A molecular approach to unravel trophic interactions between parasitoids and hyperparasitoids associated with pecan aphids.

Advances in molecular ecology can overcome many challenges in understanding host-parasitoid interactions. Genetic characterization of the key-players in systems helps to confirm species and identify trophic linkages essential for ecological service delivery by biological control agents; however, relatively few agroecosystems have been explored using this approach. Pecan production consists of a large tree perennial system containing an assortment of seasonal pests and natural enemies. As a first step to characterizing host-parasitoid associations in pecan food webs, we focus on aphid species and their parasitoids. Based on DNA barcoding of field-collected and reared specimens, we confirmed the presence of 3 species of aphid, one family of primary parasitoids, and 5 species of hyperparasitoids. By applying metabarcoding to field-collected aphid mummies, we were able to identify multiple species within each aphid mummy to unravel a complex food web of 3 aphids, 2 primary parasitoids, and upward of 8 hyperparasitoid species. The results of this study demonstrate that multiple hyperparasitoid species attack a single primary parasitoid of pecan aphids, which may have negative consequences for successful aphid biological control. Although further research is needed on a broader spatial scale, our results suggest multiple species exist in this system and may suggest a complex set of interactions between parasitoids, hyperparasitoids, and the 3 aphid species. This was the first time that many of these species have been characterized and demonstrates the application of novel approaches to analyze the aphid-parasitoid food webs in pecans and other tree crop systems.

A Review of Successes and Impeding Challenges of IoT-Based Insect Pest Detection Systems for Estimating Agroecosystem Health and Productivity of Cotton.

Using artificial intelligence (AI) and the IoT (Internet of Things) is a primary focus of applied engineering research to improve agricultural efficiency. This review paper summarizes the engagement of artificial intelligence models and IoT techniques in detecting, classifying, and counting cotton insect pests and corresponding beneficial insects. The effectiveness and limitations of AI and IoT techniques in various cotton agricultural settings were comprehensively reviewed. This review indicates that insects can be detected with an accuracy of between 70 and 98% using camera/microphone sensors and enhanced deep learning algorithms. However, despite the numerous pests and beneficial insects, only a few species were targeted for detection and classification by AI and IoT systems. Not surprisingly, due to the challenges of identifying immature and predatory insects, few studies have designed systems to detect and characterize them. The location of the insects, sufficient data size, concentrated insects on the image, and similarity in species appearance are major obstacles when implementing AI. Similarly, IoT is constrained by a lack of effective field distance between sensors when targeting insects according to their estimated population size. Based on this study, the number of pest species monitored by AI and IoT technologies should be increased while improving the system's detection accuracy.

Toxicity of Photorhabdus luminescens and Xenorhabdus bovienii bacterial metabolites to pecan aphids (Hemiptera: Aphididae) and the lady beetle Harmonia axyridis (Coleoptera: Coccinellidae).

Toxicity of the metabolites of two bacteria, Photorhabdus luminescens and Xenorhabdus bovienii, symbionts of entomopathogenic nematodes, were tested in the laboratory against the multicolored Asian lady beetle, Harmonia axyridis, the black pecan aphid, Melanocallis caryaefoliae, and the blackmargined aphid, Monellia caryella. Bacterial broth prepared from both P. luminescens and X. bovienii demonstrated high levels of toxicity equivalent to the pyrethroid insecticide bifenthrin and caused higher insect mortality than tryptic soy broth plus yeast extract (TSY) (blank control) against M. caryella; broth culture of P. luminescens was more effective than TSY against M. caryaefoliae. At the levels tested, the metabolites were not toxic to H. axyridis.

Discovery of Aphis ruborum (Hemiptera: Aphididae) and Aphelinus varipes (Hymenoptera: Aphelinidae) on Cultivated Strawberry in Mississippi, USA.

An adventive aphid and novel host-parasitoid association from cultivated strawberry (Fragaria × ananessa Duch. cv. Chandler; Fragaria × ananessa Duch. cv. Camarosa) in Mississippi, USA are reported herein. The aphid, first detected in high tunnel cultivation, was found predominately on newly emerged, not fully developed leaflets of daughter plants in the Fall of 2016. By 2017, aphids and their associated mummies were observed on fully developed leaflets on mother plants of both cultivars. The aphid was identified as Aphis ruborum (Börner & Schilder) using morphology and DNA barcoding studies. In addition, DNA barcoding identified parasitoid adults emerging from aphid mummies as two cryptic species, Aphelinus varipes (Foerster) and Aphelinus albipodus Hayat and Fatima. Occurrence of A. ruborum in Mississippi represents a new state record and the eastern-most established record in the United States. The A. ruborum - A. varipes or A. albipodus host-parasitoid association is reported for the first time anywhere in the world.

Predator-prey trophic relationships in response to organic management practices.

A broad range of environmental conditions likely regulate predator-prey population dynamics and impact the structure of these communities. Central to understanding the interplay between predator and prey populations and their importance is characterizing the corresponding trophic interactions. Here, we use a well-documented molecular approach to examine the structure of the community of natural enemies preying upon the squash bug, Anasa tristis, a herbivorous cucurbit pest that severely hinders organic squash and pumpkin production in the United States. Primer pairs were designed to examine the effects of organic management practices on the strength of these trophic connections and link this metric to measures of the arthropod predator complex density and diversity within an experimental open-field context. Replicated plots of butternut squash were randomly assigned to three treatments and were sampled throughout a growing season. Row-cover treatments had significant negative effects on squash bug and predator communities. In total, 640 predators were tested for squash bug molecular gut-content, of which 11% were found to have preyed on squash bugs, but predation varied over the season between predator groups (coccinellids, geocorids, nabids, web-building spiders and hunting spiders). Through the linking of molecular gut-content analysis to changes in diversity and abundance, these data delineate the complexity of interaction pathways on a pest that limits the profitability of organic squash production.

Predator interference alters foraging behavior of a generalist predatory arthropod.

Interactions between predators foraging in the same patch may strongly influence patch use and functional response. In particular, there is continued interest in how the magnitude of mutual interference shapes predator-prey interactions. Studies commonly focus on either patch use or the functional response without attempting to link these important components of the foraging puzzle. Predictions from both theoretical frameworks suggest that predators should modify foraging efforts in response to changes in feeding rate, but this prediction has received little empirical attention. We study the linkage between patch departure rates and food consumption by the hunting spider, Pardosa milvina, using field enclosures in which prey and predator densities were manipulated. Additionally, the most appropriate functional response model was identified by fitting alternative functional response models to laboratory foraging data. Our results show that although prey availability was the most important determinant of patch departure rates, a greater proportion of predators left enclosures containing elevated predator abundance. Functional response parameter estimation revealed significant levels of interference among predators leading to lower feeding rates even when the area allocated for each predator was kept constant. These results suggest that feeding rates determine patch movement dynamics, where interference induces predators to search for foraging sites that balance the frequency of agonistic interactions with prey encounter rates.

From weeds to natural enemies: implications of weed cultivation and biopesticides for organic onion production.

Weed management is challenging for vegetable crops that are highly sensitive to weed competition, such as onions. Thrips (Thysanoptera: Thripidae) are major insect pests of onions, causing damage through feeding, and vectoring bacterial pathogens causing bulb rot. Both thrips and their associated pathogens are known to survive on many weed species in onion growing regions. Combining weeding with biopesticides may synergistically manage thrips and reduce disease prevalence. However, disturbances from weeding may negatively impact natural enemies. We estimated the effects of organic weed management and biopesticides on weed density, thrips and natural enemy activity, disease severity, and yield. The experiment was a randomized complete block design, with 4 replications of each weeding (control, tine-weeded twice, tine-weeded 4 times, and hand-weeded) and biopesticide (control, OxiDate 2.0, Serenade) combination. Arthropods were monitored using yellow sticky cards, and weed counts, marketable yield, and bulb rot prevalence were estimated. Hand-weeding resulted in the lowest weed density and thrips abundance. Additionally, hand-weeding produced a 9× higher yield compared to all other treatments. Significant interactions were observed between tine-weeding and biopesticide treatments on the prevalence of bulb rot. Natural enemy abundance was slightly negatively impacted by weeding, dependent on the year. DNA metabarcoding results showed high parasitoid diversity in this onion system and high numbers of reads for multiple genera containing important known biological control agents. Our study suggests hand-weeding is necessary in the southeast for maximum onion yield. Future research should focus on exploring the impact of management on natural enemy communities in onion systems on a large scale.

Warmer temperatures trigger insecticide-associated pest outbreaks.

BACKGROUND: Rising global temperatures are associated with emerging insect pests, reflecting earlier and longer insect activity, faster development, more generations per year and changing species' ranges. Insecticides are often the first tools available to manage these new threats. In the southeastern US, sweet potato whitefly (Bemisia tabaci) has recently become the major threat to vegetable production. We used data from a multi-year, regional whitefly monitoring network to search for climate, land use, and management correlates of whitefly activity. RESULTS: Strikingly, whiteflies were detected earlier and grew more abundant in landscapes with greater insecticide use, but only when temperatures were also relatively warm. Whitefly outbreaks in hotter conditions were not associated with specific active ingredients used to suppress whiteflies, which would be consistent with a regional disruption of biocontrol following sprays for other pests. In addition, peak whitefly detections occurred earlier in areas with more vegetable production, but later with more cotton production, consistent with whiteflies moving among crops. CONCLUSION: Altogether, our findings suggest possible links between warmer temperatures, more abundant pests, and frequent insecticide applications disrupting biological control, though this remains to be explicitly demonstrated. Climate-initiated pesticide treadmills of this type may become an increasingly common driver of emerging pest outbreaks as global change accelerates. © 2023 Society of Chemical Industry.

Low Incidence of Avian Predation on the Brown Marmorated Stink Bug, Halyomorpha halys (Hemiptera: Pentatomidae), in Southeastern Orchard Systems.

In many agroecosystems, brown marmorated stink bugs (Halyomorpha halys) (Hemiptera: Pentatomidae) are polyphagous pests that cause significant economic losses to numerous crops every year. Insectivorous birds may provide a means of sustainable predation of invasive pests, such as H. halys. In forest margins surrounding peach, pecan, and interplanted peach-pecan orchards, we monitored H. halys populations with pheromone-baited traps, mist-netted birds, and collected avian fecal samples for molecular gut content analysis. We screened 257 fecal samples from 19 bird species for the presence of H. halys DNA to determine whether birds provide the biological control of this pest. Overall, we found evidence that four birds from three species consumed H. halys, including Northern cardinal (Cardinalis cardinalisis), Tufted titmouse (Baeolophus bicolor), and Carolina wren (Thryothorus ludovicianus). Halyomorpha halys captured in traps increased over time but did not vary by orchard type. Although incidence of predation was low, this may be an underestimate as a result of our current avian fecal sampling methodology. Because birds are members of the broader food web, future studies are needed to understand avian ecosystem services, especially in terms of pest control, including H. halys and other pest species.

Diet composition and diversity does not explain fewer, smaller urban nestlings.

The reproductive success of animals breeding in cities is often lower compared to counterparts that inhabit rural, suburban, and peri-urban areas. Urban dwelling may be especially costly for offspring development and survival. Diet composition and diversity may underlie factors that lead to lower fitness, particularly if prey abundance and quality decline in modified environments. Moreover, breeding success may change over the course of a season, an effect that may be augmented in urban areas. In this study, we tested the hypothesis that habitat and date affected nestling house wren (Troglodytes aedon) body condition and survival, and examined whether diet explained differences in nestling success. We monitored urban and rural populations of house wrens breeding in nest boxes, and tested whether clutch size, nestling survivorship, and nestling body condition varied by habitat or by date, and then characterized the diet of a subset of nestlings with DNA metabarcoding of fecal samples. Urbanization had clear impacts on house wren nestling fitness: urban broods contained fewer, smaller nestlings. Early nestling survival decreased as the breeding season progressed, and this effect was more pronounced in the urban population. However, the diets of urban and rural nestlings were similar and did not explain differences in body condition. Instead, across populations, diet changed with date, becoming less diverse, with fewer Lepidoptera and more Orthoptera. Regardless of habitat, adult house wrens provide nestlings with similar types of foods, but other factors, such as quantity or quality of prey delivered, may lead to fitness disparities between urban and rural nestlings.

First Documented Wild Population of the "Hunter Fly", Coenosia attenuata Stein (Diptera: Muscidae) in North America.

Coenosia attenuata is a member of the tigrina-group of Coenosia (sensu Hennig 1964) and is a capable generalist predator in its larval and adult stages. C. attenuata is common in greenhouses worldwide, however, there are few documented cases of its presence in the wild. Here, we estimated C. attenuata presence in the southeastern USA peach orchards using pan traps. Over two years, a total of 717 specimens were collected from both commercially managed and fungicide-only managed peach orchards. C. attenuata is a known biological control agent in artificial greenhouse settings, but its impact on pest species in the wild is still unknown. For the first time in North America, we document an established wild population of C. attenuata, provide an overview of basic identification, and review potential benefits for biological control.

Rapid PCR-based method for herbivore dietary evaluation using plant-specific primers.

Polyphagous pests cause significant economic loss worldwide through feeding damage on various cash crops. However, their diets in agricultural landscapes remain largely unexplored. Pest dietary evaluation in agricultural fields is a challenging task currently approached through visual observation of plant feeding and microscopic identification of semi-digested plant material in pest's guts. While molecular gut content analysis using metabarcoding approaches using universal primers (e.g., rbcl and trnL) have been successful in evaluating polyphagous pest diet, this method is relatively costly and time-consuming. Hence, there is a need for a rapid, specific, sensitive, and cost-effective method to screen for crops in the gut of pests. This is the first study to develop plant-specific primers that target various regions of their genomes, designed using a whole plant genome sequence. We selected Verticillium wilt disease resistance protein (VE-1) and pathogenesis related protein-coding genes 1-5 (PR-1-5) as our targets and designed species-specific primers for 14 important crops in the agroecosystems. Using amplicon sizes ranging from 115 to 407 bp, we developed two multiplex primer mixes that can separate nine and five plant species per PCR reaction, respectively. These two designed primer mixes provide a rapid, sensitive and specific route for polyphagous pest dietary evaluation in agroecosystems. This work will enable future research to rapidly expand our knowledge on the diet preference and range of crops that pests consume in various agroecosystems, which will help in the redesign and development of new crop rotation regimes to minimize polyphagous pest pressure and damage on crops.

Parasitoid Communities in the Variable Agricultural Environments of Blueberry Production in the Southeastern United States.

In blueberry crops, there are multiple pest species, and some of those can be suppressed by natural enemies including parasitoid wasps and predators. Parasitoid wasps occur within the environment often tracking pest species for food resources to complete their lifecycle. These small wasps are also sensitive to agricultural environments including agrichemicals, habitat availability, and climate. We investigated how the structure of parasitoid communities varied between organic and conventional blueberry systems, and how the communities of these parasitoids varied within field spatial scales (forested border vs edge vs interior). With the lower intensity of agricultural interventions occurring in organic systems and forested borders, we predicted more stable parasitoid numbers that would be insulated from predicted climate variability. In our study, parasitoids were observed in low abundance in each cropping system, with community structure dependent on both management practice and field position. Unmanaged blueberry fields and forested field borders contained more parasitoid families, and in conventional systems, we saw fewer families present in the field interior as compared to field borders. In this first study to characterize Southern parasitoid communities in blueberry production systems, we observed over 50 genera of parasitoids, with a few dominant families (Braconidae and Ichneumonidae) that would contribute to biological control in blueberry systems. Overall, we captured few parasitoids, which indicates a potential vulnerability in biological control, and the need for further research using other sampling techniques to better understand these parasitoid communities.

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.

Identifying Molecular-Based Trophic Interactions as a Resource for Advanced Integrated Pest Management.

Biodiversity is an essential attribute of sustainable agroecosystems. Diverse arthropod communities deliver multiple ecosystem services, such as biological control, which are the core of integrated pest management programs. The molecular analysis of arthropod diets has emerged as a new tool to monitor and help predict the outcomes of management on the functioning of arthropod communities. Here, we briefly review the recent molecular analysis of predators and parasitoids in agricultural environments. We focus on the developments of molecular gut content analysis (MGCA) implemented to unravel the function of community members, and their roles in biological control. We examine the agricultural systems in which this tool has been applied, and at what ecological scales. Additionally, we review the use of MGCA to uncover vertebrate roles in pest management, which commonly receives less attention. Applying MGCA to understand agricultural food webs is likely to provide an indicator of how management strategies either improve food web properties (i.e., enhanced biological control), or adversely impact them.

Opportunistic predator prefers habitat complexity that exposes prey while reducing cannibalism and intraguild encounters.

Structural features of habitat are known to affect the density of predators and prey, and it is generally accepted that complexity provides some protection from the environment and predators but may also reduce foraging success. A next step in understanding these interactions is to decouple the impacts of both spatial and trophic ingredients of complexity to explicitly explore the trade-offs between the habitat, its effects on foraging success, and the competition that ensues as predator densities increase. We quantified the accumulation of spiders and their prey in habitat islands with different habitat complexities created in the field using natural plants, plant debris and plastic plant mimics. Spiders were observed at higher densities in the complex habitat structure composed of both live plants and thatch. However, the numerically dominant predator in the system, the wolf spider Pardosa milvina, was observed at high densities in habitat islands containing plastic mimics of plants and thatch. In a laboratory experiment, we examined the interactive effects of conspecific density and habitat on the prey capture of P. milvina. Thatch, with or without vertical plant structure, reduced prey capture, but the plastic fiber did not. Pairwise interactions among spiders reduced prey capture, but this effect was moderated by thatch. Taken together, these experiments highlight the flexibility of one important predator in the food web, where multiple environmental cues intersect to explain the role of habitat complexity in determining generalist predator accumulation.

Plant-animal interactions between carnivorous plants, sheet-web spiders, and ground-running spiders as guild predators in a wet meadow community.

Plant-animal interactions are diverse and widespread shaping ecology, evolution, and biodiversity of most ecological communities. Carnivorous plants are unusual in that they can be simultaneously engaged with animals in multiple mutualistic and antagonistic interactions including reversed plant-animal interactions where they are the predator. Competition with animals is a potential antagonistic plant-animal interaction unique to carnivorous plants when they and animal predators consume the same prey.The goal of this field study was to test the hypothesis that under natural conditions, sundews and spiders are predators consuming the same prey thus creating an environment where interkingdom competition can occur.Over 12 months, we collected data on 15 dates in the only protected Highland Rim Wet Meadow Ecosystem in Kentucky where sundews, sheet-web spiders, and ground-running spiders co-exist. One each sampling day, we attempted to locate fifteen sites with: (a) both sheet-web spiders and sundews; (b) sundews only; and (c) where neither occurred. Sticky traps were set at each of these sites to determine prey (springtails) activity-density. Ground-running spiders were collected on sampling days. DNA extraction was performed on all spiders to determine which individuals had eaten springtails and comparing this to the density of sundews where the spiders were captured.Sundews and spiders consumed springtails. Springtail activity-densities were lower, the higher the density of sundews. Both sheet-web and ground-running spiders were found less often where sundew densities were high. Sheet-web size was smaller where sundew densities were high.The results of this study suggest that asymmetrical exploitative competition occurs between sundews and spiders. Sundews appear to have a greater negative impact on spiders, where spiders probably have little impact on sundews. In this example of interkingdom competition where the asymmetry should be most extreme, amensalism where one competitor experiences no cost of interaction may be occurring.

Can Generalist Predators Control Bemisia tabaci?

The whitefly, Bemisia tabaci, has developed resistance to many insecticides, renewing interest in the biological control of this global pest. Generalist predators might contribute to whitefly suppression if they commonly occur in infested fields and generally complement rather than interfere with specialized natural enemies. Here, we review literature from the last 20 years, across US cropping systems, which considers the impacts of generalist predators on B. tabaci. Laboratory feeding trials and molecular gut content analysis suggest that at least 30 different generalist predator species willingly and/or regularly feed on these whiteflies. Nine of these predators appear to be particularly impactful, and a higher abundance of a few of these predator species has been shown to correlate with greater B. tabaci predation in the field. Predator species often occupy complementary feeding niches, which would be expected to strengthen biocontrol, although intraguild predation is also common and might be disruptive. Overall, our review suggests that a bio-diverse community of generalist predators commonly attacks B. tabaci, with the potential to exert substantial control in the field. The key challenge will be to develop reduced-spray plans so that generalist predators, and other more specialized natural enemies, are abundant enough that their biocontrol potential is realized.

Natural Enemy Abundance in Southeastern Blueberry Agroecosystems: Distance to Edge and Impact of Management Practices.

Natural enemies are valuable components of agroecosystems as they provide biological control services to help regulate pest populations. Promoting biocontrol services can improve sustainability by decreasing pesticide usage, which is a major challenge for the blueberry industry. Our research is the first to compare natural enemy populations in managed (conventional and organic) and unmanaged blueberry systems, in addition to the effects of non-crop habitat. We conducted our study in 10 blueberry orchards during the growing season across the major blueberry producing counties in Georgia, United States. To estimate the spatial distribution of natural enemies, we conducted suction sampling at three locations in each orchard: within the forested border, along the edge of blueberry orchard adjacent to forested border, and within the interior of the blueberry orchard. Natural enemies maintained higher abundance over the season in unmanaged areas when compared with organic or conventional production systems. In the conventional orchards, natural enemies were more abundant in the surrounding non-crop area compared with the interior of the orchard. Populations were more evenly distributed in less intensive systems (organic and unmanaged). Our results indicate spatial structure in natural enemy populations is related to management practice, and less intensive management can retain higher abundance of natural enemies in blueberry systems. Considerations must be made towards promoting ecologically based management practices to sustain natural enemy populations and potentially increase the delivery of biological control services.