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Miami University – the Graduate School MIAMI UNIVERSITY – THE GRADUATE SCHOOL CERTIFICATE FOR APPROVING THE DISSERTATION We hereby approve the Dissertation of Kata C. Gurski Candidate for the Degree Doctor of Philosophy Mercedes A. Ebbert, Director Thomas O. Crist, Reader Dennis L. Claussen, Reader Marcia R. Lee, Reader Marjorie M. Cowan, Graduate School Representative ABSTRACT THE NATURAL PREVALENCE OF TRYPANOSOMATIDS (KINETOPLASTIDA: TRYPANOSOMATIDAE) IN AQUARIUS REMIGIS (SAY) (HEMIPTERA: GERRIDAE), AND THEIR EFFECT ON GERRID MORPHOLOGY By Kata C. Gurski Insect-parasite interactions and their possible effects on the surrounding community are rarely studied in the context of a natural environment. Typically, studies examine the effect of parasitic infections under controlled conditions often varying one condition at a time with respect to infection. While these studies are important for isolating the effects parasites exert on insects, they may provide only limited insight to the actual host-parasite interaction as they occur in a natural setting when both organisms are exposed to a multitude of environmental stresses. Long- term observational studies of parasite prevalence are a logical starting point for studies of host- parasite interactions. Thus, the purpose of this dissertation was to address the following questions with respect to trypanosomatid parasites of Aquarius remigis hosts. First, what is the natural prevalence of trypanosomatids in gerrids within and among annual field seasons? Second, how does uninfected gerrid morphology vary spatially and temporally, and with respect to mating status? And third, does trypanosomatid infection affect morphological development of field-caught gerrids? From 1999 to 2002 I sampled 7633 adult and nymph Aquarius remigis gerrids from eight locations in four streams in Butler County, Ohio. I assayed 6836 gerrids for trypanosomatid infection and measured nine morphological traits of 688 individuals. Trypanosomatids were present in all four streams, and persisted at each site over the course of the study. Prevalence increased with host age, but did not differ between males and females. Patterns were similar among streams and years. Variation within a year was consistent with variation in gerrid mating periods, but not gerrid density. Gerrid morphology varied, but not consistently, between host generations, and among streams and location within stream. Trypanosomatid infections were associated with smaller adult males, but not females, and this effect was variable within and among streams. I suggest that both variation in parasite prevalence over time and in gerrid morphology over time and space is influenced by fluctuating environmental conditions. This study not only demonstrates the importance of long-term studies of parasite prevalence and host-parasite interactions, but it also suggests that variation in these interactions may be overlooked if only a single population is examined. THE NATURAL PREVALENCE OF TRYPANOSOMATIDS (KINETOPLASTIDA: TRYPANOSOMATIDAE) IN AQUARIUS REMIGIS (SAY) (HEMIPTERA: GERRIDAE), AND THEIR EFFECT ON GERRID MORPHOLOGY A DISSERATATION Submitted to the Faculty of Miami University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Zoology by Kata C. Gurski Miami University Oxford, OH 2003 Dissertation Director: Dr. Mercedes A. Ebbert TABLE OF CONTENTS ACKNOWLEDGMENTS.….…………………………………………………….iii LIST OF TABLES………………………………………………………………....iv LIST OF FIGURES………………………………………………………………..vi DEDICATION……………………………………………………………………vii CHAPTER 1: Dissertation Introduction …………………………………………. 1 CHAPTER 2: Changes in reproductive life history patterns of the gerrid, Aquarius remigis (Say) (Hemiptera: Gerridae), alter trypanosomatid (Kinetoplastida: Trypanosomatidae) prevalence …………………………………………………...12 CHAPTER 3: Spatial and temporal variation in Aquarius remigis (Say) (Hemiptera: Gerridae) morphology ……………………………………………………………45 CHAPTER 4: Trypanosomatid (Kinetoplastida: Trypanosomatidae) infection reduces adult Aquarius remigis (Say) (Hemiptera: Gerridae) body size ………...69 CHAPTER 5: Dissertation Conclusion ………………………………………….83 LITERATURE CITED……………………………………………………………88 TABLES…………………………………………………………………………103 FIGURES………………………………………………………………………...146 APPENDIX A……………………………………………………………………176 APPENDIX B……………………………………………………………………198 ii ACKNOWLEDGMENTS I am grateful for the assistance, encouragement and patience of my advisor, Dr. Mercedes Ebbert. Thank you to my dissertation committee, Dr. Thomas Crist, Dr. Dennis Claussen, Dr. Marcia Lee, and Dr. Marjorie Cowan. Thanks to Kelly Buchanan, Jennifer Avondet, Ben Knopp, Sarah McMasters, and Dan Thomas for their field and laboratory support. Funds for this project were provided by Miami University. iii LIST OF TABLES 1. Breakdown of gerrids caught, assayed and analyzed………………………..…103 2. Experimental design……………………………………………………………104 3. Collection dates and gerrid density…………………………………………….105 4. Monthly average for gerrids caught and analyzed…………………………..…109 5. Average monthly and seasonal adult and nymph density………………………110 6. ANOVA of gerrid density………………………………………………………112 7. Contingency table for gerrid location paired analysis………………………….113 8. Contingency table for gerrid mating status paired analysis…………………….114 9. Contingency table for gerrid sex paired analysis……………………………….115 10. Contingency table for gerrid overwintering paired analysis……………………116 11. Contingency table for gerrid stage paired analysis…………………………….117 12. Yearly and monthly trypanosomatid prevalence in adults per stream…………118 13. Yearly and monthly trypanosomatid prevalence in nymphs per stream……….121 14. Monthly and seasonal trypanosomatid prevalence…………………………….124 15. Chi-square analysis of prevalence……………………………………………...126 16. MANOVA of stream location and adult morphology………………………….127 17. Summary statistics for stream location and adult morphology………………...128 18. MANOVA of generation, sex and stream on adult morphology………………129 19. Summary statistics for generation and adult morphology……………………..130 20. Summary statistics for generation, stream and adult morphology……………. 131 21. ANOVA of stream location and fluctuating asymmetry.………………………132 iv 22. MANOVA of mating status and adult morphology……………………………133 23. ANOVA of mating status and fluctuating asymmetry…………………………134 24. MANOVA of nymph morphology……………………………………………..135 25. Summary statistics for stream location and nymph morphology………………136 26. Summary statistics for sex, age and nymph morphology………………………137 27. MANOVA of infection, stream location and adult male morphology…………138 28. MANOVA of four-way interaction on adult morphology……………………..139 29. MANOVA of infection, stream and adult G1 male morphology………………140 30. Summary statistics for infection, stream and adult G1 male morphology……..141 31. MANOVA of infection and adult morphology………………………………...142 32. Summary statistics for infection, stream and adult male morphology…………143 33. ANOVA of infection, stream location and fluctuating asymmetry…………….144 34. ANOVA of infection, stream and fluctuating asymmetry……………………..145 v LIST OF FIGURES 1. Host-parasite interactions………………………………………………………..146 2. Study area map…………………………………………………………………..148 3. Precipitation……………………………………………………………………...150 4. Temperature……………………………………………………………………...152 5. Nymph density…………………………………………………………………...154 6. Adult density……………………………………………………………………..156 7. Trypanosomatid prevalence and density correlation…………………………….158 8. Gerrid mating activity……………………………………………………………160 9. Trypanosomatid prevalence in nymphs year 2000………………………………162 10. Trypanosomatid prevalence in adults year 2000………………………………..164 11. Trypanosomatid prevalence in adults year 2001………………………………..166 12. Trypanosomatid prevalence in adults year 2002………………………………..168 13. Trypanosomatid prevalence in adults year 1999………………………………..170 14. Hypothetical host-parasite interactions…………………………………………172 15. Adult body length and fluctuating asymmetry correlation……………………...174 vi Dedicated to the memory of my dad, Dr. Richard Joseph Gurski vii CHAPTER 1 DISSERTATION INTRODUCTION 1 Parasites play an important role in the biology of animals. They are a significant source of host mortality and thus indirectly influence the interactions of populations within a community (Fuxa and Tanada, 1987; Thompson, 1994; Freeland, 1983; Price et al., 1986; Price et al., 1988; Minchella and Scott, 1991; Combs, 1995; Combs, 1996; Hudson and Greenman, 1998). The impact of parasites can be more subtle and complex than directly causing host mortality. For example, parasites can affect host interactions with the environment: when stressed by limited food availability or cold environments, the negative effects of parasites on their hosts may be enhanced (Spence, 1986). Sublethal infections may influence host population structure in this manner (e.g., Klingenberg et al., 1997) and thus, indirectly shape the structure of the surrounding community. Although ecologists acknowledge the importance of parasites in communities, their effects remain under-investigated (Thomas et al., 2000). Parasites can also alter, directly or indirectly, host life-history traits, such as fecundity, growth or survival (review in Michalakis and Hochberg, 1994). Changes in host traits result in variation among both individuals and populations and can affect species coexistence (Thomas et al., 2000; Poulin, 1999). For example, parasites can affect the developmental rate of hosts and thus cause temporal segregation between competitors. Parasites that affect the dispersal
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