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4.61 Biological Control and Biotechnological Amelioration in Managed Ecosystems Peter Kevan, University of Guelph, Guelph, Canada Les Shipp, Greenhouse and Processing Crops Research Centre, Harrow, ON, Canada © 2011 Elsevier B.V. All rights reserved.

4.61.1 4.61.2 4.61.3 4.61.4 4.61.5 4.61.6 4.61.7 4.61.8 4.61.9 4.61.10 References

Introduction Biocontrol of Weeds Biocontrol of Plant Pathogens Biocontrol of Plant Pathogens and Insect Pests by Pollinator Vectors Biocontrol of Insect, Mite, and Nematode Pests Biocontrol of Vertebrate Pests Biocontrol in Veterinary and Medical Applications Production, Deployment, and Establishment of Biocontrol Agents Genetic Engineering and Biological Control Ecological Considerations

Glossary affinity to substrate The ability of microbial cells to use active membrane transport to consume nutrients out of diluted solutions. In a simplest case of applicability of the Monod’s model, the affinity is measured by saturation constant, Ks ; the lower the Ks, the higher the affinity. autoselection A selection mechanism operating within a single microbial population (‘not’ in the mixed culture) and observed mainly in a long-term continuous culture, for example, as a displacement of original population by mutant spontaneously acquiring higher affinity to a growth-limiting substrate. balanced growth A proportional increase in the amounts of all cell components; in other words, in microorganisms, balanced growth produces cells of the same quality without any variation in composition. conserved (anabolic) nutrient substrates Ingredients of nutrient media, which are sources of biogenic elements forming cellular material, for example, sources of N, P, K, and Fe and other elements. Contrary to ‘catabolic substrates’ (energy sources), their consumption is not accompanied by dissipation of chemical species into nonreusable wastes (H2 O, CO2, and heat), instead, the consumed element is incorporated into de novosynthesized cell components, being conserved. kinetics Derived from the Greek word κινετικοσ, meaning ‘forcing to move’. In scientific disciplines, it is a study of

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development of any processes in time – physical, chemical, or biological – which uses a combination of experiments with mathematical modeling to achieve a better understanding of the underlying mechanisms. maintenance A concept postulating that any viable cell should divert certain amount of available energy on metabolic functions other than growth. The commonly recognized specific maintenance functions are turnover of cell material, osmotic work to maintain concentration gradients between the cell and its exterior, and cell motility. secondary metabolites Products of cellular syntheses that are not directly involved in the normal growth, development, or reproduction of organisms. They may play an important role in adaptation of microorganisms to unfavorable conditions. stoichiometry Derived from the Greek word στωικη"ιον, meaning element. It is the quantitative relationship between reactants and products in a chemical or biological reaction and application of the mass-balance conservation conditions to studied process. structured kinetic models Describe growth-associated changes in the composition of microbial cells, such as amount of reserved compounds, ribosomal particles, and mitochondria, and content/activity of particular enzymes or enzymatic complexes.

4.61.1 Introduction Pest management is important to agriculture and forestry. Chemical control measures against pests became standard after the invention and proof of efficacy of chemical pesticides. However, other approaches have proven valuable. Biological control is simply the use of biological agents in pest management for the production of food and fiber for human consumption. Many ecologists argue that biological control is, and always has been, nature’s way of regulating populations. The idea that organisms can be pests is an anthropocentric construct whereby the pest is an organism that detracts from the production of resources that human

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beings want. Pests come in various guises. Predators are pest of livestock, herbivores are pests of crops, parasites and pathogens are pests of livestock or crops, and competitors may become so numerous as to detract from plant or animal production. Biological control agents are simply living organisms (or parts of living organisms) that interfere with the productivity of other living organisms. In terms of biotechnology, biological control agents are used by human beings for the protection of the resources that they want. Just as pests run the gamut from vertebrates to virus, so do biocontrol agents.

4.61.2 Biocontrol of Weeds For weed control, insects, fungi, bacteria, and virus agents have been developed. The most famous example of biological control of weeds is the use of a cactus moth, Cactoblastis cactorum, for control of prickly pear cactus in Australia (DeFelice 2004) [18]. This plant was introduced into Australia for the production of red dye that was produced by the cochineal insects that fed on the cactus. Also, the cactus made excellent hedgerows around fields and homes and was favored by gardeners, soon spreading throughout the country destroying millions of hectares of agricultural land. All attempts to control the ‘weed’ using chemicals or mechanical means failed. However, this situation changed dramatically with the introduction of a tiny moth that fed only on the prickly pear cactus, and the cactus was quickly destroyed. In six years, millions of hectares were restored for pasture use for sheep and cattle and for grain production. This is a good example of how an introduced plant species can become a pest and is also one of our best examples of using an insect to control a weed pest. The cactus moth is being used in other parts of the world where prickly pear cactus is a pest. A more recent example of weed biocontrol is the control of purple loosestrife, which is commonly found in wetlands throughout North America and which causes changes in the resident plant community and wetland ecosystem. Five insect biocontrol agents (two species of leaf beetles, one root-feeding weevil, and two flower-feeding weevils) were introduced [1]. In this case, several biocontrol agents were required to provide effective management of the pest by attacking different life stages (leaves, roots, and seed production) of the plant. In Canada, we have three bioherbicides (fungi) registered for weed control. Colletotrichum gloeosporioides f. sp. malvae and Sclerotinia minor are used for broadleaf control, such as dandelions. We also have a novel fungal biocontrol agent (Chondrostereum purpureum) for management of deciduous ‘weeds’ in reforestation sites and other areas where bush control is required [2].

4.61.3 Biocontrol of Plant Pathogens For control of plant pathogens in agriculture and forestry (fungal, bacterial, or viral), other microbes have been developed. Trichoderma fungal species have been known for a long period to be able to suppress soil pathogens such as Fusarium spp., Pythium ultimum, and Rhizoctonia solani, which can cause damping-off disease of many conifers and horticultural plants at the early growth stages. Once such species, Trichoderma virens (GL-21), has been shown to be quite successful in the United States for controlling damping-off disease of vegetable transplants and in the greenhouse industry [3]. Trichoderma stromaticum, which was isolated from witches’ broom disease on cacao in the Amazon basin, is now being marketing for control of the disease on commercial cacao cultivation [4]. In Canada, the mycoparasite, Microsphaeropsis ochracea, is being promoted as an effective biocontrol agent for apple scab. The mycoparasite has 80–90% efficacy against the apple scab fungus, Venturia inaequalis, and is as cost-effective as fungicides [5].

4.61.4 Biocontrol of Plant Pathogens and Insect Pests by Pollinator Vectors Part of the problems of using some microbial/fungal biocontrol agents has been due to the delivery system. Technology has been developed for the delivery of biocontrol agents by pollinators of Clonostachys rosea, Trichoderma harzianum, Pseudomonas fluorescens, Bacillus subtilis, and possibly Metschnikowia fruticola against several plant pathogens, such as gray mold, fire blight, and mummy berry, that afflict a number of fruit crop plants. Moreover, the formulation of the biocontrol agent aimed at the plant pathogen has been adapted to include bio-insecticidal agents, such as Beauveria bassiana and Bacillus thuringiensis (Bt, see below). This resulted in simultaneous suppression of plant pathogens and several serious insect pests, such as tarnished plant bugs, peach aphids, thrips, and whitefly, while augmenting pollination and crop yields (review in [6]).

4.61.5 Biocontrol of Insect, Mite, and Nematode Pests To control the hosts of insect, mite, and nematode pests afflicting crop and tree production, an even wider array of biocontrol agents has been deployed. Classical biological control is the most common form of biological control where exotic natural enemies are introduced to control exotic pests. Classical biological control is used on 300 million hectares of land (8% of the agricultural land) [7]. Approximately 2000 species of exotic arthropod agents have been introduced for arthropod pests in 196 countries or islands during the past 120 years. Commercially, over 170 species are available for pest control. One of the first large-scale success stories for biological control of insect pests was the introduction of Rodolia ladybird beetle against cottony cushion scale on commercial citrus in southern California. Rodolia has now been controlling cotton cushion scale for over 100 years in more than 50 countries.

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Successful use of biological control has not been limited to citrus crops. Biological control of phytophagous mites of apples is becoming a common practice. Initially, the predatory mite, Neoseiulus fallacies, was released inundatively to control mite pests, but this proved to be impractical on a large scale. The biocontrol strategy then changed to a philosophy of conservation, augmentation, and transfer of natural predators from an orchard where biological control was established to new orchards [8]. A recent survey in Quebec indicated that more tha n 80% of the orchards have adopted this approach. Predatory mites are not the only biocontrol agent used against orchard pests. Insect-specific viruses, such as baculoviruses, have been isolated, evaluated, and mass-produced for use against codling moth in apple orchards. Two products (Madex® and VirosoftCP4 ®) have been registered in Europe and Canada [9]. Organic producers of apples are particularly interested in these types of control products due to a shortage of available control options. The best resu lts for management of codling moth occur when virus applications are combined with mating disruption. Parasitic wasps (Hymenoptera: Encyrtidae) are also used as biocontrol agents in orchards. Ageniaspis fuscicollis, a European parasitoid, was introduced for control of apple ermine moth in British Columbia in the mid-1980s and again in the mid-1990s. Mean parasitism levels by A. fuscicollis have reached as high as 23% on Vancouver Island, and apple ermine moth populations have decreased where the parasitoid was released [10]. Another parasitoid that is commonly used and commercially mass-produced is the egg parasitoid, Trichogramma spp. Several species of Trichogramma are released against a range of moth pests on important crops such as cotton, sugarcane, and maize and in processing tomatoes [11]. In most cases, Trichogramma will not provide sole control of the pest, but when combined with other biocontrol agents or mating disruption, effective pest control is achieved. Trichogramma minutum was even evaluated for control of spruce budworm in Canadian publicly owned forest land. Smith et al. [12] showed that T. minutum parasitized 70% of the larval spruce budworm and reduced defoliation by 50%. However, release rates were too high to be cost-effective with other biocontrol agents such as B. thuringiensis. With microbial biopesticides, B. thuringiensis is the most successful and commonly used agent. B. thuringiensis kills its host by producing toxins that attack and rupture the insect midgut, followed by invasion of the hemocoel with bacterial cells. Different strains of B. thuringiensis have been developed that attack the larvae of lepidopteran, dipteran, and coleopteran pests [11]. In greenhouse vegetable crops, all the types of biocontrol agents mentioned above (parasitoids, predators, and entomopathogens) are used in an integrated approach to control the range of pests that can occur on these crops. Because it is a monoculture crop grown in essentially an enclosed environment and climate, and fertigation (water and fertilizer) are computer controlled, biological control of pests and plant diseases is the main management strategy. More than 90% of the tomato, pepper, and cucumber acreages use biological control. Almost 90 natural enemies are commercially reared for greenhouse biocontrol and of which ∼25 are mass-produced in large numbers for greenhouse crops [13]. In Canada, there are ∼23 arthropod pests of greenhouse vegetable crops. A new pest or disease occurs almost every year. Bumble bees are the industry norm for pollination of greenhouse tomatoes, which is the largest crop grown. The switching to bees for pollination in the 1990s was a major reason for the significant increase and adoption of biological control in tomatoes that year, as bees are very sensitive to pesticides. Today, bees are also used to pollinate sweet pepper and eggplant. As a result of the success with biocontrol in greenhouse vegetable crops, greenhouse ornamental growers are switching and have become more successful in implementing similar strategies for their crops. Ontario ornamental growers lead Canada with 40–50% adoption of biocontrol in greenhouse ornamental crops and are viewed as model systems in North America for their innovative and successful adoption of biological control (Graeme Murphy (OMAFRA), personal communication).

4.61.6 Biocontrol of Vertebrate Pests Biological control technology has been directed also against vertebrate pests (rabbits, rats, etc.) and veterinary and medical pests (nuisances, parasites, and diseases). The most successful cases of biological control of vertebrate pests have occurred in island situations. One of the higher profile examples is the use of pathogens for control of rabbits in Australia. In 1950, the myxoma virus (Leporipoxvirus, Poxviridae), which causes myxomatosis, was introduced into Australia and soon spread rapidly throughout, reducing the rabbit population by 75–95% [11]. In Australia, mosquitoes were the main carriers for spreading the virus among rabbits. Eventually, the rabbits developed immunity to the virus with virulence declining to 50%. In 1995, a new virus, rabbit hemorrhagic disease (RHD), was established on the mainland of Australia [11]. Again, rabbit mortality ranged from 50% to 90%, with the greatest in the dry regions. Vectors this time include flies, mosquitoes, and rabbit fleas. In the temperate areas, rabbit populations returned again to pre-RHD levels. Thus, the use of viral pathogens resulted in dramatic decline initially, but vertebrate pests eventually developed varying degrees of genetic resistance. The latest tactic for control of vertebrate pests is application of the concept of immunoconception. The hypothesis here is that proteins associated with male and female gametes are potentially foreign antigens if introduced into the animal’s body outside the reproductive tract [11]. Subcutaneous or intramuscular inoculation of sperm into females causes an immune response inducing permanent or temporary infertility [14]. Immunocontraception by using baits or injections has been used for population control of free-ranging horses and elephants. In New Zealand, it has been speculated that sterilizing antigens in transgenic carrots could provide possum control if 50% of the population were sterilized [15]. However, the main stumbling block to this approach is cost. It is usually much less expensive to poison or shoot the pests.

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4.61.7 Biocontrol in Veterinary and Medical Applications With veterinary pests, the classical example of biological control is the use of sterile insect techniques (SITs) for control of screwworm fly on cattle. For this approach to be successful, the adult female fly must mate only once. Thus, mating with a sterilized male would result in infertile progeny. The sterilized males must be as competitive as the feral males. There are many factors that will influence the outcome of this technique, but this novel control strategy was a savior to the cattle industry in the southern United States. This approach has also been used against tropical fruit flies (Diptera: Tephritidae). In the United States, SIT has been used against infestations of Mediterranean fruit flies (medfly) in southern California and has reduced medfly infestations by 97% in the Los Angeles area [16]. B. thuringiensis ssp. israelensis (Bti) and Bacillus sphaericus are the most commonly used biocontrol agent for medical pests, such as mosquitoes and black flies [17]. These pests are carriers of important human diseases, such as malaria, dengue, yellow fever, encephalitis, filariasis, and onchocerciasis or just a public nuisance. Many mosquito and black fly control programs are based on chemical pesticides. However, pesticides often have a negative impact on the natural ecosystems and on humans. Bacillus biocontrol agents are safe for vertebrates and for the majority of the nontarget invertebrates. Both Bti and B. sphaericus can be used in integrated management programs with other biocontrol agents such as fungal agents and nematodes.

4.61.8 Production, Deployment, and Establishment of Biocontrol Agents Deployment of biocontrol agents has been variously successful. This deployment usually first requires that sufficient agent be produced to be introduced into the environment of the pest and to be effective in control. The biotechnological production facilities range from large-scale insectaries, growth chambers, and fermenters in which conditions are maintained to maximize production of virulent agents. The agents once produced and, nowadays, after having been subjected to screening for host specificity, efficacy, and environmental concerns are released. Establishment of the agent with the population of the pest is the most desired effect by which the population of the pest is held in check by the agent, and the population of the agent is continually limited by the availability of its host(s), the pest. An example of this situation is the release and establishment of the parasitoid, Encarsia formosa, for control of greenhouse whitefly on greenhouse tomatoes. In many instances, the populations of the pest and agent do not become co-established. If the pest is driven to extinction, for example, two-spotted spider mites, so much the better. Usually, the population of the age...