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

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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 to many C. formosanus and reduced mulch consumption by up insecticides. Although L. decemlineata is susceptible to 71%. A second example is that of Japanese beetle to B. bassiana and can be contaminated with the larvae, Popillia japonica (Newman), which avoided fungus when pre-pupae and adults move across soil soil containing M. anisopliae for up to 20 days after and make contact with conidia deposited on either the applications (Villani et al. 1994). The tawny mole substrate or on infected beetle cadavers (Long et al. cricket Scapteriscus vicinus (Scudder) and the South- 2000), B. bassiana cadavers had no effect on ern mole cricket Scapteriscus borellii (Giglio-Tos) orientation by the beetle nor was there avoidance of both avoid making contact with B. bassiana (Thomp- areas containing B. bassiana-sporulating cadavers son and Brandenburg 2005). Surface tunnelling, (Klinger et al. 2006). Mortality of the Western flower vertical tunnels descending into the soil and tunnel- thrips, Frankliniella occidentalis (Pergrande), on ling along the perimeter were reduced in containers chrysanthemums was similar when B. bassiana was treated with B. bassiana strain DB-2 compared to applied on its own or combined with an attractant, untreated containers (Thompson and Brandenburg indicating that the fungus did not affect plant 2005). However, this was not observed when the soil colonisation by thrips (Ludwig and Oetting 2002). was treated with B. bassiana strain 10–22, suggesting A final example is that of the aphid-specific fungal that strain selection should be taken into account pathogen P. neoaphidis which had no effect on the when assessing the repellency of entomopathogenic colonisation of bean plants by the pea aphid, fungi towards insects (Thompson and Brandenburg Acyrthosiphon pisum (Harris), in cage experiments 2005). Scapteriscus vicinus has also been shown to (Baverstock et al. 2005a). This resulted in transmis- avoid making contact with M. anisopliae (Villani sion of conidia during plant colonisation and, to a et al. 2002). lesser extent, during in situ feeding. However, the ability of an insect to detect entomopathogenic fungi Non-avoidance of entomopathogenic fungi may not only be dependent on the species and isolate of the fungus, but also on the substrate on which the Although there is evidence of insects being attracted fungus is deposited. Meyling and Pell (2006) found to fungi, this is predominantly to non-entomopatho- that whilst the generalist aphid predator Anthocoris genic fungi. Female wood living beetles Malthodes nemorum (L.) avoided leaf surfaces contaminated fuscus (Waltl), Anaspis marginicollis (Lindberg) and with B. bassiana and rapidly withdrew from contact Anaspis rufilabris (Gyllenhall) and the moth Epinotia with B. bassiana-sporulating cadavers, its behaviour tedella (Clerck) were all attracted to volatiles on soil was not altered by the presence of the fungus.

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In contrast, Ormond (2007) found that the seven-spot Contrary to this there are examples of parasitoids ladybird Coccinella septempunctata (L.) detected and being able to detect hosts infected with entomopath- avoided B. bassiana on leaves and in soil. ogenic fungi. Encarsia formosa (Gahan) is used as a Whilst an inability to avoid entomopathogenic control agent against the greenhouse whitefly Tria- fungi is beneficial for control of a pest, it may be leurodes vaporariorum (Westwood) to protect several detrimental towards other natural enemies of the pest. glasshouse crops including vegetables and ornamen- For entomopathogenic fungi to be effective control tals. Fransen and van Lenteren (1993) assessed the agents, repellence by the fungus and/or a minimal interaction between E. formosa and the entomopath- loss of the other guild members to infection is ogenic fungus Aschersonia aleyrodis (Webber) required (Lord 2001). In some cases this threat may (Ascomycota: Hypocreales). Although the parasitoid come indirectly via the target pest. For example, the adopted an oviposition posture on hosts showing hosts of hymenopteran parasitoids face a greater risk signs of infection, these were rejected after probing, of infection by entomopathogenic fungi than the indicating that the parasitoid could detect the pres- parasitoid itself. Parasitoids would therefore gain a ence of the fungus. Further studies revealed that if selective advantage through detecting and avoiding fungal infection occurred within three days of para- hosts that are contaminated with fungus (Baverstock sitisation, there was a significant reduction in the et al. 2005b; Powell et al. 1986). The ability of number of parasitised hosts. However, if parasitisa- parasitoids to detect and avoid hosts infected with tion occurred 4, 7 or 10 days after parasitisation, entomopathogenic fungi from both the Hypocreales there was no effect on the number of parasitised and Entomophthorales has been assessed (Baverstock hosts. This suggested that E. formosa and A. aleyrodis et al. 2005b; Fransen and van Lenteren 1993; Lord could be used together to control T. vaporariorum. 2001). Larval saw-toothed grain beetles Oryzaephilus Unlike parasitoids which suffer a direct fitness cost surinamensis (L.) are attacked by the ectoparasitoid from ovipositing in hosts infected with entomopath- Cephalonomia tarsalis (Ashmead) and are also ogenic fungi, competition with fungal pathogens for susceptible to infection by B. bassiana (Lord 2001). prey items is not always detrimental to predators. The However, C. tarsalis larvae are also susceptible to seven-spot ladybird C. septempunctata and P. neoa- B. bassiana and died within one day of oviposition on phidis are both commonly occurring natural enemies host larvae infected with the fungal pathogen (Lord of aphids in temperate regions. Although both of 2001). Despite this, C. tarsalis was unable to detect these species compete for aphids, the coccinellid does the presence of B. bassiana and entered grain samples not avoid foraging on plants where the fungus is containing the fungus where it subsequently ovipos- present (Baverstock 2004). This is unsurprising given ited on B. bassiana-infected larvae (Lord 2001). A that C. septempunctata is not susceptible to infection second example is the interaction between the aphid by the fungus. Indeed, C. septempunctata is an parasitoid Aphidius ervi (Haliday) and P. neoaphidis. asymmetric intraguild predator of P. neoaphidis, Baverstock et al. (2005b) found that A. ervi would predating living aphids infected with the fungus as enter aphid colonies containing P. neoaphidis and well as dead sporulating cadavers (Pell et al. 1997; forage on plants contaminated with the fungus. On Roy and Pell 2000; Roy et al. 1998, 2001). However, making contact with fungus-infected aphids the some species of entomopathogenic fungi can have a parasitoid would attempt to oviposit. Indeed, it was direct negative effect on a predator if infected hosts only once the aphid had succumbed to infection and are less suitable as prey, and it is surprising that was sporulating that the parasitoid appeared to detect avoidance of sub-optimal prey items has not been the presence of the fungus and did not attempt to observed. Simelane et al. (2008) found that adult oviposit (Baverstock et al. 2005b). The apparent and larval C. septempunctata readily predated aphids inability of A. ervi to detect and respond to infected with Neozygites fresenii (Nowakowski) P. neoaphidis-infected hosts may be due to spatial (Entomophthorales: Neozygitaceae), this is despite and temporal separation reducing the encounter rate the fungus having significant negative effects on the between the two natural enemies and, therefore, the development of the coccinellid, even without direct selection pressure for avoidance behaviour to evolve infection. When consuming aphids infected with (Baverstock et al. 2005b). N. fresenii, the development time of the coccinellid

123 92 Reprinted from the journal Entomopathogenic fungi and insect behaviour was significantly longer, mortality between second pathogen (Hajek and St. Leger 1994). Transmission and fourth instars was significantly greater, body size can occur horizontally (within a generation) and was significantly smaller and egg production signif- vertically (between generations) within a species, icantly lower compared to conspecifics fed a diet of between species and from a local scale on a single uninfected aphids (Simelane et al. 2008). Similar plant to a landscape scale. Movement of entomo- results were found by Roy et al. (2008) who showed pathogenic fungi by host and non-host invertebrates that the fecundity of the harlequin ladybird, Harmo- to susceptible hosts is one of the most important nia axyridis (Pallas), was reduced dramatically when mechanisms for transmitting to new habitats (Fuxa it was infected with B. bassiana at doses of 105–109 and Tanada 1987; Roy et al. 2001). conidia ml-1, although only a low number of harlequin ladybirds succumbed to the fungal disease. Within species transmission Whilst the reproductive success of the two-spot ladybird, Adalia bipunctata (L.), was also reduced Horizontal transmission between individuals of the when inoculated with a dose of 109 conidia ml-1, same species (autodissemination) can occur through mortality was also high (Roy et al. 2008). direct contact between contaminated and uncontam- Although there is a large body of research which inated individuals or indirectly via conidia that have indicates that insects are either not attracted to been deposited on the substrate (Quesada-Moraga entomopathogenic fungi or are not able to detect et al. 2008; Roy and Pell 2000; Vega et al. 2000). their presence, there are exceptions. Dromph and Whilst it is relatively simple to quantify fungal Vestergaard (2002) assessed the susceptibility of transmission, the determination of the underlying three species of collembolans (Folsomia fimet aria mechanisms is more challenging. For example, (L.), Hypogastrura assimilis (Krausbauer) and Pro- although it was observed in the 1980’s that collem- isotoma minuta (Tullberg)) to three species of bolans are able to transmit B. bassiana, M. anisopliae entomopathogenic fungi, B. bassiana, Beauveria and Paecilomyces farinosus (Holm ex Gray) A. H. S. brongniartii (Saccardo) Petch (Ascomycota: Hypo- Brown & G. Sm. (Ascomycota: Eurotiomycetes), it creales) and M. anisopliae. Folsomia fimet aria was was not until 2001 that the mechanisms that facilitate shown to be susceptible to both B. brongniartii and this dispersal were described (Dromph 2001; Visser M. anisopliae when fed them on inoculated sphag- et al. 1987; Zimmermann and Bode 1983). Dromph num, however, it was attracted to these fungal (2001) found that F. fimet aria, H. assimilis and pathogens in a choice arena. In a pair-wise compar- P. minuta were able to transmit viable conidia of ison test, the order of attractiveness was found to be B. bassiana, B. brongniartii and M. anisopliae on similar for all three species of collembolan, with B. either their cuticle or within their gut. Transmission brongniartii being the most attractive pathogen and of the three species of entomopathogenic fungi by each B. bassiana the least attractive. Further to this, a of the species of collembolan was similar. However, positive relationship was found between the concen- whilst ingestion had no affect on the viability of tration of all three fungi and the attractiveness to B. bassiana or B. brongniartii, the viability of collembolans. M. anisopliae was reduced from 98.8% in the undi- gested control to 24.3% and 54% following ingestion by F. fimet aria and P. minuta respectively. Transmission of entomopathogenic fungi Direct transmission between contaminated and between insects uninfected individuals is less variable and more efficient than indirect transmission via conidia that Transmission is a key parameter that determines the have been deposited on the substrate, and can lead to rate of spread of entomopathogenic fungi within host high mortality rates even when the number of populations and, therefore, the pathogens potential contaminated individuals is low (DeKesel 1995). for use as a microbial control agent (Steinkraus Kreutz et al. (2004) found that a lethal dose of 2006). Transmission is the dispersal of infective B. bassiana could be transmitted from a single contact propagules from an infected host to a new host and is between treated male and untreated female adult the most ‘‘perilous’’ part of the lifecycle of a fungal spruce bark beetles, Ips typographus (L.), resulting in

Reprinted from the journal 93 123 J. Baverstock et al. a 75% mortality rate when there was a 1:20 ratio of hypothesised that the difference in transmission treated and untreated beetles. This mortality rate between the two species of fungi may have been due increased to 90% when the ratio was 1:1 (Kreutz et al. to a greater concentration of B. bassiana being applied 2004). Direct transmission of B. bassiana and to the male moths, the infective secondary conidia M. anisopliae between termite workers (C. formosanus) were then dislodged and contaminated uninfected and other colony members occurred readily whilst P. xylostella. However, subsequent secondary trans- conidia of Laboulbenia slackensis (Cepede and mission amongst larvae was less for B. bassiana than Picard) (Ascomycota: Laboulbeniales), which form for Z. radicans (Furlong and Pell 2001). adherent thread-like structures, enabled direct trans- mission between contaminated and uninfected salt Effect of insect movement on transmission marsh beetles, Pogonus chalceus (Marsham) (Carabi- of entomopathogenic fungi dae) (DeKesel 1995; Jones et al. 1996). Direct transmission from males to females during copulation A positive relationship between insect movement and is widespread and has been reported for both asco- transmission of entomopathogenic fungi has been mycetous and entomophthoralean fungi (Furlong and observed in a number of systems. Aphids release Pell 2001; Quesada-Moraga et al. 2008; Kaaya and alarm pheromone (E-b-farnesene) when threatened Okech 1990; Toledo et al. 2007). Potentially, direct with attack or during predation. This induces an transmission between males and females could be escape response in surrounding conspecifics in which exploited for biological control through releasing they unplug their stylets and move to another part of males inoculated with an entomopathogenic fungus the plant. Roy et al. (1999) demonstrated the effects into wild populations (Toledo et al. 2007). Male tsetse of P. neoaphidis infection on the alarm response flies (Glossinidae) were able to transmit B. bassiana of infected pea aphids, A. pisum. Infected aphids and M. anisopliae to females, successfully infecting produced alarm pheromone but ceased responding to 65% and 55% of females, respectively (Kaaya and it. Therefore, infected aphids would continue to elicit Okech 1990). Transmission of B. bassiana to the a response in neighbouring aphids, which could Mexican fruit fly, Anastrepha ludens (Loew), occurred enhance transmission. Indeed, Roditakis et al. (2000) during mating and, to a lesser extent, through contact found that the number of peach potato aphids, Myzus during courtship (Toledo et al. 2007). The efficiency persicae (Sulzer), which became infected with a of transmission during copulation varies depending on Lecanicillium spp. (=Verticillium lecanii (Zimmer- whether it is the male or the female that is contam- mann) Vie´gas) that had been deposited on the leaf inated. Male-to-female transmission of M. anisopliae surface was increased when alarm pheromone was within populations of the Mediterranean fruit fly, released. However, the authors did not believe that Ceratitis capitata (Wiedemann), was greatest when the addition of alarm pheromone would be a practical males were inoculated with the fungus (Quesada- pest control option and explored different methods to Moraga et al. 2008). However, the efficiency of increase aphid movement. An alternative was to use a horizontal transmission could be reduced if females sub-lethal dose of the chloronicotinyl insecticide, preferentially selected uninfected males over those imidacloprid. This insecticide inhibited aphid settling contaminated with entomopathogenic fungi. and increased searching behaviour and, therefore, the The efficiency of direct transmission between probability of the insect making contact with conidia males and females can also be dependent on the on the leaf surface was enhanced (Roditakis et al. species and/or dose of entomopathogenic fungi. The 2000). The use of imidacloprid to alter behaviour and transmission of B. bassiana from inoculated male increase fungal infection has been assessed in other diamond-back moths, Plutella xylostella (L.), to male insect orders. Imidacloprid reduced larval mobility of and females was greater than the transmission of the root weevil, Diaprepes abbreviatus (L.), and has Zoophthora radicans (Brefeld) Batko (Zygomycetes: been associated with a decrease in conidial avoidance Entomophthorales) (Furlong and Pell 2001). Simi- and increased infection with B. bassiana and M. larly, transmission of B. bassiana from inoculated anisopliae whereas in the termite, R. flavipes, imida- males to foraging larvae was greater than transmission cloprid was found to affect hygiene function (e.g. of Z. radicans (Furlong and Pell 2001). It was grooming) resulting in increased infection with

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B. bassiana (Boucias et al. 1996; Roditakis et al. 2000; (Baverstock et al. 2008). In addition to this, foraging Quintela and McCoy 1998). In addition to increasing by caterpillars of the peacock butterfly, Inachis io contact between insects and entomopathogenic fungi, (L.), also enhanced transmission of P. neoaphidis to sub-lethal doses of insecticides may provide immedi- M. carnosum (Baverstock et al. 2008). However, it ate protection through affecting the behaviour of the was speculated that enhanced transmission in the pest, which ultimately succumbs to infection by the presence of an herbivore is dependent on the degree slower acting fungus. For example, Shah et al. (2007) of herbivory, with low levels of herbivory increasing found that sub-lethal doses of imidacloprid or a second transmission through the disturbance of aphids insecticide, fipronil, prevented feeding by black vine whereas high levels of herbivory would reduce weevils, Otiorhynchus sulcatus (F.), which were transmission due to the displacement of aphids. subsequently killed by M. anisopliae. Transmission of entomopathogenic fungi to hosts Insect behaviour, such as foraging or predator is also affected by abiotic conditions and the substrate avoidance, may also affect transmission of entomo- on which they are deposited. Growth and topography pathogenic fungi. Transmission of P. neoaphidis to of the host plant influenced the susceptibility of the A. pisum is approximately double during plant mustard beetle, Phaedon cochleariae (F.), to colonisation and subsequent feeding than through in M. anisopliae that has been sprayed on the plant situ feeding alone (Baverstock et al. 2005a). In (Inyang et al. 1998). At higher temperatures, leaf addition to this, transmission of P. neoaphidis to A. expansion diluted the inoculum density of the path- pisum colonising bean plants is also enhanced in the ogen resulting in decreased mustard beetle mortality. presence of foraging predators and parasitoids. Roy In addition to this, host plant species affected et al. (1998) found that C. septempunctata increased transmission, with the number of larvae that acquired transmission of P. neoaphidis despite the coccinellid conidia on oilseed rape being greater than those on predating sporulating fungal cadavers. Foraging by Chinese cabbage or turnip. Shanley and Hajek (2008) the hymenopteran parasitoid A. ervi has also been found that rainfall increased the transmission of shown to increase transmission of P. neoaphidis to M. anisopliae through aiding dispersal from fungal A. pisum, however, the increased reproductive suc- bands onto bark where it could infect the Asian cess of the fungus was correlated with a decrease in longhorn beetle, Anoplophora glabripennis (Motsc- the reproductive success of the parasitoid (Baverstock hulsky) whilst, in contrast, Pell et al. (1998) showed et al. 2009). The enhanced transmission of entomo- that heavy rainfall was capable of knocking pathogenic fungi in the presence of foraging arthro- P. neoaphidis-sporulating cadavers from leaves onto pods is not limited to interactions that occur within soil where they were subsequently destroyed. crops and has been observed in populations of non- pest aphids found on plants in field margins. The Vectoring of entomopathogenic fungi nettle aphid, Microlophium carnosum (Buckton), and the aphid predator A. nemorum (L.) were able to Vectoring of fungal conidia occurs when the fungus distribute B. bassiana from the soil to nettle leaves is transported by a third party that is either not (Meyling et al. 2006) whilst foraging C. septempunc- susceptible to the fungus or is not the target prey tata increased the transmission of P. neoaphidis in species. Vectoring of conidia from either the sub- populations of Uroleucon jacea (L.) infesting knap- strate or from an infected host has been reported for a weed and M. carnosum infesting nettles (Ekesi et al. variety of insect-entomopathogenic fungi associa- 2005). Insects that co-occur with aphids and entomo- tions. Collembolans interact with entomopathogenic pathogenic fungi but are not within the same guild fungi in soil and, although they have been reported as have also been reported as enhancing fungal trans- consuming pathogens, they also enhanced the dis- mission. Transmission of P. neoaphidis to M. carno- persal of the fungi by transporting conidia that had sum was enhanced to a similar level in the presence become attached to their cuticles or in their guts of the parasitoid Aphidius microlophii (Pennacchio & (Broza et al. 2001; Dromph 2001). Three species Tremblay), which is an enemy of the aphid, and the of collembolans (F. fimet aria, H. assimilis and non-enemy parasitoid Aphidius colemani (Viereck), P. minuta) were all able to vector a sufficient quantity which feeds on the honeydew produced by the aphid of B. bassiana, B. brongniartii or M. anisopliae from

Reprinted from the journal 95 123 J. Baverstock et al. soil to cause mortality in the mealworm, Tenebrio at a local scale. However, long distance transmission molitor (L.) (Dromph 2003). The ability to vector of fungal pathogens within infected alate insects also fungi was primarily dependent on body size, with occurs. Aphids are able to disperse up to 1,600 km larger insects being able to vector more conidia through a combination of active hovering and passive (Dromph 2003). Vectoring of entomopathogenic flight on wind currents (Robert 1987). Various fungi could also be exploited to control pest insects. species of entomopathogenic fungi have been iden- For example, when artificially contaminated with tified in migratory alate aphids trapped from the air L. longisporum, the common black ant, Lasius niger (Chen and Feng 2004a; Feng et al. 2007; Huang, et al. (L.), was able to vector conidia of the fungus to 2008). Zhang et al. (2007) found that the dispersal colonies of the rosy apple aphid Dysaphis plantag- ability of alate M. persicae that were inoculated with inea (Passerini), resulting in mortality of 68.3%, Conidiobolus obscurus (Hall & Dunn) (Zygomycota: 30.8% and 3.7% of aphids when assessed under Entomophthorales) was not different to uninfected laboratory, semi-field and field conditions, respec- aphids and, following dispersal, infected aphids were tively (Bird et al. 2004). However, L. niger workers able to reproduce and transmit the pathogen to their were also observed removing L. longisporum- progeny. Several other species of aphid have been infected aphid cadavers, a process that would remove recorded as transmitting entomopathogenic fungi an inoculum source which may otherwise have when migrating as alates, including S. avenae, infected aphids within the colony. Lasius niger also Rhopalosiphum padi (L.) and Schizaphis graminum vectors L. longisporum to the black-bean aphid, Aphis (Rondani) (Feng et al. 2004). In a field study by Chen fabae (Scopoli) (Flower 2002). The coccinellid and Feng (2002), 760 alate M. persicae were trapped Hippodamia convergens (Guerin) was able to vector and observed for fungal infection. Of these, 87.6% conidia of Isaria (Paecilomyces) fumosoroseus died due to mycosis, 94.4% of which succumbed to (Wize) Brown & Smith (Ascomycota: Eurotiomyce- infection by Entomophthorales with the remaining tes) to uninfected Russian wheat aphids, Diuraphis being infected with the Hypocrealean B. bassiana.Of noxia (Kurdjumov), if it became contaminated when those infected with Entomophthorales over two-thirds sprayed directly with the fungus, through predating were infected with P. neoaphidis. This study was aphids that had been sprayed with the fungus or repeated at a larger scale, trapping 7,139 migratory through foraging on plants that contained sporulating alates from nine species of aphids, from which eight D. noxia cadavers (Pell and Vandenberg 2002). A species of fungal pathogens were identified (Feng second coccinellid, C. septempunctata, was also et al. 2004). Using a computer-monitored flight mill reported as being able to vector entomopathogenic system, S. avenae that had been inoculated with fungi. Both adult and larvae that were artificially P. neoaphidis were able to fly for several hours before contaminated with P. neoaphidis vectored the fungus initiating colonies, reproducing and transmitting the directly to colonies of uninfected pea aphids, fungus to their progeny (Chen and Feng 2004b; Feng A. pisum, and indirectly through the deposition of et al. 2004). Further studies have revealed that whilst infective conidia on the leaf surface (Roy et al. 2001). the number of aphids trapped does not vary consis- Further studies have revealed that C. septempunctata tently with temperature or humidity, there is a vectors P. neoaphidis from non-crop plants that are positive relationship between humidity and mortality commonly found in field margins such as nettle, due to fungal infection, and this is most apparent with knapweed or bird’s-foot trefoil to A. pisum feeding on insects infected with Entomophthorales (Chen et al. bean plants, resulting in an aphid mortality rate of up 2008). It is not just entomopathogenic fungi that are to 13% (Ekesi et al. 2005). However, vectoring dispersed within aphids, alates that are parasitised by efficiency is affected by prey species and although either Aphidius gifuensis (Ashmead) or Diaeretiella C. septempunctata was able to vector P. neoaphidis rapae (McIntosh) have also been recorded (Feng to populations of A. pisum, it was unable to vector the et al. 2007). Whilst co-infection between two species fungus to the cereal aphid Sitobion avenae (F.) (Roy of entomopathogenic fungi within migratory alates is et al. 2001). rare, low numbers of alates have been recorded as The examples described illustrate that transmis- being co-infected with P. neoaphidis and either sion and vectoring of entomopathogenic fungi occurs Zoophthora anhuiensis (Li) Humber (Zygomycetes:

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Environ Microbiol 9: Sullivan BT, Berisford CW (2004) Semiochemicals from 859–868 fungal associates of bark beetles may mediate host loca- Zimmermann G, Bode E (1983) Investigations on the dispersal tion behavior of parasitoids. J Chem Ecol 30:703–717 of the entomopathogenic fungus Metarhizium-anisopliae Sun JZ, Fuxa JR, Richter A, Ring D (2008) Interactions of (Fungi Imperfecti, Moniliales) by soil arthropods. Pedo- Metarhizium anisopliae and tree-based mulches in re- biologia 25:65–71 pellence and mycoses against Coptotermes formosanus (Isoptera: Rhinotermitidae). Environ Entomol 37:755– Author Biographies 763 Thompson SR, Brandenburg RL (2005) Tunnelling responses of mole crickets (Orthoptera: Gryllotalpidae) to the Jason Baverstock works in Dr Judith K. Pell’s group in the entomopathogenic fungus, Beauveria bassiana. Environ Department for Plant and Invertebrate Ecology at Rothamsted Entomol 34:140–147 Research. The group’s research focuses on the ecology of Toledo J, Campos SE, Flores S, Liedo P, Barrera JF, Villasenor entomopathogenic fungi, to elucidate their role in population A, Montoya P (2007) Horizontal transmission of Beau- regulation and community structure and to inform biological veria bassiana in Anastrepha ludens (Diptera: control strategies. Specifically: intraguild interactions; the

Reprinted from the journal 101 123 J. Baverstock et al. relationships between guild diversity, habitat diversity and The focus of her research is insect community interactions with ecosystem function; pathogen-induced host behavioural particular emphasis on the effects of environmental change. change. Judith K. Pell is the head of the group in the Department for Helen E. Roy leads zoological research in the Biological Plant and Invertebrate Ecology at Rothamsted Research. Records Centre at the NERC Centre for Ecology & Hydrology.

123 102 Reprinted from the journal J. K. Pell et al.

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