BioControl (2010) 55:159–185 DOI 10.1007/s10526-009-9248-3 Ecological factors in the inundative use of fungal entomopathogens Stefan T. Jaronski Received: 1 September 2009 / Accepted: 19 October 2009 / Published online: 24 November 2009 Ó US Government 2009 Abstract Fungal entomopathogens have been understanding of these ecological aspects is imper- developed in numerous countries as biocontrol agents fect, especially in a holistic, dynamic sense. with more than 100 mycoinsecticide products com- mercially available in 2006. The chief, perhaps sole, Keywords Metarhizium Á Beauveria Á use of these mycoinsecticides has been as inundative Persistence Á Efficacy Á UV Á Humidity Á agents, within a chemical paradigm. Large numbers Temperature Á Phylloplane Á Soil of propagules are applied in an attempt to overwhelm by brute force many of the factors that keep a pathogen in nonepizootic equilibrium with its host. Introduction This review attempts to summarize what we know about the abiotic and biotic factors that affect the The advent of chemical insecticides in the mid efficacy of these mycoinsecticides in both foliar and twentieth century created the concept that insect pests soil applications. Sunlight, humidity, temperature, could be all but eliminated from threatened crops. A and phylloplane-associated factors can affect both succession of compounds has appeared since then. immediate efficacy and persistence on plants. Like- Initially, many were quite toxic and environmentally wise, soil texture-moisture interactions, temperature, damaging. In recent years, however, new materials and a host of biotic factors can affect mycoinsecti- have appeared, which address human and environ- cides in the soil. Despite much research, our mental safety concerns caused by the earlier materi- als. In parallel, we have realized the inadvisability of using chemicals as stand-alone, catastrophic mortal- Handling Editor: Helen Roy. ity factors, and integrated pest management schemes have evolved to employ a variety of cultural, Mention of trade names or commercial products in this chemical, and biological tools to manage (not erad- publication is solely for the purpose of providing specific icate) pest invasion to a point below an economic information and does not imply recommendation or threshold. Biological tools, including microbial endorsement by the US Department of Agriculture. agents, have received increasing attention as alterna- S. T. Jaronski (&) tives to chemicals within this context. Nevertheless, US Department of Agriculture, Agricultural Research the chemical paradigm, in which a material is used to Service, Northern Plains Agricultural Research efficiently, simply, and quickly eradicate a pest Laboratory, 1500 N. Central Ave., Sidney, MT 59270, USA problem, still persists. Microbials are too often e-mail: [email protected] merely substituted for chemical pesticides. 123 160 S. T. Jaronski Among entomopathogens, fungi have attracted a entomopathogens in field crops are those of Feng lot of attention as biologically based pesticides. Per et al. (1994), Wraight and Carruthers (1999), Inglis Faria and Wraight (2007), 129 mycoinsecticide prod- et al. (2001), Shah and Pell (2003), and Goettel et al. ucts (fungus-based formulations targeting insects) (2005). My review will focus on the ecological were commercially available worldwide in 2006. aspects affecting the efficacy of these fungi when Fungi used in these products are primarily ascomy- they are used in an inundative approach in foliar and cetes including: Beauveria bassiana (Bals.) Vuill.; soil arenas. Understanding these factors, which affect B. brongniartti (Sacc.) Petch; Metarhizium anisopliae both efficacy and persistence, will allow intelligent (Metsch.) Sorokin., sensuo latum, M. acridum (for- manipulation of insect, pathogen, crop, and especially merly M. anisopliae var. acridum) (Driver and their environment, to achieve satisfactory manage- Milner) J.F. Bischof., Rehner and Humber stat. nov.; ment of an insect pest population within the context Isaria fumosorosea Wize (formerly Paecilomyces of inundative use. fumosoroseus); Lecanicillium longisporum and mus- Why inundate a crop with an entomopathogenic carium (Petch) R. Zare and W. Gams (formerly fungus? There are regulatory and economic, as well Verticillium lecanii); and Hirsutella thompsoni F.E. as technical, reasons. Pesticide regulations, which Fisher. In addition, the Oomycete Lagenidium gigant- include microbial agents, require generation of eum Couch has been commercialized in the US. human and environmental safety, and in some Inundative use of Nomuraea rileyi (Farl.) Samson and countries, replicated verification of efficacy, a process Aschersonia aleyrodis Webber has been studied and that can require approximately US$1–1.5 M, in the latter fungus was briefly commercialized in addition to normal development costs. If money is Europe. Despite the number of products, mycoinsec- to be invested in commercializing a microbial pest ticides have not captured a significant market share of control agent, there must be return on investment, the biopesticide market, especially in the US and EU. which in turn means repeat sales. Inoculation of a A principle reason is that, compared to chemical crop with a self-replicating organism (classical bio- pesticides, these mycoinsecticides lack consistent, control) defeats this purpose. speedy efficacy in combating insect pest problems, There are technical reasons for employing inun- and are more complicated to use, despite their obvious dative use. Unlike the Entomophthorales, the Hypo- safety. The chemical paradigm too often pervades the creales, particularly Beauveria spp. and Metarhizium use of biopesticides. spp., do not commonly cause natural, large-scale Fungal entomopathogens, as well as other micro- epizootics among insects in annual crops, nor have bial agents, can be used in several ways (Fuxa 1987; many classical or inoculative biological control Eilenberg et al. 2001). Classical biological control introductions been successful, with the possible involves introducing a novel fungus for permanent exception of Lecanicillium spp. (Hajek et al. 2005). establishment and long term pest control. This subject Most cropping systems and their insect pests are is discussed by Hajek and Delalibera (2009). Inoc- transient in nature, being present for only one ulative biological control has the expectation that the growing season, sometimes for only a few weeks. agent will multiply, spread, and provide extended In addition, widespread adoption of crop rotation on control of an insect pest, but only for a finite period. large areas of monoculture creates a very temporally These approaches require several key characteristics, unstable environment for any microbial agent. notably the ability for reproduction and horizontal Annual disruption in habitat not only removes the transmission to create epizootic spread. Alternatively, insect hosts, but in many cases directly destroys the the crop environment can be manipulated to enhance microbial agent. Inundation with a microbial agent, resident microbial agent populations (conservation sometimes repeatedly, is therefore necessary. Inun- biocontrol), as discussed by Pell et al. (2009). dation attempts to overcome many of the factors that The fourth approach is to inundate a crop with a keep a pathogen in nonepizootic equilibrium with its microbial agent in much the same manner as a host, by overwhelming the habitat with sheer num- chemical pesticide. Insect control is achieved only by bers of infectious propagules. Inundative use also fits, the organisms that were applied; there is little or no for better or worse, into the familiar chemical epizootic spread. Several reviews on the use of fungal paradigm—farmers simply apply the fungus as they 123 Ecological factors in the inundative use of fungal entomopathogens 161 would a chemical pesticide with the expectation of spray applications. For insects that actively move rapid, extreme efficacy. about their habitat, e.g., thrips and Heteroptera, The entomopathogenic Hypocreales have, in par- acquisition of spores from the environment can be ticular, received considerable commercial attention more important. Some insects, e.g., nongregarious over the past 30–35 years because they lend them- locusts and grasshoppers, present a mixed picture, in selves to in vitro mass production of sufficient which both direct and indirect acquisition of propa- quantities of infective propagules (aerial conidia, gules are important (Lobo Lima et al. 1992; Johnson submerged conidia, or blastospores) for use in an et al. 1992). In other cases, the situation is more inundative approach. In most or all cases, the complex. An example is larval Trichoplusia ni propagules need to be formulated with additives to (Hu¨bner) on cabbage versus beans. With cabbage, provide shelf life, inert diluents, spreaders, stickers, applications of a B. bassiana resulted in nearly equal and emulsifiers (Jaronski 1997; Burges 1998). The mortalities among insects exposed to direct spray propagule types and ecological considerations in contact or exposed to spray residue, whereas on formulating entomopathogenic fungi are discussed by beans, direct spray contact provided significant insect Jackson et al. (2009). For the sake of simplicity, I will mortality, but mortality due to residual contact was use ‘‘spore’’ as a generic description of the different ineffective (Behle 2006). Nevertheless, efficacy is propagules in this review, unless a specific propagule