Behavioural and genetic approaches to evaluate the effectiveness of deterrent marking by a parasitoid wasp

In: Behaviour
View More View Less
  • 1 Metapopulation Research Group, Department of Biosciences, P.O. Box 65, FI-00014 University of Helsinki, Finland
  • 2 CoE in Biological Interactions, Department of Biosciences, P.O. Box 65, FI-00014 University of Helsinki, Finland
  • 3 Cornell University, Department of Ecology and Evolutionary Biology, Ithaca, NY 14853, USA

Purchase instant access (PDF download and unlimited online access):

$30.00

Some parasitoids deposit chemical signals after oviposition as an indication that the host has already been parasitized. This marking can deter subsequent conspecifics or one’s self from laying eggs in previously exploited hosts, thus reducing the risk of superparasitism. We investigated the egg laying behaviour of the parasitoid wasp Hyposoter horticola. In a laboratory experiment, we tested whether oviposition, post-oviposition marking, or both together deter subsequent oviposition by conspecifics. We then tested the effectiveness of the deterring mark under natural conditions using maternity assignment based on 14 polymorphic DNA microsatellite markers. The behavioural experiment showed that patch marking deters conspecifics from probing the host eggs, and oviposition deters those that probe from laying eggs in previously parasitized host clusters. These results were confirmed by the maternity assignment showing that under natural conditions, host egg clusters are primarily parasitized by a single H. horticola female.

  • Agboka K., Schulthess F., Chabi-Olaye A., Labo I., Gounou S., Smith H. (2002). Self-, intra-, and interspecific host discrimination in Telenomus busseolae Gahan and T. isis Polaszek (Hymenoptera: Scelionidae), sympatric egg parasitoids of the African cereal stem borer Sesamia calamistis Hampson (Lepidoptera: Noctuidae). — J. Insect Behav. 15: 1-12.

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

    • Search Google Scholar
    • Export Citation
  • Brodeur J., Boivin G. (2004). Functional ecology of immature parasitoids. — Annu. Rev. Entomol. 49: 27-49.

  • Chow A., Mackauer M. (1999). Marking the package or its contents: host discrimination and acceptance in the ectoparasitoid Dendrocerus carpenteri (Hymenoptera: Megaspilidae). — Can. Entomol. 131: 495-505.

    • Search Google Scholar
    • Export Citation
  • Couchoux C., Seppä P., van Nouhuys S. (2015). Microsatellites for the parasitoid wasp Hyposoter horticola. — Conserv. Gen. Res., DOI:10.1007/s12686-015-0437-3.

    • Search Google Scholar
    • Export Citation
  • Couchoux C., van Nouhuys S. (2014). Effects of intraspecific competition and host-parasitoid developmental timing on foraging behaviour of a parasitoid wasp. — J. Insect Behav. 273: 283-301.

    • Search Google Scholar
    • Export Citation
  • Cronin J.T., Strong D.R. (1993). Superparasitism and mutual interference in the fairyfly parasitoid Anagrus delicatus. — Ecol. Entomol. 18: 293-302.

    • Search Google Scholar
    • Export Citation
  • d’Ettorre P. (2008). Sociobiology of communication: an interdisciplinary perspective. — Oxford University Press, New York, NY.

  • Field S.A., Keller M.A. (1999). Short-term host discrimination in the parasitoid wasp Trissolcus basalis Wollaston (Hymenoptera: Scelionidae). — Austr. J. Zool. 47: 19-28.

    • Search Google Scholar
    • Export Citation
  • Fisher R.C. (1961). A study in insect multiparasitism. 2. Mechanism and control of competition for possession of host. — J. Exp. Biol. 38: 605-629.

    • Search Google Scholar
    • Export Citation
  • Gauthier N., Monge J.P. (1999). Could the egg itself be the source of the oviposition deterrent marker in the ectoparasitoid Dinarmus basalis?J. Insect Physiol. 45: 393-400.

    • Search Google Scholar
    • Export Citation
  • Godfray H.C.J. (1994). Parasitoids: behavioural and evolutionary ecology. — Princeton University Press, Princeton, NJ.

  • Grillenberger B.K., Koevoets T., Burton-Chellew M.N., Sykes E.M., Shuker D.M., van de Zande L., Bijlsma R., Gadau J., Beukeboom L.W. (2008). Genetic structure of natural Nasonia vitripennis populations: validating assumptions of sex-ratio theory. — Mol. Ecol. 17: 2854-2864.

    • Search Google Scholar
    • Export Citation
  • Gross M.R. (1996). Alternative reproductive strategies and tactics: diversity within sexes. — Trends Ecol. Evol. 11: 92-98.

  • Hanski I.A. (2011). Eco-evolutionary spatial dynamics in the Glanville fritillary butterfly. — Proc. Natl. Acad. Sci. USA 108: 14397-14404.

    • Search Google Scholar
    • Export Citation
  • Harvey J.A., Strand M.R. (2002). The developmental strategies of endoparasitoid wasps vary with host feeding ecology. — Ecology 83: 2439-2451.

    • Search Google Scholar
    • Export Citation
  • Hoffmeister T.S., Roitberg B.D. (1997). To mark the host or the patch: decisions of a parasitoid searching for concealed host larvae. — Evol. Ecol. 11: 145-168.

    • Search Google Scholar
    • Export Citation
  • Kankare M., Jensen M.K., Kester K.M., Saccheri I.J. (2004). Characterization of microsatellite loci in two primary parasitoids of the butterfly Melitaea cinxia, Cotesia melitaearum and Hyposoter horticola (Hymenoptera). — Mol. Ecol. Notes 4: 231-233.

    • Search Google Scholar
    • Export Citation
  • Kuussaari M., van Nouhuys S., Hellmann J., Singer M.C. (2004). Larval biology of checkerspot butterflies. — In: On the wings of checkerspots: a model system for population biology ( Ehrlich P.R., Hanski I., eds). Oxford University Press, Oxford, p.  138-160.

    • Search Google Scholar
    • Export Citation
  • Lepais O., Darvill B., O’Connor S., Osborne J.L., Sanderson R.A., Cussans J., Goffe L., Goulson D. (2010). Estimation of bumblebee queen dispersal distances using sibship reconstruction method. — Mol. Ecol. 19: 819-831.

    • Search Google Scholar
    • Export Citation
  • Liu S., Zhao B., Bonjour E. (2012). Host marking and host discrimination in phytophagous insects. — In: Recent advances in entomological research ( Liu T., Kang L., eds). Springer, Dordrecht, p.  73-85.

    • Search Google Scholar
    • Export Citation
  • Mackauer M. (1990). Host discrimination and larval competition in solitary endoparasitoids. — In: Critical issues in biological control ( Mackauer M., Ehler L.E., Rolands J., eds). Intercept, Andover, p.  41-62.

    • Search Google Scholar
    • Export Citation
  • McKay T., Broce A.B. (2004). Discrimination of self-parasitized hosts by the pupal parasitoid Muscidifurax zaraptor (Hymenoptera: Pteromalidae). — Ann. Entomol. Soc. Am. 97: 592-599.

    • Search Google Scholar
    • Export Citation
  • Montovan K., Couchoux C., Jones L.E., Reeve H.K., van Nouhuys S. (2015). The puzzle of sub-maximal resource use by a parasitoid wasp. — Am. Nat. 185: 538-550.

    • Search Google Scholar
    • Export Citation
  • Mougeot F., Redpath S.M., Leckie F., Hudson P.J. (2003). The effect of aggressiveness on the population dynamics of a territorial bird. — Nature 421: 737-739.

    • Search Google Scholar
    • Export Citation
  • Nufio C.R., Papaj D.R. (2001). Host marking behavior in phytophagous insects and parasitoids. — Entomol. Exp. Appl. 99: 273-293.

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

    • Search Google Scholar
    • Export Citation
  • Prokopy R.J. (1981). Epideictic pheromones that influence spacing patterns of phytophagous insects. — In: Semiochemicals: their role in pest control ( Nordlund R.L.J., Lewis W.J., eds). Wiley, New York, NY, p.  181-213.

    • Search Google Scholar
    • Export Citation
  • R Core Team (2012). R: a language and environment for statistical computing. — R Foundation for Statistical Computing, Vienna.

  • Roitberg B.D., Prokopy R.J. (1987). Insects that mark host plants. — Bioscience 37: 400-406.

  • Saastamoinen M. (2007). Life-history, genotypic, and environmental correlates of clutch size in the Glanville fritillary butterfly. — Ecol. Entomol. 32: 235-242.

    • Search Google Scholar
    • Export Citation
  • Seppä P., Queller D.C., Strassmann J.E. (2012). Why wasp foundresses change nests: relatedness, dominance, and nest quality. — PLoS ONE 7: 9.

    • Search Google Scholar
    • Export Citation
  • Shaw M.R., Stefanescu C., van Nouhuys S. (2009). Parasitoids of European butterflies. — In: Ecology of butterflies in Europe ( Settele J., Shreeve T.G., Konvicka M., Van Dyck H., eds). Cambridge University Press, Cambridge, p.  130-156.

    • Search Google Scholar
    • Export Citation
  • Stelinski L.L., Oakleaf R., Rodriguez-Saona C. (2007). Oviposition-deterring pheromone deposited on blueberry fruit by the parasitic wasp, Diachasma alloeum. — Behaviour 144: 429-445.

    • Search Google Scholar
    • Export Citation
  • Taborsky M. (1998). Sperm competition in fish: ‘bourgeois’ males and parasitic spawning. — Trends Ecol. Evol. 13: 222-227.

  • van Alphen J.J.M., Visser M.E. (1990). Superparasitism as an adaptive strategy for insect parasitoids. — Annu. Rev. Entomol. 35: 59-79.

    • Search Google Scholar
    • Export Citation
  • van Baaren J., Nenon J.P., Boivin G. (1995). Comparison of oviposition behavior of a solitary and a gregarious parasitoid (Hymenoptera, Mymaridae). — J. Insect Behav. 85: 671-686.

    • Search Google Scholar
    • Export Citation
  • van Lenteren J.C. (1981). Host discrimination by parasitoids. — In: Semiochemicals: their role in pest control ( Nordlund R.L.J., Lewis W.J., eds). Wiley, New York, NY, p.  153-173.

    • Search Google Scholar
    • Export Citation
  • van Nouhuys S., Ehrnsten J. (2004). Wasp behavior leads to uniform parasitism of a host available only a few hours per year. — Behav. Ecol. 15: 661-665.

    • Search Google Scholar
    • Export Citation
  • van Nouhuys S., Hanski I. (2002). Multitrophic interactions in space: metacommunity dynamics in fragmented landscapes. — In: Multitrophic level interactions ( Tscharntke T., Hawkins B.A., eds). Cambridge University Press, Cambridge, p.  124-147.

    • Search Google Scholar
    • Export Citation
  • van Nouhuys S., Kaartinen R. (2008). A parasitoid wasp uses landmarks while monitoring potential resources. — Proc. Roy. Soc. Lond. B: Biol. Sci. 275: 377-385.

    • Search Google Scholar
    • Export Citation
  • van Nouhuys S., Punju E. (2010). Coexistence of competing parasitoids: which is the fugitive and where does it hide?Oikos 119: 61-70.

    • Search Google Scholar
    • Export Citation
  • van Nouhuys S., Singer M.C., Nieminen M. (2003). Spatial and temporal patterns of caterpillar performance and the suitability of two host plant species. — Ecol. Entomol. 28: 193-202.

    • Search Google Scholar
    • Export Citation
  • Venables W.N., Ripley B.D. (2002). Modern applied statistics with S. — Springer, New York, NY.

  • Wang J.L. (2004). Sibship reconstruction from genetic data with typing errors. — Genetics 166: 1963-1979.

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 147 53 2
Full Text Views 150 2 0
PDF Downloads 6 2 0