Pine weevils modulate defensive behaviour in response to parasites of differing virulence
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)
- et al.
Strategies for the avoidance of faeces by grazing sheep
Applied Animal Behaviour Science
(2000) - et al.
Suppression of the large pine weevil Hylobius abietis (L.) (Coleoptera: Curculionidae) in pine stumps by entomopathogenic nematodes with different foraging strategies
Biological Control
(2006) - et al.
Aggressive and evasive behaviors in Popillia japonica (Coleoptera: Scarabaeidae) larvae: defenses against entomopathogenic nematode attack
Journal of Invertebrate Pathology
(1994) Behavioral adaptations to pathogens and parasites: 5 strategies
Neuroscience and Biobehavioral Reviews
(1990)- et al.
Plasticity in antiparasite behaviours and its suggested role in invasion biology
Animal Behaviour
(2007) - et al.
Sheep avoidance of faeces-contaminated patches leads to a trade-off between intake rate of forage and parasitism in subsequent foraging decisions
Animal Behaviour
(2001) - et al.
Synergism of entomopathogenic nematodes and imidacloprid against white grubs: greenhouse and field evaluation
Biological Control
(2000) - et al.
Grooming decisions by damselflies, age-specific colonisation by water mites, and the probability of successful parasitism
International Journal for Parasitology
(1999) - et al.
Behavioral ecology of entomopathogenic nematodes
Biological Control
(2006) - et al.
Relationship between the successful infection by entomopathogenic nematodes and the host immune response
International Journal for Parasitology
(2007)
Relationship between virulence and repellency of entomopathogenic isolates of Metarhizium anisopliae and Beauveria bassiana to the termite Macrotermes michaelseni
Journal of Insect Physiology
The resistance mechanism of the Asian honey bee, Apis cerana Fabr, to an ectoparasitic mite, Varroa jacobsoni Oudemans
Journal of Invertebrate Pathology
Explanations for the low susceptibility of Leptinotarsa decemlineata to Steinernema carpocapsae
Biological Control
Crickets groom to avoid lethal parasitoids
Animal Behaviour
Slugs (Deroceras reticulatum and Arion ater agg.) avoid soil treated with the rhabditid nematode Phasmarhabditis hermaphrodita
Biological Control
Susceptibility and behavioral responses of the dampwood termite Zootermopsis angusticollis to the entomopathogenic nematode Steinernema carpocapsae
Journal of Invertebrate Pathology
Laboratory and field evaluations of an entomopathogenic nematode (Nematoda: Steinernematidae) for German cockroach (Dictyoptera: Blattellidae) control
Journal of Economic Entomology
Conflict between antipredator and antiparasite behaviour in larval damselflies
Oecologia
Behavioral defenses of honey bees against Varroa jacobsoni Oud
Apidologie
Heterorhabditis, Steinernema and their bacterial symbionts: lethal pathogens of insects
Nematology
Nictation behaviour and its ecological implications in the host search strategies of entomopathogenic nematodes (Heterorhabditidae and Steinernematidae)
Behaviour
Inter-specific variation in entomopathogenic nematode foraging strategy: dichotomy or variation along a continuum?
Fundamental and Applied Nematology
Parasitism: the Ecology and Evolution of Intimate Interactions
Virulence mechanisms
Susceptibility and behavioral response of red imported fire ant (Hymenoptera: Formicidae) to selected entomogenous nematodes (Rhabditida: Steinernematida and Heterorhabditidae)
Journal of Economic Entomology
Susceptibility of adults of Hylobius congener Dalle Torre, Shenkling, and Marshall (Coleoptera: Curculionidae) to entomopathogenic nematodes
Canadian Entomologist
Xenorhabdus and Photorhabdus spp.: bugs that kill bugs
Annual Review of Microbiology
Ecology in the service of biological control: the case of entomopathogenic nematodes
Oecologia
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Sex-related differences in the susceptibility of Periplaneta americana and Capnodis tenebrionis to the entomopathogenic nematode Steinernema carpocapsae
2013, Journal of Invertebrate PathologyCitation Excerpt :Similarly, Renn (1998) observed aggregations of juveniles only on the cloaca 2 h after applying S. feltiae against adult houseflies, Musca domestica L. (Diptera: Muscidae). The lesser number of nematodes on the head region may be related to defense mechanisms to reduce invasion of EPNs (grooming and evasion) that have been studied in various insects such as beetles (Ennis et al., 2010; Gaugler et al., 1994; Koppenhöfer et al., 2000; Schroeder et al., 1993; Wang et al., 1995), flies (Renn, 1998), termites (Mankowski et al., 2005; Wilson-Rich et al., 2007), ants (Drees et al., 1992) and cockroaches (Appel et al., 1993; Koehler et al., 1992) or other arthropoda like Forficula auricularia L. (Dermaptera: Forficulidae) (Hodson et al., 2011). However, as there were no differences in the number of IJs on the surface of males and females, grooming behavior cannot help to understand sex differences in susceptibility reported in this study.
Environmental safety of entomopathogenic nematodes - Effects on abundance, diversity and community structure of non-target beetles in a forest ecosystem
2012, Biological ControlCitation Excerpt :With such a wide host range, it has been suggested that EPN could pose a risk to non-target insects, but the risk in the field may be reduced by limited dispersal and lack of persistence (van Lenteren et al., 2003; Lynch and Thomas, 2000). Avoidance of EPN infected insects or EPN occupied areas may further reduce adverse effects on non-target species under natural conditions (Ennis et al., 2010; Gouge, 2002). As such, detailed post application studies are the most realistic means of investigating potential non-target effects of EPN.
European earwig (Forficula auricularia) as a novel host for the entomopathogenic nematode Steinernema carpocapsae
2011, Journal of Invertebrate PathologyCitation Excerpt :It is possible that earwigs would respond to the addition of any nematode. However, Ennis et al. (2010) found that pine weevils (Hylobius abietis Linnaeus) groomed more when their bodies were contaminated with S. carpocapsae than the less virulent Heterorhabditis downesi Stock, indicating that insects defend themselves more against more virulent parasites. Other studies have also shown that insect larvae groom more often in the presence of EPNs and that restrained larvae are more likely to become infected (Gaugler et al., 1994; Wang et al., 1995; Koppenhöfer et al., 2000).
Behavioural avoidance by slugs and snails of the parasitic nematode Phasmarhabditis hermaphrodita
2016, Biocontrol Science and Technology
- 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.