Steven E. Naranjo

Bt Crop Effects on Functional Guilds of Non-Target Arthropods: A Meta-Analysis

Background Uncertainty persists over the environmental effects of genetically-engineered crops that produce the insecticidal Cry proteins of Bacillus thuringiensis (Bt). We performed meta-analyses on a modified public database to synthesize current knowledge about the effects of Bt cotton, maize and potato on the abundance and interactions of arthropod non-target functional guilds. Methodology/Principal Findings We compared the abundance of predators, parasitoids, omnivores, detritivores and herbivores under scenarios in which neither, only the non-Bt crops, or both Bt and non-Bt crops received insecticide treatments. Predators were less abundant in Bt cotton compared to unsprayed non-Bt controls. As expected, fewer specialist parasitoids of the target pest occurred in Bt maize fields compared to unsprayed non-Bt controls, but no significant reduction was detected for other parasitoids. Numbers of predators and herbivores were higher in Bt crops compared to sprayed non-Bt controls, and type of insecticide influenced the magnitude of the difference. Omnivores and detritivores were more abundant in insecticide-treated controls and for the latter guild this was associated with reductions of their predators in sprayed non-Bt maize. No differences in abundance were found when both Bt and non-Bt crops were sprayed. Predator-to-prey ratios were unchanged by either Bt crops or the use of insecticides; ratios were higher in Bt maize relative to the sprayed non-Bt control. Conclusions/Significance Overall, we find no uniform effects of Bt cotton, maize and potato on the functional guilds of non-target arthropods. Use of and type of insecticides influenced the magnitude and direction of effects; insecticde effects were much larger than those of Bt crops. These meta-analyses underscore the importance of using controls not only to isolate the effects of a Bt crop per se but also to reflect the replacement of existing agricultural practices. Results will provide researchers with information to design more robust experiments and will inform the decisions of diverse stakeholders regarding the safety of transgenic insecticidal crops.

Impacts of Bt crops on non-target invertebrates and insecticide use patterns

The ubiquitous nature of Bacillus thuringiensis (Bt), a Gram-positive bacterium capable of producing crystal proteins with insecticidal activity during sporulation, is now being mirrored in major crops plants that have been engineered through recombinant DNA to carry genes responsible for producing these crystal proteins and providing host plant resistance to major lepidopteran and coleopteran pests. In 2007, the 11th year of commercial production, Bt maize and Bt cotton were commercially produced on a total of 42 million hectares in 20 countries. Assessment of environmental safety has been and continues to be a key element of transgenic crop technology. This review focuses on two environmental elements, effects on non-target invertebrates and changes in insecticide use patterns since the adoption of Bt maize and cotton. Meta-analyses of the extant literature on invertebrate non-target effects reveals that the pattern and extent of impact varies in relation to taxonomy, ecological or anthropomorphic guild, route of exposure and the non-Bt control against which effects are gauged. Hazards identified in the laboratory may not always manifest in the field and the minor negative effects of Bt crops demonstrated in the field pale in comparison with alternative pest suppression measures based on insecticides. The efficacy of Bt maize and cotton against major pest species has been associated with an estimated 136.6million kg global reduction in insecticide active ingredient used between 1996 and 2006 (29.9% reduction). Benefits vary by country and region and are heavily weighted towards cotton production, which has historically been one of the largest users of insecticides in the world.

Long-Term Assessment of the Effects of Transgenic Bt Cotton on the Abundance of Nontarget Arthropod Natural Enemies

Abstract A 6-yr field study assessed the long-term impact of Bt cotton producing the Cry1Ac δ-endotoxin on 22 taxa of foliar-dwelling arthropod natural enemies in Arizona. No chronic, long-term effects of Bt cotton were observed over multiple generations of nontarget taxa. Zero-2 taxa declined significantly in unsprayed Bt compared with non-Bt cotton each year. In contrast, positive control studies showed that insecticide applications for caterpillars and other pests in both non-Bt and Bt cotton had much greater negative effects on 10 taxa. Multivariate principal response curves supported the findings of univariate analyses for the entire natural enemy community, showing no effect of Bt cotton but large and long-lasting negative effects from the use of insecticides. Multi-year analyses provided greater statistical power and indicated significant reductions that averaged 19% in five arthropod predator taxa in unsprayed Bt compared with non-Bt cotton. Most of these reductions were likely associated with reductions in lepidopteran prey. However, results of a companion study examining natural enemy function suggest that these minor reductions in Bt cotton have little ecological meaning. Multi-year analyses showed an average significant reduction of 48% in 13 taxa for plots receiving insecticide applications. On average, a 3-yr study with four replicates per year was sufficient to discern changes of ≈20%, with 80% power in unsprayed cotton. This long-term study indicates that the effects of Bt cotton on a representative nontarget community are minor, especially in comparison with the alternative use of broad-spectrum insecticides. Guidelines for improving nontarget field studies are discussed.

Conservation and evaluation of natural enemies in IPM systems for Bemisia tabaci

Abstract Conservation biological control emphasizes the preservation and enhancement of natural enemies and is the cornerstone of all approaches to biological control. This review critically examines recent and current research efforts in conservation biological control by predators and parasitoids of Bemisia tabaci worldwide. A large number of natural enemy species have been identified from many agricultural systems. Further research has demonstrated that these natural enemies may act along with other mortality agents to inflict high levels of mortality on populations of B. tabaci. Less effort has been placed on determining the factors constraining or potentially enhancing biological control. The widespread use of broad-spectrum insecticides in many crops has severely hampered the contribution of predators and parasitoids to pest suppression. However, the arsenal of selective insecticides has grown in the past decade and their increased usage may permit the true integration of biological control into IPM systems. The effects of species interactions (e.g., intraguild predation) and host-plant attributes on disruption of biological control are poorly understood in most systems. Research in the area of habitat manipulation and enhancement is minimal. Very little research has addressed the evaluation of natural enemy effects on B. tabaci population dynamics in any system. As a result our ability to predict and exploit these effects for pest suppression are limited. Problems in estimating and interpreting parasitism are highlighted. Recent life table studies of B. tabaci in Arizona cotton are summarized to demonstrate how integration of natural enemies with use of selective insecticides resulted in the development of an efficient pest management system. Avenues for future research are discussed that may enhance the use of conservation biological control as a key tactic in IPM of B. tabaci.

Mortality dynamics and population regulation in Bemisia tabaci

Natural mortality is an important determinant of the population dynamics of a species, and an understanding of mortality forces should aid in the development of better management strategies for insect pests. An in situ, observational method was used to construct cohort‐based life tables for Bemisia tabaci (Gennadius) Biotype B (Homoptera: Aleyrodidae) over 14 generations on cotton in central Arizona, USA, from 1997 to 1999. In descending order, median marginal rates of mortality were highest for predation, dislodgment, unknown causes, egg inviability, and parasitism. The highest mortality occurred during the 4th nymphal stadium, and the median rate of immature survival over 14 generations was 6.6%. Predation during the 4th nymphal stadium was the primary key factor. Irreplaceable mortality was highest for predation and dislodgment, with the absence of these mortality factors leading to the greatest increases in estimated net reproduction. There was little evidence of direct or delayed density‐dependence for any mortality factor. Wind, rainfall, and predator densities were associated with dislodgment, and rates of predation were related to densities of Geocoris spp., Orius tristicolor (White), Chrysoperla carnea s.l. Stephens, and Lygus hesperus Knight. Simulations suggest that immigration and emigration play important roles in site‐specific dynamics by explaining departures from observed population trajectories based solely on endogenous reproduction and mortality. By a direct measurement of these mortality factors and indirect evidence of adult movement, we conclude that efficient pest management may be best accomplished by fostering greater mortality during the 4th stadium, largely through a conservation of predators and by managing immigrating adult populations at their sources.

Long-Term Assessment of the Effects of Transgenic Bt Cotton on the Function of the Natural Enemy Community

Abstract Field studies to assess effects of transgenic crops on nontarget organisms primarily have focused on nontarget abundance and diversity, whereas few have examined effects on nontarget community function. A 5-yr field study in Arizona assessed whether transgenic cotton producing the Cry1Ac toxin of Bacillus thuringiensis (Bt) had an effect on the natural enemy community’s impact on three key pests. Predator:prey ratios for Bemisia tabaci (Gennadius) and Lygus hesperus Knight were similar in unsprayed Bt and non-Bt cotton. Insecticide applications in positive control plots inconsistently altered ratios for B. tabaci. Predation indices based on the known feeding activity of selected predators showed that potential predator impact was unaltered by Bt cotton but was consistently depressed with insecticide applications. Sentinel eggs and pupae of Pectinophora gossypiella (Saunders) experienced the same rates of predation in both unsprayed Bt and non-Bt cotton. Cohort-based life tables for B. tabaci showed that rates of sucking predation, parasitism, and dislodgement (chewing predation in part) were unchanged by Bt cotton. Underlying experimental designs were sufficient to consistently detect changes of <20% in predator:prey ratios and predation indices and changes of <10% in rates of P. gossypiella and B. tabaci mortality with >80% power (α = 0.05). These long-term studies showed essentially no effects of Bt cotton on natural enemy function in Arizona cotton and further showed that minor reductions in density of several predator taxa in Bt cotton observed in a companion study may have little ecological meaning relative to natural enemy impact on key pests in the system.

Fifty years of the integrated control concept: moving the model and implementation forward in Arizona.

Fifty years ago, Stern, Smith, van den Bosch and Hagen outlined a simple but sophisticated idea of pest control predicated on the complementary action of chemical and biological control. This integrated control concept has since been a driving force and conceptual foundation for all integrated pest management (IPM) programs. The four basic elements include thresholds for determining the need for control, sampling to determine critical densities, understanding and conserving the biological control capacity in the system and the use of selective insecticides or selective application methods, when needed, to augment biological control. Here we detail the development, evolution, validation and implementation of an integrated control (IC) program for whitefly, Bemisia tabaci (Genn.), in the Arizona cotton system that provides a rare example of the vision of Stern and his colleagues. Economic thresholds derived from research-based economic injury levels were developed and integrated with rapid and accurate sampling plans into validated decision tools widely adopted by consultants and growers. Extensive research that measured the interplay among pest population dynamics, biological control by indigenous natural enemies and selective insecticides using community ordination methods, predator:prey ratios, predator exclusion and demography validated the critical complementary roles played by chemical and biological control. The term ‘bioresidual’ was coined to describe the extended environmental resistance from biological control and other forces possible when selective insecticides are deployed. The tangible benefits have been a 70% reduction in foliar insecticides, a >

Economic Value of Biological Control in Integrated Pest Management of Managed Plant Systems

200 million saving in control costs and yield, along with enhanced utilization of ecosystem services over the last 14 years. Published in 2009 by John Wiley & Sons, Ltd.

Integrated management approaches for pink bollworm in the southwestern United States

Biological control is an underlying pillar of integrated pest management, yet little focus has been placed on assigning economic value to this key ecosystem service. Setting biological control on a firm economic foundation would help to broaden its utility and adoption for sustainable crop protection. Here we discuss approaches and methods available for valuation of biological control of arthropod pests by arthropod natural enemies and summarize economic evaluations in classical, augmentative, and conservation biological control. Emphasis is placed on valuation of conservation biological control, which has received little attention. We identify some of the challenges of and opportunities for applying economics to biological control to advance integrated pest management. Interaction among diverse scientists and stakeholders will be required to measure the direct and indirect costs and benefits of biological control that will allow farmers and others to internalize the benefits that incentivize and accelerate adoption for private and public good.

Setting the record straight: a rebuttal to an erroneous analysis on transgenic insecticidal crops and natural enemies

The pink bollworm (PBW), Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), is the key pest in cotton (Gossypium spp.) production areas in the southwestern United States and in many other cotton-producing areas of the world. The high costs of chemical control, continuing economic losses, secondary pest problems and environmental considerations suggest the need for ecologically oriented PBW management strategies. Extensive research has resulted in a broad array of monitoring, biological control, cultural, behavioural, genetic and host plant resistance methods that can serve as a base for the formulation of integrated PBW management systems. The life history characteristics of the PBW, in particular the high mobility of adults, indicate the need for combinations of selected integrated pest management (IPM) components implemented over large geographical areas. The areas involved present a wide range of PBW population densities, differences in cotton production methods and social and environmental considerations. The best option is tailor-made systems for targeted management areas with the selection of IPM components based on the PBW population density, crop production methods and economic feasibility. The unlikelihood of eradication indicates the need for long-term monitoring and programme maintenance following successful area-wide management. The success of area-wide PBW management is highly dependent on participation in the planning, site selection, implementation and assessment phases of the programme by all segments of the agricultural community. A highly effective extension--education communication programme is an essential component. Local uncoordinated efforts have not reduced the economic status of this pest in any area where it is an established pest. The potential long-term benefits of PBW population suppression on an area-wide basis appear to justify area-wide efforts in terms of reduced costs, more effective control, less environmental contamination and other peripheral problems associated with conventional control approaches.