SCALE-DEPENDENT VARIATION IN MOLECULAR AND ECOLOGICAL PATTERNS OF INFECTION FOR ENDOHELMINTHS FROM CENTRARCHID FISHES BY KYLE E. LUTH A Dissertation Submitted to the Graduate Faculty of WAKE FOREST UNIVERSITY GRADAUTE SCHOOL OF ARTS AND SCIENCES in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY Biology May 2016 Winston-Salem, North Carolina Approved By: Gerald W. Esch, Ph.D., Advisor Michael V. K. Sukhdeo, Ph.D., Chair T. Michael Anderson, Ph.D. Herman E. Eure, Ph.D. Erik C. Johnson, Ph.D. Clifford W. Zeyl, Ph.D. ACKNOWLEDGEMENTS First and foremost, I would like to thank my PI, Dr. Gerald Esch, for all of the insight, all of the discussions, all of the critiques (not criticisms) of my works, and for the rides to campus when the North Carolina weather decided to drop rain on my stubborn head. The numerous lively debates, exchanges of ideas, voicing of opinions (whether solicited or not), and unerring support, even in the face of my somewhat atypical balance of service work and dissertation work, will not soon be forgotten. I would also like to acknowledge and thank the former Master, and now Doctor, Michael Zimmermann; friend, lab mate, and collecting trip shotgun rider extraordinaire. Although his need of SPF 100 sunscreen often put our collecting trips over budget, I could not have asked for a more enjoyable, easy-going, and hard-working person to spend nearly 2 months and 25,000 miles of fishing filled days and raccoon, gnat, and entrail-filled nights. You are a welcome camping guest any time, especially if you do as good of a job attracting scorpions and ants to yourself (and away from me) as you did on our trips. To my “biggest fans” back in the Hoosier state, I am eternally grateful for your ever- present love and support. Mother, I cannot easily express what your continued faith in me (yes, the restless, passionate, and hard-headed person I am) means to me; I know it has not always been easy… Much of the unwavering strength, dedication, drive, and passion I now possess, I truly believe came from the example set by you and Grandma Luth (who both exude these qualities as a rule). Aaron, I am so tremendously proud of you and all that you have accomplished in your life. I could not be more proud of my “little” brother for saving all those four-legged lives, and I cannot wait to see where life takes us both. My only hope is that we remain as close into the future as we have been to the present. To my other “little” brother, Kedrick, thank you for your friendship, love, and all-around awesomeness the past 5 years (holy cow!). Half my age and at least 2 inches taller (as of now), ii we may not be brothers in the traditional sense, but we will always be brothers in my heart and mind. I cannot express how grateful I am for your friendship and for the respite from my dissertation work our experiences together have provided. Hikes, food, fishing, movies, kayaking, volunteering, and on and on… You are an amazing young man and I cannot wait to see where life takes you. Keep working hard and remain the kind, loving, and polite guy you I (and others) know you to be. Finally, thanks to all my friends both in and out of the Department of Biology at Wake Forest. To my Winston Salem mom and dad, I love you both and I am so very thankful for the kindness, compassion, forgiveness, and support you have both shown me these past several years. To my Winston Salem running family, the Twin City Track Club, thanks for helping me continue to develop my love of running, for providing an escape from long hours at the microscope, and for helping me stave off excessive weight gain. I have had (and continue to have) many dear friends from the Wake Forest University Biology Department (Yoda, Friend, Katie Riley [and Gumdrop], Doo Doo, Franiel, and Mike Zimmermann, to name only a few), with whom bonds of friendship were formed through mutual suffering in the pursuit of advanced degrees. Perhaps forged in the furnace of mutual misery, these friendships persist because these people are simply amazing (and willing to deal with my numerous soap-boxes, impassioned monologues, and endearing hard-headedness [endearing, right?]). Thanks for still being my friends, through thick and thin. iii TABLE OF CONTENTS LIST OF ILLUSTRATIONS AND/OR TABLES......................................................................... vii ABSTRACT .................................................................................................................................. xiv CHAPTER I INTRODUCTION .............................................................................................................. 1 LITERATURE CITED ....................................................................................................... 4 CHAPTER II .................................................................................................................................... 6 Crypticity in the Bass Tapeworm, Proteocephalus ambloplitis (Leidy) (Cestoda: Proteocephalidae), Does Not Explain Regional Seasonal Life Cycle Differences In Revision: Journal of Parasitology ABSTRACT .......................................................................................................... 7 INTRODUCTION ................................................................................................. 8 MATERIALS AND METHODS ......................................................................... 11 RESULTS ............................................................................................................ 15 DISCUSSION ...................................................................................................... 17 LITERATURE CITED ........................................................................................ 22 CHAPTER III ................................................................................................................................ 34 Large-scale Patterns of Endoparasitic Helminth Infection in Green Sunfish ( Lepomis cyanellus ), Bluegills ( Lepomis macrochirus ), and Largemouth Bass (Micropterus salmoides ) from Freshwater Ponds and Lakes Across the United States In Revision: Journal of Parasitology ABSTRACT ........................................................................................................ 35 INTRODUCTION ............................................................................................... 36 MATERIALS AND METHODS ......................................................................... 38 RESULTS ............................................................................................................ 42 iv DISCUSSION ...................................................................................................... 47 LITERATURE CITED ........................................................................................ 53 CHAPTER IV A Survey of the Endoparasitic Helminths of Centrarchids across the United States: I. Those Occurring in Bluegills ( Lepomis macrochirus ) .................................................. 70 In Review: Comparative Parasitology ABSTRACT ........................................................................................................ 71 INTRODUCTION ............................................................................................... 72 MATERIALS AND METHODS ......................................................................... 74 RESULTS ............................................................................................................ 76 DISCUSSION .................................................................................................... 103 LITERATURE CITED ...................................................................................... 104 II. Those Occurring in Green Sunfish ( Lepomis cyanellus ) ............................................ 109 In Review: Comparative Parasitology ABSTRACT ...................................................................................................... 110 INTRODUCTION ............................................................................................. 111 MATERIALS AND METHODS ....................................................................... 113 RESULTS .......................................................................................................... 113 DISCUSSION .................................................................................................... 129 LITERATURE CITED ...................................................................................... 130 III. Those Occurring in the True Basses, Smallmouth Bass ( Micropterus dolomieu ) and Largemouth Bass ( Micropterus salmoides ) .................................................................... 134 In Review: Comparative Parasitology ABSTRACT ...................................................................................................... 135 INTRODUCTION ............................................................................................. 136 MATERIALS AND METHODS ....................................................................... 137 v RESULTS .......................................................................................................... 137 DISCUSSION .................................................................................................... 150 LITERATURE CITED ...................................................................................... 151 IV. Those occurring in Ambloplites rupestris , Lepomis spp., Pomoxis