David J. Biddinger

Toxic and Behavioral Effects to Carabidae of Seed Treatments Used on Cry3Bb1- and Cry1Ab/c-Protected Corn

Abstract Most transgenic corn seed is now treated with systemic neonicotinoid insecticides. To address potential direct nontarget effects of these combined technologies, 16 Carabidae species from 10 genera (Agonum, Amara, Anisodactylus, Bembidion, Chlaenius, Harpalus, Patrobus, Poecilus, Pterostichus, and Scarites) field-collected from corn were directly exposed to Bacillus thuringiensis (Bt) Cry toxin-laden pollens and seed treatments in feeding and defined-dose bioassays. All adults readily fed on field or sweet corn pollens that expressed coleopteran-specific Cry3Bb1 or lepidopteran-targeting Cry1Ab/c, and no significant toxicity was observed. Adult survivorship ranged from 47 d for the predator Pterostichus melanarius (Illiger) to a year for the more omnivorous Scarites quadriceps Chaudoir, feeding solely on pollen containing 30–90 μg Cry3Bb1/g and water. In contrast, commercial doses of neonicotinoid seed treatments (imidacloprid, thiamethoxam, or clothianidin) elicited nearly complete mortality for 18 carabid species in 4-d bioassays containing corn seedlings. Carabid consumption of fungicide-only (fludioxonil plus mefenoxam) seed treatments was generally observed within 1 d, compared with a 2-d latency on neonicotinoid treatments, suggesting an antifeedant effect of the insecticide. In microcosm bioassays containing a corn seedling and five prey, clothianidin seed treatments killed adult western corn rootworm, Diabrotica virgifera virgifera LeConte and S. quadriceps, although the smaller Harpalus pensylvanicus (DeGeer) was more tolerant. We conclude that the neonicotinoid/fungicide seed treatments, and not Cry3Bb1 or CryIAb/c, are a major direct mortality factor for ground beetles. Field studies are needed to determine population and community level effects on Carabidae when these transgenic and seed-treatment technologies are combined.

Comparative Toxicities and Synergism of Apple Orchard Pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski)

The topical toxicities of five commercial grade pesticides commonly sprayed in apple orchards were estimated on adult worker honey bees, Apis mellifera (L.) (Hymenoptera: Apidae) and Japanese orchard bees, Osmia cornifrons (Radoszkowski) (Hymenoptera: Megachilidae). The pesticides were acetamiprid (Assail 30SG), λ-cyhalothrin (Warrior II), dimethoate (Dimethoate 4EC), phosmet (Imidan 70W), and imidacloprid (Provado 1.6F). At least 5 doses of each chemical, diluted in distilled water, were applied to freshly-eclosed adult bees. Mortality was assessed after 48 hr. Dose-mortality regressions were analyzed by probit analysis to test the hypotheses of parallelism and equality by likelihood ratio tests. For A. mellifera, the decreasing order of toxicity at LD50 was imidacloprid, λ-cyhalothrin, dimethoate, phosmet, and acetamiprid. For O. cornifrons, the decreasing order of toxicity at LD50 was dimethoate, λ-cyhalothrin, imidacloprid, acetamiprid, and phosmet. Interaction of imidacloprid or acetamiprid with the fungicide fenbuconazole (Indar 2F) was also tested in a 1∶1 proportion for each species. Estimates of response parameters for each mixture component applied to each species were compared with dose-response data for each mixture in statistical tests of the hypothesis of independent joint action. For each mixture, the interaction of fenbuconazole (a material non-toxic to both species) was significant and positive along the entire line for the pesticide. Our results clearly show that responses of A. mellifera cannot be extrapolated to responses of O.cornifrons, and that synergism of neonicotinoid insecticides and fungicides occurs using formulated product in mixtures as they are commonly applied in apple orchards.

Fecundity and fertility reductions in adult leafrollers exposed to surfaces treated with the ecdysteroid agonists tebufenozide and methoxyfenozide.

The effects on the fecundity and fertility of redbanded leafroller, Argyrotaenia velutinana (Walker), and obliquebanded leafroller,Choristoneura rosaceana (Harris), exposed as adults to surfaces treated with the ecdysone agonists tebufenozide (RH‐5992) and methoxyfenozide (RH‐2485) were examined. The first part of the study consisted of recently emerged moths being exposed to treated surfaces continuously throughout their lives (including mating and oviposition). Continuous exposure to tebufenozide‐ or methoxyfenozide‐treated surfaces significantly reduced the mean number of eggs laid and the percent of eggs that hatched in both species. The second part of the study involved exposure of recently emerged virgin moths (by sex) to treated surfaces for 24 h, after which, the exposed moths were paired with a nontreated partner to mate and oviposit on nontreated surfaces. In this experiment, for A. velutinana, significant reductions in fecundity occurred only when the female was exposed to methoxyfenozide‐treated surfaces. Significant reductions in A. velutinana egg fertility occurred with both male and female exposure in the methoxyfenozide treatments and only female exposure in the tebufenozide treatments. For C. rosaceana, significant reductions in fecundity occurred with both male and female exposure in the tebufenozide and methoxyfenozide treatments. Significant reductions in C. rosaceana egg fertility occurred with both male and female exposure in the tebufenozide treatments and only with female exposure in the methoxyfenozide treatments.

Transgenes Sustain Epigeal Insect Biodiversity in Diversified Vegetable Farm Systems

Abstract Many ecological studies have focused on the effects of transgenes in field crops, but few have considered multiple transgenes in diversified vegetable systems. We compared the epigeal, or soil surface-dwelling, communities of Coleoptera and Formicidae between transgenic and isoline vegetable systems consisting of sweet corn, potato, and acorn squash, with transgenic cultivars expressing Cry1(A)b, Cry3, or viral coat proteins. Vegetables were grown in replicated split plots over 2 yr with integrated pest management (IPM) standards defining insecticide use patterns. More than 77.6% of 11,925 insects from 1,512 pitfall traps were identified to species, and activity density was used to compare dominance distribution, species richness, and community composition. Measures of epigeal biodiversity were always equal in transgenic vegetables, which required fewer insecticide applications than their near isolines. There were no differences in species richness between transgenic and isoline treatments at the farm system and individual crop level. Dominance distributions were also similar between transgenic and isoline farming systems. Crop type, and not genotype, had a significant influence on Carabidae and Staphylinidae community composition in the first year, but there were no treatment effects in the second year, possibly because of homogenizing effects of crop rotations. Communities were more influenced by crop type, and possibly crop rotation, than by genotype. The heterogeneity of crops and rotations in diversified vegetable farms seems to aid in preserving epigeal biodiversity, which may be supplemented by reductions in insecticide use associated with transgenic cultivars.

Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe

Since the establishment of the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in North America and Europe, there has been a large, multi-group effort to characterize the composition and impact of the indigenous community of arthropod natural enemies attacking this invasive pest. In this review, we combine 98 indigenous natural enemy datasets spanning a variety of sampling methods, habitats, and geographic areas. To date, the vast majority of H. halys biological control research has focused on the egg stage, using sentinel egg masses to characterize indigenous parasitoid and predator communities and their contribution to H. halys egg mortality. Although egg parasitism and predation levels by indigenous natural enemies are low (typically <10% each) in most surveys, total egg mortality attributable to natural enemies can be higher (typically between 5 and 25%; up to 83%)—even though these values were likely underestimated in most cases because some mortality due to biological control was not recognized. In North America, where the most data are available, it appears that the relative prevalence of different indigenous parasitoid species varies among habitat types, particularly between crop and non-crop habitats. Predator species responsible for egg mortality are much less commonly identified, but appear to include a wide variety of generalist chewing and sucking predators. To date, studies of natural enemies attacking H. halys nymphs and adults are relatively rare. Based on our review, we identify a number of key research gaps and suggest several directions for future research.

Sublethal Effects of Chronic Exposure to Tebufenozide on the Development, Survival, and Reproduction of the Tufted Apple Bud Moth (Lepidoptera: Tortricidae)

The lethal and sublethal effects of tebufenozide on the survival, development, and reproduction of a field strain of tufted apple bud moth, Platynota idaeusalis (Walker) (Lepidoptera: Tortricidae), were assessed by feeding first and third instars tebufenozide-treated diet until pupation. Larval mortality was 27.4 and 44.7% at 0.1 and 0.2 ppm for first instars and 21.9 and 57.8% at 0.2 and 0.4 ppm for third instars, respectively. Treated larvae exhibited higher pupal mortalities, lower pupal weights, and generally more deformed adults than untreated larvae. Larval development was not affected by tebufenozide when neonates were exposed, but development was accelerated slightly at 0.4 ppm for both males and females when third instars were exposed. All treatments produced sex ratios biased toward males. When paired with either treated or untreated males, females resulting from neonates treated at 0.2 ppm and from third instars treated at both 0.2 and 0.4 ppm laid from 37 to 65% fewer eggs. A reduction in fertility was only found when third instars were treated at the higher 0.4 ppm rate. These results suggest that tebufenozide can exhibit a significant effect on the population dynamics of the tufted apple bud moth.

Carabidae Population Dynamics and Temporal Partitioning: Response to Coupled Neonicotinoid-transgenic Technologies in Maize

ABSTRACT Insecticidal Bt crops and seed treatments represent additional pest management tools for growers, prompting ecological studies comparing their impact on farm system inputs and effects to nontarget organisms compared with conventional practices. Using high taxonomic and temporal resolution, we contrast the dominance structure of carabids and dynamics of the most abundant species in maize (both sweet and field corn) agroecosystems using pest management tactics determined by the purchase of seed and application of pyrethroid insecticides. In the seed-based treatments, sweet corn contained Cry1Ab/c proteins, whereas field corn contained the coupled technology of Cry3Bb1 proteins for control of corn rootworm and neonicotinoid seed treatments aimed at secondary soil-borne pests. The insecticide treatments involved foliar pyrethroids in sweet corn and at-planting pyrethroids in field corn. The carabid community, comprised of 49 species, was dominated by four species, Scarites quadriceps Chaudoir, Poecilus chalcites Say, Pterostichus melanarius Illiger, and Harpalus pensylvanicus DeGeer, that each occupied a distinct temporal niche during the growing season. Two species, Pt. melanarius and H. pensylvanicus, exhibited differences between treatments over time. Only H. pensylvanicus had consistent results in both years, in which activity densities in field corn were significantly higher in the control in July and/or August. These results, along with laboratory bioassays, led us to hypothesize that lower adult captures resulted from decrease in prey availability or exposure of H. pensylvanicus larvae to soil-directed insecticides—either the neonicotinoid seed treatment in the transgenic field corn or an at-planting soil insecticide in the conventional field corn.

Conventional and seed-based insect management strategies similarly influence nontarget coleopteran communities in maize.

ABSTRACT Seed-based pest management tools, such as transgenes and seed treatments, are emerging as viable alternatives to conventional insecticide applications in numerous crops, and often occur as coupled technologies. Seed-based technologies have been readily adopted in maize, for which ecological studies are needed to examine effects to farmland biodiversity. We compared the response of nontarget coleopteran communities in Cry1Ab/c sweet corn and Cry3Bb field corn to conventional pyrethroid applications and a control. Of particular interest was the Cry3Bb field corn, which was coupled with a neonicotinoid seed treatment and was not rotated across years. A functionally diverse subset of the coleopteran community, consisting of three families (Carabidae, Chrysomelidae, and Nitidulidae) and 9,525 specimens, was identified to species. We compared coleopteran diversity and dynamics using rarefaction and ordination techniques. There were no differences in species richness among treatments; however, higher activity densities were more common in the control. In the nonrotated field corn, principal response curves showed a consistent pattern of treatment communities deviating from the control communities over time, whereas crop rotation in the sweet corn negated treatment effects. Treatment effects could not be detected when beetles were grouped based on functional roles. Results indicate that neonicotinoid seed-based treatments may have effects on some nontarget coleopterans, but these effects are similar to conventional pyrethroid applications.

First Report of Zaprionus indianus (Diptera: Drosophilidae) in Commercial Fruits and Vegetables in Pennsylvania

ABSTRACT. Zaprionus indianus (Gupta) (Diptera: Drosophilidae), an invasive vinegar fly, was found for the first time in Adams County, Pennsylvania, in 2011. It was found in a commercial tart cherry orchard using apple cider vinegar (ACV) traps that were monitoring another invasive vinegar fly, the spotted wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae). Coincidentally, the first record of D. suzukii found in Pennsylvania was also found in this same cherry orchard only 3 months earlier as part of a spotted wing drosophila survey effort in raspberry, blackberry, grape, and tart cherry in Adams County. These same crops plus blueberry and tomato were monitored again in 2012. In this article, adult Z. indianus captures in ACV traps and other traps deployed in the aforementioned crops during 2012 season are presented and the economic importance of Z. indianus is discussed.

Local Plant Diversity Across Multiple Habitats Supports a Diverse Wild Bee Community in Pennsylvania Apple Orchards

Abstract Wild pollinators supply essential, historically undervalued pollination services to crops and other flowering plant communities with great potential to ensure agricultural production against the loss of heavily relied upon managed pollinators. Local plant communities provision wild bees with crucial floral and nesting resources, but the distribution of floristic diversity among habitat types in North American agricultural landscapes and its effect on pollinators are diverse and poorly understood, especially in orchard systems. We documented floristic diversity in typical mid-Atlantic commercial apple (Malus domestica Borkh.) orchards including the forest and orchard-forest edge (“edge”) habitats surrounding orchards in a heterogeneous landscape in south-central Pennsylvania, USA. We also assessed the correlation between plant richness and orchard pollinator communities. In this apple production region, edge habitats are the most species rich, supporting 146 out of 202 plant species recorded in our survey. Plant species richness in the orchard and edge habitats were significant predictors of bee species richness and abundance in the orchard, as well as landscape area of the forest and edge habitats. Both the quantity and quality of forest and edges close to orchards play a significant role in provisioning a diverse wild bee community in this agroecosystem.