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ZOOS AS EXPERIMENT ENVIRONMENTS: BIOLOGY of LARVAL and ADULT MOSQUITOES (DIPTERA: CULICIDAE) Holly Tuten Clemson University, [email protected]

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ZOOS AS EXPERIMENT ENVIRONMENTS: BIOLOGY of LARVAL and ADULT MOSQUITOES (DIPTERA: CULICIDAE) Holly Tuten Clemson University, Htuten@Gmail.Com Clemson University TigerPrints All Dissertations Dissertations 8-2011 ZOOS AS EXPERIMENT ENVIRONMENTS: BIOLOGY OF LARVAL AND ADULT MOSQUITOES (DIPTERA: CULICIDAE) Holly Tuten Clemson University, [email protected] Follow this and additional works at: https://tigerprints.clemson.edu/all_dissertations Part of the Entomology Commons Recommended Citation Tuten, Holly, "ZOOS AS EXPERIMENT ENVIRONMENTS: BIOLOGY OF LARVAL AND ADULT MOSQUITOES (DIPTERA: CULICIDAE)" (2011). All Dissertations. 769. https://tigerprints.clemson.edu/all_dissertations/769 This Dissertation is brought to you for free and open access by the Dissertations at TigerPrints. It has been accepted for inclusion in All Dissertations by an authorized administrator of TigerPrints. For more information, please contact [email protected]. ZOOS AS EXPERIMENT ENVIRONMENTS: BIOLOGY OF LARVAL AND ADULT MOSQUITOES (DIPTERA: CULICIDAE) A Dissertation Presented to the Graduate School of Clemson University In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy Entomology by Holly Coleen Tuten August 2011 Accepted by: Peter H. Adler, Committee Chair William C. Bridges, First Reader Kimberly S. Paul, Second Reader William Wills, Third Reader ABSTRACT Zoos are a unique environment where humans and animals are in close daily contact, potential mosquito habitats exist, exotic plants and animals are introduced regularly, and wild animals roam. Studies of mosquito behaviors in zoos will lead to a better understanding, both within and outside zoos, of disease transmission routes and mosquito biology. To investigate whether the unique assemblage of habitats in zoos affects mosquito behavior, I sampled larvae and adults in the Greenville Zoo and the Riverbanks Zoo, South Carolina, USA, from March 2008 to January 2011. The objectives of my study were to investigate mosquito oviposition behavior, blood-host usage, and transmission of the causative agent of dog heartworm (Dirofilaria immitis); document the structure of the mosquito pyloric armature; and provide zoos with suggestions for mosquito control. My results underscore the medical and veterinary importance of studying mosquito blood feeding ecology in zoos, and the experimental utility of zoos for studying mosquito behavior. A total of 1,630 larvae and 4,349 adults representing 16 species was collected and identified. The most common species were Aedes albopictus, Ae. triseriatus, Culex erraticus, Cx. restuans, and Cx. pipiens complex. Principal components and multiple logistic regression analyses showed that across both zoos the overall larval mosquito presence (regardless of species) was predicted by ambient and site temperature, precipitation, dissolved oxygen, presence of natural habitats, and absence of aquatic vegetation. Pairwise species associations indicated significant habitat-based relationships ii between larvae of Ae. albopictus and Ae. triseriatus, and Cx. pipiens complex and Cx. restuans. Recommendations to zoo personnel, regarding larval mosquito habitat management, were to reduce or eliminate artificial containers and shade sources greater than or equal to 2 m above standing water, use mosquito larvicides when source reduction is not possible, and receive training in recognizing and mitigating larval mosquito habitats. Mosquitoes fed on captive animals, humans, and wild animals, and took mixed bloodmeals. Blood hosts included 1 amphibian species, 16 bird species, 10 mammal species (including humans), and 2 reptile species. Minimum flight distances (dispersal) from host locations ranged from 15.5 m to 327.0 m, with a mean of 94.1 m ± 13.4 m. No mosquitoes tested (n = 45) were positive for D. immitis. The pyloric spines of Ae. albopictus, Ae. j. japonicus, Ae. triseriatus, An. punctipennis, Cx. pipiens complex, Cx. restuans, Or. signifera, and Tx. rutilus were photographed and measured. Differences exist in qualitative and quantitative spine structure, with Aedes spp. forming one general group, Culex spp. another, and An. punctipennis and Or. signifera a third. The one specimen of Toxorhynchites rutilus examined was most like Culex spp. mosquitoes. Larval mosquito-habitat, adult mosquito-host associations, and pyloric armature and spine structures generally conformed to previously published accounts, indicating that mosquito biology inside zoos represents mosquito biology outside zoos. Therefore, zoos can be used for experiments not feasible in the field. However, novel variation (e.g., new, exotic host records) recorded in mosquito species warrants further investigation in zoos. iii My study demonstrates that zoos can be used as experiment environments to study mosquito behaviors (e.g., oviposition cues, innate versus learned host preferences, mosquito dispersal, and home range memory), and that findings can be extrapolated to non-zoo areas, while also providing medical and veterinary benefits to zoo animals, visitors, and the public. iv DEDICATION To my friends and family and the ―World‘s Greatest Medical Entomologist‖, William Wills & To Chris M. Stone, this work would not be what it is without your enthusiastic support and our rambling conversations. I can‘t wait to see where our adventures take us next. v ACKNOWLEDGMENTS I will forever be gladly indebted to W. Wills for guiding me into this profession. Thank you for finding me in the forest. I gratefully acknowledge the guidance of P.H. Adler, a graceful leader and outstanding person. ―The best of leaders when the job is done, when the task is accomplished, the people will say we have done it ourselves.‖ – Lao Tzu. I would like to thank the staff of both zoos including K. Benson DVM, H. Miller DVM, J. Bullock, B. Foster, K. Gilchrist, J. Lineberger, A. Norris, and S. Reno. Additionally, my thanks go to C. Beard, T. Brewer, C. Climer (―Exo-AP‖ protocol), C. Evans (Richland Co. DHEC collections), K. Korneva, J. McCall, J. McCreadie, M. Nelder, D. Swanson (identifications of Ceratopogonidae and Corethrellidae), and P. Vigueira. And, I am grateful to the lab of Dr. W. Foster at The Ohio State University for serving as my surrogate lab. I would also like to thank the W.C. Nettles Endowed Research Grant for partial research funding, the Nettles Travel Grant and Clemson GSG Professional Enrichment Grant for funding most of my professional presentations, the Terminix and Cochran Fellowships, the Filaria Research Reagent Repository in Athens, GA for materials and training (thank you E. Burkman), the SC Department of Health and Environmental Control for equipment, and the National Science Foundation Graduate Research Fellowship Program for financial support. vi TABLE OF CONTENTS Page TITLE PAGE .................................................................................................................... i ABSTRACT ..................................................................................................................... ii DEDICATION ................................................................................................................. v ACKNOWLEDGMENTS .............................................................................................. vi LIST OF TABLES .......................................................................................................... ix LIST OF FIGURES ......................................................................................................... x CHAPTER I. INTRODUCTION ......................................................................................... 1 II. LITERATURE REVIEW .............................................................................. 5 Mosquitoes in zoos .................................................................................. 5 Environmental characters of larval mosquito habitats ............................. 8 Blood hosts of mosquitoes ..................................................................... 16 Mosquitoes vectors of Dirofilaria immitis ............................................. 19 Pyloric armature of mosquitoes ............................................................. 23 III. HABITAT CHARACTERISTICS OF LARVAL MOSQUITOES IN SOUTH CAROLINA ZOOS ................ 27 Materials and methods ........................................................................... 29 Results .................................................................................................... 34 Discussion .............................................................................................. 40 IV. MOSQUITO HOSTS IN SOUTH CAROLINA ZOOS ............................................................................... 46 Materials and methods ........................................................................... 48 Results .................................................................................................... 56 Discussion .............................................................................................. 67 vii Table of Contents (Continued) Page V. PYLORIC ARMATURE OF MOSQUITOES ............................................ 72 Materials and methods ........................................................................... 75 Results .................................................................................................... 80 Discussion .............................................................................................. 90 VI. CONCLUSION ............................................................................................ 95 Public summary ..................................................................................
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