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Ecological Interactions of the Trematode Parasite Zoogonus Rubellus and Its First and Second Intermediate Hosts

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Ecological Interactions of the Trematode Parasite Zoogonus Rubellus and Its First and Second Intermediate Hosts University of New Hampshire University of New Hampshire Scholars' Repository Doctoral Dissertations Student Scholarship Spring 2021 Ecological interactions of the trematode parasite Zoogonus rubellus and its first and second intermediate hosts Sara Edquist University of New Hampshire, Durham Follow this and additional works at: https://scholars.unh.edu/dissertation Recommended Citation Edquist, Sara, "Ecological interactions of the trematode parasite Zoogonus rubellus and its first and second intermediate hosts" (2021). Doctoral Dissertations. 2567. https://scholars.unh.edu/dissertation/2567 This Dissertation is brought to you for free and open access by the Student Scholarship at University of New Hampshire Scholars' Repository. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of University of New Hampshire Scholars' Repository. For more information, please contact [email protected]. Ecological interactions of the trematode parasite Zoogonus rubellus and its first and second intermediate hosts By Sara Edquist BA Boston University, 2008 DISSERTATION Submitted to the University of New Hampshire in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in Zoology May 2021 This dissertation was examined and approved in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Zoology by: Dissertation Director: Larry G. Harris Ph.D. Professor Emeritus, Biological Sciences. University of New Hampshire Dissertation Committee: Jessica A. Bolker Ph.D. Professor, Biological Sciences. University of New Hampshire James Haney Ph.D. Professor, Biological Sciences. University of New Hampshire Walter Lambert Ph.D. Professor, Department of Biology. Framingham State University Thomas Lee Ph.D. Professor Emeritus, Natural Resources. University of New Hampshire April 21, 2021 Approval signatures are on file with the University of New Hampshire Graduate School. ii ACKNOWLEDGEMENTS First, I must thank my advisor Larry Harris for his mentorship and patience over the years and for giving me the freedom and encouragement to explore my research interests (including those that are not included in this dissertation). I would like to thank my Dr. Walter Lambert, Dr. Jessica Bolker, Dr. James Haney, Dr. Tom Lee, and Dr. Marian Litvitis for their guidance throughout my dissertation that led me to ideas and connections that I might not have discovered on my own. Thank you to my labmates and undergraduate assistants without whom I would not have been able to complete this work. A special thank you to Kayla Pope, Dusty Durant, my sister Erin Edquist, Kathryn Totten, Mary Offutt, Deena Hardy, Seth Goodnight, Kaitlin van Volkom, and Anna Chase, all of whom ventured into the mudflats to help me dig for worms. A special thank you to my friends and family whose unwavering support throughout this entire process has been invaluable. Thank you, in particular, to my husband, Stephen Mahnke, without whose love, patience, and encouragement I would not have been able to complete this work. And finally, thank you to my daughter Summer, who has been an unknowing source of comfort and encouragement on the toughest days. Thank you to the UNH Department of Biological Sciences and the UNH School of Marine Science and Ocean Engineering for financial support. Thank you to the UNH Graduate School for funding my research through the Summer TA Fellowship. iii TABLE OF CONTENTS ACKNOWLEDGEMENTS…………………………………………………………… iii LIST OF TABLES…………………………………………………………….…......... vi LIST OF FIGURES……………………………………………………….…………… vii ABSTRACT…………………………………………………………………………… ix INTRODUCTION…………………………………………………………………….. 1 CHAPTER 1: Spatial and temporal distribution of Zoogonus rubellus in first and second intermediate hosts in Great Bay Estuary……………………………………………… 12 Introduction…………………………………………………………………… 12 Methods……………………………………………………………………….. 14 Results…………………………………………………………………………. 23 Discussion……………………………………………………………………… 64 Conclusion……………………………………………………………………... 94 CHAPTER 2: Cercarial emergence patterns of Zoogonus rubellus and infection risk to second intermediate hosts…………………………………………………………………….. 98 Introduction…………………………………………………………………… 98 Methods……………………………………………………………………….. 100 Results…………………………………………………………………………. 103 Discussion……………………………………………………………………… 108 iv Conclusion……………………………………………………………………... 117 CHAPTER 3: Effects of Zoogonus rubellus infection on the predation activity and growth of the second intermediate nereid worm hosts………………………………………………. 119 Introduction…………………………………………………………………… 119 Methods……………………………………………………………………….. 123 Results…………………………………………………………………………. 127 Discussion……………………………………………………………………… 136 Conclusion……………………………………………………………………… 146 GENERAL CONCLUSION…………………………………………………………… 149 REFERENCES…………………………………………………………………………. 153 APPENDIX A: GPS coordinates for survey sites……………………………………… 170 APPENDIX B: Larval stages of trematodes found within Z. rubellus…………………. 171 v LIST OF TABLES Table 1: Trematode species of I. obsoleta…………………………………………..…………….8 Table 1.1: Site characteristics and I. obsoleta demographics summary ....................................... 30 Table 1.2: Infection prevalence among I. obsoleta with a shell length ≥12mm ........................... 36 Table 1.3: ANOVA results of comparison of trematode species prevalence within sites ............ 37 Table 1.4: ANOVA results of comparison of density of each trematode infected snail population between sites ................................................................................................................................. 39 Table 1.5: Statistical results from correlation analyses ................................................................ 51 Table 1.6: Correlation analyses of infection patterns in I. obsoleta and nereid worms ................ 59 Table A.A.1: GPS coordinates for sites surveyed in yearly and seasonal surveys (Ch. 1)……..170 vi LIST OF FIGURES Figure 1: Life cycle of Zoogonus rubellus………………………………………………..……… 3 Figure 1.1: Survey sites within Great Bay Estuary ....................................................................... 15 Figure 1.2: Density of first intermediate host I. obsoleta at six sites in Great Bay Estuary ......... 31 Figure 1.3: Mean shell length of I. obsoleta at six sites in Great Bay Estuary ............................. 32 Figure 1.4: Mean shell length (mm) of trematode infected and uninfected I. obsoleta ................ 33 Figure 1.5: Correlation between shell aperture thickness (mm) and shell length (mm) for uninfected and infected I. obsoleta ............................................................................................... 34 Figure 1.6: Infection prevalence among I. obsoleta ..................................................................... 35 Figure 1.7: Infection prevalence of each trematode among I. obsoleta by sites ........................... 37 Figure 1.8: Density of infected snails by site ................................................................................ 38 Figure 1.9: Density of second intermediate hosts Hediste diversicolor, Neanthes succinea, and Alitta virens in Great Bay Estuary ................................................................................................ 40 Figure 1.10: Wet mass of H. diversicolor, N. succinea, and A. virens ......................................... 51 Figure 1.11: Infection prevalence of Z. rubellus within the nereid worms................................... 52 Figure 1.12: Infection intensity of Z. rubellus within the nereid worms ...................................... 53 Figure 1.13: Cumulative density of Z. rubellus metacercariae from all nereid worms ................ 54 Figure 1.14: Infection prevalence of Himasthla sp. and L. setiferoides within the nereid worms 55 Figure 1.15: Infection intensity of Himasthla sp. and L. setiferoides within the nereid worms ... 56 Figure 1.16: Aggregation of Z. rubellus metacercariae within nereid worm hosts ...................... 57 Figure 1.17: Correlation between infection intensity of Z. rubellus metacercariae within nereid worm hosts and the density of I. obsoleta infected with Z. rubellus. ........................................... 58 vii Figure 1.18: Correlation between the mean infection intensity of Z. rubellus metacercariae among nereid worms within a site and the mean intensity of old cysts ........................................ 60 Figure 1.19: Seasonal infection intensity of Z. rubellus, Himasthla sp., and L. setiferoides in the three nereid worm hosts. ............................................................................................................... 61 Figure 1.20: Seasonal infection prevalence of Z. rubellus, Himasthla sp., and L. setiferoides in the three nereid worm hosts. ......................................................................................................... 62 Figure 2.1: Effect of temperature and salinity on the cercarial shedding of Z. rubellus ............ 105 Figure 2.2: Salinity trial 1 - cercarial shedding of Z. rubellus from I. obsoleta ......................... 106 Figure 2.3: Salinity trial 2 - cercarial shedding of Z. rubellus from I. obsoleta ......................... 106 Figure 2.4: Mean daily water temperature in Great Bay Estuary. .............................................. 107 Figure 2.5: Mean daily salinity in Great Bay Estuary ................................................................ 107 Figure 3.1: Susceptibility trials: infection intensity of Z. rubellus metacercariae
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