Introduction

A species is described as an invader when it colonizes and persists in an ecosystem in which it has never been before (Mooney and Drake, 1989). Invasions by insects seem to be rather well documented, but that is a false impression. It is only for two categories of insect species that documentation of successful invasions is complete: (i) for pest species (usually herbivores); and (it) for natural enemies (predators and parasitoids of insect pests, or phytophagous insects used in weed control). This information relates mainly to agro-ecosystems and few or no data are available for insect invasions in other ecosystems. This might mean that such ecosystems are not frequently invaded, that the effect of invaders is not dramatic (but see Howarth, 1991; also, see Hopper, Chapter 6 and Andow et al, Chapter 10), or that these other ecosystems are considered economically so unimportant that they receive no attention. The first view seems to be supported by the general literature on colonization, where the massive restructuring of natural ecosystems is usually regarded as the main cause for making invasions possible. Complex natural systems are replaced by a few plants and animals that are of direct use to humans (Mooney and Drake, 1986a).

This paper is structured as follows: first, some general facts about insect invasions are stated and then several case studies are provided to illustrate problems created by insect invasions. Following this the characteristics of the insect invaders and the systems which are invaded are discussed. Finally, some specific questions related to the predictability of the effects of insect invasions are answered.

Introduction

Introductions of parasitic wasps have often led to economic control of introduced insect pests (Clausen, 1978). Biological control practitioners argue that such introductions have fewer and less severe detrimental impacts than alternative controls (DeBach and Rosen, 1992). However, others have challenged this viewpoint (Howarth, 1983, 1991) with the argument that introduced biological control agents can drive non-target populations extinct, especially if these are already rare. Others have responded that the impact on conservation of insects species is unlikely if introductions are done carefully (Samways, 1988). Unfortunately, this controversy has given rise to more heat than light, being plagued by excessive generalization, lack of hard data on adverse impacts, and lack of concrete recommendations about how to reduce the risks of introductions. The lack of data on adverse impacts arises, in part, because many biological control projects lack the funds for evaluating the impact of the introduced agent on the target species, let alone on non-target species. The low level of funding, relative to the complexity of the problems involved, also means that methods to reduce risks will have to rely heavily on extant knowledge, if biological control introductions are to continue. In this chapter, I will address the following questions: How can one predict the potential impacts on threatened and endangered insect species from introductions of parasitic Hymenoptera for the control of insect pests in the continental United States?; and, What are the potential impacts from selected introductions? I have chosen a narrow scope of impacts and types of introductions to avoid overgeneralization.

Introduction

The use of chemical pesticides has resulted in a considerable increase in crop yields throughout the world. There is, however, increasing public pressure against the use of chemical pesticides due to their adverse effects on human health and the environment. The very concept of using chemical pesticides has been challenged by the green movement, which is constantly gaining momentum. World-wide, annual agrochemical sales amount to approximately $US 25 billion (Powell & Jutsum, 1993). Biocontrol agents and biopesticides currently contribute only about 0.5% to the total (Meneley, 1990; Anonymous, 1992). Products based on Bacillus thuringiensis account for 90-95% of biopesticide sales (Feitelson et at., 1992). Bacillus thuringiensis is a biologically produced pesticide, but the active ingredient is not a living organism.

The economics of pesticide use can be considered at three levels: the producer/distributor, the user and society. A pesticide must eventually bring profit for the producer and it must give ample economic return to the user. From society's point of view, the economic benefits from use of a pesticide must clearly offset the adverse effects (Pimentelera/., 1991).

There are scant historical data on the economics of biopesticides other than for Bacillus thuringiensis-based products. Most of the data are proprietary. In this chapter, I discuss the economic aspects of biopesticides from the viewpoint of a company commercializing biopesticides (see Cullen and Whitten, Chapter 26 for a discussion of the economics of biocontrol from a research perspective). The scope is limited to microbial biopesticides. Special emphasis is given to the risks involved in various steps of the development and commercialization process.

Introduction

The application of biological control agents is an established if under-exploited method for the control of agricultural pests and diseases. There are considerable benefits to be gained from this approach, however caution is necessary in the introduction of biocontrol agents because of possible effects on non-target organisms. In some situations the biocontrol organism itself may become a pest.

There are numerous examples of experimental biocontrol treatments for fungal and bacterial plant root diseases, though on a practical level there are less examples than for control of insect pests. Plant root diseases can often be controlled by management practices such as rotation with a non-host crop or by several years of crop monoculture, a practice which can lead to the build-up of a disease-suppressive soil (Hornby, 1983). Microbially mediated disease suppression can also occur in soil-less potting mixes (Hoitink and Fahy, 1986). Fungicides (e.g. Baytan for control of take-all) are used for control of disease, but success has been limited especially when applied to field crops. Biological control agents used to control soil-borne root diseases are most commonly soil bacteria or fungi.

On the whole, there are relatively few publications dealing with risk assessment in the literature on biocontrol. Recent papers include that by de Jong et al (1990). The need for risk assessment is now much greater, particularly as genetic manipulation is beginning to be used more often in biological control (Jones and Kerr, 1989; Ryder and Jones, 1991). The use of recombinant DNA technology brings its own risks and benefits. Given that there are both risks and benefits for pest control methods, procedures for their estimation are desirable.

Introduction

Insects are susceptible to a wide range of viral pathogens, but viruses of the family Baculoviridae, which occur only in arthropods, have received most attention because their high pathogenicity, narrow host range, and complete safety to vertebrates and plants, make them particularly promising candidates for biological pest control agents (see Huber, Chapter 18). Although natural strains of these viruses can in many cases provide highly satisfactory levels of control, the past 5 years has seen several attempts to produce genetically engineered baculoviruses with improved insecticidal properties. The chief target for these improvements has been reduction in the crop damage that continues to occur after infection of the insects.

A second reason for using genetically engineered baculovirus insecticides is to provide marked strains for ecological studies in a manner somewhat analogous to the way that animals are often marked physically in order to study in a more detailed way their behaviour and survival. Marked viruses may contain simply a short stretch of introduced DNA in their genome. This can be detected by various methods such as dot blotting, Southern blotting, restriction enzyme analysis (especially if the introduced DNA contains additional restriction sites), or, with much greater sensitivity, by use of the polymerase chain reaction. Alternatively, marked viruses may contain a reporter gene that expresses a protein, usually an enzyme, which can be detected easily and specifically. The E. colt lacZ gene, which codes for P-galactosidase, has been found particularly useful.

Introduction

Progress in agronomy over the last 30 years has allowed world food production to almost double. In part, this was possible through the control of diseases caused by air-borne pathogens. However, the damage caused by soil-borne pathogens has increased during the same period; this has resulted in important yield reduction in protected and unprotected crops. To date, satisfactory methods of control have not been developed. Few plant varieties are resistant to soil-borne pathogens. Unfortunately, crop rotation is often not possible for economic reasons. Pesticides are seldom effective in soil and growing concern for the environment restricts their use. Biological control of root diseases can be considered as an alternative for the future. The pseudomonads are currently receiving attention world-wide because some strains, added at a few grams or milligrams per hectare, effectively increase crop yield and improve plant health. These beneficial effects are well documented, however the mechanisms involved are only partially understood. A better understanding of these mechanisms is crucial to safety if pseudomonads are to be released on a large scale. Data on safety are scarce because the investigation of potential risks associated with the release of pseudomonads has just begun. This review will mainly focus on the results obtained with strain CHAO of Pseudomonas fluorescens.

Beneficial effect of resident populations of pseudomonads

Resident populations of pseudomonads are part of the natural disease suppressiveness of soils and of suppressiveness induced by monoculture or solarization (Smiley, 1979; Scher and Baker, 1980; Rovira and Wildermuth, 1981; Cook and Weller, 1987; Defago and Haas, 1990; Gamliel and Katan, 1991). It is important to realize that natural suppressiveness occurs only in distinct areas.

Introduction

The Industries Assistance Commission of Australia, in their review of the economics of agricultural research using the CSIRO Division of Entomology as an example, concluded that the majority of projects were ‘dry holes’ in that they yielded negligible economic return, but that it only needed one or two successes to pay for the entire operation of a large research agency over a decade or more (Marsden et ah, 1980). Biological control was a major area considered in that review and these two principal conclusions are as true for this field as they are for the general case. Less than half of biological control projects produce substantial success, but those that do are the really big winners.

We would like to review briefly the history of application of economics to biological control in Australia and then consider the benefits and costs in a more general sense. There is nothing unique about biological control from an economic viewpoint, though it does have some special properties that assist the process and increase benefits, and others that require particular consideration.

The examples that we propose to cover concern classical (inoculative) or inundative biological control where the natural enemies have been selected from naturally occurring species or biotypes. We do not cover the release of genetically improved natural enemies, whether modified by conventional methods or by genetic engineering. Many of the concepts we canvas are equally relevant to the ‘new technologies’ in terms of assessing the costs of research, the likelihood of success and the ensuing economic benefits. Even the risks are not dissimilar in nature.

Introduction

To develop successful biocontrol of plant diseases by the introduction of naturally occurring (see Défago et al., Chapter 12) or genetically engineered (see Dowling et al. Chapter 14) antagonistic pseudomonads, careful research is needed to assess risks. This includes viability and translocation of the microbes in soil ecosystems, transfer of genetic material to and from the indigenous soil microbial communities, effects of introductions on biochemical functions of the soil microflora and so on. The development of detection methods is important, not only for risk assessment of survival or dispersal of biocontrol microorganisms, such as genetically engineered microorganisms (GEMs) in soil, but also to evaluate the efficacy of biocontrol agents against plant diseases.

Pseudomonas cepacia Palleroni & Holmes, was initially described as a phytopathogen (Burkholder, 1950) as well as a saprophyte in soil (Sinsabaugh and Howard, 1975). It has been reported to provide biological control of certain soil-borne diseases, such as Fusarium-wilt of onion (Kawamoto and Lorbeer, 1976), damping-off of radish, Fusarium-wilt of tomato and Verticilliumwilt of eggplant (Homma et al., 1985). This bacterium is also known to produce various antibiotics, such as pyrrolnitrin (Elander et al., 1968; Janisiewicz and Roitman, 1988; Homma et al., 1989) and pseudane derivatives (Homma et al 1989), which are supposed to contribute to disease suppression. On the other hand, P. cepacia is extremely resistant to antimicrobial agents and is able to survive and multiply even in purified waters (Carson et at., 1973). In addition, it is known to be an opportunistic pathogen and has been described as a synonym for P. kingii and P. multivorans, and as aetiological agents of clinical infection (Ederer and Matsen, 1972; Randall, 1980).

Introduction

Currently the only one commercialized biological control product against foliar fungal diseases exists, namely, ‘Trichodex’ (Makhteshim Chemical Works) for the control of grey mould of cucumber, tomato and grapevine (Y. Elad, personal communication). A few other products based on fungi are in the final stage of development or registration. Therefore, this review will primarily deal with the state of the art, which ranges from interesting hypotheses to promising research achievements under controlled and natural conditions. Compared with research efforts on biological control of soil-borne diseases, biological control of foliar diseases has up till now received little attention. The main reason for this appears to be the relatively efficient control of many above-ground pathogens by aerial applications of fungicides, while soil-borne pathogens are more difficult targets.

Nowadays, however, the world-wide awareness of the potential danger to the environment from many currently available chemical control agents and the increasing occurrence of fungicide resistance in a number of foliar pathogens has boosted research aimed at alternative means of disease control. For instance, in the Netherlands, a ‘Multi-Year Crop Protection Plan’ has been launched in 1990. This aims at a reduction in total amount of pesticide used of at least 35% by 1995 and 50% by the year 2000 (Anonymous, 1991). More importantly, the average emissions (the average pesticide emissions (to air, soil/ground water, surface water) to the environment are to be reduced to 50% in 1995 and to 30% in the year 2000.

Introduction

While integrated pest management research has sought to reduce the use of pesticides in agriculture over the past 30 years, current public and political pressure has increased dramatically the urgency of the search for alternatives. Few are immediately available, and this places particular reliance on some key biological control agents. One such agent is Bacillus thuringiensis Berliner (Bt), which is the most widely used biopesticide. Sales have doubled in the past 4 years and are conservatively forecast to rise by 20% per year in the future, leading to a market of US$ 300-500 million by 1995 or 5–10% of global insecticide sales by the year 2000 (Anonymous, 1991–6). In addition to the expanding use of Bt as a microbial pesticide, the Bt genes responsible for its efficacy as a pesticide have become a primary source of insect toxins for those who seek to produce transgenic crops resistant to insects. It was reported by Watkinson (1992) that at least 50 plant species have been transformed with Bt genes and the list is being constantly added to. This brings closer the prospect of Bt toxins becoming widely and persistently distributed in the environment.

There is a growing criticism and concern about this genetic approach to pest control (Harris, 1991; van Emden, 1991; Anderson, 1992). Insects have exceeded most projections of their ability to develop resistance to pest control methods applied against them, and this now includes Bt.

Introduction

Root rot and damping-off pathogens often cause severe problems both in extensively grown field crops and in protected crops such as vegetables and ornamental plants. New control measures are being sought both for environmental reasons and since the possibilities for chemical control are limited. Among these, biological control (Sewell, 1965) seems promising: it is generally believed that the use of biological control will be beneficial and that risks and unwanted side effects are limited. In this chapter, the use of fungal antagonists as biocontrol agents (BCAs) will be discussed.

Most fungi used for biological control of damping-off and root rot are Hyphomycetes, and among these the genera Penicillium, Trichoderma and Gliocladium have received most attention (Kommedahl and Windels, 1981). Mycoparasitic Pythium spp. (Paulitz and Baker, 1987; Lewis et al, 1989; Hockenhull et at., 1992) and nonpathogenic Fusarium spp. (Alabouvette, 1990; Komada, 1990) and other species are also potential BCAs. Although the potential for using fungal antagonists for biological control is well documented (e.g. Papavizas, 1985), there are as yet only a few examples of their use on a commercial scale. However, BCAs such as non-pathogenic Fusarium oxysporum (Rajnchapel-Messai, 1990), Pythium oligandrum (Vesely, 1989), Gliocladium virens (Lumsden et al 1991; see Lumsden and Walter, Chapter 25) and Trichoderma harzianum (Harman and Tronsmo, 1992) are examples of agents that are expected to be on the market in the near future.

This review will be focused mainly on the use of Trichoderma spp. and Gliocadium spp. for the control of root rot and damping-off caused by soilborne pathogens. Possibilities for using biological control for seed-borne diseases will also be mentioned briefly.

Introduction

Today, about 1200 viruses are known to infect insects (Martignoni and Iwai, 1986). These do not form a taxonomic unit but belong to a range of different virus families including the Iridoviridae, Parvoviridae, Poxviridae, Reoviridae and Baculoviridae. Most of these families also have representatives that infect not only insects, but also vertebrates and even plants. There is one exception to this rule: viruses that belong to the family Baculoviridae have so far only been isolated from arthropod hosts. More than 60% of all insect viruses known today belong to this family. Some baculoviruses have been found in shrimps and mites, but most of them have been isolated from insects, in particular lepidopterans.

Baculoviruses are characterized by doublestranded circular DNA, which is included in rodshaped nucleocapsids (Federici, 1986). They are formed mainly in the nucleus of the host cells. In common with many insect viruses from other virus families, the virions of most baculoviruses are contained within proteinacious paracrystalline formations, the so called occlusion bodies, which are often polyhedral (hence the name polyhedrosis virus for one group of the baculoviruses). The thick layers of polyhedral protein provide protection against adverse physical and chemical factors within the environment, allow the viruses to survive outside the host cell, and enable them to kill their host rapidly, without jeopardizing their own existence (Jaques, 1977). It is obvious that protection of the virus particles by the occlusion bodies is a great advantage for the use of these viruses as biological insecticides. The natural infection process is by ingestion of food contaminated with virus.

Introduction

Species of the genus Sitona Germar (Col., Curculionidae) have been recorded on all continents and all develop at the expense of a number of Leguminosae. In their larval stages, they attack the root system and may be especially injurious to the nodules (Aeschlimann, 1986), whereas the longlived adults consume the stems and foliage of their host plants. The four palaearctic representatives which comprise the S. humeralis group of species all depend upon Medicago spp. as host plants (Aeschlimann, 1984). One of these, S. discoideus Gyllenhal, was accidentally introduced into the southern hemisphere, where it has become a pest of economic importance to both perennial cultivated lucerne and volunteer annual Medicago species used for pasture throughout southeastern Australia and subsequently in the south island of New Zealand.

As a consequence of the importance of S. discoideus, surveys were carried out from 1973 to 1985 over most of the Mediterranean basin (Aeschlimann, 1980) with the aim of identifying efficient natural enemies of the various stages of S. discoideus that would be suitable for deliberate introduction into Australia. These investigations demonstrated that the parasitoid Microctonus aethiopoides Loan (Hym., Euphorinae) was the most promising biological control agent for use against adult Sitona weevils. Based on these findings, several biotypes of this natural enemy were imported between 1975 and 1979 from various parts of the western Mediterranean region to Australia for mass-rearing in quarantine and subsequent field release against S. discoideus (Aeschlimann, 1983a). Initial establishment followed by spreading was recorded in Australia 2 years after the start of the release programme (Aeschlimann, 1983a).

The primary concept of this Series of books is to produce volumes covering the integration of plant and microbial biology in modern biotechnological science. Illustrations abound, for example the development of plant molecular biology has been heavily dependent on the use of microbial vectors, and the growth of plant cells in culture has largely drawn on microbial fermentation technology. In both of these cases the understanding of microbial processes is now benefiting from the enormous investments made in plant biotechnology. It is interesting to note that many educational institutions are also beginning to see things in this way and integrating departments previously separated by artificial boundaries.

Having set the scope of the Series, the next objective was to produce books on subjects which had not been covered in the existing literature and, it was hoped, to set some new trends.

Two of the first books of this Series addressed the opportunities of protein engineering (Peter Shewry and Steve Gutteridge) and transformation (Kan Wang, Alfredo Herrera-Estrella and Marc van Montagu), while another concerned the release of genetically engineered and other microorganisms (John Fry and Martin Day). One of the major targets of agricultural technology is the biological control of pests and diseases. Some of the debates on genetic engineering have clouded the issue that biological products could reduce the chemical load on the environment while providing more effective products that are less prone to resistance. On the other hand, introduction of any exotic, whether it is genetically engineered or not, into the environment should only be sanctioned when the risks are fully evaluated.

Introductions of organisms in general

Introductions of organisms into new environments can be intentional, accidental, or migratory and may encompass practically any kind of living material. Intentional introductions fall into two broad categories: crop plants and domestic animals, and agents for the biological control of pests or other beneficial purposes, such as microbes to degrade toxic compounds. Benefits from the introduction of crop plants and domestic animals are obvious, but good economic assessments of these introductions are rare. Rigorous evaluations have been done for some classical biological control programmes (see Cullen and Whitten, Chapter 26; Greathead, Chapter 5; and Pimentel, Chapter 2), and overall, a return to investment of 30:1 has been estimated. An example of outstanding economic success is the biological control of Rhodes grass scale in Texas, which cost only US$ 0.2 million, but from which annual economic benefit has been estimated at about US$ 200 million. Other benefits of introducing biocontrol agents include the avoidance of unwanted side-effects associated with chemical pesticides, important from environmental, occupational health and social points of view.

Introductions of living material are always associated with a risk of unwanted side-effects (see Pimentel, Chapter 2; and van Lenteren, Chapter 3). Thus, of all intentional introductions of species some 25–68% result in permanent establishment, and 0–2% of these organisms become pests. In contrast, only about 5% of unintentional introductions result in species establishment, but 7% of those become pests in their new environment. In total, 128 intentionally introduced crop and ornamental plants have become weeds in the USA (2.2% of all introductions of plants), including Johnson grass, Missisippi chick corn, goatsrue and crotalaria (crop plants); and multiflora rose, water hyacinth and lantana (ornamentals).

Introduction

Biological control of arthropod pests using arthropod natural enemies has been practised for centuries (Flint and van den Bosch, 1981), and although it has been widely appreciated that these natural enemies can have adverse effects on the environment, it has been largely assumed that they are either absolutely small or small relative to the benefits of biological control. For example, Samways (1988) suggested that there are no quantified cases where the introduction of an arthropod agent has been shown to have harmed a specific conservation programme or has been conclusively damaging to native fauna. This suggestion has proved difficult to test under natural conditions. For example, many natural enemies have been released to control forest Lepidoptera pests. Some of these enemies kill non-target, nonpest insects, and it has been suggested that such unintended mortality might destabilize these nonpest populations thus causing them to become sporadic pests. Recently, Pimentel et al. (1984) reviewed the evidence that biological control agents can cause adverse environmental effects. Their review clearly documented that biological control can entail environmental risk and that categorical dismissal of this concern is unwarranted. More recently, Howarth (1991) argued that the introduction of biological control agents into Hawaii and New Zealand is one of the major causes of extinctions of the native, insular, endemic arthropod faunae associated with these two islands. In most of those cases, vertebrate natural enemies were implicated, but Howarth (1991) developed a reasonable argument that arthropod natural enemies could also affect the native faunae.

Introduction

Although many mermithid, tylenchid, aphelenchid and rhabditid nematodes are known to be important antagonists of insects, very few nematode species have so far been used for biological control. The mermithid Romanomermis culicivorax was used in field trials to control malariatransmitting mosquitos (Petersen and Cupello, 1981). However, with the discovery of the larvicide Bacillus thuringiensis var. israelensis this nematode lost its significance. In Australia, the neotylenchid parasite Deladenus siricidicola is successfully released to control the introduced European sawfly Sirex noctilio (Bedding, 1984). Other species have never gone beyond the scientific research level, with the exception of rhabditid nematodes of the genus Steinemema and Heterorhabditis and their bacterial symbionts Xenorhabdus spp., which are widely used for biological control of insect larvae in cryptic environments.

Biology

The nematode's life cycle consists of a free-living and a propagative phase. The only stage occurring outside the host insect is the infective third stage dauer juvenile (Fig. 11.1), which is developmentally arrested and morphologically and physiologically adapted for long-term survival under detrimental environmental conditions in the soil. The dauer juveniles (DJs) do not take up nourishment and carry cells of their bacterial symbiont Xenorhabdus sp. in the intestinal lumen (Fig. 11.2) (Bird and Akhurst, 1983; Endo and Nickle, 1991). They actively seek out suitable host insects and penetrate the haemocoel where they find favourable conditions for propagation. The DJs start feeding, release the symbiotic bacteria into the haemolymph and enter into the propagative phase of the life cycle. Provided that the insect's humoral and cellular defence mechanisms do not succeed in the elimination of the nematodebacterium complex, the host will die within 2 days after infection.