Entomology Theses and Dissertations

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    TREE GENETICS AND GREENSPACE MANAGEMENT INTENSITY INFLUENCE URBAN TREE INSECT COMMUNITIES, DAMAGE, AND FOLIAR TRAITS
    (2024) Perry, Eva Emma; Burghardt, Karin T; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
    Trees are essential to well-functioning urban systems, providing services that benefit humans and wildlife. For example, arthropods that use trees in cities perform key roles in the urban food web as both prey and predators, but they can also be vulnerable to environmental stressors associated with cities. Previous work documents broad patterns in arthropod communities associated with management practice gradients in urban areas. How these patterns relate to changes in tree genetic background across management types remains a largely unexplored topic. To disentangle the genetic and management associated effects on arboreal insect abundance, communities, and foliar damage, I repeatedly sampled trees of known genetic relatedness for two commonly planted tree species: Acer rubrum (n = 65), and its non-native congener Acer platanoides (n = 71), in June and August of 2023 and 2024. I systematically selected about 3 individual trees growing in four human management intensity categories (street trees, parks and residential yards, urban forest patches, or rural forests) for each of 5 genetic lineages per tree species. I used vacuum sampling to collect mobile arthropods from the lower canopy of each focal tree in June and August of 2023 and 2024, and identified samples to order. I also assessed insect and systemic foliar damage, gall abundance, and select physiological traits in August 2024. I found the general trend of increasing total arthropod abundance with increasing management intensity. However, management effects differed across genetic background with almost ubiquitous interactions between management type and genetic lineage. The most dominant group of insects found on study trees belonged to the order Hemiptera. This group of primarily herbivorous piercing/sucking insects were the primary drivers of these overarching abundance patterns. Spiders, which were the most abundant primarily predatory arthropod order, exhibited the opposite pattern, increasing in overall abundance in the later season, decreasing with increasing management intensity, and generally not responding to tree genetic lineage. In 2024, increasing management intensity negatively affected cumulative insect herbivore damage and gall abundance, and did not vary by genetic lineage. Gall formers were found only on native Acer rubrum, with no galls sampled from the non-native A. platanoides. In contrast, systemic foliar damage did not change with management, and only varied by tree genetic lineage for Acer platanoides. Foliar photosynthetic traits’ variance by management intensity or tree genetic lineage was species dependent; A. rubrum traits varied by tree genetic lineage, while A. platanoides traits varied by management intensity. Overall, my results suggest that tree genetic background plays an important role in mediating management effects on insect populations, particularly for piercing-sucking herbivorous species, but genetic background’s effect on other metrics such as foliar damage and traits may be species-specific. Further studies should be sure to consider the structure of genetic populations when describing patterns of insect use. Results of this thesis will serve to inform best practices for urban tree management and pest mitigation, as cities work to maintain and increase urban canopy cover.
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    THE EFFECTS OF LEAF LITTER MANAGEMENT PRACTICES ON OVERWINTERING INSECT COMMUNITIES AND ECOSYSTEM FUNCTION: IMPACTS AND APPLICATIONS IN RESIDENTIAL LANDSCAPES
    (2024) Ferlauto, Max; Burghardt, Karin T; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
    Fallen leaf management is a widespread landscaping practice in urban areas that not only influences soil health but also affects the overwintering individuals of subsequent year's aboveground arthropod communities. There has been considerable public and scientific interest in the ecological effects of this disturbance, yet little experimental research making it difficult to provide evidence-based landscaping recommendations to stakeholders. This dissertation aims to narrow this knowledge gap, provide information for the creation of best management practices, and encourage further research on this critical topic. In Chapter 2, I compare spring arthropod emergence in residential areas where fallen leaves were removed or retained across different levels of maintenance intensity. In Chapter 3, I focus on the legacies of long-term leaf removal to soil organic carbon dynamics. And in Chapter 4, I examine the efficacy of alternative leaf management practices—such as shredding and leaf piling—on soil microclimates, arthropod biodiversity, and decomposition rates while exploring if tree canopy diversity mitigated impacts to these ecosystem functions. The results of these three experimental studies were consistent across years and habitat types. Leaf removal reduced the spring emergence of Lepidoptera by about 35-45% and reduced spiders by about 50-67%, altered parasitic wasp community composition, reduced soil moisture and temperature buffering, and ultimately led to legacy effects in the soil of reduced decomposition and soil organic carbon. The context in which leaves were managed also mattered, as unique resources attracted overwintering arthropods more when they were scarce in the environment. Despite the potential for high plant diversity in leaf-managed areas to create ecosystem traps for arthropods, tree diversity actually mitigated some negative effects of fallen leaf disturbance to ecosystem function. Overall, I find that some practices like leaf removal and shredding degrade ecosystem processes while others like piling leaves and planting a diverse tree canopy can support ecosystem services. This dissertation is the first to quantify the ecological impacts of leaf management as an urban disturbance and addresses critical questions necessary for developing urban best management practices.
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    THE EVOLUTIONARY TRAJECTORY OF METARHIZIUM ROBERTSII ENDOPHYTIC CAPABILITY AND ENTOMOPATHOGENICITY
    (2024) Sheng, Huiyu; St. Leger, Raymond; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
    Metarhizium fungi are a keystone genus of soil-inhabiting ascomycetes providing essential ecosystem services as saprotrophs, plant symbionts and insect pathogens, among other roles. Recent studies have looked at how Metarhizium niches have evolved and shaped genome evolution over large time scales within the Metarhizium genus. This dissertation uses Metarhizium robertsii (M. robertsii) as a model to explore the evolution of its dual roles as an entomopathogen and endophyte by examining phenotypic and genomic differences among eight closely related strains. The study found that early diverged strains, characterized by slow germination on insect cuticles, low virulence, and extensive sporulation, exhibit a biotrophic lifestyle, systemically colonizing living hosts. In contrast, recently diverged strains exhibited rapid germination, high virulence, and reduced sporulation, indicating a shift towards a necrotrophic lifestyle. The study highlighted the influence of host immune responses in shaping M. robertsii-insect interactions, and showed that strong insect virulence correlated with better colonization of plant roots. Comparative genomics revealed that recently diverged strains expanded a small number of gene families related to gene expression as well as carbohydrate-degrading enzymes and proteases enhancing metabolic capabilities, insect virulence, and endophytic potential. Some early diverged strains exhibited high Repeat-Induced Point mutation activity, suggesting cryptic sexual reproduction in their evolutionary past. Overall, M. robertsii strains maintained a conserved genome with similar protein family sizes, with differences in gene expression patterns driving their varied lifestyles. This research provides new insights into M. robertsii’s recent co-evolution with plants and insects, highlighting the importance of understanding the ecological and evolutionary dynamics of these interactions for optimizing its use in sustainable agriculture.
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    EXAMINING INTERACTIONS AMONG FUNGAL INFECTION, SLEEP, AND HOST DEFENSE IN POPULATIONS OF WORLDWIDE, SLEEP INBRED PANEL, AND MUTANT DROSOPHILA MELANOGASTER
    (2024) Nan, Mintong; St. Leger, Raymond; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
    Previous studies with mutant Drosophila melanogaster lines and the Drosophila Genetic Reference Panel (DGRP) reveal substantial variation in susceptibility to infection with Metarhizium anisopliae strain Ma549. These differences likely arise from variations in immunity, physiology, and behavior, yet the role of selection pressures in maintaining these disparities remains understudied. Using global Drosophila populations, the Sleep Inbred Panel (SIP), and sleep-deprived mutants, we investigated the interactions among fungal infection, sleep, and host defense. Testing 14,957 male and 15,287 female flies from 43 lines across 28 locations, we found that resistance to Ma549 correlates with latitudinal gradients in sleep duration, temperature, and humidity. Tropical populations may exhibit stronger defenses due to fungal diversity; however, the most disease-resistant males were also more susceptible to desiccation, indicating trade-offs between abiotic stress and disease resistance. Longer-sleeping males and virgin flies survived infections longer, and increased daytime sleep post-infection was particularly protective in resistant flies. These findings suggest that sleep and disease resistance are interrelated traits possibly shaped by clinal evolution. Using 10,917 males and 11,166 females selected for extreme long or short nighttime sleep duration, we found that short-sleepers, despite having fragmented sleep when healthy, outlived long-sleepers after Ma549 infection. Resistance differences were sex-specific: males were more resistant among short-sleepers, while females showed higher resistance among long-sleepers. Daytime sleep bout numbers correlated with dimorphic disease resistance. Additionally, Ma549 infection increased daytime sleep in both short- and long-sleepers, with short-sleeping males nearly matching long-sleepers in sleep duration post-infection. Virgins, regardless of sleep status, slept more and survived infection longer, indicating that sleep traits, sex, and mating status are closely linked to disease resistance. The study highlights that circadian rhythms influence sleep and immunity, with the sleep-deprived Shmns mutant failing to undergo sickness sleep and succumbing quickly to infection. Mutants with disrupted circadian rhythms (PER and CLK) also showed impaired sickness sleep; however, only the per gene offered protection against disease, while the Clk mutant had increased survival. Independent of mutant status, males slept more than females, and virgins slept more than mated flies, emphasizing the significance of circadian rhythms in sleep and disease resistance.
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    MECHANISMS REGULATING GREENHOUSE GAS EMISSIONS AND SOIL CARBON STORAGE IN MID-ATLANTIC COASTAL PLAIN WETLANDS
    (2024) Stewart, Graham; Palmer, Margaret; Williams, Michael; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
    Wetlands are key components of the global carbon (C) cycle, storing significant amounts of C while emitting methane (CH4), a greenhouse gas. As wetland restoration emerges as a potential climate mitigation strategy, understanding the factors that influence wetland greenhouse gas exchange across land uses is essential for aligning management with ecology and biogeochemistry. This dissertation investigates variability in soil organic carbon (SOC) storage and CH4 flux in mid-Atlantic Coastal Plain wetlands, focusing on the roles of hydrology, vegetation, and land-use history in shaping underlying ecosystem processes.In Chapter 1, I surveyed SOC stocks across neighboring least-disturbed wetlands with similar vegetation and hydrogeomorphology and found substantial variation. Hydrologic regimes and relative topography partially explained variability, highlighting the importance of landscape heterogeneity in determining wetland C storage capacity. In Chapter 2, I measured CH4 fluxes across five dominant vegetation patch types in a freshwater wetland using a multi-scale approach. I found that vegetation patches had distinct CH4 signals throughout the growing season, likely driven by differences in the mechanisms that regulate fluxes. The magnitude of the CH4 source was linked to patch identity, suggesting that CH4 fluxes were properties of patch types, and that a patch-explicit representation may be needed for modeling and estimating wetland greenhouse gas exchange. In Chapter 3, I explored the temporal dynamics of CH4 flux across wetlands with different land-use histories, identifying key biophysical drivers at multiple time scales. I found that after two decades, CH4 dynamics in a restored wetland appeared to have converged with those at a natural wetland and diverged with those at a cultivated former wetland. Together, these findings demonstrate the importance of acknowledging and accounting for the inherent variability and context-specificity in wetland C dynamics and suggest that wetland management and restoration for climate mitigation requires a detailed understanding of wetland ecosystem processes.
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    ODONATA SPECIES COMPOSITION IN AGROECOSYSTEMS: PRELIMINARY SURVEYS WITH AN EMPHASIS ON POTENTIAL FOR BIOLOGICAL CONTROL ON FARMS
    (2024) Hartman, Margaret Elizabeth; Lamp, William O; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
    Adult dragonflies and damselflies are efficient aerial predators that provide ecosystem service as consumers of pest arthropods. However, their role as predators of agricultural pests in agroecosystems has been understudied. The prey of odonates has been historically difficult to quantify but new molecular methods can make diet analysis easier. I conducted visual encounter surveys across four farms in 2020 and 2021. I found odonates were present on all farms surveyed but there were significant differences in abundance and richness. Fecal pellets were collected from 94 odonates in 2021 for prey DNA analysis using next generation sequencing. Nine odonate samples produced exceptional libraries, resulting in a large quantity of identifiable prey sequences. This preliminary study can help future researchers develop best practices for maintaining healthy farm water bodies and optimizing fecal DNA analysis methodology to better understand odonates’ potential for agricultural pest suppression.
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    UNDERSTANDING NON-TARGET INSECTICIDE IMPACTS AND OPPORTUNITIES FOR BIOLOGICAL CONTROL IN FIELD CORN
    (2024) Cramer, Maria; Hamby, Kelly; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
    Natural enemies can be important regulators of pest populations, replacing chemical pesticides, or where compatible complementing them. To effectively incorporate these biological control services into crop production, we need to understand how pesticides and other management practices impact natural enemies, pests, and their interactions with one another. Using Mid-Atlantic field corn production systems, I evaluated at-planting insecticides and transgenic Bt corn hybrids as tools for insect pest control. In addition, I quantified their impact on predation and on carabid beetle communities. Carabid beetles may be important predators of pest slugs; therefore, I also examined carabid-slug interactions. Finally, I investigated whether a novel pest-management technique (RNAi) could travel up the food chain through pests to predators. At-planting insecticides provided limited pest-management benefits in a three-year field study across Maryland, suggesting that their use could be scaled back to reduce environmental and economic costs. Field and lab experiments revealed carabid beetles are diverse and abundant in corn fields, and a slug predatory carabid species may exert non-consumptive effects on a pest slug. Finally, I determined that a predatory lady beetle species is likely less susceptible to RNAi oral exposure in the adult stage. However, RNAi may still pose risks to predators via trophic exposure. My work supports the adoption of current and future corn pest management practices that protect natural enemies, enhancing biological control ecosystem services and their associated environmental benefits.
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    Using CRISPR/Cas9 to functionally dissect Blimp1, a newly identified pair-rule gene in the hemipteran Oncopeltus fasciatus
    (2024) Reding, Katie; Pick, Leslie; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
    Genetic screens in the fruit fly Drosophila melanogaster identified a class of mutants displaying half as many segments as seen in wild type fly larvae (Nüsslein-Volhard and Wieschaus 1980). Careful examination of the larval cuticle revealed that one out of every two segments were deleted across the anterior-posterior (AP) axis, an unexpected phenotype suggesting that segmentation in Drosophila follows a ‘pair rule’. Thanks in part to the many genetic tools available for this model species, we now have a clear picture of how the AP axis of the Drosophila embryo is polarized and subsequently divided into distinct segments, and how the pair-rule genes (PRGs) define alternate segments during this process. Since all insects share a similar body plan, it is reasonable to expect that the processes regulating establishment of this body plan would be conserved. However, studies of the Drosophila segmentation gene orthologs in non-model insects suggest that this is not always the case. While the use of model organisms enables an unmatched depth of understanding of the mechanisms underlying development, it comes at the expense of understanding the diversity of these mechanisms across taxa. The milkweed bug Oncopeltus fasciatus (Ofas) (Hemiptera) is a particularly useful insect to study in this regard, as none of the orthologs of the Drosophila PRGs have clear PR-function in this species (Liu and Kaufman 2005b; Auman and Chipman 2018; Reding et al. 2019), while the gene E75A, which has no role in segmentation in Drosophila, is expressed in a PR pattern and its knockdown yields PR segmentation defects (Erezyilmaz et al. 2009). These results suggested that PR-regulation of segmentation in Oncopeltus might require a different set of factors than those discovered in Drosophila. To identify other non-canonical PRGs in this species, I conducted an expression pattern-based screen of transcription factor-encoding genes that are co-expressed with E75A during embryogenesis, and have identified the gene Blimp1 as an Oncopeltus PRG. Like the Drosophila PR mutants, Ofas-Blimp1 mutants display loss of alternate segments across the AP axis. No roles of Blimp1 in insect segmentation had been identified prior to this finding. This result suggests that while insect segmentation may be constrained to follow a pair rule, the genes responsible for regulating PR-segmentation are evolutionarily labile. Further, a major barrier to studying gene function in non-models is the lack of genetic tools such as visible markers and established methods for gene editing. Here I will describe deployment of CRISPR/Cas9 technology in Oncopeltus for targeted mutagenesis. While mutation of the ABC transporter-encoding gene white proved to be recessive lethal, I was able to generate a viable visible marker line by disrupting the X-linked gene Ofas-vermilion (v). Of-v is required for production of dark brown eye pigments, thus Ofas-v mutants have bright red eyes, easily discernible from the black eyes of wild type bugs. I show that a co-CRISPR approach using Of-v as a marker of germline mutation is a helpful strategy to identify mutations of interest at unlinked loci, enabling many future genetic manipulations in this species.
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    ENHANCING BIOLOGICAL CONTROL BY GROUND BEETLES (COLEOPTERA: CARABIDAE) THROUGH AGRICULTURAL DRAINAGE DITCH MANAGEMENT PRACTICES
    (2024) Shokoohi, Alireza; Lamp, William; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
    The establishment of semi-natural habitats on crop field margins is an increasingly popular integrated pest management (IPM) tool for conservation biological control of crop pests, decreasing reliance on harmful chemical pesticides. Agricultural drainage ditches are uncropped areas built to mitigate flooding on farms, but they may also provide suitable habitats for beneficial arthropods such as ground beetles, which are generalist predators of many common plant and invertebrate pests. In this study, I aimed to evaluate the potential of drainage ditches as natural habitats that promote biological control by ground beetles. To do this, my objectives were (1) to assess the impact of altered ditch management practices on ground beetle communities within a ditch and (2) to investigate ground beetle community composition and dynamics between ditch and adjacent crop field habitats across the Delmarva peninsula. Addition of straw to ditch banks in the fall increased ground beetle numbers by 97% in subsequent years, and ground beetle activity-density in drainage ditches was proportional to activity-density in adjacent fields for most genera. Results of this study suggest that altering drainage ditch management practices may provide additional ecological benefits by enhancing populations of ground beetles, thus reducing pest damage in adjacent crop fields.
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    PESTICIDE RESIDUES IN BEESWAX PREDICT THE OCCURRENCE OF VARROA WITH ALLELES THAT CONFER AMITRAZ RESISTANCE.
    (2024) Hartel, Eric; vanEngelsdorp, Dennis; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
    Honey bees are important pollinators and are essential to modern industrial agriculture. One of the largest threats to honey bee health is the parasitic varroa mite Varroa destructor. A common method beekeepers use to control varroa is the application of synthetic varroacides. Following years of treatment, varroa have developed resistance to multiple varroacides leading to treatment failures. This project set out to examine the relationship between pesticide residues within beeswax and resistance alleles in varroa. I expected that the presence of varroacides would be positively related to the occurrence of known mutated alleles that confer varroacide resistance to varroa. We looked for 3 different known varroacide resistance alleles, and only found 2, (N87S and Y215H). Both N87s and Y215H confer resistance to amitraz and her metabolite DMPF. Only one mutation, the Y215H mutation, was widespread, occurring in 68% of the 195 mites we examined. We found that the mutation occurred more frequently in mites that were collected from apiaries that had higher DMPF levels. Surprisingly, the presence of other unrelated pesticides (e.g. not having the same mode of action as amitraz) were also positively correlated with the proportion of mutated alleles found. Both the total number of pesticides found in an apiary, and increasing concentrations of fungicides, insecticides, and varroacides (including and excluding DMPF data), predicted higher odds of finding the Y215H mutation. It is unclear if this relationship is a result of a correlation between pesticide levels, if the mutation help benefits the mites resist pesticide more generally, or if the gene has become fixed in the population. It is important to monitor resistance conferring mutations in the varroa mite population in order to help beekeepers make proper varroa management decisions.