IPM reduces insecticide applications by 95% while maintaining or enhancing crop yields through wild pollinator conservation.

Pest management practices in modern industrial agriculture have increasingly relied on insurance-based insecticides such as seed treatments that are poorly correlated with pest density or crop damage. This approach, combined with high invertebrate toxicity for newer products like neonicotinoids, makes it challenging to conserve beneficial insects and the services that they provide. We used a 4-y experiment using commercial-scale fields replicated across multiple sites in the midwestern United States to evaluate the consequences of adopting integrated pest management (IPM) using pest thresholds compared with standard conventional management (CM). To do so, we employed a systems approach that integrated coproduction of a regionally dominant row crop (corn) with a pollinator-dependent specialty crop (watermelon). Pest populations, pollination rates, crop yields, and system profitability were measured. Despite higher pest densities and/or damage in both crops, IPM-managed pests rarely reached economic thresholds, resulting in 95% lower insecticide use (97 versus 4 treatments in CM and IPM, respectively, across all sites, crops, and years). In IPM corn, the absence of a neonicotinoid seed treatment had no impact on yields, whereas IPM watermelon experienced a 129% increase in flower visitation rate by pollinators, resulting in 26% higher yields. The pollinator-enhancement effect under IPM management was mediated entirely by wild bees; foraging by managed honey bees was unaffected by treatments and, overall, did not correlate with crop yield. This proof-of-concept experiment mimicking on-farm practices illustrates that cropping systems in major agricultural commodities can be redesigned via IPM to exploit ecosystem services without compromising, and in some cases increasing, yields.

Parasitism of Adult Pentatomidae by Tachinidae in Soybean in the North Central Region of the United States.

Stink bugs (Hemiptera: Pentatomidae) are agricultural pests of increasing significance in the North Central Region of the United States, posing a threat to major crops such as soybean. Biological control can reduce the need for insecticides to manage these pests, but the parasitism of stink bugs by Tachinidae (Diptera) is poorly characterized in this region. The objective of this study was to evaluate the rate of parasitism of stink bugs by tachinids over 2 yr from nine states across the North Central Region. Parasitism was assessed by quantifying tachinid eggs on the integument of stink bug adults. Parasitism rates (i.e., percent of adult stink bugs with tachinid eggs) were compared across stink bug species, states, stink bug sex, and years. The mean percent parasitism of stink bugs by tachinids was about 6% across the region and did not differ among stink bug species. Mean percent parasitism was significantly higher in Missouri than in northern and western states. In addition, male stink bugs had significantly higher mean percent parasitism than females. Stink bug species commonly found in soybean in the region showed some parasitism and are therefore potentially vulnerable to oviposition by these parasitoids. This is the first study to characterize the level of parasitism of stink bugs by tachinids across the North Central Region.

Movement of the Neonicotinoid Seed Treatment Clothianidin into Groundwater, Aquatic Plants, and Insect Herbivores.

Agricultural use of the neonicotinoid clothianidin (CLO) as a seed treatment of corn and soybeans has been linked to contamination of waterways and irrigation water. By analyzing samples collected from field lysimeters with liquid chromatography tandem mass spectrometry (LC-MS), this study reports the highest CLO concentrations within leachate following planting, with maximum concentrations occurring 4 weeks post-planting (3370 ng L-1). This concentration is approximately 10× greater than previously reported CLO concentrations in streams/rivers and prairie wetlands, likely the result of reduced dilution and photolysis impacts. To document nontarget vegetation translocation dynamics, the macrophyte Lemna gibba was exposed to varying CLO concentrations for 12 h within a laboratory setting. Quantification of CLO uptake occurred every 4 h. Finally, trophic level impacts were investigated by exposing the water lily aphid Rhopalosiphum nymphaeae to L. gibba grown in CLO-contaminated water. Aphids lived and fed on contaminated duckweed for 48 h, after which an LC50 of 8.71 ng g of the plant tissue-1 was calculated. While uptake of CLO by duckweed was rapid, aphids are unlikely to suffer acute mortality at previously reported environmental CLO concentrations. Future research should expand on this work with other macrophytes/herbivores and longer-term experiments to more realistically mimic chronic field exposures.

Effect of Seed Blends and Soil-Insecticide on Western and Northern Corn Rootworm Emergence from mCry3A+eCry3.1Ab Bt Maize.

Seed blends containing various ratios of transgenic Bt maize (Zea mays L.) expressing the mCry3A+eCry3.1Ab proteins and non-Bt maize (near-isoline maize) were deployed alone and in combination with a soil applied pyrethroid insecticide (Force CS) to evaluate the emergence of the western corn rootworm, Diabrotica virgifera virgifera LeConte, in a total of nine field environments across the Midwestern United States in 2010 and 2011. Northern corn rootworm, Diabrotica barberi Smith & Lawrence emergence was also evaluated in four of these environments. Both western and northern corn rootworm beetle emergence from all Bt treatments was significantly reduced when compared with beetle emergence from near-isoline treatments. Averaged across all environments, western corn rootworm beetle emergence from 95:5, 90:10, and 80:20 seed blend ratios of mCry3A+eCry3.1Ab: near-isoline were 2.6-, 4.2-, and 6.7-fold greater than that from the 100:0 ratio treatment. Northern corn rootworm emergence from the same seed blend treatments resulted in 2.8-, 3.2-, and 4.2-fold more beetles than from the 100:0 treatment. The addition of Force CS (tefluthrin) significantly reduced western corn rootworm beetle emergence for each of the three treatments to which it was applied. Force CS also significantly delayed the number of days to 50% beetle emergence in western corn rootworms. Time to 50% beetle emergence in the 100% mCry3A+eCry3.1Ab treatment with Force CS was delayed 13.7 d when compared with western corn rootworm beetle emergence on near-isoline corn. These data are discussed in terms of rootworm resistance management.

Effects of common co-occurring pesticides (a neonicotinoid and fungicide) on honey bee colony health in a semi-field study.

Multiple stressors are linked to declines of insects and important pollinators, such as bees. Recently, interactive effects of multiple agrochemicals on bees have been highlighted, including fungicides, which increase toxicity of neonicotinoid insecticides. Here, we use a semi-field study across two seasons in controlled foraging tunnels to test the effects of a field application of a commercial fungicide product with two active ingredients (pyraclostrobin and metconazole) applied at label rates. We also examine its interactive effects with the neonicotinoid insecticide clothianidin, at a conservative field-realistic dose of 2.23 ppb, on 48 honey bee colonies. We found combined effects of pesticide exposure, including additive 2.93-fold increases in mortality, and an additional effect of increased infestation levels of the ectoparasitic mite, Varroa destructor. Pesticide treatments also reduced colony activity, reduced colony weight, and increased sugar consumption of whole colonies. These findings indicate that typical sublethal exposure levels to common, co-occurring agrochemicals in the field significantly affect the health of whole honey bee colonies, highlighting an unintended consequence of increasing pesticide applications.

Implementing IPM in crop management simultaneously improves the health of managed bees and enhances the diversity of wild pollinator communities.

Impacts of insecticide use on the health of wild and managed pollinators have been difficult to accurately quantify in the field. Existing designs tend to focus on single crops, even though highly mobile bees routinely forage across crop boundaries. We created fields of pollinator-dependent watermelon surrounded by corn, regionally important crops in the Midwestern US. These fields were paired at multiple sites in 2017-2020 with the only difference being pest management regimes: a standard set of conventional management (CM) practices vs. an integrated pest management (IPM) system that uses scouting and pest thresholds to determine if/when insecticides are used. Between these two systems we compared the performance (e.g., growth, survival) of managed pollinators-honey bees (Apis mellifera), bumble bees (Bombus impatiens)-along with the abundance and diversity of wild pollinators. Compared to CM fields, IPM led to higher growth and lower mortality of managed bees, while also increasing the abundance (+ 147%) and richness (+ 128%) of wild pollinator species, and lower concentrations of neonicotinoids in the hive material of both managed bees. By replicating realistic changes to pest management, this experiment provides one of the first demonstrations whereby tangible improvements to pollinator health and crop visitation result from IPM implementation in agriculture.

Removing neonicotinoid seed treatments has negligible effects on refuge function and crop protection in transgenic maize targeting western corn rootworm (Coleoptera: Chrysomelidae).

Nearly all maize seed sold in the United States includes a neonicotinoid seed treatment (NST), meant to protect seedlings against early-season insect pests. For key pests, including western corn rootworm (Diabrotica virgifera virgifera LeConte) (D.v.v), insecticidal proteins derived from Bacillus thuringiensis (Bt) are expressed in plant tissues as alternatives to soil-applied insecticides. Insect resistance management (IRM) plans use non-Bt "refuges" to encourage survival of Bt-susceptible D.v.v., which maintains susceptible alleles in the population. In non-cotton producing regions, IRM guidelines require a minimum 5% blended refuge for maize expressing more than 1 trait targeting D.v.v. Prior work has shown that 5% blends yield insufficient proportions of refuge beetles to contribute reliably to IRM. Whether NSTs interfere with survivorship of refuge beetles is unknown. Our objective was to determine whether NSTs affect proportions of refuge beetles, and secondarily, to determine whether NSTs provide agronomic advantages over Bt seed alone. To reveal host plant type (i.e., Bt or refuge), we used a stable isotope (15N) to mark refuge plants in plots with 5% seed blends. To assess refuge performance between treatments, we compared proportions of beetles from respective natal hosts. In all site-years, NSTs showed inconsistent effects on proportions of refuge beetles. Treatment comparisons showed inconsistent agronomic benefits of NSTs when combined with Bt traits. Our results demonstrate that NSTs have a negligible impact on refuge performance and reinforces the assertion that 5% blends are serving little benefit for IRM. Plant stand and yield were not improved by NSTs.

Spatial distribution of Aphis glycines (Hemiptera: Aphididae): a summary of the suction trap network.

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is an economically important pest of soybean, Glycine max (L.) Merrill, in the United States. Phenological information of A. glycines is limited; specifically, little is known about factors guiding migrating aphids and potential impacts of long distance flights on local population dynamics. Increasing our understanding of A. glycines population dynamics may improve predictions of A. glycines outbreaks and improve management efforts. In 2005 a suction trap network was established in seven Midwest states to monitor the occurrence of alates. By 2006, this network expanded to 10 states and consisted of 42 traps. The goal of the STN was to monitor movement of A. glycines from their overwintering host Rhamnus spp. to soybean in spring, movement among soybean fields during summer, and emigration from soybean to Rhamnus in fall. The objective of this study was to infer movement patterns of A. glycines on a regional scale based on trap captures, and determine the suitability of certain statistical methods for future analyses. Overall, alates were not commonly collected in suction traps until June. The most alates were collected during a 3-wk period in the summer (late July to mid-August), followed by the fall, with a peak capture period during the last 2 wk of September. Alate captures were positively correlated with latitude, a pattern consistent with the distribution of Rhamnus in the United States, suggesting that more southern regions are infested by immigrants from the north.

Seeds of change: corn seed mixtures for resistance management and integrated pest management.

The use of mixtures of transgenic insecticidal seed and nontransgenic seed to provide an in-field refuge for susceptible insects in insect-resistance-management (IRM) plans has been considered for at least two decades. However, the U.S. Environmental Protection Agency has only recently authorized the practice. This commentary explores issues that regulators, industry, and other stakeholders should consider as the use of biotechnology increases and seed mixtures are implemented as a major tactic for IRM. We discuss how block refuges and seed mixtures in transgenic insecticidal corn, Zea mays L., production will influence integrated pest management (IPM) and the evolution of pest resistance. We conclude that seed mixtures will make pest monitoring more difficult and that seed mixtures may make IRM riskier because of larval behavior and greater adoption of insecticidal corn. Conversely, block refuges present a different suite of risks because of adult pest behavior and the lower compliance with IRM rules expected from farmers. It is likely that secondary pests not targeted by the insecticidal corn as well as natural enemies will respond differently to block refuges and seed mixtures.

Evaluating aggregation membership and copulatory success in the stink bug, Euschistus conspersus, using field and laboratory experiments.

The aggregation and mating behavior of the stink bug, Euschistus conspersus Uhler (Hemiptera: Pentatomidae) was investigated in a series of field and laboratory experiments. Marking of E. conspersus mating in aggregations in the field demonstrated that both sexes mate multiple times within aggregations on successive nights and with different partners, although ≈ 20% of the individuals of both sexes returned to aggregations but did not mate. Further analysis of mating patterns in caged aggregations revealed that heavy males and light females mated more frequently than their respective counterparts. Data are interpreted in terms of elucidating the function of benefits of multiple mating within aggregations for males and females.

Presence-Absence Sampling Plans for Stink Bugs (Hemiptera: Pentatomidae) in the Midwest Region of the United States.

Stink bugs represent an increasing risk to soybean production in the Midwest region of the United States. The current sampling protocol for stink bugs in this region is tailored for population density estimation and thus is more relevant to research purposes. A practical decision-making framework with more efficient sampling effort for management of herbivorous stink bugs is needed. Therefore, a binomial sequential sampling plan was developed for herbivorous stink bugs in the Midwest region. A total of 146 soybean fields were sampled across 11 states using sweep nets in 2016, 2017, and 2018. The binomial sequential sampling plans were developed using combinations of five tally thresholds at two proportion infested action thresholds to identify those that provided the best sampling outcomes. Final assessment of the operating characteristic curves for each plan indicated that a tally threshold of 3 stink bugs per 25 sweeps, and proportion infested action thresholds of 0.75 and 0.95 corresponding to the action thresholds of 5 and 10 stink bugs per 25 sweeps, provided the optimal balance between highest probability of correct decisions (≥ 99%) and lowest probability of incorrect decisions (≤ 1%). In addition, the average sample size for both plans (18 and 12 sets of 25 sweeps, respectively) was lower than that for the other proposed plans. The binomial sequential sampling plan can reduce the number of sample units required to achieve a management decision, which is important because it can potentially reduce risk/cost of management for stink bugs in soybean in this region.

A novel method for estimating soybean herbivory in western corn rootworm (Coleoptera: Chrysomelidae).

The western corn rootworm, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae), is the key pest of corn, Zea mays L., in North America. The western corn rootworm variant is a strain found in some parts of the United States that oviposits in soybean, Glycine max (L.) Merr., thereby circumventing crop rotation. Soybean herbivory is closely associated with oviposition; therefore, evidence of herbivory could serve as a proxy for rotation resistance. A digital image analysis method based on the characteristic green abdominal coloration of rootworm adults with soybean foliage in their guts was developed to estimate soybean herbivory rates of adult females. Image analysis software was used to develop and apply threshold limits that allowed only colors within the range that is characteristic of soybean herbivory to be displayed. When this method was applied to adult females swept from soybean fields in an area with high levels of rotation resistance, 54.3 +/- 2.1% were estimated to have fed on soybean. This is similar to a previously reported estimate of 54.8%. Results when laboratory-generated negative controls were analyzed showed an acceptably low frequency of false positives. This method could be developed into a management tool if user-friendly software were developed for its implementation. In addition, researchers may find the method useful as a rapid, standardized screen for measuring frequencies of soybean herbivory.

Dispersal and mating behavior of Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) in Bt cornfields.

Understanding of the mating and dispersal behavior of the western corn rootworm, Diabrotica virgifera virgifera (LeConte), is essential to predicting potential resistance to Bt corn technologies recently deployed to combat this pest. To quantify movement of male beetles, field studies were conducted during 2006 and 2007 in commercial Bt cornfields that included the Environmental Protection Agency-mandated 20% refuge acreage. Wing traps containing a single virgin female beetle were placed along transects throughout these fields. Male beetles were collected from the sticky bottoms of traps to compare the mean number of beetles captured at the different transect distances. Gut contents of each captured male were assayed with protein test strips to determine if the Bt protein (Cry3Bb1) was present. This provided an estimate of the distances traveled by males to reach virgin females. These data indicated that the mean number of males captured approximately 200 m from refuge corn was not significantly different than the mean number of males captured close to the refuge (< 22 m). Complementary field observations were conducted to determine how far newly emerged female beetles moved before mating and the time of day mating occurs. Results indicated that females do not move far from the site of emergence before mating and do not mate within the first 4 h of adult life. The implications of these data for movement and mating patterns of adult rootworms in Bt/refuge environments are discussed.

Likelihood of multiple mating in Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae).

We evaluated the mating ability of male western corn rootworms, Diabrotica virgifera virgifera Leconte (Coleoptera: Chrysomelidae), for 20 d after initial mating, using a series of laboratory experiments. Males mated an average of 2.24 times within 10 d after their first mating and averaged 0.15 matings between days 11 and 20 after their first mating. Because estimating the mating frequency in Bt/refuge cornfields is critical to developing robust and reliable models predicting Bt resistance development in this pest, we discuss how these laboratory findings may influence development and evaluation of current and future insect resistance management plans.

Community Composition, Abundance, and Phenology of Stink Bugs (Hemiptera: Pentatomidae) in Soybean in the North Central Region of the United States.

Stink bugs (Hemiptera: Pentatomidae) are an increasing threat to soybean (Fabales: Fabaceae) production in the North Central Region of the United States, which accounts for 80% of the country's total soybean production. Characterization of the stink bug community is essential for development of management programs for these pests. However, the composition of the stink bug community in the region is not well defined. This study aimed to address this gap with a 2-yr, 9-state survey. Specifically, we characterized the relative abundance, richness, and diversity of taxa in this community, and assessed phenological differences in abundance of herbivorous and predatory stink bugs. Overall, the stink bug community was dominated by Euschistus spp. (Hemiptera: Pentatomidae) and Chinavia hilaris (Say) (Hemiptera: Pentatomidae). Euschistus variolarius (Palisot de Beauvois) (Hemiptera: Pentatomidae), C. hilaris and Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) were more abundant in the northwestern, southeastern and eastern parts, respectively, of the North Central Region of the United States. Economically significant infestations of herbivorous species occurred in fields in southern parts of the region. Species richness differed across states, while diversity was the same across the region. Herbivorous and predatory species were more abundant during later soybean growth stages. Our results represent the first regional characterization of the stink bug community in soybean fields and will be fundamental for the development of state- and region-specific management programs for these pests in the North Central Region of the United States.

Spatial Patterns and Sequential Sampling Plans for Estimating Densities of Stink Bugs (Hemiptera: Pentatomidae) in Soybean in the North Central Region of the United States.

Stink bugs are an emerging threat to soybean (Fabales: Fabaceae) in the North Central Region of the United States. Consequently, region-specific scouting recommendations for stink bugs are needed. The aim of this study was to characterize the spatial pattern and to develop sampling plans to estimate stink bug population density in soybean fields. In 2016 and 2017, 125 fields distributed across nine states were sampled using sweep nets. Regression analyses were used to determine the effects of stink bug species [Chinavia hilaris (Say) (Hemiptera: Pentatomidae) and Euschistus spp. (Hemiptera: Pentatomidae)], life stages (nymphs and adults), and field locations (edge and interior) on spatial pattern as represented by variance-mean relationships. Results showed that stink bugs were aggregated. Sequential sampling plans were developed for each combination of species, life stage, and location and for all the data combined. Results for required sample size showed that an average of 40-42 sample units (sets of 25 sweeps) would be necessary to achieve a precision of 0.25 for stink bug densities commonly encountered across the region. However, based on the observed geographic gradient of stink bug densities, more practical sample sizes (5-10 sample units) may be sufficient in states in the southeastern part of the region, whereas impractical sample sizes (>100 sample units) may be required in the northwestern part of the region. Our findings provide research-based sampling recommendations for estimating densities of these emerging pests in soybean.

Neonicotinoid seed treatments of soybean provide negligible benefits to US farmers.

Neonicotinoids are the most widely used insecticides worldwide and are typically deployed as seed treatments (hereafter NST) in many grain and oilseed crops, including soybeans. However, there is a surprising dearth of information regarding NST effectiveness in increasing soybean seed yield, and most published data suggest weak, or inconsistent yield benefit. The US is the key soybean-producing nation worldwide and this work includes soybean yield data from 194 randomized and replicated field studies conducted specifically to evaluate the effect of NSTs on soybean seed yield at sites within 14 states from 2006 through 2017. Here we show that across the principal soybean-growing region of the country, there are negligible and management-specific yield benefits attributed to NSTs. Across the entire region, the maximum observed yield benefits due to fungicide (FST = fungicide seed treatment) + neonicotinoid use (FST + NST) reached 0.13 Mg/ha. Across the entire region, combinations of management practices affected the effectiveness of FST + NST to increase yield but benefits were minimal ranging between 0.01 to 0.22 Mg/ha. Despite widespread use, this practice appears to have little benefit for most of soybean producers; across the entire region, a partial economic analysis further showed inconsistent evidence of a break-even cost of FST or FST + NST. These results demonstrate that the current widespread prophylactic use of NST in the key soybean-producing areas of the US should be re-evaluated by producers and regulators alike.

Factors influencing mate choice in Euschistus conspersus Uhler (Heteroptera: Pentatomidae).

The patterns of mating and possible factors influencing mate choice in the consperse stink bug, Euschistus conspersus Uhler, were studied in a series of laboratory experiments. Males were found to transfer a significant percentage of their body mass during the initial mating. Mating was also found to reduce male longevity by 37.8% but had no significant effect on female longevity or fecundity. There was no evidence of male or female choice based on weight of potential mating partners. There was assortative mating based on experience, however, with males mating preferentially with virgin females and females preferring mated males when given the choice. The implications of these findings within the mating dynamics of this aggregating species are discussed.

Correction: Effects of clothianidin on aquatic communities: Evaluating the impacts of lethal and sublethal exposure to neonicotinoids.

[This corrects the article DOI: 10.1371/journal.pone.0174171.].

Correction: Translocation of the neonicotinoid seed treatment clothianidin in maize.

[This corrects the article DOI: 10.1371/journal.pone.0173836.].