Elsevier

Animal Behaviour

Volume 80, Issue 2, August 2010, Pages 283-288
Animal Behaviour

Pine weevils modulate defensive behaviour in response to parasites of differing virulence

https://doi.org/10.1016/j.anbehav.2010.05.006Get rights and content

Grooming and avoidance of contaminated areas are among the behavioural defences employed by animals against parasites. Antiparasite defence behaviour is costly in terms of time, energy and/or food foregone and therefore animals are expected to modulate their defences depending on the risk of attack and/or the severity of the symptoms caused. We tested the hypothesis that an insect host invests more in defence against more virulent (more likely to cause death) than less virulent parasites. We tested avoidance and grooming of adult pine weevils, Hylobius abietis, in response to infective juveniles of two species of entomopathogenic nematodes, the more virulent Steinernema carpocapsae and less virulent Heterorhabditis downesi. Weevils avoided feeding on a substrate contaminated with S. carpocapsae but not H. downesi. Weevils also groomed more when their bodies were contaminated with S. carpocapsae than either H. downesi or water. We also made direct observations of nematodes on weevils. When equal numbers of nematodes were applied to weevils more S. carpocapsae than H. downesi moved actively on the weevil’s cuticle. Thus, the differential response of weevils to the two nematode species can be explained by the weevils detecting the more aggressive behaviour of S. carpocapsae than H. downesi, which corresponds to a higher probability of death.

Section snippets

Nematodes

The nematodes, S. carpocapsae All and H. downesi K122, were cultured with late-instar larvae of the wax moth Galleria mellonella (Woodring & Kaya 1988). Infective juveniles were stored in tap water (2000 infective juveniles/ml) at 9 °C and were used within 3–5 weeks after emergence from the host cadaver. All experiments were repeated using different batches of infective juveniles.

Insects

Pine weevils develop in timber of recently killed conifers, such as stumps of felled trees. Adults emerge and feed on

Grooming Response

Weevils with S. carpocapsae applied to their heads groomed nearly four times longer than weevils with H. downesi and 36 times longer than the water-only controls (mean ± SE: S. carpocapsae: 44.6 ± 8.44 s; H. downesi: 11.3 ± 2.53 s; control: 1.23 ± 0.58 s; N = 50). Differences between treatments in grooming time were highly significant (Kruskal–Wallis test: H2 = 54.54, P < 0.001). We next asked whether differences between treatments were due to different numbers of weevils grooming, and/or the length of time

Discussion

Adult pine weevils displayed two behavioural reactions to entomopathogenic nematodes: reduced feeding on a contaminated substrate in a choice test, and increased grooming when nematodes were on their bodies. There were marked differences in their response to the two nematode species tested: only S. carpocapsae caused food avoidance, and this species also had a much greater effect than H. downesi on grooming. More weevils groomed in response to both species but grooming insects groomed for

Acknowledgments

The work was financially supported by the European Regional Development Fund (INTERREG IIIA) administered through the Welsh European Funding Office, and by the Irish National Development Plan through COFORD, the National Council for Forest Research and Development (ABATE project).

References (57)

  • D.M. Mburu et al.

    Relationship between virulence and repellency of entomopathogenic isolates of Metarhizium anisopliae and Beauveria bassiana to the termite Macrotermes michaelseni

    Journal of Insect Physiology

    (2009)
  • Y.S. Peng et al.

    The resistance mechanism of the Asian honey bee, Apis cerana Fabr, to an ectoparasitic mite, Varroa jacobsoni Oudemans

    Journal of Invertebrate Pathology

    (1987)
  • G.S. Thurston et al.

    Explanations for the low susceptibility of Leptinotarsa decemlineata to Steinernema carpocapsae

    Biological Control

    (1994)
  • C.M. Vincent et al.

    Crickets groom to avoid lethal parasitoids

    Animal Behaviour

    (2010)
  • M.J. Wilson et al.

    Slugs (Deroceras reticulatum and Arion ater agg.) avoid soil treated with the rhabditid nematode Phasmarhabditis hermaphrodita

    Biological Control

    (1999)
  • N. Wilson-Rich et al.

    Susceptibility and behavioral responses of the dampwood termite Zootermopsis angusticollis to the entomopathogenic nematode Steinernema carpocapsae

    Journal of Invertebrate Pathology

    (2007)
  • A.G. Appel et al.

    Laboratory and field evaluations of an entomopathogenic nematode (Nematoda: Steinernematidae) for German cockroach (Dictyoptera: Blattellidae) control

    Journal of Economic Entomology

    (1993)
  • R.L. Baker et al.

    Conflict between antipredator and antiparasite behaviour in larval damselflies

    Oecologia

    (1997)
  • O. Boecking et al.

    Behavioral defenses of honey bees against Varroa jacobsoni Oud

    Apidologie

    (1999)
  • A.M. Burnell et al.

    Heterorhabditis, Steinernema and their bacterial symbionts: lethal pathogens of insects

    Nematology

    (1999)
  • J.F. Campbell et al.

    Nictation behaviour and its ecological implications in the host search strategies of entomopathogenic nematodes (Heterorhabditidae and Steinernematidae)

    Behaviour

    (1993)
  • J.F. Campbell et al.

    Inter-specific variation in entomopathogenic nematode foraging strategy: dichotomy or variation along a continuum?

    Fundamental and Applied Nematology

    (1997)
  • C. Combes

    Parasitism: the Ecology and Evolution of Intimate Interactions

    (2001)
  • B. Dowds et al.

    Virulence mechanisms

  • B.M. Drees et al.

    Susceptibility and behavioral response of red imported fire ant (Hymenoptera: Formicidae) to selected entomogenous nematodes (Rhabditida: Steinernematida and Heterorhabditidae)

    Journal of Economic Entomology

    (1992)
  • D.C. Eidt et al.

    Susceptibility of adults of Hylobius congener Dalle Torre, Shenkling, and Marshall (Coleoptera: Curculionidae) to entomopathogenic nematodes

    Canadian Entomologist

    (1995)
  • S. Forst et al.

    Xenorhabdus and Photorhabdus spp.: bugs that kill bugs

    Annual Review of Microbiology

    (1997)
  • R. Gaugler et al.

    Ecology in the service of biological control: the case of entomopathogenic nematodes

    Oecologia

    (1997)
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    1

    D. E. Ennis is at the Entomology Research Laboratory, Biology Department, Concordia University, 7141 Sherbrooke St. West, Montreal, Quebec H4B 1R6, Canada.

    2

    A. B. Dillon is at Coillte Teoranta, Newtownmountkennedy, Co. Wicklow, Ireland.

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