Most people who garden are aware of insects that apparently are colonised by microbes. The small discoloured carcasses of larvae or adults are unearthed as you dig through soil. The microbes colonising the insects are called entomopathogens and one group of microbes that parasitise insects are the fungi. Insects are common and economically important pests of agricultural and horticultural crops. Several fungi, like those seen in parasitised garden insects, have been used to control insect pests in the field.
A diverse array of fungi associate with insects, and the nature of the interaction is also diverse. This section will only deal with pathogenic fungi, but see reference below for a detailed discussion of all types of association.
Biocontrol of insect pests can take one of several different approaches. The most common approaches are inundative application and classical control.
Several species of fungus have a reputation for biocontrol of insects. The fungi come from all divisions. The most commonly used ascomycetous fungi include the genera Beauvaria, Metarrhizium, Tolypocladium, Isaria and Lecanicillium. These fungi have been applied inundatively, in the manner of a chemical application, with the goal of killing most, if not all, insects. In comparison to chemical controls, knockdown is slower and generally incomplete. However, establishment of the pathogen may result in death of insects well beyond the period attained by chemical controls. Indeed, the risks of resistance are less and the effects on non-target organisms hugely reduced. Many substantial reasons point towards the use of entomopathogens becoming the most important control of insect pests. However, we still have not explored the depths of the interaction and much remains to be examined before fuller exploitation of fungi and other agents.
The most historically important of the commonly used fungi is Beauvaria bassiana. The Chinese have a long history of successfully culturing silkworms. However, when the industry was taken to Europe, cultures of insects were devastated by Muscadine disease. The causative agent was determined to be Beauvaria bassiana, a fungus that grows on and in larvae. Determination by Bassi that the infectious agent was a fungus, was one of the first examples where germs were shown to cause disease. The fungus has since been used successfully to control the larvae of many Lepidopteran insects.
Metarrhizium, also an asexual stage of an Ascomycete, has been successfully used to control spittlebugs in South America, Rhinoceros beetle in the South Pacific islands, and in Australia to control plague locusts.
Lecanicillium lecanii infects sucking insects such as aphids, white flies and scale insects. The fungus is used to control sucking insects mostly in greenhouses where humidity is high. Some plant-sucking aphids also have the nasty habit of transmitting viruses, thus control of the insect and the viruses it transmits are both possible.
Tolypocladium and Isaria have been reported to colonise a wide range of insects. Tolypocladium is particularly interesting because it effectively controls mosquitos in experimental conditions.
Penetration: In general, when a spore comes in contact with the insect cuticle, the spore attaches, germinates, penetrates the cuticle (from outside in, or inside out, depending on whether the spore lands on the outer surface, or is ingested). Penetration may involve physical force, LINK or more commonly physical and enzymic action combined. Inside the haemocoel, the form of the fungus may change to yeast-like LINK, though filaments and wall-less protoplasts are also found.
Penetration from outside-in appears more common. Many insects avoid disease when spores are ingested. In particular, large spores may be crushed by mandibles during ingestion. Smalll spores pass through the gut unaffected by the changing conditions, perhaps being unable to germinate because of suppressive conditions inside the gut. Sucking insects avoid ingestion altogether. However, sedentary insects may be exposed to epiphytic spores, especially as they walk about the surface of a leaf.
Secondary Metabolites: Many insect pathogens release metabolites that increase the chance of insect death. Indeed, many entomopathogens are closely related to fungi known to release a wide array of toxins and molecules that induce change in or modify behaviour (Cordycipitales, Trichocomaceae etc). The wide range of pathogenicity factors come from different metabolic pathways. The factors may be toxins, immunosuppressants or antibiotics. For instance, destruxens from Metarrhizium are polypeptides that appear to be directly toxic to the insect. Cyclosporin-like immunosuppressants from Tolypocladium increase the rate at which the fungus colonises the haemocoel. LINK Better understanding of the formation and mode of action of secondary metabolites will be important if rapid knock-down of insects remains the goal of inundative biocontrol.
The control of pasture cockchafers (Aphodius sp) has been achieved in the Adelaide Hills of South Australia by the release of an isolate of Metarrhizium specific to the host. The larvae of the insect burrow through soil where they feed from roots of pasture grasses and incidentally, contact spores of the fungus. Colonisation of the larvae results in death after several days, with the subsequent release of spores of the pathogen, followed by subsequent cycles of contact, colonisation and insect death. The underlying assumption is that the fungus survives as a saprotroph or on carcases of insects, though this may be incorrect. Survival of the pathogen and rates of contact between insect and pathogen are key to successful control of the insect pest.
In principle, the density of the fungus increases when high levels of insect are present in the soil. As a result the insect population declines, enough for most of the larvae to miss contact with the fungus. However, the fungus is sustained in soil at a low density, to become active only as the larval densities increase. While simple and cheap, classical interactions between pest and pathogen, even when several pathogens are included, may not be sufficient control of the pest for highly intensive pasture systems.
At present, the use of genetically modified plants is seen as the most promising technology for the control of insect pests in intensive agriculture. However, usually a single gene is inserted to the plant, and insect tolerance to the gene product soon develops. Multiple gene insertions are not yet common. Thus alternative and complementary methods are needed for insect control.
Fungi may interact with insects directly and indirectly. Several insects are of major concern in Australia. One, Helicoverpa armigera is a serious pest of many different crops and pastures. In cotton, larvae eat foliage and bore into boles. Helicoverpa has several stages where it is vulnerable to biocontrol agents: as eggs on the plant surface, as larvae on the plant surface and as long-lived pupae in the soil.
Fungi may play a direct role at each stage. Fungi that live on the leaf surface may colonise eggs. This interaction requires relatively high humidity on the leaf surface for the interaction to be initiated. Fungi that live in the leaf may deter insects from laying eggs or feeding in the leaf, or poison larvae feeding from the leaf LINK. Fungi may colonise pupae in soil, much as happens with pasture cockchafers. Again, as for cockchafers, success relies on contact between fungus and insect. We know very little about the overlap of life cycles of the two groups of organisms or how we can increase the chances of contact between the two.
Interestingly, while it has been known for some time that many entomopathogens can be isolated from soil, and occasionally plants, recent research has found that a few entomopathogenic fungi can colonise healthy plants (endophytes) where they are biologically active. For instance Beauvaria bassiana can be inoculated on to seed from which it will establish a systemic colony in a wide variety of plants. Other fungi (Metarrhizium, Lecanicilliumand Isaria) will colonise inoculated leaves or roots, though not necessarily spread beyond the initial colony. The degree of plant colonisation appears to be isolate specific, and environmental conditions are important. Effective insect control will require clearer understanding of the genetics of interaction, environmental conditions neded for insect colonisation and methods of application of the biocontrol agent(s). Endophytic entomopathogens have enormous potential in the biocontrol of insect pests because the fungi are protected from environmental stresses, though not the protective responses of the host plant.
Each fungal isolate may have widely differing effects on the plant and insect host. This wide variation of interaction opens up the possibility of breeding plants capable of supporting endophytes specifically to reduce damage caused by insect pests. While the nature of the interaction of endophytic entomopathogens remains to be clarified, this field has enormous potential economic, social and environmental benefit.
Fungi may also influence the way target plants respond to the insect pest. The first is direct, via release of insect toxins by the fungus. So far, only a few fungi have had their entomotoxins characterised. Indirect interactions are also documented. Induction of a plant response to fungal pathogens is well recognised. A similar response to insects is induced in plants by some fungi. The biosynthetic pathways are becoming clearer. Indirect control or induction of plant mediated defences to insect pests requires considerable research before it can be used in field control of insect pests.
Insects and fungi interact in various ways. The interactions where fungi kill the insect or regulate insect growth rates or behaviour may be used in specific cases. Our overriding impression is that we know so little about the interactions, we are probably going to find many associations beyond the obvious that can be manipulated to initiate an economically important decline in pest activity.
Butt TM, Jackson CW & Magan N 2001 Fungi as Biocontrol Agents. CABI.
Lawrence JF, and Milner RJ. (1996). Associations between fungi and arthropods. Fungi of Australia Vol 1B, 137 – 202.
Robson GD, van West P & Gadd GM (eds) 2007. Exploitation of Fungi. CUP