MAMMAL AND FLEA OCCURRENCE IN ASSOCIATION WITH BLACK-TAILED PRAIRIE DOG (CYNOMYS LUDOVICIANUS) COLONIES: IMPLICATIONS FOR INTERSPECIFIC PLAGUE TRANSMISSION By ROBERT JORIS BRINKERHOFF B.S. University of Illinois, Urbana/Champaign, 1998 M.S. North Carolina State University, Raleigh, 2002 A thesis submitted to the Graduate School of the University of Colorado in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology 2008 This thesis entitled: Mammal and Flea Occurrence in Association With Black-Tailed Prairie Dog (Cynomys ludovicianus) Colonies: Implications for Intraspecific Plague Transmission Written by Robert Joris Brinkerhoff Has been approved for the department of Ecology and Evolutionary Biology _________________________________ Sharon Collinge (Committee Chair) _________________________________ Andrew Martin _________________________________ Jason Knouft _________________________________ David Armstrong _________________________________ Michelle Sauther Date _____________ The final copy of this thesis has been examined by the signatories, and I find that both the content and the form meet acceptable presentation standards of scholarly work in the above mentioned discipline ii Brinkerhoff, Robert Joris (Ph.D. Ecology and Evolutionary Biology) Mammal and Flea Occurrence in Association With Black-Tailed Prairie Dog (Cynomys ludovicianus) Colonies: Implications for Intraspecific Plague Transmission Thesis directed by Associate Professor Sharon K. Collinge Sylvatic plague is an enigmatic disease affecting over 200 mammalian species worldwide, yet its dynamics and ecology are poorly understood. Transmitted by fleas, plague was introduced into North America in the 19th century and threatens humans and wildlife species, most notably, the black-tailed prairie dog. This thesis focuses on elucidating potential mechanisms of plague transmission among mammals in Colorado by examining the community of alternate disease hosts and vectors in which plague exists in four ways. First, I examined spatial and temporal patterns of plague emergence in mammalian species most likely to acquire infection. Second, I described and evaluated occurrence patterns of fleas on a variety of mammalian species associated with black-tailed prairie dog colonies. Third, I tested for interactions within and between flea species on black-tailed prairie dogs. Fourth, I analyzed the population genetic structure of fleas collected from nine prairie dog colonies with different histories of plague occurrence. I detected universally low levels of plague exposure in mammals associated with prairie dog colonies, suggesting that plague is uncommon between epizootic events. Patterns of flea species occurrence among mammalian species suggest that the small rodents hypothesized to be involved in plague dynamics may play only a small role in plague iii transmission, whereas predators of prairie dogs may be responsible for harboring and transporting plague-infected fleas among colonies. Flea species apparently do not compete for resources and the presence of one flea species on a host may facilitate colonization by other flea species. Finally, the population genetic structure of prairie dog fleas is reflective of plague history at a given site and lends insights into patterns of recolonization following plague events. Taken as a whole, these results provide a uniquely detailed assessment of patterns of host and vector occurrence in the context of plague and they challenge previously held beliefs about plague dynamics in wildlife communities. iv Dedication To my parents, for their support, encouragement, and for never suggesting that I reconsider my career in ecology in favor of more traditional occupational pursuits. Acknowledgments Countless individuals provided a variety of assistance with the collection, analysis and interpretation of the data presented in this dissertation. Among those who deserve recognition for their help are: Renee Culver, Bianca Breland, Jeff Mitton, Katie Driscoll, Jessica Metcalf, Rob Baker, Tom Ranker, Jennifer Winther, Mitch Eaton, Ken Keefover-Ring, Sylvia Iorio, Al Petkus, Valerie McKenzie, John Montenieri, Becky Eisen, Katarina Dittmar de la Cruz, Dave Wagner, Todd Felix, Mike Threlkeld, Kevin Markey, Susan Perkins, Toni Piaggio, Jane Zelikova, Lety Sanchez, Jia Hu, Mark Bradburn, Blake Schmidt, Yan Linhart, Jamie Voyles, Jenny Ramp-Neale, Kelly Ramirez, and Sarah Hellmuth, Anthony Darrouzet-Nardi, and Sarah Wise. Furthermore, I would like to acknowledge the administrative and support staff at the Department of Ecology and Evolutionary Biology at the University of Colorado: Jill Skarstad, Melissa Keller, Linda Bowden, and Melanie Green. In particular, I need to give special thanks to the members of the multi-state plague research group representing Kansas State University, the Centers for Disease Control, and the University of Colorado. These individuals include: Jack Cully, Bala Thiagarajan, Tammi Johnson, Loren Sackett, Katherine McClure, Chris Ray, Ying Bai, Ken Gage, Dave Conlin, Ryan Jones, Amy Markeson, Sarah Wylie, Kimberly Kosmenko, and Ellen Bean. Each participant in this group participated in contributing invaluable feedback and discussion regarding the ideas and hypotheses vi presented in this paper. I am also indebted to the logistical support provided by Mark Brennan, Sheldon Frost, and Kevin of Boulder County Parks and Open Space. Most of all, however, I would like to thank my adviser, Sharon Collinge, and the other members of my graduate committee, Andy Martin, Jason Knouft, Dave Armstrong, and Michelle Sauther. Without their intellectual and moral support and encouragement, I would not have been able to complete this dissertation. My research was supported by funding from a variety of sources. I received small grants from the Colorado Chapter of the Wildlife Society, the Department of Ecology and Evolutionary Biology at the University of Colorado (three awards), The Beverly Sears Fund at the University of Colorado (two awards), the Edna Bailey Sussman Environmental Internship Program, Boulder County Parks and Open Space, the American Society of Mammalogists, and the Boulder County Nature Association. In addition, I was supported for five semesters by research assistantships through grants awarded to Sharon Collinge from the NSF/NIH joint Program in Ecology of Infectious Diseases (DEB-0224328), and from the National Center for Environmental Research (NCER) STAR program of the US-EPA (R-82909101-0). I was also supported for three semesters by teaching assistantships from the department of Ecology and Evolutionary Biology and for one semester by the Rozella Smith Fellowship. vii Table of Contents ABSTRACT…………………………………………………………...……………iii DEDICATION………………………………………………………………………v ACKNOWLEDGMENTS……………………………………………………...…vii LIST OF TABLES………………………………………………………………….x LIST OF FIGURES………………………………………………………………...xii CHAPTER 1: INTRODUCTION……………………………………………………1 Literature Cited……………………………………………………………….7 CHAPTER 2: PATTERNS OF PLAGUE EXPOSURE IN MAMMALIAN CARNIVORES……………………………………………………………..17 Introduction…………………………………………………………………18 Methods……………………………………………………….…………….22 Results………………………………………………………………………24 Discussion…………………………………………………………………..26 Literature Cited……………………………………………………………...30 CHAPTER 3: FLEA ASSEMBLAGES OF MAMMALS ASSOCIATED WITH BLACK-TAILED PRAIRIE DOG COLONIES: IMPLICATIONS FOR INTERSPECIFIC PLAGUE TRANSMISSION……………………..…….42 Introduction…………………………………………………………..……..43 Methods……………………………………………………………..………47 Results……………………………………………………………….……...52 Discussion…………………………………………………………………..56 viii Literature Cited…………………………………………………………….65 CHAPTER 4: POPULATION GENETIC STRUCTURE OF THE PRAIRIE DOG FLEA AND POTENTIAL PLAGUE VECTOR, OROPSYLLA HIRSUTA……....89 Introduction……………………………………………………….……….91 Methods…………………………………………………………….……...94 Results……………………………………………………………….……..98 Discussion…………………………………………………………….……99 Literature Cited…………………………………………………………….107 CHAPTER 5: OCCURRENCE PATTERNS OF TWO OROPSYLLA SPECIES ON BLACK-TAILED PRAIRIE DOG HOSTS………………………………124 Introduction………………………………………………………………..126 Methods………………………………………………………………..…..128 Results……………………………………………………………………..131 Discussion…………………………………………………………………133 Literature Cited………………………………………………...…………..141 CHAPTER 6: CONCLUSION……………………………………………………154 ix List of Tables Table 2.1: Proportions of each species of carnivores from each habitat type that tested positive for plague with sample sizes in parentheses……………….………39 Table 2.2: Individuals sampled in close spatial and temporal proximity to prairie dog die-offs or other confirmed plague occurrence…………………………..…..………40 Table 3.1: List of mammalian species sampled and flea species collected from each……………………………………………….………..…….….….……75 Table 3.2: List of flea species encountered in this study and host species from which each was collected……………………………..…………………..….….….76 Table 3.3: Samples size for each host species with number of fleas collected, total flea prevalence, mean abundance, and mean intensity……………….…..…77 Table 3.4: Matrix indicating Sorensen’s similarity index values for each pair of host species calculated from the raw incidence dataset……………..……….……78 Table 3.5: Matrix indicating Sorensen’s similarity index values for each pair of host species calculated from the raw incidence dataset…………….….…...….…79 Table 3.6: Matrix indicating Morisita-Horn similarity index values for each pair of host species calculated from natural-log transformed data……………..…....80