Introduction
Bioengineered transgenic insecticidal crops are among the most significant tech- nological developments in insect pest management since the advent of synthetic insecticides (Persley, 1996; Cannon, 2000; Perlak et al., 2001). Transgenic cotton and maize that produce insecticidal toxins derived from genes transferred from the bacterium Bacillus thuringiensis kurstaki(Btk), for protection against lepidopter- an pests, have been planted widely in selected countries (Cannon, 2000; Fitt, 2000; Pray et al., 2002; Shelton et al., 2002). The planting of transgenic Bt maize is one of the most commonly used methods for suppression of the European corn borer,Ostrinia nubilalis, in maize-growing regions of the USA. Since 1996, the area of Bt cotton planted in the USA has increased nearly 2.5 times, to approx- imately 1.8 million ha (Perlak et al., 2001; Shelton et al., 2002). Transgenic Bacillus thuringiensis tenebrionis(Btt) potatoes created to resist the Colorado potato beetle, Leptinotarsa decemlineata, were grown on relatively small areas in the USA until 2001, when transgenic Bt potatoes were no longer sold (Shelton et al., 2002).
Additional transgenic insecticidal crops have been bioengineered for insect resist- ance using digestive inhibitors, e.g. snowdrop lectin (Galanthus nivalisagglutinin, GNA) and several protease inhibitors (Gatehouse et al.,1996; Michaud, 2000).
The widespread planting of transgenic crops with tissues containing high levels of insecticidal toxins has raised concerns about gene flow, selection for tol- erant pest populations and ecological disruptions of food webs (Rissler and Mellon, 1996; Snow and Palma, 1997; Gould, 1998; Beringer, 2000; Cannon, 2000; Hails, 2000; Poppy, 2000; Watkinson et al., 2000; Wolfenbarger and Phifer,
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Interactions Between Natural
2000; Marvier, 2001; Obrycki et al., 2001; Schmidt and Hilbeck, 2001;
d’Oultremont and Gutierrez, 2002; Letourneau and Burrows, 2002; Manachini and Lozzia, 2002). The role of transgenic crops within the concept of integrated pest management has been discussed extensively (Persley, 1996; Waage, 1997;
Hoy et al., 1998; Way and van Emden, 2000; Hilbeck, 2001; Obrycki et al., 2001).
For example, Hoy et al. (1998) proposed that the conservation of natural enemies be considered in the design of transgenic crops because of their potential role in reducing rates of evolution of tolerant pest populations. Way and van Emden (2000) presented a thorough discussion of the potential to select for pest popula- tions that will overcome Bt transgenic toxins and the likely role of biotic mortal- ity factors in this process (Gould et al., 1991). They also emphasized the importance of using appropriate comparisons when evaluating the relative envi- ronmental risks and benefits of transgenic crops (Way and van Emden, 2000).
Hilbeck (2001) argued that the current use of transgenic insecticidal crops in a high toxin expression strategy is not compatible with the ecological principles of integrated pest management.
The potential benefits of transgenic insecticidal crops for natural enemies have been presented by several authors (Gould, 1998; Hoy et al., 1998; Way and van Emden, 2000) and include: (i) reduction in insecticide use, thus limiting a major source of natural enemy mortality; (ii) increased prey/host availability for generalist natural enemies via increased densities of secondary insect pest species that may have been previously suppressed due to the use of insecticides for the primary target pest species; and (iii) altered behaviours, physiology or retarded development of insect herbivores that may increase their vulnerability to natural enemies. Balanced against these potential benefits are possible negative aspects of this transgenic technology on natural enemies, paralleling those common to the use of many insecticides: (i) significant reductions of populations of the target pest in transgenic fields; (ii) direct effects of transgenic-plant-produced toxins on natural enemies; and (iii) negative effects that are mediated through insect herbi- vore hosts, e.g. premature mortality, altered host suitability for growth and devel- opment of natural enemies, and altered host–parasitoid behavioural interactions.
The effects of transgenic insecticidal toxins on selected natural enemies have been considered (Schuler et al., 1999a; Cannon, 2000; Groot and Dicke, 2002).
Obrycki et al. (2001) specifically discussed the interactions between transgenic Btk maize and natural enemies. Schuler et al. (1999a) discussed the effects of trans- genic insecticidal toxins on the behaviour, life history and ecology of natural enemies, including consideration of population dynamics of natural enemies and hosts within transgenic cropping systems. In a review of the influence of plant resistance on tri-trophic-level interactions, Hare (2002) presents ten examples of transgenic Bt crop–natural enemy interactions (eight involved predatory species and two focused on parasitoids). Seven of the ten studies showed positive inter- actions (additive or synergistic effects), one study showed no effect, and two neg- ative interactions involved the predator, Chrysoperla carnea. By comparison, Hare (2002) also summarized 33 studies that evaluated the interactions between para- sitoids and selectively bred resistant crop varieties: 27% were antagonistic, 53%
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were additive, 10% were synergistic and 10% were disruptive. Seventeen inter- actions of predators with resistant crops were listed: 59% were additive, 23%
were synergistic and 18% were antagonistic (Hare, 2002). In this review, similar percentages of positive interactions of predators and parasitoids were noted with bioengineered resistance factors and with traits derived from selective breeding techniques.
In this chapter, we emphasize recent laboratory and field studies of the inter- actions of natural enemies with transgenic insecticidal plants, focusing on their influence on biological control. After a decade examining the interactions between natural enemies and transgenic insecticidal toxins, are there emerging patterns that can be used as the basis for future investigations? As background to the interactions between transgenic crops and natural enemies, we briefly discuss the bases of studies that have documented negative interactions between micro- bial insecticide Bt formulations and natural enemies.
Bacillus thuringiensis Versus Predators and Parasitoids
Relatively few effects of Bt sprays on natural enemies have been documented, due to the selective nature of Bt toxins, modes of exposure and short exposure times (Glare and O’Callaghan, 2000). However, negative effects of microbial insecticide formulations of Bt on selected natural enemy species have been reported (Salama et al., 1982; Flexner et al., 1986; Croft, 1990; Laird et al., 1990;
Blumberg et al., 1997). For example, when Bt causes premature death of a host, parasitoid species developing within these hosts also die (Blumberg et al., 1997).
Adverse effects of Bt infections on 13 parasitoid species (eight Braconidae and five Ichneumonidae), due to premature host death, were summarized by Brooks (1993). However, studies of the interactions between natural enemies and micro- bial sprays of Bt are not necessarily reflective of the possible Bt exposure and Bt expressions in transgenic crops, due to differences in the length of exposure, con- centration and form of Bt toxins experienced by hosts and natural enemies.
Emergence of two parasitoid species,Cotesia marginiventrisand Microplitis croceipes, from larval Heliothis virescenshosts, continuously fed Bt toxins, was inversely related to B. thuringiensis concentration in H.virescens diets (Atwood et al., 1997, 1999).
This type of study is analogous to the potential exposure of larval parasitoids developing in or on hosts on transgenic crops that continuously produce relative- ly high concentrations of Bt toxins.
Similarly, few studies of the interactions of Bt sprays and predatory species have documented effects on predators, due to the selective activity of Bt toxins and the relatively short exposure times (Salama et al., 1982; Flexner et al., 1986;
Croft, 1990). High concentrations of a microbial insecticide formulation of B.
thuringiensis tenebrionis (Btt) for L. decemlineata reduced predation rates by adult Coleomegilla maculata, and prolonged larval development when applied to pollen fed to C.maculatalarvae (Giroux et al., 1994). These effects were observed when Bt concentrations were much higher than the recommended field application
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