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Host Handling Time in a Polyembryonic Wasp is Affected both by Previous Experience and by Host State (Parasitized or Not)

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Abstract

Foraging behavior for hosts in parasitoids resembles that of predators with respect to finding, evaluating and manipulating of the prey. Host handling time may depend on the life history of the parasitoid and can be affected by oviposition experience. Additionally, handling time can be affected by host aggregation, species, size and state (parasitized or not). We studied handling times in the egg-larval parasitoid wasp Copidosoma koehleri. We allowed naïve female wasps to oviposit into three consecutive unparasitized hosts, and measured time until oviposition, and the duration of ovipositor insertion. We recorded the same data for naïve females ovipositing into already parasitized hosts. We found that both previous experience by females and previous parasitism of hosts reduced handling time. The results suggest that host handling durations reflect the interplay between host state and parasitoid internal state.

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References

  • Alcock J (2005) Animal behavior: an evolutionary approach. Sinauer Associates, Sunderland

    Google Scholar 

  • Amaya KE, Asgari S, Jung R, Hongskula M, Beckage NE (2005) Parasitization of Manduca sexta larvae by the parasitoid wasp Cotesia congregata induces an impaired host immune response. J Insect Physiol 51:505–512

    Article  PubMed  CAS  Google Scholar 

  • Andrew N, Basio M, Kim Y (2006) Additive effect of teratocyte and calyx fluid from Cotesia plutellae on immunosuppression of Plutella xylostella. Physiol Entomol 31:341–347

    Article  Google Scholar 

  • Ardeh MJ, de Jong PW, van Lenteren JC (2005) Selection of Bemisia nymphal stages for oviposition or feeding, and host-handling times of arrhenotokous and thelytokous Eretmocerus mundus and arrhenotokous E. eremicus. Biocontrol 50:449–463

    Article  Google Scholar 

  • Barzman MS, Daane KM (2001) Host-handling behaviours in parasitoids of the black scale: a case for ant-mediated evolution. J Anim Ecol 70:237–247

    Article  Google Scholar 

  • Bokononganta AH, Neuenschwander P, Vanalphen JJM, Vos M (1995) Host stage selection and sex allocation by Anagyrus Mangicola (Hymenoptera, Encyrtidae), a parasitoid of the mango mealybug, Rastrococcus Invadens (Homoptera, Pseudococcidae). Biol Control 5:479–486

    Article  Google Scholar 

  • Chow A, Mackauer M (1999) Host handling and specificity of the hyperparasitoid wasp, Dendrocerus carpenteri (Curtis) (Hym., Megaspilidae): importance of host age and species. J App Entomol 123:83–91

    Article  Google Scholar 

  • Conti E, Jones WA, Bin F, Vinson B (1997) Oviposition behavior of Anaphes iole, an egg parasitoid of Lygus hesperus (Hymenoptera: Mymaridae; Heteroptera: Miridae). Ann Entomol Soc Am 90:91–101

    Google Scholar 

  • Daane KM, Sime KR, Dahlsten DL, Andrews JW, Zuparko RL (2005) The biology of Psyllaephagus bliteus Riek (Hymenoptera: Encyrtidae), a parasitoid of the red gum lerp psyllid (Hemiptera: Psylloidea). Biol Control 32:228–235

    Article  Google Scholar 

  • Doutt RL (1947) Polyembryony in Copidosoma koehleri Blanchard. Am Nat 81:435–453

    Article  Google Scholar 

  • Giron D, Ross KG, Strand MR (2007) Presence of soldier larvae determines the outcome of competition in a polyembryonic wasp. J Evol Biol 20:165–172

    Article  PubMed  CAS  Google Scholar 

  • Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton

    Google Scholar 

  • Goubault ME, Fourrier J, Krespi L, Poinsot D, Cortesero AM (2004) Selection strategies of parasitized hosts in a generalist parasitoid depend on patch quality but also on host size. J Insect Behav 17:99–113

    Article  Google Scholar 

  • Gross P (1993) Insect behavioral and morphological defenses against parasitoids. Ann Rev Entomol 38:251–273

    Article  Google Scholar 

  • Guerrieri E, Noyes J (2005) Revision of the European species of Copidosoma Ratzeburg (Hymenoptera: Encyrtidae), parasitoids of caterpillars (Lepidoptera). Systematic Entomol 30:97–174

    Article  Google Scholar 

  • Haspel G, Rosenberg LA, Libersat F (2003) Direct injection of venom by a predatory wasp into cockroach brain. J Neurobiol 56:287–292

    Article  PubMed  Google Scholar 

  • Hays DB, Vinson SB (1971) Acceptence of Heliothis virescens (F.) (Lepidoptera, Noctuidae) as the host by the parasite Cardiochiles nigriceps viereck (Hymenoptera, Braconidae). Anim Behav 19:344–352

    Article  Google Scholar 

  • Heimpel GE, Rosenheim JA, Mangel M (1997) Predation on adult Aphytis parasitoids in the field. Oecologia 110:346–352

    Article  Google Scholar 

  • Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398

    Article  Google Scholar 

  • Horne PA (1990) The influence of introduced parasitoids on the potato moth, Phthorimaea operculella (Lepidoptera: Gelechiidae) in Victoria. Australia Bull Entomol Res 80:159–163

    Article  Google Scholar 

  • Keasar T, Segoli M, Barak R, Steinberg S, Giron D, Strand MR, Bouskila A, Harari AR (2006a) Costs and consequences of superparasitism in the polyembryonic parasitoid Copidosoma koehleri (Hymenoptera: Encyrtidae). Ecol Entomol 31:277–283

    Article  Google Scholar 

  • Keasar T, Sheffer N, Glusman G, Libersat F (2006b) Host-handling behavior: An innate component of foraging behavior in the parasitoid wasp Ampulex compressa. Ethology 112:699–706

    Article  Google Scholar 

  • Kfir R (1981) Fertility of the polyembryonic parasite Copidosoma koehleri, effect of humidities on life length and relative abundance as compared with that of Apanteles subandinus in Potato-Tuber Moth. Ann Appl Biol 99:225–230

    Article  Google Scholar 

  • Kfir R (2003) Biological control of the Potato Tuber Moth Phthorimaea operculella in Africa. In: Neuenschwander P, Borgemeister C, Langewald J (eds) Biological control in IPM systems in Africa. CABI, Cotonou, pp 77–85

    Google Scholar 

  • King BH (1994) How do female parasitoid wasps assess host size during sex-ratio manipulation. Anim Behav 48:511–518

    Article  Google Scholar 

  • Kouame KL, Mackauer M (1991) Influence of aphid size, age and behavior on host choice by the parasitoid wasp Ephedrus californicus—a test of host-size models. Oecologia 88:197–203

    Article  Google Scholar 

  • Libersat F (2003) Wasp uses venom cocktail to manipulate the behavior of its cockroach prey. J Comp Physiol [A] 189:497–508

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Mansfield S, Mills NJ (2004) A comparison of methodologies for the assessment of host preference of the gregarious egg parasitoid Trichogramma platneri. Biol Control 29:332–340

    Article  Google Scholar 

  • Mills NJ, Kuhlmann U (2004) Oviposition behavior of Trichogramma platneri Nagarkatti and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) in patches of single and clustered host eggs. Biol Control 30:42–51

    Article  Google Scholar 

  • Nurindah, Cribb BW, Gordh G (1999) Experience acquisition by Trichogramma australicum Girault (Hymenoptera: Trichogrammatidae). Aust J Entomol 38:115–119

    Article  Google Scholar 

  • Ode PJ, Strand MR (1995) Progeny and sex allocation decisions of the polyembryonic wasp Copidosoma floridanum. J Anim Ecol 64:213–224

    Article  Google Scholar 

  • Quicke DLJ (1997) Parasitic wasps. Chapman and Hall, London

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    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 

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

    Article  Google Scholar 

  • Rosenheim JA, Rosen D (1991) Foraging and oviposition decisions in the parasitoid Aphytis lingnanensis—Distinguishing the influences of egg load and experience. J Anim Ecol 60:873–893

    Article  Google Scholar 

  • Segoli M, Bouskila A, Harari AR, Keasar T (2009) Developmental patterns in the polyembryonic parasitoid wasp Copidosoma koehleri. Arthrop Struct Dev 38:84–90

    Article  Google Scholar 

  • Shettleworth SJ, Reid PJ, Plowright CMS (1993) The psychology of diet selection. In: Hughes RN (ed) diet selection. Blackwell Scientific Publications, Oxford, pp 56–77

    Google Scholar 

  • Sih A (1993) Effect of ecological interactions on forager diets: competition, predation risk, parasitism and prey behavior. In: Hughes RN (ed) Diet Selection. Blackwell Scientific Publications, Oxford, pp 182–213

    Google Scholar 

  • Slansky F (1986) Nutritional ecology of endoparasitic insects and their hosts—an overview. J Insect Physiol 32:255–261

    Article  Google Scholar 

  • Stephens DW (1993) Learning and behavioral ecology: incomplete information and environmental predictability. In: Papaj DR, Lewis AC (eds) Insect learning: ecological and evolutionary perspectives. Chapman & Hall, New York, pp 195–218

    Google Scholar 

  • Strand M (2003) Polyembryony. In Carde R, Resch V (eds) Encyclopedia of insects. Academic Press, pp. 928–932

  • Strand MR, Meola SM, Vinson SB (1986) Correlating pathological symptoms in Heliothis virescens eggs with development of the parasitoid Telenomus heliothidis. J Insect Physiol 32:389–402

    Article  Google Scholar 

  • Takasu K, Hirose Y (1991) The parasitoid Ooencyrtus nezarae (Hymenoptera, Encyrtidae) prefers hosts parasitized by conspecifics over unparasitized hosts. Oecologia 87:319–323

    Article  Google Scholar 

  • Vinson SB (1985) The behavior of parasitoids. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 9. Pergamon, New York, pp 417–469

    Google Scholar 

  • Vinson SB (1998) The general host selection behavior of parasitoid hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol Control 11:79–96

    Article  Google Scholar 

  • Vinson SB, Iwantsch GF (1980) Host regulation by insect parasitoids. Q Rev Biol 55:143–165

    Article  CAS  Google Scholar 

  • von Ende CN (1993) Repeated-measures analysis: growth and other time-dependent measures. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. New York, Chapman and Hall, pp 113–137

    Google Scholar 

  • Weisser WW, Houston AI, Volkl W (1994) Foraging strategies in solitary parasitoids—the trade-off between female and offspring mortality risks. Evol Ecol 8:587–597

    Article  Google Scholar 

  • Wiedemann LM, Canto-Silva CR, Romanowski HP, Redaelli LR (2003) Oviposition behaviour of Gryon gallardoi (Hym.; Scelionidae) on eggs of Spartocera dentiventris (Hem.; Coreidae). Braz J of Biol 63:133–139

    CAS  Google Scholar 

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Acknowledgments

We thank Ori Becher, Sara Baranes, Adi Sadeh, and Daphna Gottlieb for assistance and discussions. This research was supported by THE ISRAEL SCIENCE FOUNDATION (grant No. 184/06)

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Correspondence to Michal Segoli.

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Segoli, M., Harari, A.R., Bouskila, A. et al. Host Handling Time in a Polyembryonic Wasp is Affected both by Previous Experience and by Host State (Parasitized or Not). J Insect Behav 22, 501–510 (2009). https://doi.org/10.1007/s10905-009-9189-9

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  • DOI: https://doi.org/10.1007/s10905-009-9189-9

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