REVIEW Eur. J. Entomol. 105: 391–398, 2008 http://www.eje.cz/scripts/viewabstract.php?abstract=1342 ISSN 1210-5759 (print), 1802-8829 (online) Forgotten natural enemies: Interactions between coccinellids and insect-parasitic fungi HELEN E. ROY1 and TED E. COTTRELL2 1NERC Centre for Ecology and Hydrology, Monks Wood, Huntingdon, Cambridgeshire, PE28 2LS, UK; e-mail: [email protected] 2USDA, Agricultural Research Service, Southeastern Fruit and Tree Nut Research Laboratory, 21 Dunbar Road, Byron, GA 31008 USA; e-mail: [email protected] Key words. Entomopathogenic fungi, ladybeetles, ladybirds, Coccinellidae, Beauveria bassiana, Hesperomyces virescens Abstract. The role of predators and parasitoids in the regulation of insect populations is widely reported in the context of both pest and non-pest insects. However, this is not the case for pathogens (entomopathogens). Indeed, most studies on insect life history refer only to predators and parasitoids when considering natural enemy guilds, even though naturally occurring entomopathogens are undoubtedly more diverse and widespread. This is certainly the case with the Coccinellidae; the natural enemies of coccinellids have been the subject of a number of review articles but pathogens receive only brief mention. In this review we attempt to address the balance and consider the interactions of natural populations of Coccinellidae with entomopathogenic fungi. Most research on ento- mopathogens and Coccinellidae focuses on the non-target impact of biorational insecticides against coccinellids and the impact of fungal infections upon aggregations of overwintering coccinellids; with the former overwhelmingly dominating the literature. Given the prominence of coccinellids in classical and conservation biological control, it is surprising that studies have not measured the natural impact of pathogenic fungi upon introduced species or natural populations of Coccinellidae, as has been done with numerous insect pest species. Here we review the literature on the intriguing interactions between coccinellids and fungal pathogens. We examine the literature on direct infection (sub-lethal and lethal) of coccinellids by pathogenic (Beauveria bassiana, Metarhizium ani- sopliae, Paecilomyces fumosoroseus) or parasitic (Hesperomyces virescens). We also consider the role of intra-guild predation (on the aphid-specific fungus Pandora neoaphidis and Beauveria bassiana) and finally indirect interactions such as coccinellids dis- persing P. neoaphidis. We suggest that fungal pathogens are all too often forgotten natural enemies and future research should address the profound absence of knowledge in this field. INTRODUCTION particularly the case for fungal pathogens, which are There have been considerable advances in the field of widely regarded as important natural enemies of coccinel- insect pathology over the last few decades, but the role of lids (Majerus, 1994; Hodek & HonČk, 1996) but the rela- pathogens (entomopathogens) as natural enemies of non- tionship is very poorly understood. We suggest that pest insects is seldom considered. Indeed, most studies on fungal pathogens are all too often forgotten natural ene- insect life history refer only to predators and parasitoids mies and future research should address the profound when considering natural enemy guilds, even though absence of knowledge. naturally occurring entomopathogens are undoubtedly Much of the literature in this field is in relation to the more diverse and widespread (Lacey et al., 2001); 50% of impacts of fungal-based biorational pesticides on non- living organisms are microbial (Watson et al., 1995) and target insects such as coccinellids (James et al., 1995; insect pathogens are ubiquitous in both above and below- Pingel & Lewis, 1996; Todorova et al., 1996; Roy & Pell, ground ecosystems (Hajek, 2004). 2000; Smith & Krischik, 2000; Pell & Vandenberg, Coccinellids are attacked by a suite of natural enemies 2002). Considerably less information exists on coccinel- lids and their interactions with naturally-occurring fungal (Majerus, 1994; Hodek & HonČk, 1996; Roy et al., 2006a, b) including: predators [such as: the predatory bug pathogens, even though fungi, such as B. bassiana, are Deraeocoris ruber L. (Hemiptera: Miridae)], a hymenop- documented as major mortality factors of overwintering teran parasitoid [Dinocampus coccinellae (Schrank) coccinellids (Iperti, 1966; Ceryngier & Hodek, 1996; (Hymenoptera: Braconidae)], dipteran parasites [such as Barron & Wilson, 1998; Ormond et al., 2006). Phalacrotophora fasciata Fallén (Diptera: Phoridae)], a In this paper we aim to review our current under- mite [Coccipolipus hippodamiae (McDaniel & Morril) standing of the interactions between coccinellids and (Acari: Podapolipidae)], various male-killing bacteria fungal pathogens and to suggest future research directions (Wolbachia, Spiroplasma, Rickettsia) and insect patho- and priorities. This review was initiated after discussions genic fungi [such as Hesperomyces virescens Thaxter at the Aphidophaga 10 meeting (Athens, 2007) in (Ascomycota: Laboulbeniales) and Beauveria bassiana response to two papers on the interactions between fungal (Balsamo) Vuillemin (Ascomycota: Hypocreales)]. The pathogens and coccinellids (Cottrell & Shapiro-Ilan, role of natural enemies in regulating coccinellid popula- 2008; Roy et al., 2008a, b). tions generally requires more research, however, this is 391 TAXONOMY tion prior to host death in species which require continued Entomopathogenic fungi are common natural enemies host activity to ensure conidia dispersal (Roy et al., of arthropods Worldwide. Fungal systematics, particu- 2006a). Species in the Entomophthorales do not produce larly at the higher levels of classification, is continually toxins as part of the infection cycle and are obligate being reviewed and restructured (Hibbett et al., 2007). pathogens. They are characteristically biotrophic and Hibbett et al. (2007) propose a system of classification for have a narrow host range among foliar arthropods. They all groups of fungi based on recent molecular phyloge- are not known to be pathogens of coccinellids. netic studies. There are over 700 species of insect patho- In contrast two Hypocrealean (Ascomycota: Clavicipti- genic fungi and these can be found within two main aceae) fungi have been found infecting ladybirds: Metar- groups: phylum Ascomycota (subkingdom Dikarya) and hizium anisopliae (Matschnikoff) (Ginsberg et al., 2002) the order Entomophthorales from the subphylum Ento- and B. bassiana (James et al., 1995; Cottrell & Shapiro- mophthoromycotina. Ilan, 2003; Roy et al., in press). Hypocrealean fungi are The Entomophthorales, obligate pathogens of arthro- hemibiotrophic, switching from a parasitic, biotrophic pods, are an extremely important group of insect patho- phase in the haemocoel to a saprophytic phase colonizing gens historically placed within the Zygomycota. the body after death. The most aggressive strains of However, the Zygomycota is not an accepted phylum Hypocreales achieve host death usually by the production within the revised classification (Hibbett et al., 2007). of secondary metabolites. Conidia are not actively dis- Therefore, the Entomophthorales have not been assigned charged. Species belonging to the order Hypocreales have a phylum in the current classification but will be pending characteristically broad host ranges when associated with resolution of clades from the Zygomycota (Hibbett et al., soil-inhabiting arthropods in temperate regions. Similar to 2007). the Entomophthorales, the Hypocreales produce resting The taxonomy of the Ascomycota is more clearly structures for survival in the absence of new hosts or defined and contains two major orders: Hypocreales under adverse environmental conditions. (class: Sordariomycetes; subclass: Hypocreomycetidae) Another important group of fungi in relation to cocci- and Laboulbeniales (class: Laboulbeniomycetes). It is nellids is the Laboulbeniales (Ascomycota: Laboulbeni- worth noting that the ascomycete fungi were previously aceae). There are estimated to be between 10,000 and divided into two groups: Ascomycota and the Deuteromy- 50,000 species of Laboulbeniales on Coleoptera world- cota. The Deuteromycota were known as the Fungi wide (Weir & Hammond, 1997). Smaller numbers are Imperfecti (Deuteromycota: Hyphomycetes) and were thought to be associated with other insect orders (Blatto- species for which no sexual stage was known. However, dea, Dermaptera, Diptera, Hemiptera, Hymenoptera, Isop- morphological and molecular studies have demonstrated tera, Orthoptera and Thysanoptera) and also from non- that some of these “imperfect fungi” are anamorphs insect hosts (Acari and Diplopoda). These intriguing (asexual forms) of the Ascomycota (order: Hypocreales; fungi are obligate ectoparasites that infect many coccinel- family: Clavicipitaceae). Throughout this paper we will lids (Thaxter, 1931; Nalepa & Weir, 2007) occurring refer to the classification proposed by Hibbett et al. from the tropics to the sub-Antarctic on both terrestrial (2007). and aquatic hosts (Santamaria, 2001; Harwood et al., Although the taxonomy of these fungi is in a dynamic 2006). state the basic biology has been well studied. The general Most laboulbenialean fungi have few detrimental life cycles of these fungi are remarkably similar despite effects on their hosts (Weir & Beakes, 1996) but a few their taxonomic diversity (Roy et al., 2006a). Entomo- negative fitness effects have been documented including