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Insecticide Resistance in Bed Bugs, Cimex Lectularius and Cimex Hemipterus (Hemiptera: Cimicidae), in Australia

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Insecticide Resistance in Bed Bugs, Cimex Lectularius and Cimex Hemipterus (Hemiptera: Cimicidae), in Australia Insecticide Resistance in Bed Bugs, Cimex lectularius and Cimex hemipterus (Hemiptera: Cimicidae), in Australia A thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy By David Lilly Student ID: 430446375 23rd May 2017 Supervisor: Dr Cameron Webb Associate Supervisors: Dr Rogan Lee Mr Stephen Doggett Department of Medical Entomology Sydney Medical School, University of Sydney Summary Resistance to insecticides has limited the ability to manage arthropod pests, and in the urban environment this has resulted in the persistence and spread of a range of insects of public health and nuisance-biting significance. Bed bugs (Cimex spp.) have been one such pest, and from a position of relative obscurity over => years ago the number of infestations has undergone perhaps the greatest global resurgence ever to involve an arthropod pest. The resurgence of bed bugs has affected virtually all sectors of society, and has imposed a multitude of negative health and economic impacts. Insecticide resistance is believed to have been a catalyst for the resurgence and a major limitation impacting on the safe and economical eradication of infestations. Understanding both the frequency of insecticide resistance in bed bugs across Australia and the mechanisms that confer such resistance is thus vitally important. The findings of such research can be used to inform the development of new bed bug control strategies and to direct best practice. This PhD thesis investigates the frequency of insecticide resistance in bed bugs, Cimex lectularius and C. hemipterus, in Australia to two groups of commonly used insecticides, the expression of mechanisms known to confer resistance to insecticides, and the impact of such mechanisms on the efficacy of desiccant dust insecticides. To assess the frequency of insecticide resistance in modern Australian field populations of bed bugs, a strategy to collect and successfully colonise bed bugs was undertaken. This resulted in JK field-strains from across Australia being established for use in insecticide screening studies. Discriminating-dose assays of the strains indicated that resistance to pyrethroid insecticides was widespread, and that the susceptibility of several recently-collected strains to neonicotinoid insecticides was declining (Chapter Two). To examine the potential presence and action of metabolic detoxification (a major resistance mechanism that confers reduced insecticide susceptibility to a number of insecticide classes) in the expressed resistance, four field-strains that possessed high frequencies of i resistance were selected for further investigation. Metabolic detoxification can be conferred by two major enzyme groups, cytochrome PNK> monooxygenases and/or hydrolytic esterases. Commonly, the contribution of each enzyme type to resistance can be obscured by the non- specific action of synergists that inhibit enzyme action. This is the case with piperonyl butoxide (PBO), a synergist commonly added by manufacturers to formulated insecticides, but that inhibits both cytochrome PNK> monooxygenases and hydrolytic esterases. However, with the development of a new, esterase-specific synergist, ENUV/K-U, a comparative experimental design with a non-specific synergists, such as PBO, could be employed to measure both the relative presence and contribution of each enzyme group to the observed resistance. The results of this investigation revealed that metabolic detoxification was largely responsible for the observed pyrethroid resistance in all four strains. Additionally, the action of the detoxifying enzymes was equally split between two strains with cytochrome PNK> monooxygenases dominance, and two strains with hydrolytic esterase dominance (Chapter Three). The screening of the four strains also revealed that the addition of detoxification-inhibiting synergists didn’t induce complete susceptibility, thereby suggesting that other resistance mechanisms were contributing to the observed resistance. Thickening of the insect integument is an often-overlooked mechanism of resistance as it is believed to contribute only marginally to expressed resistance, especially in comparison to other mechanisms such as metabolic detoxification and target site insensitivity. However, cuticle thickening is also non-specific to insecticide type and thus may have an important function with the evolutionary development of resistance to new insecticide groups. It may also improve the function of other underlying mechanisms, as was suspected at the conclusion of Chapter Three. Therefore, to further examine the potential presence and contribution of cuticle thickening, one highly pyrethroid-resistant strain from Chapter Three was selected and assayed according a to widely-used time-to-knockdown assay design. Examination of three response groups (‘intolerant’, ‘tolerant’, and ‘resistant’) under scanning electron microscope revealed that ii cuticle thickness was positively correlated with time-to-knockdown. Comparison to an insecticide-susceptible strain also revealed that cuticle thickness was positively and significantly associated with increased resistance (Chapter Four). The impact of resistance mechanisms within bed bugs on traditional insecticide efficacy has been extensively studied, and is often typified by the resistance expressed by the field-strains assayed in Chapters Two and Three. However, an area that had not been fully investigated is the cumulative impact of such resistance mechanisms on the performance of silica-gel and diatomaceous earth-based insecticide desiccant dusts. Desiccant dusts are a frequently recommended option for bed bug control, and have become particularly popular as a low-cost, long-term residual option for the treatment of low socio-economic multi-occupancy buildings in the USA. Therefore, to examine potential impacts on desiccant dust efficacy, the same C. lectularius strain from Chapter Four was utilised in a forced-exposure assay, which determined that tolerance is present to silica gel-based products when exposed to sub-label rates (Chapter Five). Given the present-day popularity of these dusts, the finding of tolerance is a significant development that warrants further investigation. Viewed in combination, the findings of my PhD have made an original contribution towards our knowledge and understanding of the presence of insecticide resistance in bed bugs, as well as some of the mechanisms that contribute to the expressed resistance. In particular, these findings increase our understanding of the evolutionary adaptations that have contributed to the modern resurgence of bed bugs. This information further clarifies both how and why unexpected bed bug treatment failures can occur presently, and are likely to occur into the future. iii Declaration of Originality I, David Gordon Lilly, declare that the contents of this thesis consist of original work carried out by the author unless otherwise stated and duly acknowledged. To the best of my knowledge no part of this thesis has been submitted in whole or in part for any other degree or diploma in any University. ...................................... David Lilly =Jrd May =>U^ Structure of Thesis This thesis has been written as a series of manuscripts that have been published. As such, there is redundancy in the introductions and methods of some chapters. iv Acknowledgements I would firstly like to thank my supervisors, Dr Cameron Webb, Mr Stephen Doggett, and Dr Rogan Lee, without who’s support, guidance and (when needed) gentle prodding, this thesis would be much poorer as a result. To Cameron, your constant view towards the big picture, calm approach to the highs and lows of research and publishing, and frequent encouragement to simplify the science, have made me both a better scientist and communicator. I never really understood Twitter, but we were lucky enough to witness a Cronulla Sharks premiership during my candidature, so we’ll call it even, yeah? To Stephen, your unsurpassed knowledge of bed bugs and medical entomology inspired me to learn and achieve as much as I could during the last four years. Your unceasing sense of inquiry meant that I was never short of new ideas, nor motivation when it was needed. You also taught me far more than I probably should know about the benefits of frequent flyer status – but either way, I’ll no doubt see you in the lounge! To Rogan, thank you also the motivation, support, and fascinating glimpses into the world of parasitology. If ever I get bored of entomology, I know which door to knock on. I am also deeply indebted to Merilyn Geary, Karen Willems, Cheryl Toi, John Haniotis, John Clancy, and Kai Dang of the Department of Medical Entomology for the friendship, laughs, and encouragement during my time in the lab. You’ve taught me more about entomology than any university subject could, and your collective patience as the number of bed bug colonies grew ever larger will forever be appreciated. Likewise, to the staff of the Department of Animal Care, your diligent and attentive upkeep of animal stocks, and weekly assistance with maintenance of the bed bug colonies, meant that we always had the bed bugs that we needed. Your support has been greatly appreciated. v Enormous thanks are also due to Chris and Eva of the SciTech Library document delivery team for assiduously sourcing much of the literature associated with insecticide resistance in bed bugs from the mid-=>th century. The journals were often obscure, if not long-defunct, and the language invariably foreign, but
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