Responses to environmental variability by herbivorous insects and their natural enemies within a bioenergy crop, Miscanthus x giganteus.

Precision agriculture (PA) is the application of management decisions based on identifying, quantifying, and responding to space-time variability. However, knowledge of crop pest responses to within-field environmental variability, and the spatial distribution of their natural enemies, is limited. Quantitative methods providing insights on how pest-predator relationships vary within fields are potentially important tools. In this study, phloem feeders and their natural enemies, were observed over two years across 81 locations within a field of the perennial feedstock grass in Georgia, USA. Geographically weighted regression (GWR) was used to spatially correlate their abundance with environmental factors. Variables included distance to forest edge, Normalized Difference of Vegetation Index (NDVI), slope, aspect, elevation, soil particle size distribution, and weather values. GWR methods were compared with generalized linear regression methods that do not account for spatial information. Non-spatial models indicated positive relationships between phloem-feeder abundance and wind speed, but negative relationships between elevation, proportions of silt and sand, and NDVI. With data partitioned into three seasonal groups, terrain and soil variables remained significant, and natural enemies and spiders became relevant. Results from GWR indicated that magnitudes and directions of responses varied within the field, and that relationships differed among seasons. Strong negative relationships between response and explanatory factors occurred: with NDVI during mid-season; with percent silt, during mid-, and late seasons; and with spider abundance during early and late seasons. In GWR models, slope, elevation, and aspect were mostly positive indicating further that associations with elevation depended on whether models incorporated spatial information or not. By using spatially explicit models, the analysis provided a complex, nuanced understanding of within-field relationships between phloem feeders and environmental covariates. This approach provides an opportunity to learn about the variability within agricultural fields and, with further analysis, has potential to inform and improve PA and habitat management decisions.

Predation on stink bugs (Hemiptera: Pentatomidae) in cotton and soybean agroecosystems.

Stink bugs (Hemiptera: Pentatomidae) are significant pests of cotton and soybeans in the southeastern United States with annual control costs exceeding $14 million in these crops. Three of the most prominent stink bug pests are the southern green (Nezara viridula), brown (Euschistus servus) and green (Chinavia hilaris) stink bugs. To determine trophic linkages between generalist arthropod predators and these pests, species-specific 16S molecular markers were designed and used to detect the presence of prey DNA in predator gut-contents. Over 2700 predators were collected over two growing seasons in cotton and soybean in southern Georgia in 2011 and 2012 and screened for stink bug DNA. Trophic linkages were analyzed relative to prey availability, crop type and field location. The frequency of stink bug DNA in predator guts was negligible on E. servus (0.23%) and C. hilaris (0.09%). Overall gut content detection of N. viridula was 3.3% and Geocoris sp. (Hemiptera: Geocoridae), Orius sp. (Hemiptera: Anthocoridae) and Notoxus monodon (Coleoptera: Anthicidae) were the primary predators. This contrasts with previous studies that reported a much more diverse suite of predators consuming stink bugs with much higher frequency of gut-content positives. The discrepancy between studies highlights the need for replicating studies in space and time, especially if the goal is to implement effective and durable conservation biological control in integrated pest management.

Landscape Effects on Solenopsis invicta (Hymenoptera: Formicidae) and Geocoris spp. (Hemiptera: Geocoridae), Two Important Omnivorous Arthropod Taxa in Field Crops.

The economically important brown stink bug, Euschistus servus (Say) (Hemiptera: Pentatomidae), is a native pest of many crops in southeastern United States and insecticide applications are the prevailing method of population suppression. To elucidate biological control of E. servus populations, we investigated two egg predators' (red imported fire ants, Solenopsis invicta Buren (Hymenoptera: Formicidae), and Geocoris spp. (Hemiptera: Geocoridae)) responses to both local and landscape factors that may have influenced their combined ability to cause mortality in immature E. servus. We estimated the density of fire ants and Geocoris spp. on four major crop hosts-maize, peanut, cotton, and soybean-in 16 landscapes over 3 yr in the coastal plain of Georgia, USA. Both Geocoris spp. and fire ant populations were concentrated on specific crops in this study, maize and soybean for Geocoris spp. and peanut and cotton for fire ants, but the percentage area of specific crops and woodland and pasture in the landscape and year also influenced their density in focal fields. The crop specific density of both taxa, the influence of the percentage area of specific crops and woodland in the landscape, and the variability in density over years may have been related to variable alternative resources for these omnivores in the habitats. Despite the variability over years, differential habitat use of fire ants and Georcoris spp. may have contributed to their combined ability to cause E. servus immature mortality.

Landscape Effects on Reproduction of Euschistus servus (Hemiptera: Pentatomidae), a Mobile, Polyphagous, Multivoltine Arthropod Herbivore.

Landscape factors can significantly influence arthropod populations. The economically important brown stink bug, Euschistus servus (Say) (Hemiptera: Pentatomidae), is a native mobile, polyphagous and multivoltine pest of many crops in southeastern United States and understanding the relative influence of local and landscape factors on their reproduction may facilitate population management. Finite rate of population increase (λ) was estimated in four major crop hosts-maize, peanut, cotton, and soybean-over 3 yr in 16 landscapes of southern Georgia. A geographic information system (GIS) was used to characterize the surrounding landscape structure. LASSO regression was used to identify the subset of local and landscape characteristics and predator densities that account for variation in λ. The percentage area of maize, peanut and woodland and pasture in the landscape and the connectivity of cropland had no influence on E. servus λ. The best model for explaining variation in λ included only four predictor variables: whether or not the sampled field was a soybean field, mean natural enemy density in the field, percentage area of cotton in the landscape and the percentage area of soybean in the landscape. Soybean was the single most important variable for determining E. servus λ, with much greater reproduction in soybean fields than in other crop species. Penalized regression and post-selection inference provide conservative estimates of the landscape-scale determinants of E. servus reproduction and indicate that a relatively simple set of in-field and landscape variables influences reproduction in this species.

Perennial Grass and Native Wildflowers: A Synergistic Approach to Habitat Management.

Marginal agricultural land provides opportunities to diversify landscapes by producing biomass for biofuel, and through floral provisioning that enhances arthropod-mediated ecosystem service delivery. We examined the effects of local spatial context (adjacent to woodland or agriculture) and irrigation (irrigation or no irrigation) on wildflower bloom and visitation by arthropods in a biofeedstocks-wildflower habitat buffer design. Twenty habitat buffer plots were established containing a subplot of Napier grass (Pennisetum perpureum Schumach) for biofeedstock, three commercial wildflower mix subplots, and a control subplot containing spontaneous weeds. Arthropods and flowers were visually observed in quadrats throughout the season. At the end of the season we measured soil nutrients and harvested Napier biomass. We found irrespective of buffer location or irrigation, pollinators were observed more frequently early in the season and on experimental plots with wildflowers than on weeds in the control plots. Natural enemies showed a tendency for being more common on plots adjacent to a wooded border, and were also more commonly observed early in the season. Herbivore visits were infrequent and not significantly influenced by experimental treatments. Napier grass yields were high and typical of first-year yields reported regionally, and were not affected by location context or irrigation. Our results suggest habitat management designs integrating bioenergy crop and floral resources provide marketable biomass and habitat for beneficial arthropods.

Seasonal Occurrence and Interspecific Interactions of Egg Parasitoids of Megacopta cribraria (Heteroptera: Plataspidae) in Japan.

We conducted a field study to determine seasonal egg parasitism rates of the kudzu bug Megacopta cribraria (F.) on the kudzu plant, Pueraria montana (Lour.) Merr. var. lobata (Willd.) Maesen et Almeida ex Sanjappa and Pradeep, in Tokyo, Japan, during the period from May 2014 to September 2014. The eggs of M. cribraria per 1 m2 of kudzu at four locations in Tokyo were collected weekly and parasitism rates were assessed. Eggs of M. cribraria were laid on the kudzu plant from May to September. Megacopta cribraria eggs were parasitized by two parasitoid species, Paratelenomus saccharalis (Dodd) and Ooencyrtus nezarae Ishii. Paratelenomus saccharalis first appeared in May, and its parasitism rates peaked in July and September. Ooencyrtus nezarae first appeared in June and its parasitism rates peaked in July. Except for one location which could not be statistically analyzed because of the small sample size, occurrence of parasitism by P. saccharalis and O. nezarae in M. cribraria egg masses was independent at one location and positively associated at two locations, suggesting that the use of host egg masses by P. saccharalis and O. nezarae is not mutually exclusive. Parasitism rates by P. saccharalis and O. nezarae were significantly lower for egg masses parasitized by both species than for those parasitized by a single species. The proportion of males among O. nezarae progeny was significantly higher for egg masses parasitized by O. nezarae together with P. saccharalis than for those parasitized by O. nezarae alone. These results suggest that parasitism of host egg masses by the two species is influenced by their interspecific interactions.

Competitive release and outbreaks of non-target pests associated with transgenic Bt cotton.

The adoption of transgenic Bt cotton has, in some cases, led to environmental and economic benefits through reduced insecticide use. However, the distribution of these benefits and associated risks among cotton growers and cotton-growing regions has been uneven due in part to outbreaks of non-target or secondary pests, thereby requiring the continued use of synthetic insecticides. In the southeastern USA, Bt cotton adoption has resulted in increased abundance of and damage from stink bug pests, Euschistus servus and Nezara viridula (Heteroptera: Pentatomidae). While the impact of increased stink bug abundance has been well-documented, the causes have remained unclear. We hypothesize that release from competition with Bt-susceptible target pests may drive stink bug outbreaks in Bt cotton. We first examined the evidence for competitive release of stink bugs through meta-analysis of previous studies. We then experimentally tested if herbivory by Bt-susceptible Helicoverpa zea increases stink bug leaving rates and deters oviposition on non-Bt cotton. Consistent with previous studies, we found differences in leaving rates only for E servus, but we found that both species strongly avoided ovipositing on H. zea-damaged plants. Considering all available evidence, competitive release of stink bug populations in Bt cotton likely contributes to outbreaks, though the relative importance of competitive release remains an open question. Ecological risk assessments of Bt crops and other transgenic insecticidal crops would benefit from greater understanding of the ecological mechanisms underlying non-target pest outbreaks and greater attention to indirect ecological effects more broadly.

Computational modeling and experimental validation of odor detection behaviors of classically conditioned parasitic wasp, Microplitis croceipes.

A prototype chemical sensor named Wasp hound® that utilizes five classically conditioned parasitoid wasps, Microplitis croceipes (Cresson) (Hymenoptera: Braconidae), to detect volatile odors was successfully implemented in a previous study. To improve the odor-detecting ability of Wasp Hound®, searching behaviors of an individual wasp in a confined area are studied and modeled through stochastic differential equations in this paper. The wasps are conditioned to 20 mg of coffee when associated with food and subsequently, tested to 5, 10, 20, and 40 mg of coffee. A stochastic model is developed and validated based on three positive behavioral responses (walking, rotation around odor source, and self-rotation) from conditioned wasps at four different test dosages. The model is capable to reproducing the behaviors of conditioned wasps, and can be used to improve the ability of Wasp Hound® to assess changes in odor concentration. The model simulation results show the behaviors of conditioned wasps are significantly different when tested at different coffee dosages. We conjecture that the searching behaviors of conditioned wasps are based on the temporal and spatial neuron activity of olfactory receptor neurons and glomeruli, which are strongly correlated to the training dosages. The overall results demonstrate the utility of mathematical models for interpreting experimental observations, gaining novel insights into the dynamic behavior of classically conditioned wasps, as well as broadening the practical uses of Wasp Hound.

A likelihood-based biostatistical model for analyzing consumer movement in simultaneous choice experiments.

Consumer feeding preference among resource choices has critical implications for basic ecological and evolutionary processes, and can be highly relevant to applied problems such as ecological risk assessment and invasion biology. Within consumer choice experiments, also known as feeding preference or cafeteria experiments, measures of relative consumption and measures of consumer movement can provide distinct and complementary insights into the strength, causes, and consequences of preference. Despite the distinct value of inferring preference from measures of consumer movement, rigorous and biologically relevant analytical methods are lacking. We describe a simple, likelihood-based, biostatistical model for analyzing the transient dynamics of consumer movement in a paired-choice experiment. With experimental data consisting of repeated discrete measures of consumer location, the model can be used to estimate constant consumer attraction and leaving rates for two food choices, and differences in choice-specific attraction and leaving rates can be tested using model selection. The model enables calculation of transient and equilibrial probabilities of consumer-resource association, which could be incorporated into larger scale movement models. We explore the effect of experimental design on parameter estimation through stochastic simulation and describe methods to check that data meet model assumptions. Using a dataset of modest sample size, we illustrate the use of the model to draw inferences on consumer preference as well as underlying behavioral mechanisms. Finally, we include a user's guide and computer code scripts in R to facilitate use of the model by other researchers.

Pest trade-offs in technology: reduced damage by caterpillars in Bt cotton benefits aphids.

The rapid adoption of genetically engineered (GE) plants that express insecticidal Cry proteins derived from Bacillus thuringiensis (Bt) has raised concerns about their potential impact on non-target organisms. This includes the possibility that non-target herbivores develop into pests. Although studies have now reported increased populations of non-target herbivores in Bt cotton, the underlying mechanisms are not fully understood. We propose that lack of herbivore-induced secondary metabolites in Bt cotton represents a mechanism that benefits non-target herbivores. We show that, because of effective suppression of Bt-sensitive lepidopteran herbivores, Bt cotton contains reduced levels of induced terpenoids. We also show that changes in the overall level of these defensive secondary metabolites are associated with improved performance of a Bt-insensitive herbivore, the cotton aphid, under glasshouse conditions. These effects, however, were not as clearly evident under field conditions as aphid populations were not correlated with the amount of terpenoids measured in the plants. Nevertheless, increased aphid numbers were visible in Bt cotton compared with non-Bt cotton on some sampling dates. Identification of this mechanism increases our understanding of how insect-resistant crops impact herbivore communities and helps underpin the sustainable use of GE varieties.

Impact of brown stink bug (Heteroptera: Pentatomidae) feeding on corn grain yield components and quality.

Brown stink bug, Euschistus servus (Say) (Heteroptera: Pentatomidae), damage on developing corn, Zea mays L., ears was examined in 2005 and 2006 by using eight parameters related to its yield and kernel quality. Stink bug infestations were initiated when the corn plants were at tasseling (VT), mid-silking (R1), and blister (R2) stages by using zero, three, and six in 2005 or zero, one, two, and four bugs per ear in 2006, and maintained for 9 d. The percentage of discolored kernels was affected by stink bug number in both years, but not always affected by plant growth stage. The growth stage effect on the percentage of discolored kernels was significant in 2006, but not in 2005. The percentage of aborted kernels was affected by both stink bug number and plant growth stage in 2005 but not in 2006. Kernel weight was significantly reduced when three E. sercus adults were confined on a corn ear at stage VT or R1 for 9 d in 2005, whereas one or two adults per ear resulted in no kernel weight loss, but four E. servus adults did cause significant kernel weight loss at stage VT in 2006. Stink bug feeding injury at stage R2 did not affect kernel damage, ear weight or grain weight in either year. The infestation duration (9 or 18 d) was positively correlated to the percentage of discolored kernels but did not affect kernel or ear weight. Based on the regression equations between the kernel weight and stink bug number, the gain threshold or economic injury level should be 0.5 bugs per ear for 9 d at stage VT and less for stage R1. This information will be useful in developing management guidelines for stink bugs in field corn during ear formation and early grain filling stages.