, Volume 169, Issue 4, pp 1117–1125 | Cite as

Using functional response modeling to investigate the effect of temperature on predator feeding rate and energetic efficiency

  • Arnaud Sentis
  • Jean-Louis Hemptinne
  • Jacques Brodeur
Global Change Ecology - Original research


Temperature is one of the most important environmental parameters influencing all the biological processes and functions of poikilothermic organisms. Although extensive research has been carried out to evaluate the effects of temperature on animal life histories and to determine the upper and lower temperature thresholds as well as the optimal temperatures for survival, development, and reproduction, few studies have investigated links between thermal window, metabolism, and trophic interactions such as predation. We developed models and conducted laboratory experiments to investigate how temperature influences predator–prey interaction strengths (i.e., functional response) using a ladybeetle larva feeding on aphid prey. As predicted by the metabolic theory of ecology, we found that handling time exponentially decreases with warming, but—in contrast with this theory—search rate follows a hump-shaped relationship with temperature. An examination of the model reveals that temperature thresholds for predation depend mainly on search rate, suggesting that predation rate is primarily determined by searching activities and secondly by prey handling. In contrast with prior studies, our model shows that per capita short-term predator–prey interaction strengths and predator energetic efficiency (per capita feeding rate relative to metabolism) generally increase with temperature, reach an optimum, and then decrease at higher temperatures. We conclude that integrating the concept of thermal windows in short- and long-term ecological studies would lead to a better understanding of predator–prey population dynamics at thermal limits and allow better predictions of global warming effects on natural ecosystems.


Predator–prey interactions Functional response model Temperature window Interaction strength Metabolic theory of ecology 



We thank J. Doyon, C. Beaudoin, and M. Bélanger-Morin for technical assistance, two anonymous reviewers for very helpful suggestions and comments, and L. Devine for English revision. This work was supported by the Natural Sciences and Engineering Research Council of Canada.


  1. Bale JS (2002) Insects and low temperatures: from molecular biology to distributions and abundance. Philos Trans R Soc Lond B 357:849–862CrossRefGoogle Scholar
  2. Benton AH, Crump AJ (1981) Observations on the spring and summer behavior of the 12-spotted ladybird beetle, Coleomegilla maculata (Degeer) (Coleoptera: Coccinellidae). J NY Entomol S 89:102–108Google Scholar
  3. Bolker BM (2008) Ecological models and data in R. Princeton University Press, PrincetonGoogle Scholar
  4. Briere J, Pracros P, Le Roux A, Pierre J (1999) A novel rate model of temperature-dependent development for arthropods. Environ Entomol 28:22–29Google Scholar
  5. Brose U, Williams RJ, Martinez ND (2006) Allometric scaling enhances stability in complex food webs. Ecol Lett 9:1228–1236PubMedCrossRefGoogle Scholar
  6. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789CrossRefGoogle Scholar
  7. Carter MC, Sutherland D, Dixon AFG (1984) Plant structure and the searching efficiency of coccinellid larvae. Oecologia 63:394–397CrossRefGoogle Scholar
  8. Cave RD, Gaylor MJ (1989) Functional response of Telenomus reynoldsi [Hym.: Scelionidae] at five constant temperatures and in an artificial plant arena. Biocontrol 34:3–10Google Scholar
  9. Davis JA, Radcliffe EB, Ragsdale DW (2006) Effects of high and fluctuating temperatures on Myzus persicae (Hemiptera: Aphididae). Environ Entomol 35:1461–1468CrossRefGoogle Scholar
  10. Dixon AFG, Jarošik V, Honĕk A (2005) Thermal requirements for development and resource partitioning in aphidophagous guilds. Eur J Entomol 102:407–411Google Scholar
  11. Dixon AFG, Honĕk A, Keil P, Kotela MAA, Šizling AL, Jarošik V (2009) Relationship between the minimum and maximum temperature thresholds for development in insects. Funct Ecol 23:257–264CrossRefGoogle Scholar
  12. Eggleston DB (1990) Behavioural mechanisms underlying variable functional responses of blue crabs, Callinectes sapidus feeding on juvenile oysters, Crassostrea virginica. J Anim Ecol 59:615–630CrossRefGoogle Scholar
  13. Elliott NC, Kieckhefer RW, Beck DA (2000) Adult coccinellid activity and predation on aphids in spring cereals. Biol Control 17:218–226CrossRefGoogle Scholar
  14. Englund G, Ohlund G, Hein CL, Diehl S (2011) Temperature dependence of the functional response. Ecol Lett 14:914–921PubMedCrossRefGoogle Scholar
  15. Firlej A, Chouinard G, Coderre D (2006) A meridic diet for the rearing of Hyaliodes vitripennis (Hemiptera: Miridae), a predator of mites in apple orchards. Biocontrol Sci Techn 16:743–751CrossRefGoogle Scholar
  16. Flinn PW (1991) Temperature-dependent functional response of the parasitoid Cephalonomia waterstoni (Gahan) (Hymenoptera: Bethylidae) attacking rusty grain beetle larvae (Coleoptera: Cucujidae). Environ Entomol 20:872–876Google Scholar
  17. Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251PubMedCrossRefGoogle Scholar
  18. Giroux S, Duchesne RM, Coderre D (1995) Predation of Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) by Coleomegilla maculata (Coleoptera: Coccinellidae): comparative effectiveness of predator developmental stages and effect of temperature. Environ Entomol 24:748–754Google Scholar
  19. Gordon RD (1985) The coccinellidae (Coleoptera) of America north of Mexico. J NY Entomol S 96:1–912Google Scholar
  20. Gresens SE, Cothran ML, Thorp JH (1982) The influence of temperature on the functional response of the dragonfly Celithemis fasciata (Odonata: Libellulidae). Oecologia 53:281–284CrossRefGoogle Scholar
  21. Hoekman D (2010) Turning up the heat: temperature influences the relative importance of top-down and bottom-up effects in pitcher plant inquiline communities. Ecology 91:2819–2825PubMedCrossRefGoogle Scholar
  22. Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398CrossRefGoogle Scholar
  23. Honĕk A (1985) Activity and predation of Coccinella septempunctata adults in the field (Col., Coccinellidae). Z Angew Entomol 100:399–409CrossRefGoogle Scholar
  24. Jalali MA, Tirry L, Arbab A, De Clercq P (2010a) Temperature-dependent development of the two-spotted ladybeetle, Adalia bipunctata, on the green peach aphid, Myzus persicae, and a factitious food under constant temperatures. J Insect Sci 10:1536–2442CrossRefGoogle Scholar
  25. Jalali MA, Tirry L, De Clercq P (2010b) Effect of temperature on the functional response of Adalia bipunctata to Myzus persicae. Biocontrol 55:261–269CrossRefGoogle Scholar
  26. Jeschke JM, Kopp M, Tollrian R (2002) Predator functional responses: discriminating between handling and digesting prey. Ecol Monogr 72:95–112CrossRefGoogle Scholar
  27. Jones TH, Thompson LJ, Lawton JH, Bezemer TM, Bardgett RD, Blackburn TM, Bruce KD, Cannon PF, Hall GS, Hartley SE (1998) Impacts of rising atmospheric carbon dioxide on model terrestrial ecosystems. Science 280:441–443PubMedCrossRefGoogle Scholar
  28. Juliano SA (2001) Nonlinear curve fitting: predation and functional response curve. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman & Hall, New York, pp 178–196Google Scholar
  29. Mack TP, Smilowitz Z (1982) Using temperature-mediated functional response models to predict the impact of Coleomegilla maculata (DeGeer) adults and 3rd-instar larvae on green peach aphids. Environ Entomol 11:46–52Google Scholar
  30. Menon A, Flinn PW, Dover BA (2002) Influence of temperature on the functional response of Anisopteromalus calandrae (Hymenoptera: Pteromalidae), a parasitoid of Rhyzopertha dominica (Coleoptera: Bostrichidae). J Stored Prod Res 38:463–469CrossRefGoogle Scholar
  31. Messenger PS (1968) Bioclimatic studies of the aphid parasite Praon exsoletum. I. Effects of temperature on the functional response of females to varying host densities. Can Entomol 100:728–741CrossRefGoogle Scholar
  32. Obrycki JJ, Tauber MJ (1978) Thermal requirements for development of Coleomegilla maculata (Coleoptera: Coccinellidae) and its parasite Perilitus coccinellae (Hymenoptera: Braconidae). Can Entomol 110:407–412CrossRefGoogle Scholar
  33. Obrycki JJ, Ormord AM, Giles KL (1997) Partial life table analysis for larval Coleomegilla maculata (Degeer) and Coccinella septempunctata L. (Coleoptera: Coccinellidae) in alfalfa. J Kansas Entomol Soc 70:339–346Google Scholar
  34. Omkar AP (2004) Temperature-dependent development and immature survival of an aphidophagous ladybeetle, Propylea dissecta (Mulsant). J Appl Entomol 128:510–514CrossRefGoogle Scholar
  35. Ongagna P, Giuge L, Iperti G, Ferran A (1993) Cycle de developpement d’Harmonia axyridis (Col. Coccinellidae) dans son aire d’introduction: le Sud-Est de la France. Biocontrol 38:125–128Google Scholar
  36. Persson L (1986) Temperature-induced shift in foraging ability in two fish species, roach (Rutilus rutilus) and perch (Perca fluviatilis): implications for coexistence between poikilotherms. J Anim Ecol 55:829–839CrossRefGoogle Scholar
  37. Persson L, Leonardsson K, de Roos AM, Gyllenberg M, Christensen B (1998) Ontogenetic scaling of foraging rates and the dynamics of a size-structured consumer-resource model. Theor Popul Biol 54:270–293PubMedCrossRefGoogle Scholar
  38. Petchey OL, McPhearson PT, Casey TM, Morin PJ (1999) Environmental warming alters food web structure and ecosystem function. Nature 402:69–72CrossRefGoogle Scholar
  39. Petchey OL, Brose U, Rall BC (2010) Predicting the effects of temperature on food web connectance. Philos Trans R Soc Lond B 365:2081–2091CrossRefGoogle Scholar
  40. Peters RH (1986) The ecological implications of body size. Cambridge University Press, CambridgeGoogle Scholar
  41. Portner HO, Farrell AP (2008) Physiology and climate change. Science 322:690PubMedCrossRefGoogle Scholar
  42. Portner HO, Bennett AF, Bozinovic F, Clarke A, Lardies MA, Lucassen M, Pelster B, Schiemer F, Stillman JH (2006) Trade-offs in thermal adaptation: the need for a molecular to ecological integration. Physiol Biochem Zool 79:295–313PubMedCrossRefGoogle Scholar
  43. Rall B, Guill C, Brose U (2008) Food web connectance and predator interference dampen the paradox of enrichment. Oikos 117:202–213CrossRefGoogle Scholar
  44. Rall BC, Vucic-Pestic O, Ehnes RB, Emmerson M, Brose U (2010) Temperature, predator–prey interaction strength and population stability. Glob Change Biol 16:2145–2157CrossRefGoogle Scholar
  45. Rogers D (1972) Random search and insect population models. J Anim Ecol 41:369–383CrossRefGoogle Scholar
  46. Savage VM, Gillooly JF, Woodruff WH, West GB, Allen AP, Enquist BJ, Brown JH (2004) The predominance of quarter power scaling in biology. Funct Ecol 18:257–282CrossRefGoogle Scholar
  47. Schanderl H, Ferran A, Larroque MM (1985) Les besoins trophiques et thermiques des larves de la coccinelle Harmonia axyridis Pallas. Agronomie 5:417–421CrossRefGoogle Scholar
  48. Soares AO, Coderre D, Schanderl H (2003) Effect of temperature and intraspecific allometry on predation by two phenotypes of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Environ Entomol 32:939–944CrossRefGoogle Scholar
  49. 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 47:757–767CrossRefGoogle Scholar
  50. Vasseur DA, McCann KS (2005) A mechanistic approach for modeling temperature-dependent consumer-resource dynamics. Am Nat 166:184–198PubMedCrossRefGoogle Scholar
  51. Voigt W, Perner J, Davis AJ, Eggers T, Schumacher J, Bahrmann R, Fabian B, Heinrich W, Kohler G, Lichter D (2003) Trophic levels are differentially sensitive to climate. Ecology 84:2444–2453CrossRefGoogle Scholar
  52. Vucic-Pestic O, Rall BC, Kalinkat G, Brose U (2010) Allometric functional response model: body masses constrain interaction strengths. J Anim Ecol 79:249–256PubMedCrossRefGoogle Scholar
  53. 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 17:1301–1310CrossRefGoogle Scholar
  54. West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276:122–126PubMedCrossRefGoogle Scholar
  55. Williams RJ, Martinez ND (2004) Limits to trophic levels and omnivory in complex food webs: theory and data. Am Nat 163:458–468PubMedCrossRefGoogle Scholar
  56. Xia JY, Van der Werf W, Rabbinge R (1999) Temperature and prey density on bionomics of Coccinella septempunctata (Coleoptera: Coccinellidae) feeding on Aphis gossypii (Homoptera: Aphididae) on cotton. Environ Entomol 28:307–314Google Scholar
  57. Xia JY, Rabbinge R, Van der Werf W (2003) Multistage functional responses in a ladybeetle aphid system: scaling up from the laboratory to the field. Environ Entomol 32:151–162CrossRefGoogle Scholar
  58. Zamani AA, Talebi AA, Fathipour Y, Baniameri V (2006) Temperature-dependent functional response of two aphid parasitoids, Aphidius colemani and Aphidius matricariae (Hymenoptera: Aphidiidae), on the cotton aphid. J Pest Sci 79:183–188CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Arnaud Sentis
    • 1
    • 2
  • Jean-Louis Hemptinne
    • 2
  • Jacques Brodeur
    • 1
  1. 1.Département des Sciences Biologiques, Institut de Recherche en Biologie VégétaleUniversité de MontréalQuébecCanada
  2. 2.École Nationale de Formation AgronomiqueUMR 5174 CNRS/Université Toulouse III/ENFA “Evolution et Diversité Biologique”Castanet-Tolosan CedexFrance

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