Host-Parasite Interactions of North American Guinea Worm (Nematoda: Dracunculus) and Its Mammalian Hosts
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Host-Parasite Interactions of North American Guinea Worm (Nematoda: Dracunculus) and its Mammalian Hosts By Sarah Carissa Elsasser Thesis submitted in partial fulfillment of the requirement for the degree of Doctor of Philosophy (PhD) in Boreal Ecology School of Graduate Studies Laurentian University Sudbury, Ontario © Sarah Carissa Elsasser, 2011 Library and Archives Bibliotheque et Canada Archives Canada Published Heritage Direction du 1+1 Branch Patrimoine de I'edition 395 Wellington Street 395, rue Wellington Ottawa ON K1A0N4 Ottawa ON K1A 0N4 Canada Canada Your file Votre reference ISBN: 978-0-494-87730-2 Our file Notre reference ISBN: 978-0-494-87730-2 NOTICE: AVIS: The author has granted a non L'auteur a accorde une licence non exclusive exclusive license allowing Library and permettant a la Bibliotheque et Archives Archives Canada to reproduce, Canada de reproduire, publier, archiver, publish, archive, preserve, conserve, sauvegarder, conserver, transmettre au public communicate to the public by par telecommunication ou par I'lnternet, preter, telecommunication or on the Internet, distribuer et vendre des theses partout dans le loan, distrbute and sell theses monde, a des fins commerciales ou autres, sur worldwide, for commercial or non support microforme, papier, electronique et/ou commercial purposes, in microform, autres formats. paper, electronic and/or any other formats. The author retains copyright L'auteur conserve la propriete du droit d'auteur ownership and moral rights in this et des droits moraux qui protege cette these. Ni thesis. Neither the thesis nor la these ni des extraits substantiels de celle-ci substantial extracts from it may be ne doivent etre imprimes ou autrement printed or otherwise reproduced reproduits sans son autorisation. without the author's permission. In compliance with the Canadian Conformement a la loi canadienne sur la Privacy Act some supporting forms protection de la vie privee, quelques may have been removed from this formulaires secondaires ont ete enleves de thesis. cette these. While these forms may be included Bien que ces formulaires aient inclus dans in the document page count, their la pagination, il n'y aura aucun contenu removal does not represent any loss manquant. of content from the thesis. Canada Abstract Parasites have the potential to negatively influence the fitness of host organisms. Despite this, the ecology and effects of many wildlife parasites are largely unknown. Dracunculus insignis is a nematode parasite that infects raccoon (Procyon lotor), American mink (Neovison vison), and fisher (Martes pennant!). D. lutrae is a morphologically similar dracunculoid, but has only been recovered from river otter (Lontra canadensis). Until now, species identification of these two North American guinea worms was only achievable by morphology of males and host identification. In this study, DNA barcoding was used to differentiate between D. insignis and D. lutrae, and validated the occurrence of the former in a newly discovered host: the river otter. The occurrence of D. insignis in river otter highlights the need to supplement identification methods for certain nematodes using DNA techniques. The host specialization and host exploitation strategies of the generalist D. insignis and the specialist D. lutrae were compared. According to the trade-off hypothesis, specialist parasite species should be more 'successful' in terms of prevalence and intensity than generalist parasite species due to a trade-off between how many host species a parasite can exploit and its success. As predicted, the specialist D. lutrae infected their host at higher rates and intensities than the generalist D. insignis, which supports the trade-off hypothesis. This investigation of host exploitation strategies in the generalist D. insignis revealed that this species does not exploit all host species to the same degree. In general, mink and raccoon were more likely to be infected than fisher; however, guinea iii worm grew to a larger size in fisher. This may reflect a particular strategy that D. insignis has developed in order to increase its chances of transmission in the environment. Although no evidence of sex or age bias in guinea worm prevalence or intensity were found in this study, results indicate that condition of juvenile male fisher infected with guinea worm decreases with increasing guinea worm infection intensity. Because of the sexual size dimorphism in fisher and because males take longer to mature, males have increased energetic requirements compared to females, possibly making males more susceptible to negative effects of guinea worm parasitism because of their relatively already depleted resources. Decreased body condition due to guinea worm infection may have long-term implications for host fitness or host population health. Potential effects of guinea worm on fecundity of host female fisher were also investigated. No difference in fecundity between uninfected and infected hosts was found, and guinea worm parasitism did not appear to alter the proportion of females able to achieve pregnancy; however, a significant negative relationship was found between infection intensity and fecundity. In natural systems, guinea worm has the potential to play a regulating role in population dynamics of the host. iv Acknowledgements Thank you to my supervisor Dr. Albrecht Schulte-Hostedde, and advisory committee members; Drs. Mark Forbes, Mery Martinez-Garcia, Thomas Merritt and Jean-Francois Robitaille. Thanks also to Drs. Paul Hebert and Robin Floyd from the Biodiversity Institute of Ontario, University of Guelph. I am very thankful for the comments and suggestions provided by Drs. Eric Gauthier and Daniel McLaughlin. Thanks so much to the many faculty and staff of the Biology Department and the Office of Graduate Studies throughout the years. I am very appreciative of my fellow lab mates and the waves of Biology and other LU graduate students with whom I have had the pleasure of interacting with and forming friendships with over the years, particularly Sophie, Anne, Vanessa B., Andreas, Ranji, Dean, Curtis, Mandy, the Spikin' Scientists, the Laurentian Voyeurs, and the Masters of the University. I am very grateful to the fur trappers who assisted me with sample collections. This work was supported financially by the Laurentian University Graduate Teaching and Research Assistantships, OGSST-Tembec Scholarship, Canadian Mink Breeders Association Arlen Kerr Memorial Scholarship, Ruffed Grouse Society Wildlife & Conservation Award, and National Science and Engineering Research Capacity Building grants. I have had unlimited positive energy and encouragement from my family and friends (Sudbury, Yellowknife, and beyond) throughout this process. Very special thanks to my parents, my brother David and sister Mckenna, the Grattons, my Boivin and Elsasser clans, Sydney and the Cotts, and my little buddy Diego. My very caring and loyal family means the world to me. A big masicho to my employer, the Wek'eezhii Land and Water Board, and my coworkers for their support and positive energy in the final stretch. I am eternally grateful for Pete's unwavering support and encouragement, his discussion and proofreading, his shoulder to cry on, his patience when I was going insane with this, and his optimism that the agony and suffering that persisted throughout the completion of this thesis would eventually end, and be worth it. Thank you Pete. 1 love you very much. This work is dedicated to my parents. Dad and Mom: thank you for being there for me every step of the way. I am forever appreciative of your endless supply of love, encouragement, and support. I love you both. v List of Original Papers This thesis is based on four papers, which will be referred to by their Chapter title. Chapter 2 Elsasser, S.C., R. Floyd, P.D.N. Hebert, and A.I. Schulte-Hostedde. 2009. Species identification of North American guinea worms (Nematoda: Dracunculus) with DNA barcoding. Molecular Ecology Resources 9: 707 - 712. Chapter 3 Elsasser, S.C., and A.I. Schulte-Hostedde. Host specialization and exploitation strategies of Dracunculus spp. (manuscript) Chapter 4 Elsasser, S.C., T. Kraus, J.-F. Robitaille, and G.H. Parker. The influence of guinea worm (Dracunculus insignis) infection on host body condition and fecundity of fisher (Martes pennanti). (manuscript) Chapter 5 Elsasser, S.C., and A.I. Schulte-Hostedde. The influence of guinea worm (Dracunculus spp.) on host body condition, (manuscript) vi Table of Contents List of Figures viii List of Tables x CHAPTER 1 - General Introduction 1 CHAPTER 2 - Species identification of North American guinea worms 18 (Nematoda: Dracunculus) with DNA barcoding 18 Introduction 18 Methods 21 DNA extraction, amplification and sequencing 23 Data analyses 24 Results 24 Discussion 30 CHAPTER 3 - Host Specialization and Exploitation Strategies of Dracunculus spp 33 Introduction 33 Methods 41 Results 43 Host exploitation strategies of D. insignis and D. lutrae 43 Host sex effect on Dracunculus spp. infection patterns 50 Host age effect on Dracunculus spp. infection patterns 52 Discussion 55 CHAPTER 4 - The influence of guinea worm (Dracunculus insignis) infection on body condition and fecundity of fisher [Martes pennanti) 60 Introduction 60 Methods 63 Prevalence and intensity of guinea worm infections 63 Body Condition 64 Fecundity 65 Statistical Analyses 67 Results 68 Prevalence and intensity of guinea worm infections 68 Body Condition 70 Fecundity 72 Discussion 75 CHAPTER 5 - The influence of guinea