Biological Control
6.3 Micro- and Macro-biological Control Agents
The science of biological control is the science of insect population ecology, since biological control is essentially an interac- tion between predator and prey popula- tions. There can be little doubt that classical biological control has contributed to the development of insect population ecology but there is less evidence that bio- logical control has benefited from the the- ory of population ecology (Waage, 1989).
Although the theory has provided a scien- tific framework for the practice of biologi- cal control, improved our understanding of predator–prey interactions and helped to identify suitable attributes for potential biological control agents. In practice, the assessment of natural enemies for such characters is rarely carried out prior to release due to constraints in time and resources or because of poor scientific tech- nique. Also the value of theoretical and analytical models to biological control is quite limited since they tend to operate within quite narrow criteria. Simulation modelling on the other hand is increas- ingly used because when combined with appropriate experiments it can identify the constraints on pest systems, gaps in experi-
mentation, as well as potential candidate species for control (Wratten, 1987).
The use of natural enemies has long been recognized as a fundamental aspect of insect pest management but too few sys- tems have been studied sufficiently for the pest–natural-enemy interactions to be ade- quately understood. Ecological theory undoubtedly has a role to play in the future but hopefully in more diverse ways than at present. The approach presented here tries to provide a balance between the theoreti- cal and the practical, the potential and the realistic, since it is only with a more prag- matic approach that the use of natural ene- mies in insect pest management will continue to gain credence.
6.3 Micro- and Macro-biological Control Agents
The types of natural enemy used in biologi- cal control of insects includes pathogens, and a surprising range of invertebrates act- ing as predators, true parasites and para- sitoids. Insect parasites usually kill their insect hosts and hence differ from true par- asites that do not. To recognize this funda- mental difference insect parasites have been referred to as parasitoids (Reuter, 1913).
6.3.1 Pathogens
The entomopathogens that have been used in biological control include representa- tives of bacteria, fungi, viruses, nematodes and protozoa. There tends to be an inverse relationship between the attributes of these pathogens that can successfully be employed as biopesticides and those that are appropriate for introductions, augmen- tation, inoculation and conservation. The pathogens effective in these longer term, limited release strategies generally have lower virulence than their insecticide counterparts but can survive for longer periods in the host population, or in the environment, for example through the pro- duction of resistant stages (Payne, 1988).
For instance, the European corn borer
(Ostrinia nubilalis) is host to Nosema pyrausta which has a low pathogenicity, causing some larval mortality especially under environmental stress but most host individuals survive to adults but have a reduced longevity and fecundity (Canning, 1982). The parasite is transmitted transo- varially and is highly prevalent in the field.
Other examples include the protozoan Nosema locustae, the bacterium Bacillus popilliae, the Oryctes (rhinoceros beetle) baculovirus, the nuclear polyhedrosis virus for the sawfly Gilpinia hercyniae, and the fungus Beauveria brongniartiiused in the control of the cockchafer Melontha melon- tha. However, examples of sustained nat- ural insect population regulation in crop systems by entomopathogens are rare. This is because regulation demands stable ecosystems, such as forests and rangelands, and a capacity for the pathogen to spread (Payne, 1988). Hence for the most part, entomopathogens have been considered only as biological alternatives to chemical insecticides (Waage, 1997).
Primary among the pathogens used as environmentally friendly alternatives to chemicals and commercialized for use in this way have been bacteria, particularly Bacillus thuringiensis (Bt). Bt was first recorded in 1901 in Japan but was named by Matte in 1927 from a strain isolated in Germany. By the mid-1940s, the first com- mercial preparation named ‘Sporeine’ was available in France (Deacon, 1983).
Currently, Bt products are being used on several million hectares annually to control lepidopteran pests of agriculture, forestry and stored products (Smits, 1997) and rep- resent 39% of the 185 biopesticide prod- ucts on the market (Copping, 1999). The Bt bacterium (a Gram-positive spore forming rod) is characterized by an intracellular protein crystal which contains a toxin that acts as a poison for lepidopteran larvae.
When a mixture of the spores and crystals are ingested by the insect feeding on treated vegetation, the protein crystal is solubilized in the alkaline mid-gut (pH 10.2–10.5) and the toxin is released; the toxin causes gut paralysis and the bac-
terium is then able to invade the weakened host and cause a lethal septicaemia. There are thousands of Bt isolates grouped into serotypes or subspecies that are character- ized by flagellar antigens (Smits, 1997).
Well known subspecies are Bt kurstakiand Bt azaiwai, which are active against lepi- dopteran larvae, Bt israeliensis which is active against dipteran larvae and Bt tene- brioniswhich is active against coleopteran larvae. Another species of Bacillus, B.
popilliae is also active against beetles, causing what is known as ‘milky disease’
of beetle larvae. A further species, Bacillus sphaericus, is also of some practical impor- tance because of its use against mosquito larvae. However, it is Bt that has domi- nated biopesticide development and has found most commercial success to date, although viruses, fungi and entomopatho- genic nematodes continue to grow in importance.
There are six main groups of insect viruses but only three are sufficiently dif- ferent from human viruses to be considered safe and these are: the nuclear polyhedro- sis virus (NPV), the granulosis virus (GV) and the cytoplasmic polyhedrosis virus (CPV). All three are occluded viruses, i.e.
the virus particles are enclosed in a pro- teinaceous shell which has a paracrys- talline structure called an inclusion body (Payne, 1982). Around 125 types of NPV have been described, isolated from Lepidoptera (butterflies and moths), Hymenoptera, Diptera (cranefly and mos- quitoes) and the Orthoptera (grasshoppers and locusts). NPVs tend to be family spe- cific with little or no cross infection between insect families. There are only about 50 GVs recorded, mainly form Lepidoptera, and over 200 CPVs but the CPVs are not very host specific and hence have less potential as biopesticides. All three types of virus need to be ingested, after which the inclusion body dissolves in the insect’s mid-gut, releasing the virions which penetrate the epithelial lining and start to replicate. The time taken to kill varies according to dose, insect develop- ment stage and environmental factors but
generally ranges from 6 to 24 days. The CPVs can take longer to kill and can be rel- atively unstable (Deacon, 1983). The num- ber of commercially successful products is limited (there are 24; Copping, 1999) in comparison with the number of bac- uloviruses studied (Smits, 1997); however, there are a number that proved economi- cally viable, e.g. Heliothis zea, NPV for cot- ton, vegetables and tomato, Spodoptera exigua NPV in vegetables, cotton and grapes (Georgis, 1997).
More than 750 species of fungi have been recognized as entomopathogens (McCoy et al., 1986) with the most potential as biopesticides from the Deuteromycetes (‘imperfect’ fungi), namely species of Beauveria, Metarhizium, Verticillium, Nomuraea and Hirsutella. Individual species of fungi such as Metarhizium aniso- pliae have wide host ranges including species of Coleoptera, Lepidoptera, Orthoptera, Hemiptera and Diptera (Hall and Papierok, 1982). In addition to their wide host range, a further attribute that makes these fungi attractive as biocontrol agents is their route of infection.
Entomopathogenic fungi do not need to be consumed by the insect, they can penetrate the cuticle, which means that they can be used against insects with sucking mouth- parts. Up until 10 years ago, the potential of fungi seemed limited by their need for high humidities in order to germinate.
However, more recent developments in for- mulation technology have removed this constraint so that it is now possible to use fungi for control of pests in semi-arid envi- ronments (Neethling and Dent, 1998).
Worldwide, there are currently 47 fungal based products used as biopesticides (Copping, 1999) and it is likely that many more will be developed in the near future.
The same is true of entomopathogenic nematodes of which there are currently 40 products available worldwide (Copping, 1999). The prospects for nematode prod- ucts have been aided by the lack of regis- tration requirements for these biocontrol agents. The main interest in nematodes has been concerned with those species that kill
their hosts in a relatively short time. There are three families of nematodes to which this can be considered to apply: the Steinernematidae, the Heterorhabditidae and the Mermithidae. The first two families are terrestrial nematodes that are associ- ated with symbiotic gut bacteria that kill the host by septicaemia, and the Mermithids are aquatic nematodes that kill their host upon exit through the cuticle. In agricultural systems, the searching ability of nematodes (although limited) makes them potentially ideal candidates for use in situations where chemical insecticides and microbial formulations cannot be targeted effectively, for instance the cryptic habitats of pod borers, tree boring insects or for root attacking insects in soil (Poinar, 1983). The nematode infective (which is the third stage larva ensheathed in the second stage cuticle and referred to as a dauer larva) can detect its host by responding to chemical and physical cues. The Steinernematidae enter the host via the mouth, anus or spira- cles while the Heterorhabditidae also have the ability to penetrate the host cuticle (Kaya, 1987). Once inside the host, the dauers exsheath and mechanically pene- trate through the haemocoel where symbi- otic bacteria are released to kill the host by septicaemia within 24–48 hours (Kaya, 1985). The nematodes develop and repro- duce, the Steinernematidae need both male and females per host for reproduction while Heterorhabditidae are hermaphro- dites. As the resources are depleted, the nematodes leave the cadaver in search of new hosts.
Steinernema carpocapsae products have been used in a wide range of systems including home and garden, berries, turf grass, ornamentals, citrus and mushrooms (Georgis, 1997) against Lepidoptera and Coleoptera (Curculionidae and Chrysomelidae). Steinernema feltiae has been targeted successfully at dipteran pests, particularly Sciaridae, while Heterorhabditis species have been used against lepidopteran and coleopteran pests.
Provided limitations of production and for- mulation can be overcome, the potential
use of entomopathogenic nematodes look promising.
The situation, however, is less promis- ing for protozoa as biocontrol agents. Their low levels of pathogenicity causing chronic rather than acute infections, and difficulty of large scale production makes these pathogens unattractive prospects as biopes- ticides. This is reflected in the fact that there are only two protozoan based biopes- ticides available worldwide (Copping, 1999). Despite this, further research could exploit protozoan potential for use as inoc- ulative augmentations or introductions in stable habitats such as forests and pastures.
6.3.2 Predators
Predators of insects may be ento- mophagous insect or vertebrates. Vertebrate natural enemies of insects pests can be found in each of the five animal groups, although only birds and mammals have attracted any serious attention. Reptiles and amphibians have such low consump- tion rates (Buckner, 1966) that they have little potential as biocontrol agents and although fish have been shown to be important in the control of mosquitoes (Hoy et al., 1972; Legner, 1986; Bence, 1988) and rice stemborers (Durno, 1989), more work needs to be done to evaluate the potential of this major group. Birds have long been recognized as predators of insect pests but it is only occasionally that such effects are quantified (Dempster, 1967;
Stower and Greathead, 1969; Atlegrim, 1989). Buckner (1966, 1967) considered the role of both birds and mammals in the con- trol of pest insects in forest ecosystems.
The two groups prey on insects in different parts of the forest system, with the birds feeding on free flying adult insects and on larvae inhabiting the trees while the mam- mals were mainly restricted to feeding on ground inhabiting stages of the insect’s life cycle, mainly the pupae. The importance of these natural enemies is potentially quite high because they are feeding on the later stages of the insect’s life cycle, i.e. pupae and adults, rather than the more abundant early stages. The animals may concentrate
their feeding on pest prey when they are readily abundant but are also likely to have alternative sources of prey that they can switch to as the pest numbers diminish.
Such generalist feeders are thought to be of little value as biological control agents and numbers of mammals and birds can not be easily manipulated at man’s convenience (Harris, 1990). Hence, the potential for such animals as biological control agents is low except perhaps in very special circum- stances, such as the masked shrew (Sorex cinereus cinereus) which was introduced into Newfoundland from the mainland USA to control the larch sawfly, Pristiphora erichsonii(Buckner, 1966).
Predators feed on all stages of the host, eggs – larvae (nymphs), pupae and adults – and each predator requires a number of prey individuals to enable it to reach matu- rity, unlike parasitoids which require only a single individual. The immature stages as well as adult predators then have to search, find, subdue and consume prey.
Predators can be crudely divided into those with chewing mouthparts and those with sucking mouthparts but generally they lack the highly specialized adapta- tions associated with parasitism. Predators are found among the Coleoptera, Neuroptera, Hymenoptera, Diptera, Hemiptera and the Odonata, but more than half of all predators are coleopterans (DeBach, 1974). The most important fami- lies within the Coleoptera for biological control have been the Coccinellidae and the Carabidae. Other arthropod natural enemies include predatory mites and spi- ders. Predatory mites have played an important role in biological control both in orchards and glasshouse systems by feed- ing on phytophagous mites (Gerson and Smiley, 1990), but too little attention has been paid to spiders although they are abundant in perennial systems such as orchards. A number of studies have identi- fied numerous species of spider as impor- tant predators of arthropod pests (Riechert and Lockley, 1984; Riechert and Bishop, 1990) and capture efficiencies have been determined for some species (e.g.
Sunderland et al., 1986). Individual species of spider appear incapable of track- ing population changes in specific prey species, either through increased rates of attack or through changes in effective pop- ulation densities in local areas (Riechert and Lockley, 1984). However, spiders are for the most part polyphagous and as such are not considered ideal as candidates for control agents.
6.3.3 Parasitoids
A parasitoid is only parasitic during its immature stages when the larvae develop, either within (endoparasite) or on (ectopar- asite) their host, from eggs that were either oviposited inside or near the host. The developing larva(e) usually consume(s) all or most of the host and pupate either within or near it. The adult parasitoid is free-living and usually feeds on substances such as pollen, nectar, honeydew or some- times on the body fluids of its host.
Parasitoids exhibit a number of different life habits and are themselves parasitized by secondary or hyperparasites. Endo- and ectoparasites can be solitary or gregarious;
when a single larva is produced per host individual then the parasitoid is solitary but if a number of larvae develop within a single host and all the larvae survive to maturity, then the parasitoid is described as gregarious. However, if more than one species of parasitoid parasitizes a host then it is known as multiple parasitism. In such circumstances it is rare for all species to complete their development. Where a num- ber of individuals of a single parasitoid species occur in one host but only a few survive to maturity, it is referred to as superparasitism. The host can sometimes die prematurely with the result that all the developing parasitoids are lost (van den Bosch and Messenger, 1973), or if the host does not die and a number survive then the adults may be smaller than normal (Samways, 1981). Different species of para- sitoid attack different life stages of the pest.
Thus, Trichogrammaspp. which attack the egg stage of insects are known as egg para- sitoids, Braconidae such as Cotesia glomer-
ata which attack larvae are larval para- sitoids and so on for adult and nymphal parasitoids (van Driesche and Bellows, 1996). Further details of parasitoids can be found in Askew (1971) and Waage and Greathead (1986).
The types of natural enemy used to con- trol pest species through introductions, augmentations, inoculations and conserva- tion has largely been dominated by ento- mophagous insects, and within these groups, primarily by host specific para- sitoids in preference to more generalist species. The use of birds and mammals has largely been restricted to a few specific sit- uations and is now generally considered inappropriate by responsible biocontrol practitioners. The opportunities for the use of pathogens for inundative release is now becoming increasingly important as new developments improve the performance and attributes of these agents for use as biopesticides.