Biologia, Bratislava, 61/Suppl. 21: S543—S616, 2006 Section Zoology DOI: 10.2478/s11756-007-0100-x Aphid-pathogenic Entomophthorales (their taxonomy, biology and ecology) Marek Barta & Ľudovít Cagáň Department of Plant Protection, Slovak University of Agriculture, Tr. A. Hlinku 2,SK–94901, Nitra, Slovakia; e-mail: [email protected] Abstract: Fungi of the order Entomophthorales (Zygomycota, Zygomycetes) constitute a group of mostly insect pathogenic species, which attracts attention of insect pathologists because of their high capacity for use in biological control of pest insects. This work primarily focuses on entomophthoralean species attacking aphids. The Entomophthorales are considered major pathogens of aphids in nature. In fact, the fungi are the only pathogens that regularly and effectively can affect aphid populations in natural ecosystems as well as in agroecosystems. Up to now, 33 entomophthoralean species organized into 9 genera have been recorded in aphid hosts. All fungal species are listed and organised by genus in the work. Descriptions are presented for all the fungal genera and species, including a nomenclature genesis, a geographical distribution, a host specificity/host range, a capability of cultivation in vitro, and possible prospects for their use in biological control strategies. A key to identification of the pathogens is provided as well. A general life cycle outline of the pathogens is followed by fundamental facts on biology and ecology of the fungi and analysis of primary factors that are involved in the study of epizootiology of infectious diseases in insect populations. The abiotic and biotic elements of the environment, which interfere in the pathogen–host interactions, are also underlined. In the last chapter, several examples are reviewed when the Entomophthorales were used against aphids within the four strategies of biological control, namely classical biological control, inoculation biological control, inundation biological control, and conservation biological control. The aim of this review is to cover the present status of knowledge about the natural enemies of aphids and to stimulate an interest of insect pathologists in this group of entomopathogenic fungi. Key words: Aphids, Entomophthorales, biological control. 1. Introduction and certain advances have recently been made in oth- ers. The fungi have been studied intensively in labora- Fungi of the order Entomophthorales constitute a group tories and tested in a small-scale in the field. However, of mostly zoopathogenic species and because of their there are some shortcomings of the Entomophthorales high capacity for use in biological control of pest in- as biocontrol agents coming from a fragility of infective sects in agriculture they have attracted attention of in- conidia, dormancy and an asynchronous germination of sect pathologists recently. The biological strategies of resting spores, as well as a complexity of infection cycle integrated pest management (IPM) reckon on the util- requiring successively: a contact between an infective isation of various groups of natural enemies. The En- spore and a host cuticle, germination, a penetration of tomophthorales are apt to be employed as prospective germ tube through a cuticle and, finally, a sporulation. biocontrol agents of several groups of agricultural pests. Moreover, all these phases are highly dependent upon It is especially because of their short infection cycle, a external conditions. high reproductive rate, as well as obvious and dramatic Interest in using the insect pathogens as control epizootics that may occur almost overnight. One of agents within IPM programs has generated a research particularities of the Entomophthorales, which enable in the development of microbial insecticides. Much them to spread fast, is an active projecting of conidia of this research has been focused on selection, isola- from conidiophores. Also, the Entomophthorales have tion, development, and production of highly pathogenic other characteristics making them valuable mortality species/strains with genetic characteristics favouring agents of insects. Most of the species are closely host their storage and usage. This orientation has enabled specific, so they pose no significant threat to non-target the pathogens to be applied to target hosts as re- organisms. Some of them are capable of being cultured placements for insecticides. Although some successes or produced in the laboratory or mass-scale. A tech- were noted, the majority of attempts to use the fun- nology of mass production is managed for some species gal pathogens as a substitute for insecticides resulted c 2006 Institute of Zoology, Slovak Academy of Sciences S544 M. Barta & Ľ. Cagáň in inconsistent responses. The pathogens were treated be useful to students of aphids’ natural enemies, re- mostly as direct substitutes for chemical insecticides searchers in insect pathology and microbial control of and were applied without an adequate understanding aphids, as well as to persons interested in the produc- of their population biology or their interactions within tion of microbial insecticides. a local environment. Consequently, this lack of under- standing caused the field of epizootiology to be a major 2. Fungal diseases of arthropods research priority in the insect pathology. Nowadays, the fungal biological control is an exciting and rapidly de- Fungal diseases in insect populations are common veloping research area with implications for plant pro- and widespread. They can often destroy insect pop- ductivity, food production, as well as animal and human ulations in spectacular epizootics and thus attract health. This area has an interdisciplinary character and man’s attention. Many of these fungi are consid- includes ecology, genetics, pathology, physiology, mass ered an important factor regulating pest insect pop- production, formulation, and application strategies. In ulations. Insect pathologists have been interested in the light of new knowledge of host/pathogen biology the fungal pathogens of their respective host groups and the environmental factors affecting biology, vari- for over 100 years. Until now at least 90 genera ous strategies of fungal exploitation have been devel- and more than 700 species of entomopathogenic fungi oped and discussed recently, including classical, conser- have been identified as closely associated with inver- vation, inoculation, and inundation biological controls. tebrates, predominantly insects, but only 10 of them Aphids belong to important pests of crops. They have been or are currently being developed for in- cause crop losses by extracting phloem sap mostly from sect control (e.g., Roberts & Humber, 1981; Car- leaves and stems of host plants, and excluding honey- ruthers & Soper, 1987; Hajek & St. Leger, dew. In addition, aphids are one of the most active vec- 1994; Wraight et al., 2001; Bateman & Chap- tors of various plant viruses. Their feeding can result ple, 2001). Within the wide kingdom of fungi, virtu- in deformation, wilting, even in necrosis of host tissues ally every major fungal taxonomic group but higher depending on an infestation level. Thanks to their high Basidiomycetes and dematiaceous Hyphomycetes has variability and specificities of their life cycle, aphids members pathogenic to insects (Roberts & Hum- may create forms resistant against frequently applied ber, 1981). Entomopathogenic species are distributed pesticide groups. The development of pesticide resis- mostly among the classes Chytridiomycetes, Oomyce- tance in the aphid populations highlights the impor- tes, Trichomycetes, Zygomycetes, and Hyphomycetes. tance of biological control as the pest management tac- As a matter of fact, most species attacking terrestrial tic. Many farmers and food producers have been inter- insects belong to the class Hyphomycetes or the or- ested in biological strategies of pest management with der Entomophthorales in the class Zygomycetes, while the intention of producing residue-free provisions and those attacking aquatic insects are generally from the eliminating the pesticide detrimental effects on human Chytridiomycetes and Oomycetes (Butt & Goettel, health. 2000). Although fungal pathogens share much in com- Aphids seem to be excellent hosts for studying mon with viruses, bacteria, and protozoa, there are entomopathogenic fungi, including the Entomophtho- many excellent differences and the most fundamental rales. As plant feeders, they are a significant and fre- is the route of infection. Fungal entomopathogens al- quent component of entomofauna in agroecosystems. most always attack their hosts by direct penetrating Nearly 4,000 species of aphids distributed all over the the exoskeleton and do not require ingestion with sub- world and occupying various climatic regions, mostly sequent infection through the gut wall. In contrast, vi- the temperate regions, guarantee a high species diver- ral, bacterial, and protozoan pathogens of insects or sity of the group of fungi. As individuals, aphids are other arthropods infect their host primarily via the di- small and inconspicuous; however, they live in colonies gestive tract. They must be ingested and infect the host and frequently become incredibly numerous. Existence through the gut wall. Most bacterial entomopathogens of aphids in dense colonies gives optimal conditions for infect their hosts through the gut, although bacteria fast disease dispersal and a background for epizooti- could also gain access to the haemocoele through cutic- ology studies.