Skip to main content
Log in

Influence of temperature on patch residence time in parasitoids: physiological and behavioural mechanisms

  • Original Paper
  • Published:
The Science of Nature Aims and scope Submit manuscript

Abstract

Patch time allocation has received much attention in the context of optimal foraging theory, including the effect of environmental variables. We investigated the direct role of temperature on patch time allocation by parasitoids through physiological and behavioural mechanisms and its indirect role via changes in sex allocation and behavioural defences of the hosts. We compared the influence of foraging temperature on patch residence time between an egg parasitoid, Trichogramma euproctidis, and an aphid parasitoid, Aphidius ervi. The latter attacks hosts that are able to actively defend themselves, and may thus indirectly influence patch time allocation of the parasitoid. Patch residence time decreased with an increase in temperature in both species. The increased activity levels with warming, as evidenced by the increase in walking speed, partially explained these variations, but other mechanisms were involved. In T. euproctidis, the ability to externally discriminate parasitised hosts decreased at low temperature, resulting in a longer patch residence time. Changes in sex allocation with temperature did not explain changes in patch time allocation in this species. For A. ervi, we observed that aphids frequently escaped at intermediate temperature and defended themselves aggressively at high temperature, but displayed few defence mechanisms at low temperature. These defensive behaviours resulted in a decreased patch residence time for the parasitoid and partly explained the fact that A. ervi remained for a shorter time at the intermediate and high temperatures than at the lowest temperature. Our results suggest that global warming may affect host-parasitoid interactions through complex mechanisms including both direct and indirect effects on parasitoid patch time allocation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amat I, Castelo M, Desouhant E, Bernstein C (2006) The influence of temperature and host availability on the host exploitation strategies of sexual and asexual parasitic wasps of the same species. Oecologia 148:153–161

    Article  PubMed  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

    Article  PubMed  Google Scholar 

  • Barrette M, Boivin G, Brodeur J, Giraldeau LA (2010) Travel time affects optimal diets in depleting patches. Behav Ecol Sociobiol 64:593–598

    Article  Google Scholar 

  • Boivin G, Fauvergue X, Wajnberg E (2004) Optimal patch residence time in egg parasitoids: innate versus learned estimate of patch quality. Oecologia 138:640–647

    Article  PubMed  Google Scholar 

  • Brown JH, Gillooly JF, Allen AP, Savage M, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  • Charnov EL (1976) Optimal foraging: the marginal value theorem. Theor Popul Biol 9:129–136

    Article  CAS  PubMed  Google Scholar 

  • Collett D (1994) Modelling survival data in medical research, 1st edn. Chapman & Hall, London

    Book  Google Scholar 

  • Cox DR (1972) Regression models and life tables. Biometrics 38:67–77

    Google Scholar 

  • Dill LM, Fraser AHG, Roitberg BD (1990) The economics of escape behaviour in the pea aphid, Acyrthosiphon pisum. Oecologia 83:473–478

    Article  Google Scholar 

  • Driessen G, Bernstein C, van Alphen JJM, Kacelnick A (1995) A count-down mechanism for host search in the parasitoid Venturia canescens. J Anim Ecol 64:117–125

    Article  Google Scholar 

  • Gilchrist GW (1996) A quantitative genetic analysis of thermal sensitivity in the locomotor performance curve of Aphidus ervi. Evolution 50:1560–1572

    Article  Google Scholar 

  • Goubault M, Outreman Y, Poinsot D, Cortesero AM (2005) Patch exploitation strategies of parasitic wasps under intraspecific competition. Behav Ecol 16:693–701

    Article  Google Scholar 

  • Hilker M, McNeil JN (2008) Chemical and behavioral ecology in insect parasitoids: how to behave optimally in a complex odorous environment. In: Wajnberg E, Bernstein C, van Alphen JJM (eds) Behavioral ecology of insect parasitoids, from theoretical approaches to field applications. Blackwell, Oxford, pp 92–112

    Chapter  Google Scholar 

  • Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity of ectotherms performance. Trends Ecol Evol 4:131–135

    Article  CAS  PubMed  Google Scholar 

  • IPCC (2007) In: Solomon SD, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, 996 pp

    Google Scholar 

  • Iwasa Y, Higashi M, Yamamura N (1981) Prey distribution as a factor determining the choice of optimal foraging strategy. Am Nat 117:710–723

    Article  Google Scholar 

  • Le Lann C, Outreman Y, van Alphen JJM, van Baaren J (2010) First in, last out: asymmetric competition influences patch exploitation of a parasitoid. Behav Ecol 22:101–107

    Article  Google Scholar 

  • Le Lann C, Lodi M, Ellers J (2014) Thermal change alters the outcome of behavioural interactions between antagonistic partners. Ecol Entomol 39:578–588

    Article  Google Scholar 

  • Le Ralec A, Anselme C, Outreman Y, Poirié M, Van Baaren J, Le Lann C, van Alphen JJM (2010) Evolutionary ecology of the interactions between aphids and their parasitoids. C R Biol 333:554–565

    Article  PubMed  Google Scholar 

  • Li C, Roitberg BD, Mackauer M (1997) Effects of contact kairomone and experience on initial giving-up time. Entomol Exp App 84:101–104

    Article  Google Scholar 

  • Louâpre P, Pierre JS (2012) Carbon dioxide narcosis modifies the patch leaving decision of foraging parasitoids. Anim Cogn 15:429–435

    Article  PubMed  Google Scholar 

  • Ma G, Ma CS (2012) Climate warming may increase aphids’ dropping probabilities in response to high temperatures. J Insect Physiol 58:1456–1462

    Article  CAS  PubMed  Google Scholar 

  • Meiners T, Randlkofer B, Obermaier E (2006) Oviposition at low temperatures—late season negatively affects the leaf beetle Galeruca tanaceti (Coleoptera: Galerucinae) but not its specialised egg parasitoid Oomyzus galerucivorus (Hymenoptera: Eulophidae). Eur J Entomol 103:765–770

    Article  Google Scholar 

  • Miyatake T, Okada K, Harano T (2008) Negative relationship between ambient temperature and death-feigning intensity in adult Callosobruchus maculatus and Callosobruchus chinensis. Physiol Entomol 33:83–88

    Article  Google Scholar 

  • Moiroux J, Giron D, Vernon P, van Baaren J, van Alphen JJM (2012) Evolution of metabolic rate in a parasitic wasp: the role of limitation in intrinsic resources. J Insect Physiol 58:979–984

    Article  CAS  PubMed  Google Scholar 

  • Moiroux J, Brodeur J, Boivin G (2014) Sex ratio variations with temperature in an egg parasitoid: behavioural adjustment and physiological constraint. Anim Behav 91:61–66

    Article  Google Scholar 

  • Moiroux J, Boivin G, Brodeur J (2015) Temperature influences host instar selection in an aphid parasitoid: support for the relative fitness rule. Biol J Linn Soc 115:792–801

    Article  Google Scholar 

  • Nelson JM, Roitberg BD (1995) Flexible patch time allocation by the leafminer parasitoid, Opius dimidiatus. Ecol Entomol 20:245–252

    Article  Google Scholar 

  • Nylin S, Gotthard K (1998) Plasticity in life-history traits. Annu Rev Entomol 43:63–83

    Article  CAS  PubMed  Google Scholar 

  • Outreman Y, Le Ralec A, Wajnberg E, Pierre JS (2001) Can imperfect host discrimination explain partial patch exploitation in parasitoids? Ecol Entomol 26:271–280

    Article  Google Scholar 

  • Outreman Y, Le Ralec A, Wajnberg E, Pierre JS (2005) Effects of within- and among-patch experiences on the patch-leaving decision rules in an insect parasitoid. Behav Ecol Sociobiol 58:208–217

    Article  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org

  • Roeser-Mueller K, Strohm E, Kaltenpoth M (2010) Larval rearing temperature influences amount and composition of the marking pheromone of the male beewolf, Philanthus triangulum. J Insect Sci 10:74

    Article  PubMed  PubMed Central  Google Scholar 

  • Roitberg BD, Mangel M (1988) On the evolutionary ecology of marking pheromones. Evol Ecol 2:289–315

    Article  Google Scholar 

  • Roitberg BD, Mangel M, Lalonde RG, Roitberg CA, van Alphen JJM, Vet L (1992) Seasonal dynamic shifts in patch exploitation by parasitic wasps. Behav Ecol 3:156–165

    Article  Google Scholar 

  • Roitberg BD, Sircom J, Ca R, van Alphen JJM, Mangel M (1993) Life expectancy and reproduction. Nature 364:108

    Article  CAS  PubMed  Google Scholar 

  • Sentis A, Hemptinne JL, Brodeur J (2012) Using functional response modeling to investigate the effect of temperature on predator feeding rate and energetic efficiency. Oecologia 169:1117–1125

    Article  PubMed  Google Scholar 

  • Suzuki Y, Tsuji H, Sasakawa M (1984) Sex allocation and effects of superparasitism on secondary sex ratios in the gregarious parasitoid, Trichogramma chilonis (Hymenoptera: Trichogrammatidae). Anim Behav 32:478–484

    Article  Google Scholar 

  • Tenhumberg B, Keller MA, Possingham HP (2001) Using Cox’s proportional hazard models to implement optimal strategies: an example from behavioral ecology. Math Comput Model 33:597–607

    Article  Google Scholar 

  • Therneau TM, Grambsch PM, Fleming TR (1990) Martingale-based residuals for survival models. Biometrika 77:147–160

    Article  Google Scholar 

  • van Alphen JJM, Bernstein C (2008) Information acquisition, information processing, and patch time allocation in insect parasitoids. In: Wajnberg E, Bernstein C, van Alphen JJM (eds) Behavioral ecology of insect parasitoids, from theoretical approaches to field applications. Blackwell, Oxford, pp 92–112

    Google Scholar 

  • van Baaren J, Outreman Y, Boivin G (2005) Effect of low temperature exposure on oviposition behaviour and patch exploitation strategy in parasitic wasps. Anim Behav 70:153–163

    Article  Google Scholar 

  • van Roermund HJW, Hemerik L, Van Lenteren JC (1994) Influence of intrapatch experiences and temperature on the time allocation of the whitefly parasitoid Encarsia formosa (Hymenoptera: Aphelinidae). J Insect Behav 7:483–501

    Article  Google Scholar 

  • Vigneault C, Panneton C, Cormier D, Boivin G (1997) Automated system to quantify the behavior of small insects in a four-pointed star olfactometer. Appl Eng Agric 13:545–550

    Article  Google Scholar 

  • Waage JK (1979) Foraging for patchily-distributed hosts by the parasitoid, Nemeritis canescens. J Anim Ecol 48:353–371

    Article  Google Scholar 

  • Wajnberg E (2006) Time allocation strategies in insect parasitoids: from ultimate predictions to proximate behavioral mechanisms. Behav Ecol Sociobiol 60:589–611

    Article  Google Scholar 

  • Wajnberg E (2012) Multi-objective behavioural mechanisms are adopted by foraging animals to achieve several optimality goals simultaneously. J Anim Ecol 81:503–511

    Article  PubMed  Google Scholar 

  • Wajnberg E, Rosi MC, Colazza S (1999) Genetic variation in patch time allocation in a parasitic wasp. J Anim Ecol 68:121–133

    Article  Google Scholar 

  • Wajnberg E, Gonsard PA, Tabone E, Curty C, Lezcano N, Colazza S (2003) A comparative analysis of patch-leaving decision rules in a parasitoid family. J Anim Ecol 72:618–626

    Article  Google Scholar 

  • Wajnberg E, Curty C, Colazza S (2004) Genetic variation in the mechanisms of direct mutual interference in a parasitic wasp: consequences in terms of patch time allocation. J Anim Ecol 73:1179–1189

    Article  Google Scholar 

  • Wajnberg E, Hoffmeister TS, Coquillard P (2013) Optimal within-patch movement strategies for optimising patch residence time: an agent-based modelling approach. Behav Ecol Sociobiol 67:2053–2063

    Article  Google Scholar 

  • Wang XG, Keller MA (2002) A comparison of the host-searching efficiency of two larval parasitoids of Plutella xylostella. Ecol Entomol 27:105–114

    Article  CAS  Google Scholar 

  • Wang XG, Keller MA (2003) Patch time allocation by the parasitoid Diadegma semiclausum (Hymenoptera: Ichneumonidae). I Effect of interpatch distance. J Insect Behav 16:279–293

    Article  Google Scholar 

  • Ward SA, Chambers RJ, Sunderland K, Dixon AFG (1986) Cereal aphid populations and the relation between mean density and spatial variance. Neth J Plant Pathol 92:127–132

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Josiane Vaillancourt and Josée Doyon for their help during this study. We also would like to acknowledge the two anonymous reviewers for their helpful comments on a previous version of this manuscript.

This research was part of the project “Impact of climate change on synchronism between pests and their natural enemies” supported by the Consortium on Regional Climatology and Adaptation to Climate Change, OURANOS (Québec, Canada) and the Fonds vert of the Québec Ministry of Agriculture, Fisheries and Food.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joffrey Moiroux.

Additional information

Communicated by: Sven Thatje

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moiroux, J., Abram, P.K., Louâpre, P. et al. Influence of temperature on patch residence time in parasitoids: physiological and behavioural mechanisms. Sci Nat 103, 32 (2016). https://doi.org/10.1007/s00114-016-1357-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00114-016-1357-0

Keywords

Navigation