Ph.D. - Entomology

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    Seasonal Honey Bee Colony Performance and Health in Hawai'i
    (University of Hawaii at Manoa, 2022) zhang, zhening; Wright, Mark G.; Entomology
    The European honey bee (Apis mellifera) is among the most abundant pollinator species and the most widely managed insect in the world. In temperate areas, honey bee colonies experience large fluctuations in population throughout a year without becoming completely dormant. Numerous studies conducted in temperate regions focus on those seasonal changes and examine colony performance and overall health; however, there is little known about colony dynamics in Hawaii, where in spite of more stable ambient temperature and less pronounced seasons, there are notable changes in colony strength across the year. Hawaii does not have extremes of cold winters and hot summers, and the average daily temperature variation is small (around 3 ℃). Hawaii however, has large variations in rainfall patterns both at the regional level, especially when windward and leeward areas are compared, but precipitation also varies throughout the year. The subtropical climate of the islands is part of what makes year-round beekeeping possible in Hawaii. The Hawaiian islands are also a unique place to conduct research because the bees are 100% pure European stock, with no hybridization with African bees, as is the case in the southern U.S.The overall objective of this dissertation is to describe the seasonal growth patterns of honey bee colonies and examine possible health fluctuations under Hawaii’s climate. The results from this work contribute to basic knowledge for beekeepers, not only in Hawaii but also in other tropical areas with similar climates. Four objectives are covered in this dissertation. First, this work examines how foraging activities change across different parts of the year and how queen replacement events impact foraging. The data confirm that there were seasonal trends in colony growth in Hawaii and that the growth pattern could also be different between years, possibly due to the El Niño and La Niña phenomena. The climate in Hawaii allows for colonies to attempt queen replacement, whether it is through swarming or supersedure, during the majority of months of the year. Both swarming and supersedure led to a decreased exiting foragers per minute (EF). In contrast, the proportion of pollen foragers (P%) increased after supersedure but dropped after swarming. The degree of change in EF and P% during a swarming or supersedure event were found to be linked to its initial EF and P% before the queen replacement happened. Second, a supplemental feeding experiment was conducted for the first time in Hawaii to examine the potential benefits to colonies and local beekeepers. The results showed that colonies that received supplemental food began to grow larger than control colonies by the end of the feeding period. Most interestingly, the colony strength and larger population benefits dervided from feeding carried over to the post-feeding period. Colonies that were being fed produced nearly twice as much honey compared to the control group at the end of the study. In addition, control colonies showed a higher deformed wing virus level than the fed group. Third, climate data were used to make connections with seasonal colony growth. The analysis showed that besides temperature, daylight duration was the main trigger that impacted the colony's seasonal growth in Hawaii. Fourth, two master DWV variants, A and B, were examined at both colony and apiary levels across different months in 2018 and 2019. This study showed the prevalence of DWV-B had increased since the 2016 study. DWV-A was still dominant at an apiary level in this study; however, some colonies could already be characterized as DWV A+B mix or even DWV-B only. And finally, this study showed DWV-B had a seasonal change in both viral load and prevalence, providing a perspective on the dynamic nature of DWV master variants. Overall, the findings in this dissertation help to better understand the seasonal activity and health of honey bee colonies in a sub-tropical environment. This work provides valuable data to beekeepers in Hawaii and will contribute to the improvement of the overall colony conditions in Hawaii, both from a biological and economic perspective. The emerging of DWV-B in this study apiary also showed that there are rapid evolutionary changes between the varroa mite, the honey bee, and the DWV compared to the other parts of the world.
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    Investigating Patterns And Variations In Aedes Albopictus (Diptera: Culicidae) And Its Microbiome In Hawaii
    (University of Hawaii at Manoa, 2021) Seabourn, Priscilla Sheryl; Medeiros, Matthew CI; Spafford, Helen; Entomology
    Understanding the drivers of distribution and abundance of invasive species remains a significant challenge especially on the Hawaiian Islands. Mosquitoes (Diptera: Culicidae) are non-native to Hawai’i and the diseases they vector are a contemporary threat to human and wildlife health. Despite being a well-established mosquito species, Aedes albopictus (Skuse) distribution and the factors influencing the population and its host associated microbiome in Hawaiʻi are poorly understood. In this study, I investigate how the environment influences the distribution and abundance of Ae. albopictus and the diversity and distribution of its host-associated microbiome in Hawaiʻi. In a yearlong island-wide surveillance study on Maui, the patterns of mosquito distribution were evaluated in relation to environmental factors (rainfall and temperature), elevation, space, and time using both oviposition and adult traps. Overall, four mosquito species were detected, Ae. albopictus, Ae. vexans, Culex quinquefasciatus, and Wyeomyia mitchellii. The survey determined that Aedes albopictus is abundant and widely distributed around Maui, and adult abundance and oviposition varied with site and time of collection. The oviposition of Ae. albopictus was positively associated with sites that are warm and low elevation, while the abundance of adults was not influenced by the environmental variables. The complex characteristics of each site such as vegetation, land use and host availability likely influenced the abundance of adult Ae albopictus and its ovipositional activity. However, Culex quinquefasciatus, Ae. vexans, and W. mitchellii were not frequently collected, and were not assessed in relation to space, time, or environmental variables. The trapping methods and frequency and intensity of sampling are likely to have been the main drivers behind the probability that these species and others were collected. Nonetheless, these findings can be used provide a baseline for future mosquito surveillance studies to assess new mosquito species incursions, and range expansion. Adult Ae. albopictus collected in the above survey were used to assess host associated microbiome in relation to space, time, rainfall, temperature, and host infection with a co-occurring pathosymbiont Ascogregarina taiwanensis. The microbiome of Ae. albopictus was found to vary across the island and be influenced by infection status with A. taiwanensis. The microbiome of Ae. albopictus did not shift in accordance with gradients of temperature or rainfall, suggesting that mosquitoes actively maintain their microbiome. As with the distribution of the adult mosquitoes, the complex factors associated with various sites, are diving the differences in the host-associated microbiome across geographic location. This study also highlights that inter- and intra-domain interactions may structure the Ae. albopictus microbiome. Cumulatively, understanding the explicit drivers of the mosquito microbiome assembly may have important implications in developing mosquito control strategies. I further explored how the microbiome is heterogeneous within the host and demonstrate that the environment provides the source of microbes. Results indicate that the microbiome of Ae. albopictus tissues is compositionally nested within the environmental microbiome i.e. microbes within the mosquito tissues are also found in the soil, water and on plants in the mosquito habitat. Within the mosquito, the microbiomes of the crop, midgut, Malpighian tubules, and ovaries differed in composition. The microbiomes of mosquitoes tissues formed two specialized modules, one in the crop and midgut and another in the Malpighian tubules and ovaries. The specialized modules may form based on microbe niche preferences and/or selection of mosquito tissues on specific microbes that may aid unique biological functions of the tissue types. Strong niche-driven assembly of tissue-specific microbiotas from the environmental species pool suggests that each tissue has specialized associations with microbes, which perhaps derive from host-mediated microbe selection. Overall, this study investigated the drivers of distribution, and abundance of Ae. albopictus and additionally the diversity, distribution and abundance of the host-associated microbiome present in Hawaii. These findings fill an important gap in understanding about a significant disease vector and provide information for future surveillance and studies, particularly those that lead to the development of novel methods of mosquito management.
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    Chiggers (Acari: Trombiculidae) infesting Papua New Guinea land mammals
    (University of Hawaii at Manoa, 1977) Goff, M. Lee; Entomology
    Examination of over 10,800 specimens of chiggers from the island of New Guinea has revealed the presence of 45 species in 11 genera infesting 53 kinds of mammal hosts. One of these species was in the subfamily Leeuwenhoekiinae and the remainder in the Tro
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    Enhancing Male Annihilation Technique (MAT) of Fruit Flies (Diptera: Tephritidae) Using a Binary Lure System with a Biopesticide
    (University of Hawaii at Manoa, 2020) Souder, Steven Kazunori; Spafford, Helen; Entomology
    The family Tephritidae encompasses more than 4400 species worldwide from 500 genera. This family is one of the largest in the order Diptera that includes over 200 species of economic importance (Christenson & Foote 1960, White & Elson-Harris 1992). Economically important fruit flies can be serious pests of fruits, nuts, and vegetables that create adverse social, political, and economic hardship around the globe (Papadopoulos 2014). Extensive research and regulatory resources have been put towards pestiferous flies to reduce established populations, prevent transfer to fruit fly free areas, and effect quarantines and eradications (Vargas et al 2014). One technique used to combat these invasive pests is the use of the male annihilation technique (MAT; a.k.a. male attractant treatment). Male annihilation technique is the deployment of a high density of traps or bait stations that consists of an attractant combined with an insecticide and matrix. Where more than one species of fruit flies attacks a single crop, management becomes even more difficult and further research is needed. Papaya (Carica papaya L.) is a specialty crop that is of significant importance to Hawaiʻi’s diversified agriculture. In Hawaiʻi, papaya is attacked by both Bactrocera dorsalis (Hendel, est. 1945) and melon fly, Bactrocera (Zeugodacus) cucurbitae (Coquillett, est. 1895). Male annihilation technique has been used in papaya for management of both B. dorsalis and B. cucurbitae. This system presents an opportunity to test the behavioral response of two species to a binary lure system in an economically important crop. Management using MAT to date has been typically done in a single lure format that targets one species with separate trapping materials, labor, and deployment. Given that B. dorsalis and B. cucurbitae are both routinely found in and around papaya growing areas, this study sought to understand the significance of visual and olfactory cues in resource location of papaya for both fruit fly species. It also aimed to test the application and optimization of a binary lure MAT system that would reduce the numbers of both fly species. In a series of behavioral experiments, I quantitatively measured the host resource use of B. cucurbitae on papaya and compared the sensory modalities used by two tephritids that are currently considered a “primary” pest (B. dorsalis) and an “occasional” pest (B. cucurbitae) of papaya. I recovered twenty times more adult wild B. cucurbitae flies than B. dorsalis flies from sentinel papaya fruits placed in the largest papaya growing area in the United States. Results of visual and olfactory experiments suggest that B. cucurbitae females are not primarily attracted to volatiles emitted by papaya fruit, but rather vision seems to be the main stimulus inducing landing and oviposition. Bactrocera dorsalis appears to be equally responsive to either olfactory or visual stimuli of papaya. These observations demonstrate a potential for behavioral control using visual mimics with B. cucurbitae. Furthermore, a synergistic approach using both chemical and visual stimuli to control mature male and female fruit flies shows real promise. I performed a series of field trials to evaluate a novel binary lure MAT for two species simultaneously, B. dorsalis and B. cucurbitae. The trials were conducted in a large papaya growing area using standard trapping methods to determine efficacy and optimization of a binary MAT system (SPLAT™, Specialized Pheromone and Lure Application Technology, ISCA Technologies, Riverside, CA) with a biopesticide (spinosad, Dow AgroSciences LLC, Indianapolis, IN). I found that a binary lure system may function as a generic MAT (ME + CL) against B. dorsalis and B. cucurbitae when populations of both species are associated in a cropping area. Binary lure formulation of SPLAT was optimized by increasing the amount of ME from 25.5% to 45% and decreasing the amount of CL from 10% to 8%. A single application containing both lures could potentially reduce labor, equipment and material costs by 50%. Following the results of the field trials, it was important to identify any potential interspecies dependent responses of B. dorsalis and B cucurbitae using novel binary lure MAT. In a series of cage test, the number of individuals in each species was manipulated to examine if the response changed when one species occurs in greater numbers than the other. I also evaluated male attractants ME + CL at varied ratios to understand the role each lure plays on the response and capture of each species. I found no interspecies interactions. Captures for both species were not different when each species was alone, in equal numbers, or when the other species was in greater numbers. Instead, the only factor that seems to influence capture rate was measured in cages with B. dorsalis. The response of B. dorsalis amplified considerably with increase in the amount of ME formulated into binary SPLAT mixture. Response of B. cucurbitae was not influenced in the same way by increasing the amount of CL. Maximizing ME and using a lower amount of CL in a binary lure MAT at the trap or station would provide the most benefit when B. dorsalis and B. cucurbitae are in equal numbers or B. cucurbitae is the dominant species. I further explored the potential horizontal transfer of insecticide of a binary lure MAT containing spinosad. The sprayable application, strong behavioral response to male lures, and mode of action including time to mortality induced by spinosad may facilitate horizontal transfer of insecticide. Using a series of laboratory tests, I recorded mortality of conspecific male and female flies exposed to primary fed males of B. dorsalis and B. cucurbitae. I found that horizontal transfer can occur in both males and females of both species. This transfer can occur from a single fed male to other individuals or a group of conspecifics resulting in mortality. The higher mortality of males relative to females is linked to the strong behavioral response, of males to lures. Horizontal transfers of spinosad may provide enhanced suppression of both males and females of two species in one location. Together, the results of these experiments demonstrate that use of a binary lure in papaya systems will effectively attract and kill both B. dorsalis and B. cucurbitae. Furthermore, use of a reduced risk insecticide such as spinosad, will lead to horizontal transfer and increased mortality in the populations of both species. Thus, deployment of a sprayable binary lure MAT system with reduced risk insecticide spinosad would reduce the costs associated with materials, equipment, and labor by 50% and lead to similar mortality in the field.
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    Captive Rearing And Semiochemcial Ecology Of Trichogramma Papilionis (hymenoptera: Trichogrammatidae)
    (University of Hawaii at Manoa, 2020) Ali, Abdulla Nezar; Wright, Mark G.; Entomology
    This study addressed aspects of mass rearing of Trichogramma papilionis (Hymenoptera; Trichogrammatidae), including the effects of varied colony founder size on wasp fitness, and the exploitation of the wasps to locate egg hosts in which to deposit thereof progeny. Effects of initial founder female number of T. papilionis were investigated using fitness parameters (emergency rate, sex ratio and fecundity) to quantify the effects of a severe bottleneck (single founder female) on 10 subsequent generations. Results showed that no significant difference for eggs laid per female over ten generations, suggesting that the imposed bottleneck did not result in reduced female fecundity for any founder population size. However, founder numbers did affect both the emergence rate and sex ratio of T. papilionis. Further investigation of the impacts of inbreeding on field performance of the wasps was discontinued as extremely limited host finding ability of the wasps was observed in some habitats. The emphasis of the work was thus shifted to elucidating the searching behaviors of T. papilionis in relation to chemical cues. The hypothesis that T. papilionis are attracted to host habitat by host plant or egg-associated volatile chemicals was tested. The response of T. papilionis females to olfactory cues from host eggs, host plants and induced plant volatiles were studied. The response of T. papilionis females to different info-chemical cues was tested in Y-tube olfactory assays. Wasps made a positive response to odors from corn earworm (CEW) eggs Helicoverpa zea (Lepidoptera: Noctuidae) compared with blank air, while there was a negative response to Ephestia kuehniella eggs (Lepidoptera: Pyralidae) compared blank air: T. papilionis females thus preferred odors from corn earworm eggs over the Mediterranean flour moth eggs. Further, the wasps were attracted to volatile emissions from sunn hemp Crotalaria juncea (L.) over maize Zea mays (L.), despite both plants infested with H. zea eggs. No preference was observed for plants not infested with H. zea eggs, suggesting T. papilionis showed a positive response to stimuli from sunn hemp plants that might be induced by H. zea oviposition. Chemical volatile collection and headspace analysis was conducted. Headspace analysis and thermal desorption and gas chromatography–mass spectrometry (TD-GCMS) was used to qualitatively and semi-quantitatively determine the difference in plant volatile organic components (VOCs) from Helicoverpa zea egg infested sunn hemp plants compared with intact sunn hemp plants and H. zea eggs only. TD is used as a preconcentration technique of VOCs for gas chromatography-mass spectrometry (GC–MS), making it useful to detect low-concentration analytes that would otherwise be undetectable. Results demonstrated that sunn hemp plants released 55 chemical volatiles with five compounds that were unique, or were emitted in higher concentrations, for plants infested with CEW eggs. These volatile compounds were consistent with linear alkanes, aldehydes, aromatics, polyterpene-related compounds, naphthalene derivatives, and ester-related compounds. High concentrations of anisole, β-myrcene, cis-butyric acid, trans-isoeugenol, and bis(2-ethylhexyl) phthalate were found in infested sunn hemp. The majority of GCMS peaks detected from H. zea eggs were consistent with phosphates, pheromone-related compounds, various natural products, a series of glycol-related compounds, and a series of fatty acid ester-related compounds. Several compounds were shared in sunn hemp samples and corn earworm eggs: anisole, β-myrcene, and bis (2-ethylhexyl) phthalate, but were detected in higher concentrations from the plants with H. zea eggs. Evaluation of the response and the performance of T. papilionis females in y-tube olfactory bioassays to single compounds, and blends of synthetic chemical showed that the wasps were significantly attracted to only two of the assayed chemical volatiles (anisole and bis(2-ethylhexyl) phthalate). Some concentrations of anisole and bis (2-ethylhexyl) phthalate were attractant to the wasps, whereas some concentrations of the other tested chemical compounds repelled the wasps. Wasps were attracted to a blend of anisole and bis(2-ethylhexyl) phthalate (25μL /100μL ratio) which is similar to the ratio of anisole to bis(2-ethylhexyl) phthalate detected in the (GC-DMS) chromatograph for C. juncea plants infested with H. zea eggs. No significant attraction to any other blend ratios of anisole and bis(2-ethylhexyl) phthalate was observed. Greenhouse and field experiments were conducted to determine whether the patterns observed in the y-olfactometer were consistent under less constrained conditions. The optimal blend identified above was initially tested in a greenhouse, and later in closed-canopy environments (under trees) and open habitat with no trees. The parasitism rate by T. papilionis wasps was significantly increased when the wasps were exposed to anisole and bis(2-ethylhexyl) phthalate blend in both greenhouse and outdoor trials (covered habitat), at least over short distance (up to 2m from the volatile sources). The findings presented in this dissertation underscore the importance of improving our understanding of how tri-trophic interactions (natural enemies- herbivores and host plants) interact to influence insect behavior, as well as the impact of variable environments, impact parasitoid wasps. The results may also contribute to finding a way to improve natural enemy efficacy in augmentative and conservation biocontrol efforts. Semiochemical cues can positively or negatively affect the response of parasitic wasps. This may provide an understanding of ecology that could facilitate achieving successful field parasitism and thus enhanced pest management.
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    Ecological management of insect pests using cover crops in field crops and vegetables
    (University of Hawaii at Manoa, 2013-08) Manandhar, Roshan
    This dissertation researched diversified cropping systems created through habitat management techniques, exploring whether these habitats would alter pests' behavior and/or enhance beneficial insects, and contribute to suppress pest and disease complexes in corn production systems. An exploratory study through small-scale field experiments determined sunn hemp (Crotalaria juncea) as the potentially the most suitable species for further study. In the preliminary studies, sunn hemp intercropping reduced incidence of hopperburn and Maize mosaic virus (MMV) symptomatic plants caused by Peregrinus maidis feeding, and increased parasitism of Helicoverpa zea eggs by Trichogramma spp. on the corn silks. The reduced incidence of hopperburn and MMV was attributed to an increase in P. maidis within-field activity, resulting in reduced initial colonization on corn plants. The results showed a suitable intercrop might be useful for management of persistent viruses, which are usually considered unmanageable by habitat management to cropping systems. On the basis of these preliminary studies, experiments were conducted in large-scale field with a higher corn-to sunn hemp intercropping ratio to validate results and possibly contribute new pest management options for large-scale corn production systems. Increase in within-field P. maidis activity with resulting in lower incidence of MMV symptomatic plants in the sunn hemp-intercropped treatments were consistently similar to results that were obtained from small-scale field experiments. This strategy may contribute an important component of integrated pest management for reducing spread of persistently transmitted viruses in large-scale corn production systems. Greater parasitism of H. zea eggs by Trichogramma spp. in sunn hemp-intercropped treatments was consistently similar to that obtained from small-scale field experiments. These results suggested growing strips or patches of suitable cover crop may help in sustaining the populations of beneficial insects at the time of pest outbreaks. Augmentative biological control (releases of Trichogramma pretiosum in corn monoculture) resulted in a greater parasitism of H. zea eggs, and increased ear yield compared to habitat management (sunn hemp-intercropped). This result suggested H. zea management is important component to achieve economic yield and augmentative biological control is a more effective tool than the habitat management in cornfields.
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    Foraging response of female Bactrocera dorsalis (Hendel) to a fruit fly protein food attractant
    (University of Hawaii at Manoa, 2013-08) Chou, Ming-Yi
    Oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) causes serious economic loss for papaya (Carica papaya L.) production in Hawaiʻi through direct fruit damage and restriction of export commodities. Suppression of female flies was a challenge until a protein-based bait contains reduced risk insecticide spinosad became available, GF-120 NF Fruit Fly Bait (GF-120; Dow AgroScience, Indianapolis, IN). This bait provides an environmentally sound alternative to conventional cover spraysof organophosphate insecticides. Factors that influence the attractiveness of protein bait include chemical composition, visual stimuli, and competing volatiles from host fruits. This dissertation focuses on biological factors that affect the foraging response of female B. dorsalis to volatiles emitted by protein bait. Female reproductive state and dietary experience are two biological variables that shape the manner in which a fly searches for and responds to essential resources such as food and egg-laying sites. The experiments reported in this dissertation were conducted in order to assess the influence of physiological states on the response of female B. dorsalis to protein bait in papaya orchards. In Chapter 1, baseline information on key morphological characters in B. dorsalis ovarian development and the associated morphometric parameter of each oogenesis stage is collected. Four oogenesis stages include previtellogenesis, vitellogenesis, gravid and parous. In Chapter 2, field observations were conducted to determine reproductive states of B. dorsalis females (using ovarian developmental stage as an indicator) that respond to 2 two protein bait trapping devices: visually enhanced attract-and-kill bait stations termed papaya leaf mimics (PLMs) treated with GF-120 and dome traps containing torula yeast solution. Females with ovaries at previtellogenesis stage and egg laying females are the two main classes that responded to protein bait. Visual stimuli from the bait stations enhanced the response of immature females to protein bait but this effect was not found in egg-laying females. Yellow color also increased the capture of females with greater egg loads compared to those captured by green bait stations. This is an important finding for improved fruit fly management because reducing numbers of egg-laying females within an area results in lower fruit infestation. The physiological state of foraging flies determines the level of food searching behavior. In Chapter 3, the effects of female age and dietary history on the propensity of B. dorsalis to alight on protein bait were quantified. One week old females exposed to papaya as a diet source for 4 d in the first week of adult life showed a significantly greater propensity of alighting on GF-120 protein bait than females fed on a protein or sugar diet. Delay of ovarian development from feeding on a sugar only diet resulted in significantly higher response of 4 week old females to protein bait than females fed on papaya or protein. On the contrary, ovarian development in papaya fed females was not significantly different than that of protein fed females. Feeding on papaya during weeks 2 to 4 of adult life increased the response of female flies to protein bait at a lesser level than for 1 week old females. These results are evidence of the possible physiological profile of females attracted to protein bait in the natural environments. In addition, previous exposure to papaya fruit enhanced the response of females to papaya compared to females without the experience. This is a finding that suggests sanitation practice of removing culled fruit not only removes a breeding source but may also reduce the number of females re-entering orchards. Studies conducted in this dissertation are the first documentation of the response of egg-laying female B. dorsalis to protein bait under natural and semi-natural conditions. Results suggest that protein baits such as GF-120 attract females with developing ovaries as well as egg-laying females. In addition, fruit-based diet enhances the response of female B. dorsalis to protein bait and host fruit stimuli.