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DIRECT AND INDIRECT EFFECTS OF NATIVE AND INVASIVE PLANTS ON MOSQUITO ECOLOGY BY ALLISON MAE GARDNER DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Entomology in the Graduate College of the University of Illinois at Urbana-Champaign, 2016 Urbana, Illinois Doctoral Committee: Assistant Professor Brian F. Allan, Chair, Co-Director of Research Dr. Ephantus J. Muturi, Co-Director of Research Professor May R. Berenbaum Professor Lawrence M. Hanks Assistant Professor Allison K. Hansen Abstract Container-breeding mosquitoes (Diptera: Culicidae), including the vectors of human and wildlife pathogens, interact with terrestrial plants throughout their life cycles. Inputs of leaf detritus into the aquatic habitat provide an energy base for developing larvae, and plants mediate the distribution of adult mosquitoes by influencing microclimate conditions, supplying sugar-feeding sources, and altering communities of wildlife blood-meal hosts. This dissertation examines direct and indirect effects of understory shrubs, including species both native and invasive to North America, on the ecology of Culex pipiens, an important vector of West Nile virus in the northeastern and midwestern United States. Laboratory and field bioassays demonstrated that leaf detritus from different plant species in the aquatic environment alter two key components of mosquito production (i.e., oviposition site selection and adult emergence) via the abundance and composition of bacterial flora that form on different leaf species as they decompose. In particular, an invasive plant (Lonicera maackii, Amur honeysuckle) yielded high oviposition and adult emergence rates, while in contrast, a native plant (Rubus allegheniensis, common blackberry) was identified to function as an ecological trap for Cx. pipiens, attracting gravid females to oviposit and yet deleterious to larvae yielding low emergence rates. Subsequent laboratory bioassays in which first instar larvae were exposed to mixtures of leaves from different plant species revealed that while leaf resource diversity generally yields an increase in Cx. pipiens adult emergence rates, addition of high-quality resources is not sufficient to offset the deleterious effect of R. allegheniensis leaves. I then explored two integrated vector management applications of these findings. First, a field experiment demonstrated the feasibility of exploiting a naturally-occurring ecological trap (R. allegheniensis leaves) and an artificial ecological trap ii (L. maackii leaves mixed with Bacillus thuringiensis var. israelensis larvicide) for attract-and- kill mosquito control in storm water catch basins, in which gravid females are lured to oviposit in a low-quality environment. This result provides experimental proof of concept for a novel integrated vector management tool that may enhance the effectiveness and sustainability of existing mosquito abatement strategies with minimal non-target effects and reduced potential to select for insecticide resistance. A second field experiment showed that removal of L. maackii decreases abundance of adult Culex spp. mosquitoes in forest fragments within a residential neighborhood. The mechanisms underlying this reduction in mosquito abundance most likely include effects of L. maackii removal on microclimate conditions and the availability of avian blood-meal hosts. Collectively, these studies reveal multiple ecological pathways by which terrestrial plants interact with, and alter the abundance, distribution, and life history characteristics of mosquitoes, and suggest landscape modification strategies that may be used to manage an important disease vector species in residential ecosystems. iii Acknowledgments I owe my great experience as a graduate student at the University of Illinois to numerous individuals with whom I have had the pleasure of working in the classroom and the lab. First and foremost, I would like to thank my advisors, Dr. Brian Allan and Dr. Ephantus Muturi, as well as Dr. Don Bullock and Dr. Marilyn O’Hara Ruiz, for their instruction, guidance, and unfailing support of my academic goals. Further I would like to thank my thesis committee members, Dr. May Berenbaum, Dr. Larry Hanks, and Dr. Allison Hansen. Through direct feedback on my work and by example, my professors have shown me – and enabled me to discover for myself – intellectual paths that I could not have imagined six years ago. There is little for which I could be more grateful both professionally and personally, and I intend to spend my career paying forward this exceptional mentorship and investment in my education. My research was accomplished through the dedication and energy of dozens of people, and acknowledgments for specific projects are included at the conclusion of each chapter, but I would like to begin by thanking a few current and former members of my advisors’ labs for their ideas and technical assistance on all aspects of my dissertation: Dr. Andrew Mackay, Allison Parker, Dr. Chang-Hyun Kim, Millon Blackshear, Dr. Page Fredericks, and Dr. Jeff Bara. Thank you to the independent research students who conducted lab and field work with me: Brit’nee Haskins, Lauren Frisbie, Matt Edinger, Jackie Duple, Leah Overmier, Noor Malik, Reanna Kayser, Jake Gold, Chase Robinson, Michelle Manious, Audrey Killarney, Kristen Chen, Katie Lincoln, Ali Braet, Billy LeGare, and Grace Cahill. Finally, I would like to acknowledge my family and friends who shared my experience at the University of Illinois. I would like to thank my parents and my sister, Wendy, Tom, and iv Kristy Gardner, and my friends in the department, Allison Parker, Tyler Hedlund, Tanya Josek, Erin Allmann Updyke, Erin Welsh, Natalie Pawlikowski, Elijah Juma, and Catherine Wangen, for their thoughtful comments on my writing and presentations and their encouragement and good humor as they plowed through hours and hours of conscripted field work service and witnessed their yards, homes, and freezers being transformed into field lab extensions. I would like to acknowledge my earliest research mentors, Zenaida Bongaarts and the late Dr. Robert Pavlica, for their high expectations and commitment to teaching that have been a source of motivation and inspiration for twelve years and counting. I would like to thank Brandon Lieberthal for his emotional and technical support, and for many memories – that I’m sure will become fond eventually – of late night Rural King runs and low-budget field equipment construction projects. If there is a limit to your patience and kindness, I haven’t discovered it yet! v Table of Contents Introduction .................................................................................................................................... 1 CHAPTER 1: Asymmetric effects of native and exotic invasive shrubs on ecology of the West Nile virus vector Culex pipiens (Diptera: Culicidae) ................................................................... 10 CHAPTER 2: Leaf detritus mixtures alter microbial resource composition in aquatic habitats and performance of container-breeding mosquito larvae (Diptera: Culicidae) .................................. 38 CHAPTER 3: Exploitation of ecological traps for the control of a mosquito vector for West Nile virus .............................................................................................................................................. 80 CHAPTER 4: Removal of invasive Amur honeysuckle (Lonicera maackii) decreases abundance of mosquitoes (Diptera: Culicidae) ............................................................................................ 129 vi Introduction Invasive species, defined here as non-native species whose introduction and subsequent spread are likely to cause economic or environmental harm, rank second only to habitat destruction as a threat to native biodiversity (Wilcove et al. 1998, Pimentel et al. 2005). Mechanisms by which invasive species may reduce biodiversity include altering habitat structure, acting as predators and competitors of native species, and hybridizing with native species (Mooney and Cleland 2001, Lee 2002, Levine et al. 2003). There also is evidence that invasive species may cause increased risk of exposure to infectious diseases in wildlife and human populations via the introduction of novel pathogens and parasites into susceptible populations (Daszak et al. 2000) and by altering the ecology of established infectious agents that are embedded in biological communities through complex networks of energy flow (Pejchar and Mooney 2009). The distribution and prevalence of arthropod-borne diseases depend on the interactions between an arthropod vector, the pathogen, and a human or wildlife reservoir host, and these interactions may be altered by invasive species via a diversity of mechanisms. In particular, invasive plants are among the most important threats to native ecosystems and recent research has demonstrated their potential to trigger a cascade of ecological interactions that alter vector-borne disease transmission (Mack and Smith 2011, Mackay et al. 2016). This is a problem of global health significance because nearly one-third of emerging infectious diseases that threaten ecosystem health are vector-borne (Jones et al. 2008) and terrestrial plant invasions are increasingly widespread phenomena aided by human activities (Reichard and White 2001). For example, in systems of diseases vectored by ticks (Acari: Ixodidae), invasive bush honeysuckle (Lonicera maackii)