML and JMV ran the experiment and collected data, TML analyzed the data. TML, JMV, CEC and JPD interpreted the results and TML drafted the manuscript. TML, JMV, CEC, and JPD revised and approved the manuscript. All authors contributed critically to drafts of the manuscript and gave their final approval for publication.

Compliance with ethical standards

Conflict of interest

The authors declare no competing interests.

Supplementary material

442_2019_4523_MOESM1_ESM.pdf (58 kb)
Supplementary material 1 (PDF 57 kb)


  1. Amarasekare P, Savage V (2012) A framework for elucidating the temperature dependence of fitness. Am Nat 179:178–191. CrossRefPubMedGoogle Scholar
  2. Anderson JT, Inouye DW, McKinney AM et al (2012) Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proc R Soc B Biol Sci 279:3843–3852. CrossRefGoogle Scholar
  3. Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford. CrossRefGoogle Scholar
  4. Angilletta MJ, Huey RB, Frazier MR (2010) Thermodynamic effects on organismal performance: is hotter better? Physiol Biochem Zool 83:197–206. CrossRefPubMedGoogle Scholar
  5. Atkinson D, Morley SA, Weetman D, Hughes RN (2001) Offspring size responses to maternal environment in ectotherms: genes, life histories and plasticity. In: Atkinson D, Thorndyke M (eds) Environmental and animal development. Bios Scientific Publishers, Oxford, pp 269–286Google Scholar
  6. Beckerman AP, Wieski K, Baird DJ (2007) Behavioural versus physiological mediation of life history under predation risk. Oecologia 152:335–343. CrossRefPubMedGoogle Scholar
  7. Beckerman AP, Rodgers GM, Dennis SR (2010) The reaction norm of size and age at maturity under multiple predator risk. J Anim Ecol 79:1069–1076. CrossRefPubMedGoogle Scholar
  8. Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–673. CrossRefGoogle Scholar
  9. Boersma M, Spaak P, De Meester L (1998) Predator-mediated plasticity in morphology, life history, and behavior of daphnia: the uncoupling of responses. Am Nat 152:237–248. CrossRefPubMedGoogle Scholar
  10. Brown JH, Gillooly JF, Allen AP et al (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789. CrossRefGoogle Scholar
  11. Charmantier A, Gienapp P (2014) Climate change and timing of avian breeding and migration: evolutionary versus plastic changes. Evol Appl 7:15–28. CrossRefPubMedGoogle Scholar
  12. Charmantier A, McCleery RH, Cole LR et al (2008) Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320:800–803. CrossRefGoogle Scholar
  13. Cox DR (1972) Regression models and life tables. J R Stat Soc Ser B 34:187–220Google Scholar
  14. Crawford BA, Hickman CR, Luhring TM (2012) Testing the threat-sensitive hypothesis with predator familiarity and dietary specificity. Ethology 118:41–48. CrossRefGoogle Scholar
  15. Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201. CrossRefPubMedGoogle Scholar
  16. Crowl TA, Covich AP (1990) Predator-induced life-history shifts in a freshwater snail. Science 247:949–951. CrossRefPubMedGoogle Scholar
  17. Culler LE, McPeek MA, Ayres MP (2014) Predation risk shapes thermal physiology of a predaceous damselfly. Oecologia 176:653–660. CrossRefPubMedGoogle Scholar
  18. DeLong JP, Gibert JP, Luhring TM et al (2017) The combined effects of reactant kinetics and enzyme stability explain the temperature dependence of metabolic rates. Ecol Evol 7:3940–3950. CrossRefPubMedPubMedCentralGoogle Scholar
  19. DeLong JP, Bachman G, Gibert JP et al (2018) Habitat, latitude and body mass influence the temperature dependence of metabolic rate. Biol Lett 14:20180442. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Deutsch CA, Tewksbury JJ, Huey RB et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci 105:6668–6672. CrossRefPubMedGoogle Scholar
  21. Ernest SKM, Enquist BJ, Brown JH et al (2003) Thermodynamic and metabolic effects on the scaling of production and population energy use. Ecol Lett 6:990–995. CrossRefGoogle Scholar
  22. Ghalambor CK, Martin TE (2000) Parental investment strategies in two species of nuthatch vary with stage-specific predation risk and reproductive effort. Anim Behav 60:263–267. CrossRefPubMedGoogle Scholar
  23. Giebelhausen B, Lampert W (2001) Temperature reaction norms of Daphnia magna: the effect of food concentration. Freshw Biol 46:281–289. CrossRefGoogle Scholar
  24. Gilchrist GW (1995) Specialists and generalists in changing environments. I. Fitness landscapes of thermal sensitivity. Am Nat 146:252–270. CrossRefGoogle Scholar
  25. Grigaltchik VS, Ward AJW, Seebacher F (2012) Thermal acclimation of interactions: differential responses to temperature change alter predator-prey relationship. Proc R Soc B Biol Sci 279:4058–4064. CrossRefGoogle Scholar
  26. Grigaltchik VS, Webb C, Seebacher F (2016) Temperature modulates the effects of predation and competition on mosquito larvae. Ecol Entomol 41:668–675. CrossRefGoogle Scholar
  27. Hickman CR, Stone MD, Mathis A (2004) Priority use of chemical over visual cues for detection of predators by graybelly salamanders, Eurycea multiplicata griseogaster. Herpetologica 60:203–210. CrossRefGoogle Scholar
  28. Hothorn T, Bretz F, Westfall P, Heiberger RM, Schuetzenmeister A, Scheibe S (2017) Simultaneous inference in general parametric models (multcomp). R package version 1.4-7.
  29. Hoverman JT, Relyea RA (2007) How flexible is phenotypic plasticity? Developmental windows for trait induction and reversal. Ecology. CrossRefPubMedGoogle Scholar
  30. Huey RB, Berrigan D (2001) Temperature, demography, and ectotherm fitness. Am Nat 158:204–210. CrossRefPubMedGoogle Scholar
  31. Katzenberger M, Hammond J, Duarte H et al (2014) Swimming with predators and pesticides: how environmental stressors affect the thermal physiology of tadpoles. PLoS One 9:e98265. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kerkhoff AJ, Enquist BJ, Elser JJ, Fagan WF (2005) Plant allometry, stiochiometry and the temperature-dependence of primary productivity. Glob Ecol Biogeogr 14:585–598CrossRefGoogle Scholar
  33. Kilham SS, Kreeger DA, Lynn SG et al (1998) COMBO: a defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377:147–159. CrossRefGoogle Scholar
  34. Kingsolver JG (2009) The well-temperatured biologist. Am Nat 174:755–768. CrossRefPubMedGoogle Scholar
  35. Knies JL, Izem R, Supler KL et al (2006) The genetic basis of thermal reaction norm evolution in lab and natural phage populations. PLoS Biol 4:1257–1264. CrossRefGoogle Scholar
  36. Knies JL, Kingsolver JG, Burch CL (2009) Hotter is better and broader: thermal sensitivity of fitness in a population of bacteriophages. Am Nat 173:419–430. CrossRefPubMedGoogle Scholar
  37. Kremer CT, Fey SB, Arellano AA, Vasseur DA (2018) Gradual plasticity alters population dynamics in variable environments: thermal acclimation in the green alga Chlamydomonas reinhartdii. Proc R Soc B Biol Sci 285:20171942. CrossRefGoogle Scholar
  38. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640. CrossRefGoogle Scholar
  39. Lind J, Cresswell W (2005) Determining the fitness consequences of antipredation behavior. Behav Ecol 16:945–956. CrossRefGoogle Scholar
  40. Luhring TM, DeLong JP (2016) Predation changes the shape of thermal performance curves for population growth rate. Curr Zool 62:501–505. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Luhring TM, DeLong JP (2017) Scaling from metabolism to population growth rate to understand how acclimation temperature alters thermal performance. Integr Comp Biol 57:103–111. CrossRefPubMedGoogle Scholar
  42. Luhring TM, Holdo RM (2015) Trade-offs between growth and maturation: the cost of reproduction for surviving environmental extremes. Oecologia 178:723–732. CrossRefPubMedGoogle Scholar
  43. Luhring TM, Meckley TD, Johnson NS et al (2016) A semelparous fish continues upstream migration when exposed to alarm cue, but adjusts movement speed and timing. Anim Behav 121:41–51. CrossRefGoogle Scholar
  44. Luhring TM, Vavra JM, Cressler CE, DeLong JP (2018) Predators modify the temperature dependence of life-history trade-offs. Ecol Evol 8:8818–8830. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Lynch M, Gabriel W (1987) Environmental Tolerance. Am Nat 129:283–303. CrossRefGoogle Scholar
  46. Magnhagen C (1990) Reproduction under predation risk in the sand goby, Pomatoschistus minutes, and the black goby, Gobius niger: the effect of age and longevity. Behav Ecol Sociobiol 26:331–335. CrossRefGoogle Scholar
  47. Novich RA, Erickson EK, Kalinoski RM, DeLong JP (2014) The temperature independence of interaction strength in a sit-and-wait predator. Ecosphere 5:art137. CrossRefGoogle Scholar
  48. Padfield D, Yvon-Durocher G, Buckling A et al (2016) Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton. Ecol Lett 19:133–142. CrossRefPubMedGoogle Scholar
  49. Pangle KL, Peacor SD, Johannsson OE (2007) Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88:402–412. CrossRefPubMedGoogle Scholar
  50. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. CrossRefGoogle Scholar
  51. Pigliucci M (1998) Developmental phenotypic plasticity: where internal programming meets the external environment. Curr Opin Plant Biol 1:87–91. CrossRefPubMedGoogle Scholar
  52. Poloczanska ES, Brown CJ, Sydeman WJ et al (2013) Global imprint of climate change on marine life. Nat Clim Chang 3:919–925. CrossRefGoogle Scholar
  53. R Core Team (2018). R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria.
  54. Reale D, McAdam AG, Boutin S, Berteaux D (2003) Genetic and plastic responses of a northern mammal to climate change. Proc R Soc B Biol Sci 270:591–596. CrossRefGoogle Scholar
  55. Reede T (1995) Life history shifts in response to different levels of fish kairomones in Daphnia. J Plankton Res. CrossRefGoogle Scholar
  56. Relyea RA (2004) Fine-tuned phenotypes: tadpole plasticity under 16 combinations of predators and competitors. Ecology. CrossRefGoogle Scholar
  57. Reznick D, Endler JA (1982) The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution (N Y) 36:160–177. CrossRefGoogle Scholar
  58. Riddell EA, Odom JP, Damm JD, Sears MW (2018) Plasticity reveals hidden resistance to extinction under climate change in the global hotspot of salamander diversity. Sci Adv 4:eaar5471. CrossRefPubMedPubMedCentralGoogle Scholar
  59. Riessen HP (1999) Predator-induced life history shifts in Daphnia: a synthesis of studies using meta-analysis. Can J Fish Aquat Sci 56:2487–2494. CrossRefGoogle Scholar
  60. Roff DA (1992) The evolution of life histories: theory and analysis. Chapman and Hall, New YorkGoogle Scholar
  61. Roitberg BD, Sircom J, Roitberg CA, van Alphen JJ, Mangel M (1993) Life expectancy and reproduction. Nature 364:108CrossRefGoogle Scholar
  62. Sakwińska O (1998) Plasticity of Daphnia magna life history traits in response to temperature and information about a predator. Freshw Biol. CrossRefGoogle Scholar
  63. Savage VM, Gillooly JF, Brown JH et al (2004) Effects of body size and temperature on population growth. Am Nat 163:429–441. CrossRefPubMedGoogle Scholar
  64. Schaum C-E, Barton S, Bestion E et al (2017) Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis. Nat Ecol Evol 1:0094. CrossRefGoogle Scholar
  65. Schulte PM, Healy TM, Fangue NA (2011) Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr Comp Biol 51:691–702. CrossRefPubMedGoogle Scholar
  66. Seebacher F, Grigaltchik VS (2015) Developmental thermal plasticity of prey modifies the impact of predation. J Exp Biol 218:1402–1409. CrossRefPubMedGoogle Scholar
  67. Seebacher F, White CR, Franklin CE (2015) Physiological plasticity increases resilience of ectothermic animals to climate change. Nat Clim Chang 5:61–66. CrossRefGoogle Scholar
  68. Sibly RM, Atkinson D (1994) How rearing temperature affects optimal adult size in ectotherms. Funct Ecol 8:486–493. CrossRefGoogle Scholar
  69. Sinclair BJ, Marshall KE, Sewell MA et al (2016) Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures? Ecol Lett 19:1372–1385CrossRefGoogle Scholar
  70. Stearns SC (1992) The evolution of life histories. Oxford University Press, New YorkGoogle Scholar
  71. Stibor H (1992) Predator induced life-history shifts in a freshwater cladoceran. Oecologia 92:162–165. CrossRefPubMedGoogle Scholar
  72. Stibor H, Luning J (1994) Predator-induced phenotypic variation in the pattern of growth and reproduction in Daphnia hyalina (Crustacea: Cladocera). Funct Ecol 8:97–101. CrossRefGoogle Scholar
  73. Therneau TM, Lumley T (2017) Survival: survival analysis. R package version 2.41-3.
  74. Thomas MK, Aranguren-Gassis M, Kremer CT et al (2017) Temperature–nutrient interactions exacerbate sensitivity to warming in phytoplankton. Glob Chang Biol 23:3269–3280. CrossRefPubMedGoogle Scholar
  75. Tolon V, Dray S, Loison A et al (2009) Responding to spatial and temporal variations in predation risk: space use of a game species in a changing landscape of fear. Can J Zool 87:1129–1137. CrossRefGoogle Scholar
  76. Tseng M, O’Connor MI (2015) Predators modify the evolutionary response of prey to temperature change. Biol Lett 11:20150798. CrossRefPubMedPubMedCentralGoogle Scholar
  77. Van Buskirk J, Schmidt BR (2000) Predator-induced phenotypic plasticity in larval newts: trade-offs, selection, and variation in nature. Ecology 81:3009–3028. CrossRefGoogle Scholar
  78. Vasseur DA, DeLong JP, Gilbert B et al (2014) Increased temperature variation poses a greater risk to species than climate warming. Proc R Soc B Biol Sci 281:20132612. CrossRefGoogle Scholar
  79. Walsh MR, Cooley F, Biles K, Munch SB (2014) Predator-induced phenotypic plasticity within- and across-generations: a challenge for theory? Proc R Soc B Biol Sci 282:20142205. CrossRefGoogle Scholar
  80. Walther GR, Post E, Convey P et al (2002) Ecological responses to recent climate change. Nature 416:389–395. CrossRefGoogle Scholar
  81. Williams GC (1966) Natural selection, the costs of reproduction, and a refinement of lack’s principle. Am Nat 100:687–690. CrossRefGoogle Scholar
  82. Wood SN (2006) Generalized additive models: an introduction with R. Chapman and Hall/CRC Press, Boca Raton, FLCrossRefGoogle Scholar
  83. Wood SN (2015) Package ‘mgcv’. R package version 1.8-7.
  84. Zanette LY, White AF, Allen MC, Clinchy M (2011) Perceived predation risk reduces the number of offspring songbirds produce per year. Science 334:1398–1401. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of Nebraska-LincolnLincolnUSA
  2. 2.Department of Biological SciencesWichita State UniversityWichitaUSA

Personalised recommendations