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Competition and intraguild predation between the braconid parasitoid Bracon hylobii and the entomopathogenic nematode Heterorhabditis downesi, natural enemies of the large pine weevil, Hylobius abietis

Published online by Cambridge University Press:  12 November 2008

A. Everard
Affiliation:
Department of Biology and Institute of Bioengineering and Agroecology, National University of Ireland, Maynooth, Co. Kildare, Ireland
C.T. Griffin
Affiliation:
Department of Biology and Institute of Bioengineering and Agroecology, National University of Ireland, Maynooth, Co. Kildare, Ireland
A.B. Dillon*
Affiliation:
Department of Biology and Institute of Bioengineering and Agroecology, National University of Ireland, Maynooth, Co. Kildare, Ireland
*
*Author for correspondence Fax: +353 1 708 3845 E-mail: aoifebdillon@gmail.com

Abstract

In biological control programmes introduced natural enemies compete with indigenous enemies for hosts and may also engage in intraguild predation when two species competing for the same prey attack and consume one another. The large pine weevil, Hylobius abietis L. (Coleoptera: Curculionidae), is an important pest of coniferous reforestation in Europe. Among its natural enemies, the parasitoid Bracon hylobii Ratz. (Hymenoptera: Braconidae) and entomopathogenic nematodes have potential as biological control agents. Both parasitoid and nematodes target the weevil larvae and, hence, there is potential for competition or intraguild predation.

In this study, we examine the interaction of B. hylobii with the nematode Heterorhabditis downesi Stock, Griffin and Burnell (Nematode: Heterorhabditidae), testing the susceptibility of larvae, pupae and adults of B. hylobii to H. downesi and whether female parasitoids discriminate between nematode-infected and uninfected weevils for oviposition. In choice tests, when weevils were exposed to nematodes 1–7 days previously, no B. hylobii oviposited on nematode-infected weevil larvae. Up to 24 h, healthy weevils were twice as likely as nematode-infected ones to be used for oviposition. Bracon hylobii females did not adjust clutch size; nematode-infected hosts were either rejected or the parasitoid laid a full clutch of eggs on them.

When nematodes were applied to the parasitoid feeding on weevil larvae, the nematodes parasitized the parasitoid larvae, there was a reduction in cocoon formation and fewer cocoons eclosed. Eclosion rate was not reduced when nematodes were applied to fully formed cocoons, but nearly all of the emerging adults were killed by nematodes.

Type
Research Paper
Copyright
Copyright © 2008 Cambridge University Press

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References

Battisti, A. (1994) Effects of entomopathogenic nematodes on the spruce web-spinning sawfly Cephalcia arvensis Panzer and its parasitoids in the field. Biocontrol Science and Technology 4, 95102.CrossRefGoogle Scholar
Brixey, J.M., Moore, R. & Milner, A.D. (2006) Effect of entomopathogenic nematode (Steinernema carpocapsae Weiser) application technique on the efficacy and distribution of infection of the large pine weevil (Hylobius abietis L.) in stumps of Sitka spruce (Picea sitchensis Carr.) created at different times. Forest Ecology and Management 226, 161172.CrossRefGoogle Scholar
Brooks, W.M. (1993) Host-parasitoid-pathogen interactions. pp. 231272in Beckage, N.E., Thompson, S.N. & Federici, B.A. (Eds) Parasites and Pathogens of insects. Vol 2: Pathogens. San Diego, CA, Academic Press.Google Scholar
COFORD (2007) COFORD National Council for Forest Research and Development. Annual Report 2007, pp. 4547. Dublin, Ireland.Google Scholar
Crooke, M. & Kirkland, R.C. (1956) The gale of 1954: an appraisal of its influence on forest populations in pine areas. Scottish Forestry 10, 135145.Google Scholar
Dillon, A.B., Ward, D., Downes, M.J. & Griffin, C.T. (2006) Suppression of the large pine weevil Hylobius abietis (Coleoptera: Curculionidae) in pine stumps by entomopathogenic nematodes with different foraging strategies. Biological Control 38, 217226.CrossRefGoogle Scholar
Dillon, A.B., Downes, M.J., Ward, D. & Griffin, C.T. (2007) Optimizing application of entomopathogenic nematodes to manage large pine weevil, Hylobius abietis L (Coleoptera: Curculionidae) populations developing in pine stumps, Pinus sylvestris. Biological Control 40, 253263.CrossRefGoogle Scholar
Dillon, A.B., Moore, C.P., Downes, M.J. & Griffin, C.T. (2008a) Evict or Infect? Managing populations of the large pine weevil, Hylobius abietis using a bottom-up and top-down approach. Forest Ecology and Management 225, 26342642.CrossRefGoogle Scholar
Dillon, A.B., Rolston, A.N., Meade, C.V., Downes, M.J. & Griffin, C.T. (2008b) Establishment, persistence and introgression of entomopathogenic nematodes in a forest ecosystem. Ecological Applications 18, 735747.CrossRefGoogle Scholar
Dowds, B.C.A. & Peters, A. (2002) Virulence Mechanisms. pp. 7998in Gaugler, R. (Ed.) Entomopathogenic Nematology. Wallingford, Oxon, UK, CABI Publishing.CrossRefGoogle Scholar
Eidmann, H.H & Lindelöw, A. (1997) Estimates and measurement of pine weevil feeding on conifer seedlings: their relationship and application Canadian Journal of Forest Research 27, 10681073.CrossRefGoogle Scholar
Faccoli, M. & Henry, C.J. (2003) Host location by chemical stimuli in Bracon hylobii (Ratzeburg) (Hymenoptera: Braconidae), a larval parasitoid of Hylobius abietis (L.) (Coleoptera: Curculionidae). Annales Societe Entomologique de France 39, 247256.CrossRefGoogle Scholar
Forestry Commission (2006) The natural answer to weevils – Nematodes cost effective reduction of damage caused by Hylobius abietis. Forest Research Information Leaflet, Forestry Commission UK.Google Scholar
Georgis, R. (1981) Studies on Neoplectana carpocapsae in the web-spinning larch sawfly Cephalcia larciphila. PhD thesis, University of Reading, Reading, UK.Google Scholar
Georgis, R. & Hague, N.G.M. (1982) Preliminary field trial of the nematode Neoaplectana carpocapsae against prepupae of the larch sawfly Cephalcia lariciphila. IRCS Medical Science Biochemistry 10, 616616.Google Scholar
Georgis, R., Koppenhofer, A.M., Lacey, L.A., Belair, G., Duncan, L.W., Grewal, P.S., Samish, M., Tan, L., Torr, P. & van Tol, R.W.H.M. (2006) Successes and failures in the use of parasitic nematodes for pest control. Biological Control 38, 103123.CrossRefGoogle Scholar
Gerdin, S. (1977) Observations on pathogens and parasites of Hylobius abietis (Coleoptera: Curculionidae) in Sweden. Journal of Invertebrate Pathology 30, 263264.CrossRefGoogle Scholar
Glazer, I. (1997) Effects of infected insects on secondary invasion of steinernematid entomopathogenic nematodes. Parasitology 114, 597604.Google ScholarPubMed
Godfray, H.C.J. (1994) Parasitoids: Behavioural and Evolutionary Ecology. 488 pp. Princeton University Press, Princeton, USA.CrossRefGoogle Scholar
Godfray, H.C.J., Partridge, L. & Harvey, P.H. (1991) Clutch size. Annual Review of Ecology 22, 409429.CrossRefGoogle Scholar
Hackermann, J., Rott, A.S. & Dorn, S. (2007) How two different host species influence the performance of a gregarious parasitoid: host size is not equal to host quality. Journal of Animal Ecology 76, 376383.CrossRefGoogle Scholar
Hanson, H.S. (1943) The control of bark beetles and weevils in coniferous forests in Britain. Scottish Forestry Journal 57, 1945.Google Scholar
Head, J., Palmer, L.F. & Walters, K.F.A. (2003) The compatibility of control agents used for the control of the South American leafminer, Liriomyza huidobrensis. Biocontrol Science and Technology 13, 7786.CrossRefGoogle Scholar
Henry, C. (1995) The effect of a braconid ectoparasitoid, Bracon hylobii Ratz., on larval populations of the large pine weevil, Hylobius abietis L. PhD thesis, University of Ulster at Coleraine, UK.Google Scholar
Henry, C.J. & Day, K.R. (2001a) Egg allocation by Bracon hylobii Ratz., the principle parasitoid of the large pine weevil (Hylobius abietis L.) and implications for host suppression. Agricultural and Forest Entomology 3, 1118.CrossRefGoogle Scholar
Henry, C.J. & Day, K.R. (2001b) Biocontrol of the large pine weevil: structure of host (Hylobius abietis L.) and parasitoid (Bracon hylobii Ratz.) populations in felled stumps of sitka spruce. pp. 112in Alfaro, R.I., Day, K., Salom, S., Nair, K.S.S., Evans, H., Liebhold, A., Lieutier, F., Wagner, M., Futai, K. & Suzuki, K. (Eds) Protection of World Forests from Insect Pests: Advances in Research. IUFRO World Series, Vol. 11. Vienna, IUFRO Secretariat.Google Scholar
Heqvist, K.J. (1958) Notes on Bracon hylobii Ratz. (Hym. Braconidae), a parasite of the pine weevil Hylobius abietis L. Annales Entomologici Fennici 24, 7378.Google Scholar
Hoch, G., Schopf, A. & Maddox, J.V. (2000) Interactions between an entomopathogenic microsporidium and the endoparasitoid Glyptapanteles liparidis within their host, the gypsy moth larva. Journal of Invertebrate Pathology 75, 5968.CrossRefGoogle ScholarPubMed
Hochberg, M.E., Hassell, M.P. & May, R.M. (1990) The dynamics of host-parasitoid-pathogen interactions. American Naturalist 135, 7494.CrossRefGoogle Scholar
Kaya, H.K. (1978a). Infectivity of Neoaplectana carpocapsae and Heterorhabditis heliothidis to pupae of the parasite Apanteles militaris. Journal of Nematology 10, 241244.Google ScholarPubMed
Kaya, H.K. (1978b) Interaction between Neoaplectana carpocapsae (Nematoda: Steinernematidae) and Heterorhabditis heliothidis to pupae of the parasite Apanteles militaris (Hymenoptera: Braconidiae), a parasitoid of the armyworm, Pseudaletia unipuncta. Journal of Invertebrate Pathology 31, 358364.CrossRefGoogle Scholar
Kaya, H.K. & Gaugler, R. (1993) Entomopathogenic nematodes. Annual Review of Entomology 38, 181206.CrossRefGoogle Scholar
Kaya, H.K. & Hotchkin, P.G. (1981) The nematode Neoaplectana carpocapsae Weiser (Rhabditida, Steinernematidae) and its effect on selected Ichneumonid and Braconid parasites. Environmental Entomology 10, 474478.CrossRefGoogle Scholar
Kaya, H.K., Joos, J.L., Fallon, L.A. & Berlowitz, A. (1984) Suppression of the codling moth (Lepidoptera: Olethreutidae) with the entomogenous nematode, Steinernema feltiae (Rhabditida: Steinernematidae). Journal of Economic Entomology 77, 12401244.CrossRefGoogle Scholar
Kyei-Poku, G. & Kunimi, Y. (1997) Effect of entomopoxvirues infection to Pseudaletia separata larvae on the oviposition behaviour of Cotesia kariyai. Entomologia Experimentalis et Applicata 83, 9397.CrossRefGoogle Scholar
Lacey, L.A., Unruh, T.R. & Headrick, H.L. (2003) Interactions of two parasitoids (Hymenoptera: Ichneumonidae) of codling moth (Lepidoptera: Tortricidae) with the entomopathogenic nematode Steinernema carpocapsae (Rhabditida: Steinernematidae). Journal of Invertebrate Pathology 83, 230239.CrossRefGoogle ScholarPubMed
Lack, D. (1947) The significance of clutch size. Ibis 89, 309352.CrossRefGoogle Scholar
Leather, S.R., Day, K.R. & Salisbury, A.N. (1999) The biology and ecology of the large pine weevil, Hylobius abietis (Coleoptera: Curculionidae): a problem of dispersal? Bulletin of Entomological Research 89, 316.CrossRefGoogle Scholar
Lord, J.C. (2001) Response of the wasp Cephalonomia tarsalis (hymenoptera: Bethylidae) to Beauveria bassiana (Hyphomycetes: Moniliales) as free conidia or infection in its host, the sawtoothed grain beetle, Oryzaephilus surinamensis (Coleoptera: Silvanidae) Biological Control 21, 300304.CrossRefGoogle Scholar
MacArthur, R.H. (1972) Geographical Ecology. 269 pp. New York, USA, Harper and Row.Google Scholar
McBrien, H. & Mackauer, M. (1991) Decision to superparasitize based on larval survival: competition between aphid parasitoids: Aphidius ervi and Aphidius smithi. Entomologia Experimentalis et Applicata 56, 145153.CrossRefGoogle Scholar
Meyhofer, R. & Casas, J. (1999) Vibratory stimuli in host location by parasitic wasps. Journal of Insect Physiology 45, 967971.CrossRefGoogle ScholarPubMed
Minitab Inc. (2003) MINITAB Statistical Software, Release 14 for Windows, State College, PA, USA.Google Scholar
Moore, R., Brixey, J. & Milner, A.D. (2004) Effect of time of year on the development of immature stages of the large pine weevil (Hylobius abietis L.) in stumps of Sitka spruce (Picea sitchensis Carr.) and influence of felling date on their growth, density and distribution. Journal of Applied Entomology 128, 167176.CrossRefGoogle Scholar
Mracek, Z. & Spitzer, K. (1983) Interaction of the predators and parasitoids of the sawfly, Cephalcia weevil (Pamphilidae: Hymenoptera) with its nematode Steinernema kraussei. Journal of Invertebrate Pathology 42, 397399.CrossRefGoogle Scholar
Munro, J.W. (1914) A braconid parasite of the pine weevil Hylobius abietis. Annals of Applied Biology 1, 170176.CrossRefGoogle Scholar
Nguyen, D.H., Kakai, M., Takatsuka, J., Okuno, S., Ishii, T. & Kunimi, Y. (2005) Interaction between a nucleopolyhedrovirus and the braconid parasitoid Meteorus pulchricornis (Hymenoptera: Braconidae) in the larvae of Spodoptera litura (Lepidoptera: Noctuidae). Applied Entomology and Zoology 40, 325334.CrossRefGoogle Scholar
Peters, A. (1996) The natural host range of Steinernema and Heterorhabditis spp. and their impact on insect populations. Biocontrol Science and Technology 6, 389402.CrossRefGoogle Scholar
Pexton, J.J. & Mayhew, P.J. (2005) Clutch size adjustment, information use and the evolution of gregarious development in parasitoid wasps. Behavioural Ecology and Sociobiology 58, 99110.CrossRefGoogle Scholar
Poinar, G.O. (1986) Entomopathogous nematodes. pp. 95121in Franz, B.D. (Ed.) Biological Plant and Health Protection. Stuttgart, Germany, Gustav Fischer Verlag.Google Scholar
Pye, A.E. & Burman, M. (1978) Neoaplectana carpocapsae: Infection and reproduction in large pine weevil larvae, Hylobius abietis. Experimental Parasitology 46, 111.CrossRefGoogle ScholarPubMed
Quistad, G.B., Nguyen, O., Bernasconi, P. & Leisy, D.J. (1994) Purification and characterization of insecticidal toxins from venom glands of the parasitic wasp, Bracon hebetor. Insect Biochemistry and Molecular Biology 24, 955961.CrossRefGoogle ScholarPubMed
Rosenheim, J.A., Kaya, H.K., Ehler, L.E., Marois, J.J. & Jaffee, B.A. (1995) Intraguild predation among biological control agents – theory and evidence. Biological Control 5, 303335.CrossRefGoogle Scholar
San-Blas, E. & Gowen, S.R. (2008) Facultative scavenging as a survival strategy of entomopathogenic nematodes. International Journal of Parasitology 38, 8591.CrossRefGoogle ScholarPubMed
Shannag, H.K. & Capinera, J.L. (2000) Interference of Steinernema carpocapsae (Nematoda: Steinernematidae) with Cardiochiles diaphaniae (Hymenoptera: Braconidae), a parasitoid of the melonworm and pickleworm (Lepidoptera: Pyralidae). Environmental Entomology 29, 612616.CrossRefGoogle Scholar
Sher, R.B., Parrella, M.P. & Kaya, H.K. (2000) Biological control of the leafminer, Liriomyza trifolii (Burgess): implications for intraguild predation between Diglyphus begini Ashmead and Steinernema carpocapsae (Weiser). Biological Control 17, 155163.CrossRefGoogle Scholar
Triggiani, O. (1985) Influenza dei nematodi della famiglia Steinernematidae e Heterorhabditidae sul parassitoide Apanteles ultor Rhd. (Hymenoptera: Braconidae). La Difesa delle Piante 2, 293300.Google Scholar
Turlings, T.C.J. (1985) Why is there no interspecific host discrimination in two coexisting larval parasitoids of Drosophila species: Leptopilina heterotoma (Thomson) and Asobara tabida (Nees). Oecologia 67, 353359.CrossRefGoogle ScholarPubMed
Unruh, T.R. & Lacey, L.A. (2001) Control of codling moth, Cydia pomonella (Lepidoptera: Tortricidae) with Steinernema carpocapsae: Effects of supplemental wetting and pupation site on infection rate. Biological Control 20, 4856.CrossRefGoogle Scholar
von Waldenfels, J. (1975) Verruche zur Bekampfung von Hylobius abietis L. (Coloept., Curculionidae). Anzeiger fur Schadlingskde Pflanzen-Umweltschutz 48, 2125.CrossRefGoogle Scholar
Wharton, R.A. (1993) Bionomics of the Braconidae. Annual Review of Entomology 38, 121143.CrossRefGoogle Scholar
Woodring, J.L. & Kaya, H.K. (1988) Steinernematid and Heterorhabditid Nematodes: A handbook of techniques. Arkansas Cooperative Series, Bulletin 331. Fayetteville, Arkansas, Arkansas Agricultural Experiment Station.Google Scholar
Wright, D.J. & Perry, R.N. (2002) Physiology and Biochemistry. pp. 145168in Gaugler, R. (Ed.) Entomopathogenic Nematology. Wallingford, Oxon, UK, CABI Publishing.CrossRefGoogle Scholar
Zaki, F.N., Awadallah, K.T. & Gersraha, M.A. (1997) Competitive interaction between the braconid parasitoid Meteorus rubens Nees and the entomogenous nematode Steinernema carpocapsae (Weiser) on larvae of Agrotis ipsilon Hufn. (Lep. Noctuidae). Journal of Applied Entomology 121, 151153.CrossRefGoogle Scholar
Zaviezo, T. & Mills, N. (2001) The response of Hyssopus pallidus to hosts previously parasitised by Ascogaster quadridentata: heterospecific discrimination and host quality. Ecological Entomology 26, 9199.CrossRefGoogle Scholar
Zhou, X.S., Kaya, H.K., Heungens, K. & Goodrich-Blair, H. (2002) Response of ants to a deterrent factor(s) produced by the symbiotic bacteria of entomopathogenic nematodes. Applied and Environmental Microbiology 68, 62026209.CrossRefGoogle ScholarPubMed