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State-dependent host acceptance in the parasitoid Copidosoma koehleri: the effect of intervals between host encounters

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Abstract

Choosing suitable hosts is an important component of parasitoid fitness. Many parasitoids reject already-parasitized hosts. In some species, females reject hosts in which they had recently oviposited, but accept these hosts minutes or hours later. Parasitoids were suggested to mark hosts with repellent pheromones at oviposition and to accept them again after the mark fades. We tested a complementary hypothesis, stating that parasitoids’ host acceptance thresholds decrease with time since their previous oviposition because of a change in internal state, independent of the hosts’ deterrent marking. We scored the acceptance of hosts (eggs of the moth Phthorimaea operculella, Gelechiidae) by Copidosoma koehleri (Encyrtidae) parasitoids in single-choice experiments. Acceptance of self-parasitized (low-quality) hosts increased with time since the wasps’ previous host encounter. The wasps accepted two non-parasitized (high-quality) hosts within a 5-s presentation interval, indicating that they are physiologically able to oviposit twice in quick succession. Parasitized hosts, presented after varying time intervals to conspecifics with uniform host encounter experience, were accepted at similar frequencies. However, as predicted by the working hypothesis, increasing the time elapsed since the wasps’ last oviposition significantly enhanced the acceptance rates of hosts that had been parasitized by conspecifics 2 min earlier. Learning of host-associated cues during oviposition may enable wasps to identify and reject parasitized hosts, while fading of this association from their short-term memory during periods with no host encounters could trigger acceptance of parasitized hosts. State-dependent host acceptance may adaptively allow wasps to avoid self-superparasitism and to adjust conspecific superparasitism rates to foraging conditions.

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References

  • Ardeh MJ, de Jong PW, van Lenteren JC (2005) Intra- and interspecific host discrimination in arrhenotokous and thelytokous Eretmocerus spp. Biol Control 33:74–80

    Article  Google Scholar 

  • Babendreier D, Hoffmeister TS (2002) Superparasitism in the solitary ectoparasitoid Aptesis nigrocincta: the influence of egg load and host encounter rate. Entomol Exp Appl 105:63–69

    Article  Google Scholar 

  • Bügler M, Rempoulakis P, Shacham R, Keasar T, Thuijsman F (2013) Sex allocation in a polyembryonic parasitoid with female soldiers: an evolutionary simulation and an experimental test. PLoS One 8(6):e64780

    Article  PubMed Central  PubMed  Google Scholar 

  • Chow FJ, Mackauer M (1986) Host discrimination and larval competition in the aphid parasite Ephedrus californicus. Entomol Exp Appl 41:243–254

    Article  Google Scholar 

  • Colinet H, Salin C, Boivin G, Hance TH (2005) Host age and fitness-related traits in a koinobiont aphid parasitoid. Ecol Entomol 30:473–479

    Article  Google Scholar 

  • Dorn S, Beckage NE (2007) Superparasitism in gregarious hymenopteran parasitoids: ecological, behavioural and physiological perspectives. Physiol Entomol 32:199–211

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543

    Article  Google Scholar 

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

  • Hardy IC, Blackburn TM (1991) Brood guarding in a bethylid wasp. Ecol Entomol 16:55–62

    Article  Google Scholar 

  • Hubbard SF, Harvey IF, Fletcher JP (1999) Avoidance of superparasitism: a matter of learning? Anim Behav 57:1193–1197

    Article  PubMed  Google Scholar 

  • Islam KS, Copland MJW (2000) Influence of egg load and oviposition time interval on the host discrimination and offspring survival of Anagyrus pseudococci (Hymenoptera: Encyrtidae), a solitary endoparasitoid of citrus mealybug, Planococcus citri (Hemiptera: Pseudococcidae). Bull Entomol Res 90:69–75

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Keinan Y, Kishinevsky M, Segoli M, Keasar T (2012) Repeated probing of hosts: an important component of superparasitism. Behav Ecol 23:1263–1268

    Article  Google Scholar 

  • Lampert EC, Bowers MD (2010) Host plant species affects the quality of the generalist Trichoplusia ni as a host for the polyembryonic parasitoid Copidosoma floridanum. Entomol Exp Appl 134:287–295

    Article  Google Scholar 

  • Lebreton S, Christidès JP, Bagnères AG, Chevrier C, Darrouzet E (2010) Modifications of the chemical profile of hosts after parasitism allow parasitoid females to assess the time elapsed since the first attack. J Chem Ecol 36:513–521

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Zhao B, Bonjour E (2012) Host marking and host discrimination in phytophagous insects. In: Liu T, Kang L (eds) Recent advances in entomological research. Springer, Heidelberg, Dordrecht, London, New York, pp 73–85

    Chapter  Google Scholar 

  • McKay T, Broce AB (2004) Discrimination of self-parasitized hosts by the pupal parasitoid Muscidifurax zaraptor (Hymenoptera: Pteromalidae). Ann Entomol Soc Am 97:592–599

    Article  Google Scholar 

  • Mehrnejad MR, Copland MJW (2007) Host discrimination by the endoparasitoid Psyllaephagus pistaciae (Hymenoptera: Encyrtidae): a case of time-dependent ability. Biocontrol Sci Tech 17:401–411

    Article  Google Scholar 

  • Nufio CR, Papaj DR (2001) Host marking behavior in phytophagous insects and parasitoids. Entomol Exp Appl 99:273–293

    Article  Google Scholar 

  • Ode PJ, Heinz KM (2002) Host-size-dependent sex ratio theory and improving mass-reared parasitoid sex ratios. Biol Control 24:31–41

    Article  Google Scholar 

  • Outreman Y, Le Ralec A, Plantegenest M, Chaubet B, Pierre JS (2001) Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability. J Insect Physiol 47:339–348

    Article  CAS  PubMed  Google Scholar 

  • Roitberg BD, Prokopy RJ (1983) Host deprivation influence on response of Rhagoletis pomonella to its oviposition deterring pheromone. Physiol Entomol 8:69–72

    Article  Google Scholar 

  • Rosi MC, Isidoro N, Colazza S, Bin F (2001) Source of the host marking pheromone in the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). J Insect Physiol 47:989–995

    Article  CAS  PubMed  Google Scholar 

  • Ruther J (2013) Novel insights into pheromone-mediated communication in parasitic hymenopterans. Chemical ecology of insect parasitoids. Wiley, Chichester, pp 112–144

    Book  Google Scholar 

  • Santolamazza-Carbone S, Rodrıguez-Illamola A, Cordero Rivera A (2004) Host finding and host discrimination ability in Anaphes nitens Girault, an egg parasitoid of the Eucalyptus snout-beetle Gonipterus scutellatus Gyllenhal. Biol Control 29:24–33

    Article  Google Scholar 

  • Segoli M, Bouskila A, Harari A, Keasar T (2009) Brood size in a polyembryonic parasitoid wasp is affected by the relatedness among competing larvae. Behav Ecol 20:761–767

    Article  Google Scholar 

  • Segoli M, Keasar T, Bouskila A, Harari AR (2010) Host choice decisions in the polyembryonic wasp Copidosoma koehleri (Hymenoptera: Encyrtidae). Physiol Entomol 35:40–45

    Article  Google Scholar 

  • Sirot E, Ploye H, Bernstein C (1997) State dependent superparasitism in a solitary parasitoid: egg load and survival. Behav Ecol 8:226–232

    Article  Google Scholar 

  • Stelinski LL, Oakleaf R, Rodriguez-Saona C (2007) Oviposition-deterring pheromone deposited on blueberry fruit by the parasitic wasp, Diachasma alloeum. Behaviour 144:429–446

    Article  Google Scholar 

  • Strand MR, Obrycki JJ (1996) Host specificity of insect parasitoids and predators. Bioscience 46:422–429

    Article  Google Scholar 

  • Ueno T, Tanaka T (1996) Self–host discrimination by a parasitic wasp: the role of short-term memory. Anim Behav 52:875–883

    Article  Google Scholar 

  • van Alphen JJ, Visser ME (1990) Superparasitism as an adaptive strategy for insect parasitoids. Ann Rev Entomol 35:59–79

    Article  Google Scholar 

  • van Baaren J, Boivin G (1998) Learning affects host discrimination behavior in a parasitoid wasp. Behav Ecol Sociobiol 42:9–16

    Article  Google Scholar 

  • van Baaren J, Boivin G, Nénon JP (1994) Intra-and interspecific host discrimination in two closely related egg parasitoids. Oecologia 100:325–330

    Article  Google Scholar 

  • Wang XY, Yang ZQ, Wu H, Gould JR (2008) Effects of host size on the sex ratio, clutch size, and size of adult Spathius agrili, an ectoparasitoid of emerald ash borer. Biol Control 44:7–12

    Article  Google Scholar 

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Acknowledgments

The study was supported by the Israel Science Foundation (http://www.isf.org.il/), grant number 414/10. We thank Ronen Shapir and Nina Dinov for rearing the insects. Comments from four anonymous referees on previous versions helped to improve the paper.

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Correspondence to Tamar Keasar.

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Communicated by S. Cremer

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Kishinevsky, M., Keasar, T. State-dependent host acceptance in the parasitoid Copidosoma koehleri: the effect of intervals between host encounters. Behav Ecol Sociobiol 69, 543–549 (2015). https://doi.org/10.1007/s00265-014-1865-x

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  • DOI: https://doi.org/10.1007/s00265-014-1865-x

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