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REVEALING BIOTIC DIVERSITY: HOW DO COMPLEX ENVIRONMENTS INFLUENCE HUMAN SCHISTOSOMIASIS in a HYPERENDEMIC AREA Martina R

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REVEALING BIOTIC DIVERSITY: HOW DO COMPLEX ENVIRONMENTS INFLUENCE HUMAN SCHISTOSOMIASIS in a HYPERENDEMIC AREA Martina R University of New Mexico UNM Digital Repository Biology ETDs Electronic Theses and Dissertations Spring 5-9-2018 REVEALING BIOTIC DIVERSITY: HOW DO COMPLEX ENVIRONMENTS INFLUENCE HUMAN SCHISTOSOMIASIS IN A HYPERENDEMIC AREA Martina R. Laidemitt Follow this and additional works at: https://digitalrepository.unm.edu/biol_etds Recommended Citation Laidemitt, Martina R.. "REVEALING BIOTIC DIVERSITY: HOW DO COMPLEX ENVIRONMENTS INFLUENCE HUMAN SCHISTOSOMIASIS IN A HYPERENDEMIC AREA." (2018). https://digitalrepository.unm.edu/biol_etds/279 This Dissertation is brought to you for free and open access by the Electronic Theses and Dissertations at UNM Digital Repository. It has been accepted for inclusion in Biology ETDs by an authorized administrator of UNM Digital Repository. For more information, please contact [email protected]. Martina Rose Laidemitt Candidate Department of Biology Department This dissertation is approved, and it is acceptable in quality and form for publication: Approved by the Dissertation Committee: Dr. Eric S. Loker, Chairperson Dr. Jennifer A. Rudgers Dr. Stephen A. Stricker Dr. Michelle L. Steinauer Dr. William E. Secor i REVEALING BIOTIC DIVERSITY: HOW DO COMPLEX ENVIRONMENTS INFLUENCE HUMAN SCHISTOSOMIASIS IN A HYPERENDEMIC AREA By Martina R. Laidemitt B.S. Biology, University of Wisconsin- La Crosse, 2011 DISSERT ATION Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Biology The University of New Mexico Albuquerque, New Mexico July 2018 ii ACKNOWLEDGEMENTS I thank my major advisor, Dr. Eric Samuel Loker who has provided me unlimited support over the past six years. His knowledge and pursuit of parasitology is something I will always admire. I would like to thank my coauthors for all their support and hard work, particularly Dr. Sara Brant, Mr. Martin Mutuku, Ms. Eva Zawadzki, Dr. Gerald Mkoji, Ms. Larissa Anderson and Dr. Helen Wearing. I also thank my committee members, Drs. Jennifer Rudgers, Stephen Stricker, William Evan Secor, and Michelle Steinauer for their expertise, time, insight, and critiques of this work. I thank my lab mates and members the parasitology group at UNM: Dr. Erika Gendron, Ms. Melissa Sanchez, Ms. Janeth Pena, Mr. Jon Schultz, Dr. Sarah Buddenborg, Ms. Lijun Lu, Dr. Bishoy Hanna, Dr. Ben Hanelt, Dr. Bruce Hofkin, Ms. Caitlin Babbitt, Ms. Heather Mercer, Dr. Ramesh Devkota and Dr. Si- Ming Zhang thank you for your discussions, encouragement and friendship. Also, to my collaborators, Dr. Eric Lelo, Mr. Ibrahim Mwangi, Mr. Geoffery Mania, and Joesph Kinuthia at the Kenyan Research Medical Institute for your assistance in the field and help with this work. Lastly, but most notably I would like to thank my family for their love and support over the years. I thank my childhood friends, Ms. Lacey Squier, Ms. Beth Jerabek, and Ms. Kortney Hamilton for their encouragement. They knew long before I did that I would be writing this dissertation. I particularly thank Sam Hodder for his endless support throughout this process even when I would be away from home for long periods of time in the field. Finally, I thank our dogs, Mr. iii Sheebs and River for putting up with my shenanigans and for their companionship. They may have missed a few walks over the years, but they always greeted me with a wagging tail. iv Revealing biotic diversity: How do complex environments influence human schistosomiasis in a hyperendemic area By Martina R. Laidemitt B.S. Biology, University of Wisconsin- La Crosse, 2011 Ph.D. Biology, University of New Mexico, 2018 ABSTRACT Human schistosomiasis is one of the great neglected tropical diseases (NTDs) of our time with more than 206 million individuals infected and more than 90% of those infected reside in Sub-Saharan Africa (WHO 2017). Chemotherapy based control programs play an essential role in contributing to the elimination of human schistosomiasis; however, there is an increasing consensus that chemotherapy needs to be supplemented by other means if interruption of transmission and elimination are to be achieved. Given this situation, the focus of this dissertation was to better understand transmission dynamics in a hyperendemic setting in western Kenya and to find alternative measures to supplement ongoing mass drug administration (MDA) using indigenous resources that disrupt the development of Schistosoma mansoni (the causative agent of intestinal schistosomiasis in Africa) within its obligatory aquatic snail intermediate host, Biomphalaria. The discipline of disease ecology emphasizes understanding the biotic context in which disease transmission occurs. S. mansoni and Biomphalaria exist v within a complex ecological milieu in streams, ponds and lakes in Kenya. The research in this dissertation combined DNA barcodes, phylogenetics, host use patterns and morphology to determine the diversity of trematodes that use Kenyan Biomphalaria as an intermediate host. Along with S. mansoni, we found 21 additional digenetic trematodes that also use Biomphalaria species in Kenya as an intermediate host. The presence of other trematode species in Biomphalaria affects S. mansoni by causing competition for access to snail resources. Furthermore, we used experimental approaches to understand the competitive dynamics among these trematodes and to generate a dominance hierarchy among them. We found that several trematode species are dominant to S. mansoni and long-term agricultural practices have created a situation where an amphistome parasite of cattle relies on a facilitating effect by S. mansoni for its own successful development in the snail host. Coupled with these data are four years of observational survey data to predict how these trematodes influence S. mansoni’s prevalence in Biomphalaria and consequently the likelihood of influencing human infections. vi TABLE OF CONTENTS TABLE OF CONTENTS…………………………………………………………….....vii INTRODUCTION………………………………………………………………………..1 References……………………………………………………………………....5 CHAPTER 1: Loads of trematodes: Discovering hidden diversity of paramphistomoids in Kenyan ruminants…………………………………………8 Abstract…………………………………………………………………………..9 Introduction……………………………………………………………………..10 Materials and Methods……………………………………………………..…13 Results…………………………………………………………………….……18 Discussion………………………………………………………………………22 Acknowledgements …………………………………………………………...31 Financial Support……………………………………………………………...31 References …………………………………………………………………….33 Figures and Tables……………………………………………………………46 CHAPTER 2: The diverse echinostomes from East Africa: with a focus on species that use schistosome transmitting snails as intermediate hosts...59 Abstract………………………………………………………………………....60 Introduction……………………………………………………………………..60 vii Materials and Methods………………………………………………………..65 Results………………………………………………………………………….68 Discussion……………………………………………………………………...77 Acknowledgements……………………………………………………………86 Financial Support………………………………………………………………86 References …………………………………………………………………….88 Figures and Tables…………………………………………………………....99 CHAPTER 3: Cascading effects of pastoralism, biodiversity and habitat stability on the transmission of one of the world’s most abundant neglected tropical diseases, schistosomiasis………………………………...107 Abstract………………………………………………………………………..108 Introduction………………………………………………………………..….108 Results………………………………………………………………………...110 Discussion…………………………………………………………………….123 Methods……………………………………………………………………….130 Acknowledgements…………………………………………………………..135 References……………………………………………………………………137 Figures and Tables…………………………………………………………..146 CONCLUSIONS………………………………………………………………….…..159 viii References……………………………………………………………………163 ix INTRODUCTION African countries have relied extensively on mass administration of the drug, praziquantel (PZQ) in attempt to control human schistosomiasis. However, mounting evidence suggests that even after 5-10 years of annual treatments there is little reduction in disease prevalence (Lamberton et al., 2014; Andrade et al., 2017), or in schistosome genetic diversity (Lelo et al., 2014), calling for the need of alternative measures to control human schistosomiasis (Rollinson et al., 2013; Loker et al., 2013). Interventions such as education, increased hygiene, water sanitation, and particularly snail control should be used as supplemental control strategies along with PZQ administration (Rollinson et al, 2013; Loker et al., 2013; Sokolow et al., 2017). Along these lines, we were interested in the finding alternative indigenous measures to control snails, because molluscicides (chemicals that kill snails) used for snail control are expensive and can have detrimental effects on fish and non-target gastropods (Rollinson et al., 2013). In recent years biologists have gained an increased appreciation for the reality that infectious diseases exist in complex ecological systems (Johnson and Thieltges, 2010; Keesing et al., 2010; Civitello et al., 2015). For example, according to the dilution hypothesis, a diverse community may interfere with transmission of a particular parasite by diverting the parasite into inappropriate hosts or by regulating the populations of susceptible hosts. On the other hand, transmission may be favored in diverse communities by providing more competent host species and thus more transmission options. Therefore, the biotic context in which disease transmission occurs must be considered carefully because not all host-parasite systems are 1 the same and because diversity can have both positive and negative effects in a given host-parasite system, particularly for parasites
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