ARTICLE IN PRESS Biological Control xxx (2009) xxx–xxx Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Review Mycophagy in Coccinellidae: Review and synthesis Andrew M. Sutherland *, Michael P. Parrella Department of Entomology, University of California, 370K Briggs Hall, One Shields Avenue, Davis, CA 95616, USA article info abstract Article history: Mycophagy, though often overlooked, represents an interesting and unique ecological niche within the Received 24 December 2008 Coccinellidae. Facultative mycophagy has been reported from the aphidophagous Coccinellini and the Accepted 20 May 2009 polyphagous Tytthaspidini. Members of Halyziini, a cosmopolitan tribe of the Coccinellinae, are obligate Available online xxxx mycophages specializing on the powdery mildew fungi of Erysiphales, a ubiquitous order infecting almost 10,000 angiosperm plants worldwide. Various researchers have recorded this mycophagous habit Keywords: during the past 150 years, resulting in a large list of host–powdery mildew complexes around the world Psyllobora harboring these insects. Members of the Halyziini possess several attributes conducive to biological con- Halyzia trol, including host specificity (obligation), widespread native distribution, and strong aggregative Illeis Macroilleis response to host density. We compare historical attempts to quantify powdery mildew removal by Vibidia Halyziini, and discuss the possible utility of mycophagous coccinellids for biological and integrated con- Mycophagy trol, as well as mechanical transmission of powdery mildew inoculum through insect dispersal. Mechanical disease transmission Ó 2009 Elsevier Inc. All rights reserved. Powdery mildew Erysiphales Plant pathogen Biological control Integrated disease management 1. Introduction dae or Endomychidae (S´lipin´ ski and Pakaluk, 1991; Giorgi et al., in this issue). Most members of this series are mycophagous. However, Although the overwhelming majority are predators of other the vast majority of the Coccinellidae are predators on sternorrhyn- arthropods, the Coccinellidae are not all purely entomophagous in- chan insects, and Giorgi et al. (in this issue) conclude that basal Coc- sects (Weber and Lundgren, in this issue; Giorgi et al., in this issue; cinellidae were coccidophagous. Leschen (2000) and several others Lundgren, in this issue). Phytophagy within the Epilachninae and (Lawrence and Hlavac, 1979; Crowson, 1981; Thomas, 1993) sug- mycophagy (both facultative and obligative) within the Coccinelli- gest that honeydew production by the commonly sternorrhyncan nae have evolved from a common coccidophagous ancestor (Giorgi prey of this family may have been the ecological opportunity for evo- et al., in this issue) that, in turn, may have been derived from an an- lution of predatory habits. Honeydew, a digestive by-product com- cient mycophagous group, the Cerylonid series, from which all cocc- posed of carbohydrates and proteins, often accumulates on plant inellids are descended (Sasaji, 1968; Leschen, 2000; Giorgi et al., in substrates where hemipteran insects feed and supports the growth this issue). Phytophagous ladybirds (Giorgi et al., in this issue) are of a specific group of Ascomycete fungi commonly known as sooty generally regarded as pests, but the beneficial or detrimental eco- molds. Leschen (2000) proposed a simple model whereby ancestral nomic position of the mycophagous Coccinellinae is less clear. This mycophagous beetles first accepted sooty molds as food items, then review presents some of the important historical literature associ- specialized as sooty mold consumers, and finally accepted the in- ated with mycophagous coccinellids, concentrating primarily on sects indirectly producing the mold as food items. This idea is obligate mycophages. In addition, we will discuss the taxonomy, strengthened by the fact that many predators of Hemiptera, includ- biology, ecology, and possible utility of this clade of ladybird beetles ing many coccinellids, also feed on honeydew and sooty mold to this as biological control agents. day (Majerus, 1994; Lundgren, 2009; Lundgren, in this issue). 2. Origin of mycophagy in coccinellids 3. Facultative and obligate mycophagy in coccinellids Coccinellids belong to the cerylonid series of Cucujoidea, and based on current phylogenetic data may be a sister taxon to Alexii- Within the Coccinellidae, mycophagy can be viewed as a de- rived condition, and it has only been reported from the Coccinelli- * Corresponding author. Fax: +1 530 752 1537. nae (Giorgi et al., in this issue). A molecular phylogenetic analysis E-mail address: [email protected] (A.M. Sutherland). by Giorgi et al. (in this issue) suggests that the Halyziini arose 1049-9644/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2009.05.012 Please cite this article in press as: Sutherland, A.M., Parrella, M.P. Mycophagy in Coccinellidae: Review and synthesis. Biological Control (2009), doi:10.1016/j.biocontrol.2009.05.012 ARTICLE IN PRESS 2 A.M. Sutherland, M.P. Parrella / Biological Control xxx (2009) xxx–xxx within the generally aphidophagous tribe Coccinellini. They con- managed systems (Amano, 1986). Despite the wide host range of clude that, in spite of distinctive mandible shape, presumably re- the order, individual species or biotypes within Erysiphales tend lated to mycophagy, both Halyziini and the poorly-known to be quite host-specific, often infecting only one species or genus Tytthaspidini (see below) have distinctive features which provide of plant (Amano, 1986). Thus, the evolution of PM has closely fol- further evidence for a derived condition. lowed the evolution of their hosts (Takamatsu, 2004). Similar envi- ronmental conditions are required for all PM to infect and develop, 3.1. Facultative mycophagy and unlike many other plant pathogenic fungi, spores can germi- nate and infect hosts under very low atmospheric humidity Facultative mycophagy may be commonplace in the largely (Takamatsu, 2004). Positive osmotic potential is detrimental to aphidophagous tribe Coccinellini Weise (Majerus, 1994). These the thin-membraned spores, and free water as overhead irrigation predators are often polyphagous, feeding on pollen, nectar, honey- has even been proposed as a control measure (Sivapalan, 1993; Liu, dew, fungi, fruit and foliage, but specific animal foods (e.g. aphids) 2001; Korner and Challa, 2003). Different PM fungi often infect are necessary to complete development (Hodek, 1973; Lundgren, many unrelated plants in an ecosystem simultaneously when con- in this issue). This distinction between ‘‘essential” and ‘‘alterna- ditions are favorable for PM germination and development. The tive” foods (Hodek, 1973) is important when discussing the ability of the Halyziini to feed on other fungi has not been reported polyphagy of the tribe. Additionally, at least some members of in the literature. Other lower fungi including yeast (Saccharomyce- the tribe do not have a mandatory minimum level of predation: tales) and rust fungi (Uredinales) were refused in simple laboratory Coleomegilla Timberlake and its allies can complete development no-choice trials with P. vigintimaculata (Sutherland and Parrella, on pollen alone (Lundgren and Wiedenmann, 2004; Michaud and unpublished). We suspect that PM fungi are common and abun- Grant, 2005; Majka and McCorquodale, 2006). Facultative mycoph- dant enough worldwide for this group of beetles to maintain a rel- agy, or mixed feeding on pollen, mildews (Erysiphales) and aphids atively specialized diet in many different climates and ecosystems. has been reported in Rhyzobius litura (F.) (Ricci, 1986) and Propylea The specialized feeding exhibited by the Halyziini and Tytthas- quatuordecimpunctata (L.) (Turian, 1971; Hukusima and Itoh, pidini is apparently facilitated by unique mandibular morphology. 1976). Upon finding fungal spores in the gut of Coccinellini, many The typical bifed mandibular apex of all Coccinellinae is modified researchers have suggested incidental or accidental consumption in the Halyziini such that the ventral tooth is further divided into of sooty mold fungi during honeydew grazing (Zoebelein, 1956; a row of additional teeth (Samways et al., 1997). Furthermore, Putman, 1964; Carter and Dixon, 1984). However, Triltsch (1999) the inner mandibular cutting edge of Coccinellini is smooth, while found Alternaria Nees conidia and Puccinia Persoon uredospores in the fungal-feeding tribes it is covered in minute teeth, forming a more frequently than aphids in the gut of Coccinella septempuncta- comb. These structures are presumed to help the insects to rake ta. These fungi are plant pathogens, and since the spores were fungal spores from conidial towers and spore-laden hyphae grow- found in both the presence and absence of aphids, it is likely that ing on leaf surfaces (Ricci, 1982; Lawrence, 1989; Samways et al., they represent an important seasonal food for the aphid predator. 1997). In the polyphagous Tytthaspidini these comb or rake-like Also within the Coccinellinae there is a poorly-known group of structures may also serve as tools for removing individual pollen polyphagous coccinellids that regularly include fungi in their diets grains, and fungal spores may be an alternative or incidental food along with pollen, arthropods and possibly some plants (Hodek and Honeˇk, 1996; Samways et al., 1997; Lundgren, 2009). These interesting mycophilous polyphages, closely allied to the Coccinel- lini, have