quantifying-plant-soluble-protein-digestible-carbohydrate-content

Quantifying Plant Soluble Protein and Digestible Carbohydrate Content, Using Corn (<em>Zea mays</em>) As an Exemplar

Elemental data are commonly used to infer plant quality as a resource to herbivores. However, the ubiquity of carbon in biomolecules, the presence of ...

University of Minnesota

Diverse subdisciplines within entomology recognize the detection of rare individuals as the precursor to effective management of these individuals. Unfortunately, detection methods have often developed on a case-by-case basis, and advances in one subdiscipline have not carried over to similarly related fields. The biology of a particular organism will certainly affect sampling methods, but the underlying principles governing the power of a sampling strategy to detect rare individuals will apply across taxa. Our review of the sampling literature demonstrates the common problem of detecting rare individuals, reviews the fundamentals of probability theory as a foundation for any monitoring program, and discusses the inferences that can be drawn from samples, especially when resources limit sampling efforts. Particular emphasis is placed on binomial-, beta-binomial-, and hypergeometric-based sampling strategies as they pertain to quarantine inspections for exotic pests, veterinary/medical entomology, and insecticide resistance monitoring.

Strategies and statistics of sampling for rare individuals.

The use of selective insecticides may improve conservation of natural enemies and therefore contribute to the success of integrated pest management (IPM) programs. In this study, the toxicity of two commonly used selective insecticides, indoxacarb and spinosad, to the multicolored Asian lady beetle, Harmonia axyridis (Pallas), was evaluated. Third instars and adults of H. axyridis were exposed to indoxacarb at 50 and 100% of the field rate (FR), to spinosad at 100% FR and to water (untreated check) under laboratory conditions via three routes of exposure. Treatments were applied directly on insects (i.e., topical application), on Petri dishes (i.e., residues), or on soybean aphids, Aphis glycines Matsumara (i.e., treated prey). Mortality of exposed individuals in each life stage was recorded 2 and 7 days after treatment. Logistic regression indicated that indoxacarb at 100% FR, followed by indoxacarb at 50% FR, was more insecticidal than spinosad to third instars. Mortality was higher when H. axyridis were exposed to both insecticides via residues followed by treated prey. Indoxacarb at 100 or 50% FR was insecticidal to adults. Adults were tolerant to spinosad via all routes of exposure. The present results suggest that indoxacarb may decrease H. axyridis field populations by causing mortality to larvae and adults via all routes of exposure. Implications of the toxicity of indoxacarb to H. axyridis within an IPM context and possible reasons for the differences in susceptibility of H. axyridis for each route of exposure are discussed.

Toxicity of indoxacarb and spinosad to the multicolored Asian lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae), via three routes of exposure.

Transgenic maize engineered to express insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) has become widely adopted in U.S. agriculture. In 2009, Bt maize was planted on more than 22.2 million hectares, constituting 63% of the U.S. crop. Using statistical analysis of per capita growth rate estimates, we found that areawide suppression of the primary pest Ostrinia nubilalis (European corn borer) is associated with Bt maize use. Cumulative benefits over 14 years are an estimated $3.2 billion for maize growers in Illinois, Minnesota, and Wisconsin, with more than $2.4 billion of this total accruing to non-Bt maize growers. Comparable estimates for Iowa and Nebraska are $3.6 billion in total, with $1.9 billion for non-Bt maize growers. These results affirm theoretical predictions of pest population suppression and highlight economic incentives for growers to maintain non-Bt maize refugia for sustainable insect resistance management.

Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers.

Sweet corn, Zea mays L., transformed to express a novel vegetative insecticidal protein, Vip3A (event MIR162, Syngenta Seeds, Inc..), produced by the bacterium, Bacillus thuringiensis (Bt), was evaluated over four field seasons in Maryland and two field seasons in Minnesota for efficacy against the corn earworm, Helicoverpa zea (Boddie). Hybrids expressing the Vip3A protein and pyramided in hybrids also expressing the Cry1Ab Bt protein (event Bt11, ATTRIBUTE(®), Syngenta Seeds, Inc.) were compared to hybrids expressing only Cry1Ab or to genetically similar non-Bt hybrids each year. In addition to H. zea efficacy, results for Ostrinia nubilalis (Hübner) and Spodoptera frugiperda (J.E. Smith) are presented. Over all years and locations, the non-Bt hybrids, without insecticide protection, averaged between 43 and 100% ears infested with a range of 0.24 to 1.74 H. zea larvae per ear. By comparison, in the pyramided Vip3A x Cry1Ab hybrids, no larvae were found and only minimal kernel damage (likely due to other insect pests) was recorded. Hybrids expressing only Cry1Ab incurred a moderate level of H. zea feeding damage, with surviving larvae mostly limited to the first or second instar as a result of previously documented growth inhibition from Cry1Ab. These results suggest that the Vip3A protein, pyramided with Cry1Ab, appears to provide the first "high-dose" under field conditions and will be valuable for ongoing resistance management.

Novel Vip3A Bacillus thuringiensis (Bt) maize approaches high-dose efficacy against Helicoverpa zea (Lepidoptera: Noctuidae) under field conditions: Implications for resistance management.

Pest population density oscillations have a profound effect on agroecosystem functioning, particularly when pests cycle with epidemic persistence. Here, we ask whether landscape-level manipulations can be used to restrict the cycle amplitude of the European corn borer moth [Ostrinia nubilalis (Hübner)], an economically important maize pest. We analysed time series from Minnesota (1963-2009) and Wisconsin (1964-2009) to quantify the extent of regime change in the US Corn Belt where rates of transgenic Bt maize adoption varied. The introduction of Bt maize explained cycle damping when the adoption of the crop was high (Minnesota); oscillations were damped but continued to persist when Bt maize was used less intensely (Wisconsin). We conclude that host plant quality is key to understanding both epidemic persistence and the success of intervention strategies. In particular, the dichotomy in maize management between states is thought to limit the spatial autocorrelation of O. nubilalis.

Putting the brakes on a cycle: bottom-up effects damp cycle amplitude.

A recent shift in managing insect resistance to genetically engineered (GE) maize consists of mixing non-GE seed with GE seed known as "refuge in a bag", which increases the likelihood of predators encountering both prey fed Bt and prey fed non-Bt maize. We therefore conducted laboratory choice-test feeding studies to determine if a predator, Harmonia axyridis, shows any preference between prey fed Bt and non-Bt maize leaves. The prey species was Spodoptera frugiperda, which were fed Bt maize (MON-810), expressing the single Cry1Ab protein, or non-Bt maize. The predators were third instar larvae and female adults of H. axyridis. Individual predators were offered Bt and non-Bt fed prey larvae that had fed for 24, 48 or 72 h. Ten and 15 larvae of each prey type were offered to third instar and adult predators, respectively. Observations of arenas were conducted at 1, 2, 3, 6, 15 and 24 h after the start of the experiment to determine the number and type of prey eaten by each individual predator. Prey larvae that fed on non-Bt leaves were significantly larger than larvae fed Bt leaves. Both predator stages had eaten nearly all the prey by the end of the experiment. However, in all combinations of predator stage and prey age, the number of each prey type consumed did not differ significantly. ELISA measurements confirmed the presence of Cry1Ab in leaf tissue (23-33 µg/g dry weight) and S. frugiperda (2.1-2.2 µg/g), while mean concentrations in H. axyridis were very low (0.01-0.2 µg/g). These results confirm the predatory status of H. axyridis on S. frugiperda and that both H. axyridis adults and larvae show no preference between prey types. The lack of preference between Bt-fed and non-Bt-fed prey should act in favor of insect resistance management strategies using mixtures of GE and non-GE maize seed.

Harmonia axyridis (Coleoptera: Coccinellidae) exhibits no preference between Bt and non-Bt maize fed Spodoptera frugiperda (Lepidoptera: Noctuidae).

Helicoverpa armigera has recently invaded South and Central America, and appears to be spreading rapidly. We update a previously developed potential distribution model to highlight the global invasion threat, with emphasis on the risks to the United States. The continued range expansion of H. armigera in Central America is likely to change the invasion threat it poses to North America qualitatively, making natural dispersal from either the Caribbean islands or Mexico feasible. To characterise the threat posed by H. armigera, we collated the value of the major host crops in the United States growing within its modelled potential range, including that area where it could expand its range during favourable seasons. We found that the annual value of crops that would be exposed to H. armigera totalled approximately US$78 billion p.a., with US$843 million p.a. worth growing in climates that are optimal for the pest. Elsewhere, H. armigera has developed broad-spectrum pesticide resistance; meaning that if it invades the United States, protecting these crops from significant production impacts could be challenging. It may be cost-effective to undertake pre-emptive biosecurity activities such as slowing the spread of H. armigera throughout the Americas, improving the system for detecting H. armigera, and methods for rapid identification, especially distinguishing between H. armigera, H. zea and potential H. armigera x H. zea hybrids. Developing biological control programs, especially using inundative techniques with entomopathogens and parasitoids could slow the spread of H. armigera, and reduce selective pressure for pesticide resistance. The rapid spread of H. armigera through South America into Central America suggests that its spread into North America is a matter of time. The likely natural dispersal routes preclude aggressive incursion responses, emphasizing the value of preparatory communication with agricultural producers in areas suitable for invasion by H. armigera. 

The potential distribution of invading Helicoverpa armigera in North America: is it just a matter of time?

Transgenic maize MON88017, expressing the Cry3Bb1 toxin from Bacillus thuringiensis (Bt maize), confers resistance to corn rootworms (Diabrotica spp.) and provides tolerance to the herbicide glyphosate. However, prior to commercialization, substantial assessment of potential effects on non-target organisms within agroecosystems is required. The MON88017 event was therefore evaluated under field conditions in Southern Bohemia in 2009-2011, to detect possible impacts on the above-ground arthropod species. The study compared MON88017, its near-isogenic non-Bt hybrid DK315 (treated or not treated with the soil insecticide Dursban 10G) and two non-Bt reference hybrids (KIPOUS and PR38N86). Each hybrid was grown on five 0.5 ha plots distributed in a 14-ha field with a Latin square design. Semiquantitative ELISA was used to verify Cry3Bb1 toxin levels in the Bt maize. The species spectrum of non-target invertebrates changed during seasons and was affected by weather conditions. The thrips Frankliniella occidentalis was the most abundant species in all three successive years. The next most common species were aphids Rhopalosiphum padi and Metopolophium dirhodum. Frequently observed predators included Orius spp. and several species within the Coccinellidae. Throughout the three-year study, analysis of variance indicated some significant differences (P<0.05). Multivariate analysis showed that the abundance and diversity of plant dwelling insects was similar in maize with the same genetic background, for both Bt (MON88017) and non-Bt (DK315) untreated or insecticide treated. KIPOUS and PR38N86 showed some differences in species abundance relative to the Bt maize and its near-isogenic hybrid. However, the effect of management regime on arthropod community was insignificant and accounted only for a negligible portion of the variability. 

Risk Assessment of Genetically Engineered Maize Resistant to Diabrotica spp.: Influence on Above-Ground Arthropods in the Czech Republic.

A farmer's decision on whether to control a pest is usually based on the perceived threat of the pest locally and the guidance of commercial advisors. Therefore, farmers in a region are often influenced by similar circumstances, and this can create a coordinated response for pest control that is effective at a landscape scale. This coordinated response is not intentional, but is an emergent property of the system. We propose a framework for understanding the intrinsic feedback mechanisms between the actions of humans and the dynamics of pest populations and demonstrate this framework using the European corn borer, a serious pest in maize crops. We link a model of the European corn borer and a parasite in a landscape with a model that simulates the decisions of individual farmers on what type of maize to grow. Farmers chose whether to grow Bt-maize, which is toxic to the corn borer, or conventional maize for which the seed is cheaper. The problem is akin to the snow-drift problem in game theory; that is to say, if enough farmers choose to grow Bt maize then because the pest is suppressed an individual may benefit from growing conventional maize. We show that the communication network between farmers' and their perceptions of profit and loss affects landscape scale patterns in pest dynamics. We found that although adoption of Bt maize often brings increased financial returns, these rewards oscillate in response to the prevalence of pests. 

The Effect of Farmers' Decisions on Pest Control with Bt Crops: A Billion Dollar Game of Strategy.

The brown marmorated stink bug, Halyomorpha halys (Stål), is native to eastern Asia and is presently invading North America. Little is known about the exposure to and effects of winter temperatures in newly invaded regions on H. halys The overwintering habitats that this species utilizes vary greatly in their thermal buffering capacity. They naturally overwinter in aggregations beneath loose bark on trees and in cliff outcroppings, but will also commonly aggregate in buildings. Effects of cold temperatures such as mortality and freezing have yet to be quantified in the invading population. We report that H. halys is chill intolerant (i.e., dies before reaching its freezing point), and that the degree of cold tolerance of populations in North America differs by season, sex, and acclimation location. The mean winter supercooling point (± SEM) of individuals acclimated in Minnesota was -17.06 °C ± 0.13 and in Virginia was -13.90 °C ± 0.09. By using laboratory assays of lower lethal temperatures and ambient air temperature records, we accurately forecasted mortality for field experiments in Minnesota and Virginia. Temperature refugia provided by human-built structures are likely crucial for overwintering survival during atypically cold winters and possibly contribute to the northern geographic range expansion of this economically damaging insect in the temperate climates of North America.

Cold Tolerance of Halyomorpha halys (Hemiptera: Pentatomidae) Across Geographic and Temporal Scales.

 is a major crop pest in Asia and Africa, and has recently spread to the Mediterranean region. Knowledge of its potential distribution can inform biosecurity policies aimed at limiting its further spread and efforts to reduce its impact in areas that are already invaded. Three models of the potential distribution of this insect have been published, each with significant shortcomings. We re-parameterized an existing CLIMEX model to address some parameter inconsistencies and to improve the fit to the known distribution of . The resulting model fits the known distribution better than previous models, highlights additional risks in equatorial regions and reduces modelled risks in wet and extremely dry regions. We bring new insights into the role of irrigation in the potential spread of this invasive insect and compare its potential distribution with the present known distribution of its hosts. We also distinguish regions that are suitable for supporting persistent populations from those that may be at risk from ephemeral populations during favourable seasons. We present one of the first demonstrations of a new capability in CLIMEX to automatically estimate parameter sensitivity and model uncertainty. Our CLIMEX model highlights the substantial invasion risk posed by  to cropping regions in the Americas, Australia, China, Europe, New Zealand and West Africa. Its broad host range and reported impacts suggest that it should be a pest of significant concern to biosecurity agencies in these presently uninvaded regions.

The potential global distribution of , including consideration of irrigation and cropping patterns.

Understanding indirect, trophic-level effects of genetically engineered plants, expressing insecticidal proteins derived from the bacterium, Bacillus thuringiensis (Bt), is essential to the ecological risk assessment process. In this study, we examine potential indirect, trophic-level effects of Bt-sensitive prey using the predator, Harmonia axyridis (Pallas), feeding upon Spodoptera frugiperda (J.E. Smith) larvae, which had delayed development (lower body mass) following ingestion of Cry1Ab maize leaves. We found no adverse effects on development and survival when H. axyridis larvae were fed S. frugiperda larvae that had fed on Cry1Ab maize tissue. Presence of Cry1Ab in H. axyridis decreased considerably after switching to another diet within 48 h. In a no-choice assay, H. axyridis larvae consumed more Bt-fed S. frugiperda than non-Bt-fed larvae. Preference for S. frugiperda feeding on Bt maize was confirmed in subsequent choice assays with H. axyridis predation on Bt-fed, 1-5-d-old S. frugiperda larvae. We suggest that H. axyridis preferred prey, not based on whether it had fed on Bt or non-Bt maize, but rather on larval mass, and they compensated for the nutritional deficiency of lighter larvae through increased consumption. Pest larvae with variable levels of resistance developing on Bt diet are often stunted versus sensitive larvae developing on non-Bt diet. It is possible that such larvae may be preferentially removed from local field populations. These results may have implications for insect resistance management and may be played out under field conditions where seed blends of Bt and non-Bt hybrids are planted.

Predator Preference for Bt-Fed Spodoptera frugiperda (Lepidoptera: Noctuidae) Prey: Implications for Insect Resistance Management in Bt Maize Seed Blends.

Population responses to environmental extremes often dictate the bounds to species' distributions. However, population dynamics at, or near, those range limits may also be affected by sublethal effects. We exposed late instars and pupae of an invasive leafroller, Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae), to cold temperatures and measured the effects of exposure on subsequent survivorship, development, and reproduction. Cold temperature was applied as acute exposure to -10 °C (a low, but not immediately lethal temperature for this species) or the onset of freezing (the peak of the supercooling point exotherm). Survival was defined as the ability to successfully eclose as an adult. We measured immature development times, pupal mass, and adult longevity as proxies of fitness in survivors. Additionally, surviving insects were mated with individuals that had not been exposed to cold to measure fertility. There was no difference between the proportion of larvae or pupae that survived acute exposure to -10 °C and those exposed to the control temperature. Approximately 17% of larvae and 8% of pupae survived brief periods with internal ice formation and continued development to become reproductively viable adults. Importantly, surviving the onset of freezing came with significant fitness costs but not to exposure to -10 °C; most insects that survived partial freezing had lower fertility and shorter adult lifespans than either the -10 °C or control group. These results are discussed within the context of forecasting invasive insect distributions.

Sublethal effects of subzero temperatures on the light brown apple moth, Epiphyas postvittana: fitness costs in response to partial freezing.

Transgenic crops containing the bacterium  (Bt) genes reduce pests and insecticide usage, promote biocontrol services, and economically benefit growers. Area-wide Bt adoption suppresses pests regionally, with declines expanding beyond the planted Bt crops into other non-Bt crop fields. However, the offsite benefits to growers of other crops from such regional suppression remain uncertain. With data spanning 1976-2016, we demonstrate that vegetable growers benefit via decreased crop damage and insecticide applications in relation to pest suppression in the Mid-Atlantic United States. We provide evidence for the regional suppression of  (Hübner), European corn borer, and  (Boddie), corn earworm, populations in association with widespread Bt maize adoption (1996-2016) and decreased economic levels for injury in vegetable crops [peppers ( L.), green beans ( L.), and sweet corn ( L., convar. )] compared with the pre-Bt period (1976-1995). Moth populations of both species significantly declined in association with widespread Bt maize (field corn) adoption, even as increased temperatures buffered the population reduction. We show marked decreases in the number of recommended insecticidal applications, insecticides applied, and  damage in vegetable crops in association with widespread Bt maize adoption. These offsite benefits to vegetable growers in the agricultural landscape have not been previously documented, and the positive impacts identified here expand on the reported ecological effects of Bt adoption. Our results also underscore the need to account for offsite economic benefits of pest suppression, in addition to the direct economic benefits of Bt crops.

Article	Year
Strategies and statistics of sampling for rare individuals. Annual review of entomology\| PubMed ID: 11729072	2002
Toxicity of indoxacarb and spinosad to the multicolored Asian lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae), via three routes of exposure. Pest management science\| PubMed ID: 16794989	2006
Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science (New York, N.Y.)\| PubMed ID: 20929774	2010
Novel Vip3A Bacillus thuringiensis (Bt) maize approaches high-dose efficacy against Helicoverpa zea (Lepidoptera: Noctuidae) under field conditions: Implications for resistance management. GM crops\| PubMed ID: 21844691	2010
Putting the brakes on a cycle: bottom-up effects damp cycle amplitude. Ecology letters\| PubMed ID: 22364256	2012
Harmonia axyridis (Coleoptera: Coccinellidae) exhibits no preference between Bt and non-Bt maize fed Spodoptera frugiperda (Lepidoptera: Noctuidae). PloS one\| PubMed ID: 23024772	2012
The potential distribution of invading Helicoverpa armigera in North America: is it just a matter of time? PloS one\| PubMed ID: 25786260	2015
Risk Assessment of Genetically Engineered Maize Resistant to Diabrotica spp.: Influence on Above-Ground Arthropods in the Czech Republic. PloS one\| PubMed ID: 26083254	2015
The Effect of Farmers' Decisions on Pest Control with Bt Crops: A Billion Dollar Game of Strategy. PLoS computational biology\| PubMed ID: 26720851	2015
Cold Tolerance of Halyomorpha halys (Hemiptera: Pentatomidae) Across Geographic and Temporal Scales. Environmental entomology\| PubMed ID: 26744454	2016
The potential global distribution of , including consideration of irrigation and cropping patterns. Journal of pest science\| PubMed ID: 28275325	2017
Predator Preference for Bt-Fed Spodoptera frugiperda (Lepidoptera: Noctuidae) Prey: Implications for Insect Resistance Management in Bt Maize Seed Blends. Journal of economic entomology\| PubMed ID: 28369505	2017
Sublethal effects of subzero temperatures on the light brown apple moth, Epiphyas postvittana: fitness costs in response to partial freezing. Insect science\| PubMed ID: 29193863	2017
Regional pest suppression associated with widespread Bt maize adoption benefits vegetable growers. Proceedings of the National Academy of Sciences of the United States of America\| PubMed ID: 29531049	2018

William D. Hutchison

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