BioControl (2010) 55:89–102 DOI 10.1007/s10526-009-9238-5 Entomopathogenic fungi and insect behaviour: from unsuspecting hosts to targeted vectors Jason Baverstock • Helen E. Roy • Judith K. Pell Received: 20 July 2009 / Accepted: 5 October 2009 / Published online: 29 October 2009 Ó International Organization for Biological Control (IOBC) 2009 Abstract The behavioural response of an insect to Keywords Entomopathogenic fungi Á a fungal pathogen will have a direct effect on the Attraction Á Avoidance Á Transmission Á efficacy of the fungus as a biological control agent. In Vectoring Á Autodissemination this paper we describe two processes that have a significant effect on the interactions between insects and entomopathogenic fungi: (a) the ability of target Introduction insects to detect and avoid fungal pathogens and (b) the transmission of fungal pathogens between host A co-evolutionary arms race occurs between insects insects. The behavioural interactions between insects and their pathogens. Whereas selection on the and entomopathogenic fungi are described for a pathogen is for greater exploitation of the host, variety of fungal pathogens ranging from commer- selection on the host is for greater exclusion of the cially available bio-pesticides to non-formulated pathogen (Bush et al. 2001; Roy et al. 2006). The naturally occurring pathogens. The artificial manip- evolution of this behaviour and a description of some ulation of insect behaviour using dissemination of the diverse interactions that occur between arthro- devices to contaminate insects with entomopatho- pods and fungi have recently been described in a genic fungi is then described. The implications of review by Roy et al. (2006). Whilst these interactions insect behaviour on the use of fungal pathogens as are of great interest to evolutionary biologists, biological control agents are discussed. understanding the fundamental behavioural processes that occur between insects and pathogens is also essential for insect pathologists who wish to exploit fungal entomopathogens as biological control agents. Handling Editor: Eric Wajnberg. Several species of entomopathogenic fungi are cur- rently available as formulated bio-pesticides, includ- J. Baverstock (&) Á J. K. Pell ing; VertalecÒ (Lecanicillium longisporum ((Petch) Department of Plant and Invertebrate Ecology, Zare & Gams Zimmerman)) (Ascomycota: Hypocre- Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK ales), BotaniGardÒ (Beauveria bassiana (Balsamo) e-mail: [email protected] Vuillemin) (Ascomycota: Hypocreales) and Green MuscleÒ (Metarhizium anisopliae var. acridum H. E. Roy (Metsch.)) (Ascomycota: Hypocreales) (Milner Biological Records Centre, NERC Centre for Ecology & Hydrology, Crowmarsh Gifford, Oxfordshire OX10 8BB, 1997; Shah and Pell 2003). In addition, non-formu- UK lated species of entomopathogenic fungi such as Reprinted from the journal 89 123 J. Baverstock et al. Pandora neoaphidis (Remaudie`re & Hennebert) attention from insect pathologists. Although various Humber (Zygomycota: Entomophthorales) are also species of termites are susceptible to both B. bassiana being assessed for inclusion as part of integrated pest and M. anisopliae, the use of these fungal pathogens management schemes. The overall success of using as biological control agents is technically challenging entomopathogenic fungi as biological control agents due to the lifestyle and behaviour of termites (Staples is affected by numerous abiotic and biotic factors, and Milner 2000). Direct application of entomopath- including the behavioural response of the target ogenic fungi to control subterranean pests such as insects towards the entomopathogen. This paper termites is difficult due to the logistics in applying describes pre- and post-contact responses of insects conidia into colonies (Chouvenc et al. 2008). In to entomopathogenic fungi that are under develop- addition to this, it has been demonstrated that termites ment as biological control agents. Transmission and show a variety of behavioural responses towards vectoring of entomopathogenic fungi to uninfected conspecifics infected with fungal pathogens to reduce hosts is then described along with the use of transmission of the pathogen between uninfected and dissemination devices designed to attract and con- infected individuals (Chouvenc et al. 2008; Rath taminate insects with fungi. 2000). For infection to occur, direct contact between the termite and the pathogen is required. However, termites such as Coptotermes lacteus (Froggatt) Response of insects to entomopathogenic fungi displayed an avoidance response to M. anisopliae by only making short tunnels into substrates contain- Insects and entomopathogenic fungi are under oppos- ing the pathogen, which they then seal off preventing ing selection pressures. Insects gain a selective further contact with the fungus (Staples and Milner advantage from detecting and avoiding fungal patho- 2000). Furthermore, this response appeared to be gens while successful infection of an insect by an dependent on the virulence of the isolate, with a less entomopathogen requires contact to be made between pronounced response being observed when an isolate the host and the pathogen. The behaviour of insects of low virulence was applied (Staples and Milner can influence whether contact is made, with changes 2000). It may be possible to reduce the repellence of in activity increasing or decreasing the likelihood of entomopathogenic fungi to termites through the use infection (Cory and Hoover 2006). An insect may of baits. When incorporated into a cellulose bait gain a selective advantage if it is able to detect the (cellulose powder mixed with the conidial suspen- risk of attack from entomopathogenic fungi and sion), M. anisopliae was not repellent to the termites respond via behavioural avoidance or through post- Reticulitermes flavipes (Kollar) and Coptotermes contact responses such as grooming (Chouvenc et al. formosanus (Shiraki) at inoculum levels of 1.5 9 2008). This response may reduce the efficiency of 108 and 3 9 108 conidia respectively (Wang and the fungus as a biological control agent. In contrast, Powell 2004). The development of a palatable fungal pathogens could gain an advantage by attract- formulation with an appropriate pathogen concentra- ing or remaining invisible to host insects. tion may therefore be the key to increasing the efficiency of the control agent (Wang and Powell Avoidance of entomopathogenic fungi 2004). However, an increase in application efficiency may not be enough to control termites. Indeed, post- The ability of insects to detect and respond to contact responses of termites to conspecifics contam- entomopathogenic fungi within the order Hypocre- inated with fungal pathogens may reduce the control ales has been widely assessed, with reports of potential. Myles (2002) found that uninfected avoidance of fungi by species within the Coleoptera, R. flavipes displayed a combination of alarm behaviour, Isoptera, Hemiptera and Orthoptera (Chouvenc et al. aggregation and defensive reactions towards individ- 2008; Meyling and Pell 2006; Myles 2002; Rath uals that were contaminated with M. anisopliae.This 2000; Staples and Milner 2000; Thompson and behaviour persisted for approximately 24 minutes Brandenburg 2005; Villani et al. 1994). Termites after which it was replaced by grooming, biting, are a global pest and their behavioural response to defecation and burial of the infected termite (Myles entomopathogenic fungi has received considerable 2002). Grooming can be an efficient mechanism for 123 90 Reprinted from the journal Entomopathogenic fungi and insect behaviour removing conidia from the cuticle and preventing released from the bracket fungus Fomitopsis pinicola infection in termites; Reticulitermes speratus (Kolbe) (Polyporales: Fomitopsidaceae) (Fa¨ldt et al. 1999) were able to ingest 90% of M. anisopliae conidia whilst the Deathwatch beetle, Xestobium rufovillosum deposited on their body surface within three hours (De Geer), was attracted to volatiles released from (Shimizu and Yamaji 2003). Control of termites with wood decaying fungi (Belmain et al. 2002). Hyme- entomopathogenic fungi therefore remains challeng- nopteran parasitoids have also been reported respond- ing. Chouvenc et al. (2008) found that M. anisopliae ing to volatiles released from fungi. The Pteromalid was unable to control R. flavipes even when 6.25% of Roptrocerus xylophagorum (Ratzeburg) and the the population was infected with the fungus. It was Braconid Spathius pallidus (Ashmead) were attracted concluded that successfully controlling a field pop- to the odour of bark of loblolly pine colonized by ulation where less than 1% of the termites were blue stain fungus, a fungal associate of the parasit- inoculated with entomopathogenic fungi would be oid’s Coleopteran hosts (Sullivan and Berisford difficult. 2004). However, the majority of studies to date By exploiting the repellency of a pathogen, as indicate that insects are either not able to detect opposed to its infectivity, it may still be possible to entomopathogenic fungi, or can detect the fungus but utilise entomopathogenic fungi to control termites do not perceive it as being a threat and exhibit no and other economically important pests. Sun et al. avoidance behaviour. The Colorado potato beetle, (2008) found that organic mulches supplemented Leptinotarsa decemlineata (Say) is a serious pest of with M. anisopliae significantly repelled foraging potatoes and has developed resistance