Skip to main content
Log in

Time allocation strategies in insect parasitoids: from ultimate predictions to proximate behavioral mechanisms

  • Review
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

As most parasitoids are time limited, they usually die before they have laid all their eggs. In such cases, optimal foraging theory predicts that female parasitoids will adopt behavioral reproductive strategies enabling them to maximize progeny production per unit of time. One key situation in which parasitoid females must optimize their time budget is related to the fact that most of their hosts are distributed in discrete patches in the environment. In this review, I first present the results of basic theoretical models predicting female wasp search duration on a patch of hosts. I then compile and analyze all studies investigating the effect of different factors on parasitoid patch time allocation and patch-leaving decision rules. Different patch-leaving mechanisms that were proposed to explain the results obtained are discussed, along with statistical methods that should be used to estimate them from experimental data. Finally, ideas for future research are presented.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

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

    Google Scholar 

  • Andersen PK (1982) Testing goodness of fit of Cox’s regression and life model. Biometrics 38:67–77

    Google Scholar 

  • Basset A, Fedele M, DeAngelis DL (2002) Optimal exploitation of spatially distributed trophic resources and population stability. Ecol Model 151:245–260

    Google Scholar 

  • Bell WJ (1991) Searching behaviour. The behavioural ecology of finding resources. Chapman and Hall

  • Bernstein C, Driessen G (1996) Patch-marking and optimal search patterns in the parasitoid Venturia canescens. J Anim Ecol 65:211–219

    Google Scholar 

  • Bernstein C, Kacelnik A, Krebs JR (1988) Individual decisions and the distribution of predators in a patchy environment. J Anim Ecol 57:1007–1026

    Google Scholar 

  • Bernstein C, Kacelnik A, Krebs JR (1991) Individual decisions and the distribution of predators in a patchy environment. II. The influence of travel costs and structure of the environment. J Anim Ecol 60:205–225

    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

    PubMed  Google Scholar 

  • Bressers M, Meelis E, Haccou P, Kruk M (1991) When did it really start or stop: the impact of censored observations on the analysis of duration. Behav Processes 23:1–20

    Google Scholar 

  • Carter MC, Dixon AFG (1982) Habitat quality and the foraging behaviour of coccinellid larvae. J Anim Ecol 51:865–878

    Google Scholar 

  • Casas J, Gurney WSC, Nisbet R, Roux O (1993) A probabilistic model for the functional response of a parasitoid at the behavioural time-scale. J Anim Ecol 62:194–204

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Charnov EL, Skinner SW (1984) Evolution of host selection and clutch size in parasitoid wasps. Fla Entomol 67:5–21

    Google Scholar 

  • Clark CW, Mangel M (2000) Dynamic state variable models in ecology. Methods and applications. Oxford University Press

  • Cloutier C, Bauduin F (1990) Searching behavior of the aphid parasitoid Aphidius nigripes (Hymenoptera: Aphidiidae) foraging on potato plants. Environ Entomol 19:222–228

    Google Scholar 

  • Collett D (1994) Modelling survival data in medical research. Chapman and Hall

  • Comins HN, Hassell MP (1979) The dynamics of optimally foraging predators and parasitoids. J Anim Ecol 48:335–351

    Google Scholar 

  • Cook RM, Hubbard SF (1977) Adaptive searching strategies in insect parasites. J Anim Ecol 46:115–125

    Google Scholar 

  • Cox DR (1972) Regression models and life tables. J R Stat Soc B 74:187–220

    Google Scholar 

  • Cronin JT, Strong DR (1999) Dispersal-dependent oviposition and the aggregation of parasitism. Am Nat 154:23–36

    Google Scholar 

  • Desneux N, Wajnberg E, Fauvergue X, Privet S, Kaiser L (2004) Oviposition behaviour and patch-time allocation in two aphid parasitoids exposed to deltamethrin residues. Entomol Exp Appl 112:227–235

    CAS  Google Scholar 

  • Dicke M, van Lenteren JC, Boskamp GJF, van Voorst R (1985) Intensification and prolongation of host searching in Leptopilina heterotoma (Thomson) (Hymenoptera: Eucoilidae) through a kairomone produced by Drosophila melanogaster. J Chem Ecol 11:125–136

    CAS  Google Scholar 

  • Driessen G, Bernstein C (1999) Patch departure mechanisms and optimal host exploitation in an insect parasitoid. J Anim Ecol 68:445–459

    Google Scholar 

  • Driessen G, Hemerik L (1992) The time and egg budget of Leptopilina clavipes, a parasitoid of larval Drosophila. Ecol Entomol 17:17–27

    Google Scholar 

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

    Google Scholar 

  • Emlen JM (1966) The role of time and energy in food preference. Am Nat 100:611–617

    Google Scholar 

  • Field SA (1998) Patch exploitation, patch-leaving and pre-emptive patch defence in the parasitoid wasp Trissolcus basalis (Insecta: Scelionidae). Ethology 104:323–338

    Article  Google Scholar 

  • Fretwell SD, Lucas HL (1970) On territorial behaviour and other factors influencing habitat distribution in birds. Acta Biotheor 19:16–36

    Google Scholar 

  • Galis F, van Alphen JJM (1981) Patch time allocation and search intensity of Asobara tabida Nees (Braconidae), a larval parasitoid of Drosophila. Neth J Zool 31:596–611

    Google Scholar 

  • Gardner SM, van Lenteren JC (1986) Characterisation of the arrestment responses of Trichogramma evanescens. Oecologia 68:265–270

    Google Scholar 

  • Gibb JA (1962) Tinbergen’s hypothesis of the role of specific search images. Ibis 104:106–111

    Google Scholar 

  • Giraldeau LA (1997) The ecology of information use. In: Krebs JR, Davies NB (eds) Behavioral ecology, 4th edn. Blackwell Science, pp 42–68

  • Godfray HCJ (1994) Parasitoids. Behavioral and evolutionary ecology. Princeton University Press

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

    Google Scholar 

  • Green RF (1987) Stochastic models of optimal foraging. In: Kamil AC, Krebs JR, Pulliam HR (eds) Foraging behaviour. Plenum, New York, pp 273–302

    Google Scholar 

  • Green RF, Ayal Y (1998) A simple Markov model for the assessment of host patch quality by foraging parasitoids. Oecologia 116:456–466

    Google Scholar 

  • Haccou P, Hemerik L (1985) The influence of larval dispersal in the cinnabar moth (Tyria jacobaeae) on predation by the red wook and (Formica polyctena): an analysis based on the proportional hazards model. J Anim Ecol 54:755–769

    Google Scholar 

  • Haccou P, Meelis E (1992) Statistical analysis of behavioural data. An approach based on time-structured models. Oxford University Press

  • Haccou P, de Vlas SJ, van Alphen JJM, Visser ME (1991) Information processing by foragers: effects on intra-patch experience on the leaving tendency of Leptopilina heterotoma. J Anim Ecol 60:93–106

    Google Scholar 

  • Haccou P, Sjerps M, van der Meijden E (1999) To leave or to stay, that is the question: prediction from models of patch-leaving strategies. In: Olff H, Brown VK, Drent RH (eds) Herbivores: between plants and predators. Blackwell Science, pp 85–108

  • Haccou P, Glaizot O, Cannings C (2003) Patch leaving strategies and superparasitism: an asymmetric generalised war of attrition. J Theor Biol 225:77–89

    PubMed  Google Scholar 

  • Hamelin F, Bernhard P, Nain P, Wajnberg E (2006a) Foraging under competition: evolutionarily stable patch-leaving strategies with random arrival times. 1. Scramble competition. Annals of Dynamic Games, Birkhauser (In press)

  • Hamelin F, Bernhard P, Shaiju AJ, Wajnberg E (2006b). Foraging under competition: evolutionarily stable patch-leaving strategies with random arrival times. 2. Interference competition. Annals of Dynamic Games, Birkhauser (In press)

  • Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford series in ecology and evolution. Oxford University Press

  • Hassell MP (1971) Mutual interference between searching insect parasites. J Anim Ecol 40:473–486

    Google Scholar 

  • Hassell MP (1978) The dynamics of arthropod predator–prey systems. Princeton University Press

  • Hassell MP, May RM (1974) Aggregation in predators and insect parasites and its effect on stability. J Anim Ecol 43:567–594

    Google Scholar 

  • Hassell MP, Southwood TRE (1978) Foraging strategies of insects. Ann Rev Ecolog Syst 9:75–98

    Google Scholar 

  • Heimpel GE, Rosenheim JA, Mangel M (1996) Egg limitation, host quality, and dynamic behavior by a parasitoid in the field. Ecology 77:2410–2420

    Google Scholar 

  • Hemerik L, Driessen G, Haccou P (1993) Effects of intra-patch experiences on patch time, search time and searching efficiency of the parasitoid Leptopilina clavipes. J Anim Ecol 62:33–44

    Google Scholar 

  • Henneman ML (1998) Maximization of host encounters by parasitoids foraging in the field: females can use simple rule. Oecologia 116:467–474

    Google Scholar 

  • Hertlein MB, Thorarinsson K (1987) Variable path times and the functional response of Leptopilina boulardi. Environ Entomol 16:593–598

    Google Scholar 

  • Hirose Y, Ehlers LE, Hirose Y (2003) Influence of host age on patch use by a quasi-gregarious egg parasitoid. Environ Ecol 32:789–796

    Google Scholar 

  • Houston AI (1987) The control of foraging decisions. In: Commons ML, Kacelnik A, Shettleworth SJ (eds) Quantitative analyses of behavior. Foraging, vol 4. Erlbaum, pp 41–61

  • Houston AI, Clark CW, McNamara JM, Mangel M (1988) Dynamic models in behavioral and evolutionary ecology. Nature 332:29–34

    Google Scholar 

  • Hubbard SF, Cook RM (1978) Optimal foraging by parasitoid wasps. J Anim Ecol 47:593–604

    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

    Google Scholar 

  • Janssen A (1989) Optimal host selection by Drosophila parasitoids in the field. Funct Ecol 3:469–476

    Google Scholar 

  • Kalbfleisch JD, Prentice RL (2002) The statistical analysis of failure time data, 2nd edn. Wiley, New York

    Google Scholar 

  • Keasar T, Ney-Nifle M, Mangel M, Swezey S (2001) Early oviposition experience affects patch residence time in a foraging parasitoid. Entomol Exp Appl 98:123–132

    Google Scholar 

  • Krebs JR (1973) Behavioral aspects of predation. In: Bateson PPG, Klopfer PH (eds) Perspectives in ethology. Plenum, pp 73–111

  • Lessells CM (1985) Parasitoid foraging: should parasitism be density dependent? J Anim Ecol 54:27–41

    Google Scholar 

  • Lessells CM (1995) Putting resource dynamics into continuous input ideal free distribution models. Anim Behav 49:487–494

    Google Scholar 

  • Li C, Roitberg BD, Mackauer M (1993) Patch residence time and parasitism of Aphelinus asychis: a simulation model. Ecol Model 69:227–241

    Google Scholar 

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

    Google Scholar 

  • MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609

    Google Scholar 

  • Martins EP (1996) Phylogenies and the comparative method in animal behaviour. Oxford University Press

  • Maynard Smith J (1982) Evolution and the theory of games. Cambridge University Press

  • McNair JM (1982) Optimal giving-up time and the marginal value theorem. Am Nat 119:511–529

    Google Scholar 

  • McNamara JM, Houston AI (1985) Optimal foraging and learning. J Theor Biol 117:231–249

    Google Scholar 

  • McNamara JM, Houston AI (1986) The common currency for behavioural decisions. Am Nat 127:358–378

    Google Scholar 

  • McNamara JM, Houston AI (1987) Memory and the efficient use of information. J Theor Biol 125:285–395

    Google Scholar 

  • Michaud JP, Mackauer M (1995) Oviposition behavior of Monoctonus paulensis (Hymenoptera: Aphidiidae): factors influencing reproductive allocation to hosts and host patches. Ann Entomol Soc Am 88:220–226

    Google Scholar 

  • Morrison G, Lewis WJ (1981) The allocation of searching time by Trichogramma pretiosum in host-containing patches. Entomol Exp Appl 30:31–39

    Google Scholar 

  • Moya-Laraño J, Wise DH (2000) Survival analysis: a powerful tool for evaluating fighting and assessment. Anim Behav 60:307–313

    PubMed  Google Scholar 

  • Murdoch WW, Oaten A (1975) Predation and population stability. Adv Ecol Res 9:2–132

    Google Scholar 

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

    Google Scholar 

  • Newman JA (1991) Patch use under predation hazard: foraging behavior in a simple stochastic environment. Oikos 61:29–44

    Google Scholar 

  • Nonacs P (2001) State dependent behavior and the Marginal Value Theorem. Behav Ecol 12:71–83

    Google Scholar 

  • Ohara Y, Takafuji A, Takabayashi J (2003) Factors affecting the patch-leaving decision of the parasitic wasp Diadegma semiclausum (Hymenoptera: Ichneumonidae). Appl Entomol Zool 38:211–214

    Google Scholar 

  • Ohno K (1999) Brood guarding in Trissolcus basalis (Watanabe) (Hymenoptera: Scelionidae), an egg parasitoid of the brown-winged Green Bug, Plautia crossata stali Scott (Heteroptera: Pentatomidae). Entomol Sci 2:41–47

    Google Scholar 

  • Ollason JG (1980) Learning to forage—optimally? Theor Popul Biol 18:44–56

    PubMed  CAS  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

    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

    Google Scholar 

  • Papaj DR, Snellen H, Swaans K, Vet LEM (1994) Unrewarding experiences and their effect on foraging in the parasitic wasp Leptopilina heterotoma (Hymenoptera: Eucoilidae). J Insect Behav 7:465–481

    Google Scholar 

  • Pierre JS, van Baaren J, Boivin G (2003) Patch leaving decision rules in parasitoids: do they use sequential decisional sampling? Behav Ecol Sociobiol 54:147–155

    Google Scholar 

  • Reeve JD (1987) Foraging behavior of Aphytis melinus: effects of patch density and host size. Ecology 68:530–538

    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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Romstöck-Völkl M (1990) Host refuges and spatial patterns of parasitism in an endophytic host–parasitoid system. Ecol Entomol 15:321–331

    Google Scholar 

  • Rosenheim JA (1996) An evolutionary argument for egg limitation. Evolution 50:2089–2094

    Google Scholar 

  • Rosenheim JA (1999) The relative contributions of time and eggs to the cost of reproduction. Evolution 53:376–385

    Google Scholar 

  • Rosenheim JA, Mangel M (1994) Patch-leaving rules for parasitoids with imperfect host discrimination. Ecol Entomol 19:374–380

    Google Scholar 

  • Schal C, Tobin TR, Surber JL, Vogel G, Tourtellot MK, Leban RA, Sizemore R, Bell WJ (1983) Search strategy of sex pheromone-stimulated male German cockroaches. J Insect Physiol 29:575–579

    Google Scholar 

  • Seventer JG, Ellers J, Driessen G (1998) An evolutionary argument for time limitation. Evolution 52:1241–1244

    Google Scholar 

  • Shaltiel L, Ayal Y (1998) The use of kairomones for foraging decisions by an aphid parasitoid in small host aggregations. Ecol Entomol 23:319–329

    Google Scholar 

  • Sjerps M, Haccou P (1994) Effect of competition on optimal patch leaving: a war of attrition. Theor Popul Biol 46:300–318

    Google Scholar 

  • Skinner SW (1985) Clutch size as an optimal foraging problem for insects. Behav Ecol Sociobiol 17:231–238

    Google Scholar 

  • Stamp NE (1982) Searching behaviour of parasitoids for web-making caterpillars: a test of optimal searching theory. J Anim Ecol 52:387–395

    Google Scholar 

  • Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press

  • Stillman RA, Sutherland WJ (1990) The optimal search path in a patchy environment. J Theor Biol 145:177–182

    Google Scholar 

  • Strand MR, Vinson SB (1982) Behavioral response of the parasitoid Cardiochiles nigriceps to a kairomone. Entomol Exp Appl 31:308–315

    CAS  Google Scholar 

  • Sugimoto T, Tsujimoto S (1988) Stopping rule of host searching by the parasitoid, Chrysocharis pentheus (Hymenoptera: Eulophidae), in host patches. Res Popul Ecol 30:123–133

    Google Scholar 

  • Sugimoto T, Murakami H, Yamazaki R (1987) Foraging for patchily-distributed leaf-miners by the parasitoid, Dapsilarthra rufiventris (Hymenoptera: Braconidae). J Ethol 5:95–103

    Google Scholar 

  • Sugimoto T, Minkenberg OPJM, Takabayashi J, Dicke M, van Lenteren JC (1990) Foraging for patchily-distributed leaf miners by the parasitic wasp, Dacnusa sibirica. Res Popul Ecol 32:381–389

    Google Scholar 

  • Sutherland WJ (1983) Aggregation and the ‘ideal free’ distribution. J Anim Ecol 52:821–828

    Google Scholar 

  • Sutherland WJ (1996) From individual behaviour to population ecology. Oxford University Press

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

    Google Scholar 

  • Tenhumberg B, Keller MA, Possingham HP, Tyre AJ (2001b) Optimal patch-leaving behaviour: a case study using the parasitoid Cotesia rubecula. J Anim Ecol 70:683–691

    Google Scholar 

  • Tentelier C, Wajnberg E, Fauvergue X (2005) Parasitoids use herbivore-induced information to optimise their patch residence time. Ecol Entomol 30:737–744

    Google Scholar 

  • Tentelier C, Desouhant M, Fauvergue X (2006). Habitat assessment by parasitoids: mechanisms for patch use behavior. Behav Ecol (In press)

  • Thiel A, Hoffmeister TS (2004) Knowing your habitat: linking patch-encounter rate and patch exploitation in parasitoids. Behav Ecol 15:419–425

    Google Scholar 

  • Thiel A, Driessen G, Hoffmeister TS (2006) Different habitats, different habits? Response to foraging information in the parasitic wasp Venturia canescens. Behav Ecol Sociobiol 59:614–623

    Google Scholar 

  • Thompson JN (1986) Oviposition behaviour and searching efficiency in a natural population of braconid parasitoid. J Anim Ecol 55:351–360

    Google Scholar 

  • Turlings TCJ, Wäckers FL, Vet LEM, Lewis WJ, Tumlinson JH (1993) Learning of host-finding cues by hymenopterous parasitoids. In: Papaj DR, Lewis AC (eds) Insect learning. Chapman and Hall, pp 51–78

  • van Alphen JJM (1988) Patch-time allocation by insect parasitoids: superparasitism and aggregation. In: de Jong G (ed) Population genetics and evolution. Springer, pp 216–221

  • van Alphen JJM (1993) Patch residence time and encounters with parasitised hosts: a reaction. Neth J Zool 43:340–349

    Google Scholar 

  • van Alphen JJM, Galis F (1983) Patch time allocation and parasitization efficiency of Asobara tabida, a larval parasitoid of Drosophila. J Anim Ecol 52:937–952

    Google Scholar 

  • van Alphen JJM, Vet LEM (1986) An evolutionary approach to host finding and selection. In: Waage J, Greathead D (eds) Insect parasitoids. Academic Press, pp 23–61

  • van Alphen JJM, Bernstein C, Driessen G (2003) Information acquisition and time allocation in insect parasitoids. Trends Ecol Evol 18:81–87

    Google Scholar 

  • van Alphen JJM, van Lenteren JC, Nell HW, Eebes H (1984) The response of a polyphagous parasitoid (Leptopilina heterotoma (Thomson)) to a kairomone produced by one of its hosts (Drosophila melanogaster Meigen). Neth J Zool 34:215–219

    Google Scholar 

  • van Baaren J, Boivin G, Outreman Y (2005a) Patch exploitation strategy by an egg parasitoid in constant or variable environment. Ecol Entomol 30:502–509

    Google Scholar 

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

    Google Scholar 

  • van der Meer J (1997) The ideal free distribution when predators differ in competitive abilities. Oikos 80:301–310

    Google Scholar 

  • van Dijken MJ, van Stratum P, van Alphen JJM (1992) Recognition of individual-specific marked parasitized hosts by the solitary parasitoid Epidinocarsis lopezi. Behav Ecol Sociobiol 30:77–82

    Google Scholar 

  • van Lenteren JC (1991) Encounters with parasitized hosts: to leave or not to leave a patch. Neth J Zool 41:144–157

    Google Scholar 

  • van Lenteren JC, Bakker K (1978) Behavoural aspects of the functional responses of a parasite (Pseudeucoila bochei Weld) to its host (Drosophila melanogaster). Neth J Zool 28:213–233

    Article  Google Scholar 

  • van Roermund HJW, Hemerik L, van Lenteren JC (1993) The leaving tendency of the parasitoid Encarsia formosa foraging for whitefly on tomato leaflets. Exp App Entomol 4:53–60

    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

    Google Scholar 

  • van Steenis MJ, El-Khawass MH, Hemerik L, van Lenteren JC (1996) Time allocation of the parasitoid Aphidius colemani (Hymenoptera: Aphidiidae) foraging for Aphis gossypii (Homoptera: Aphidae) on cucumber leaves. J Insect Behav 9:283–295

    Google Scholar 

  • Varaldi J, Fouillet P, Boulétreau M, Fleury F (2005) Superparasitism acceptance and patch-leaving mechanisms in parasitoids: a comparison between two sympatric species. Anim Behav 69:1227–1234

    Google Scholar 

  • Vet LEM, Schoonman G (1988) The influence of previous foraging experience on microhabitat acceptance in Leptopilina heterotoma. J Insect Behav 1:387–392

    Google Scholar 

  • Vet LEM, van der Hoeven R (1984) Comparison of the behavioural response of two Leptopilina species (Hymenoptera: Eucoilidae), living in different microhabitats, to kairomone of their host (Drosophilidae). Neth J Zool 34:220–227

    Google Scholar 

  • Visser ME, van Alphen JJM, Nell HW (1990) Adaptive superparasitism and patch time allocation in solitary parasitoids: The influence of the number of parasitoids depleting a patch. Behaviour 114:21–36

    Google Scholar 

  • Visser ME, van Alphen JJM, Hemerik L (1992a) Adaptive superparasitism and patch time allocation in solitary parasitoids: an ESS model. J Anim Ecol 61:93–101

    Google Scholar 

  • Visser ME, van Alphen JJM, Nell HW (1992b) Adaptive superparasitism and patch time allocation in solitary parasitoids: the influence of pre-patch experience. Behav Ecol Sociobiol 31:163–171

    Google Scholar 

  • Völkl W (1994) Searching at different spatial scales: the foraging behaviour of the aphid parasitoid Aphidius rosae in rose bushes. Oecologia 100:177–183

    Google Scholar 

  • Völkl W, Kranz P, Weisser W, Hübner G (1995) Patch time allocation and resource exploitation in aphid primary parasitoids and hyperparasitoids searching simultaneously within aphid colonies. J Appl Entomol 119:399–404

    Article  Google Scholar 

  • Vos M, Hemerik L, Vet LEM (1998) Patch exploitation by the parasitoids Cotesia rubecula and Cotesia glomerata in multi-patch environments with different host distributions. J Anim Ecol 67:774–783

    Google Scholar 

  • Waage JK (1978) Arrestment responses of the parasitoid, Nemeritis canescens, to a contact chemical produced by its host, Plodia interpunctella. Physiol Entomol 3:135–146

    Google Scholar 

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

    Google Scholar 

  • Waage JK (1983) Aggregation in field parasitoid populations: foraging time allocation by a population of Diadegma (Hymenoptera: Ichneumonidae). Ecol Entomol 8:447–453

    Google Scholar 

  • Waage JK (1990) Ecological theory and the selection of biological control agents. In: Mackauer M, Ehler LE, Roland J (eds) Critical issues in biological control. Intercept, pp 135–157

  • Wajnberg E (2004) Measuring genetic variation in natural enemies used for biological control: why and how? In: Ehler L, Sforza R, Mateille T (eds) Genetics, evolution and biological control. CAB International, pp 19–37

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

    Google Scholar 

  • Wajnberg E, Fauvergue X, Pons O (2000) Patch leaving decision rules and the Marginal Value Theorem: an experimental analysis and a simulation model. Behav Ecol 11:577–586

    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

    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

    Google Scholar 

  • Wajnberg E, Bernhard P, Hamelin F, Boivin G (2006) Optimal patch time allocation for time-limited foragers. Behav Ecol Sociobiol 60:1–10

    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

    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

    Google Scholar 

  • Wang XG, Keller MA (2004) Patch-time allocation by the parasitoid Diadegma semiclausum (Hymenoptera: Ichneumonidae). III. Effects of kairomone sources and previous parasitism. J Insect Behav 17:761–776

    Google Scholar 

  • Wang XG, Keller MA (2005) Patch time allocation by the parasitoid Diadegma semiclausum (Hymenoptera: Ichneumonidae). II. Effect of host density and distribution. J Insect Behav 18:171–186

    Google Scholar 

  • Wang XG, Messing RH (2003) Foraging behaviour and patch time allocation by Fopius arisanus (Hymenoptera: Braconidae), an egg-larval parasitoid of tephritid fruit flies. J Insect Behav 16:593–612

    Google Scholar 

  • Wanntorp HE (1983) Historical constraints in the adaptation theory: traits and non-traits. Oikos 41:157–160

    Google Scholar 

  • Weisser WW (1994) Age-dependent foraging behaviour and host-instar preference of the aphid parasitoid Lysiphlebus cardui. Entomol Exp Appl 70:1–10

    Google Scholar 

  • Weisser WW (1995) Within-patch foraging behaviour of the aphid parasitoid Aphidius funebris: plant architecture, host behaviour, and individual variation. Entomol Exp Appl 76:133–141

    Google Scholar 

  • Wiskerke JSC, Vet LEM (1994) Foraging for solitary and gregariously feeding caterpillars: a comparison of two related parasitoid species (Hymenoptera: Braconidae). J Insect Behav 7:585–603

    Google Scholar 

  • Yamamura N, Tsuji N (1987) Optimal patch time under exploitative competition. Am Nat 129:553–567

    Google Scholar 

  • Yano E (1978) A simulation model of searching behaviour of a parasite. Res Popul Ecol 20:105–122

    Google Scholar 

Download references

Acknowledgements

E. Mondor is thanked for his comments on an earlier version of the manuscript. This work is part of GDR 2155 ‘Ecologie Comportementale’ (CNRS commission 29) and the ESF/BEPAR scientific program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Éric Wajnberg.

Additional information

Communicated by H. Kokko

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wajnberg, É. Time allocation strategies in insect parasitoids: from ultimate predictions to proximate behavioral mechanisms. Behav Ecol Sociobiol 60, 589–611 (2006). https://doi.org/10.1007/s00265-006-0198-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-006-0198-9

Keywords

Navigation