Infestation Intensities, Attachment Patterns, and the Effect On
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INFESTATION INTENSITIES, ATTACHMENT PATTERNS, AND THE EFFECT ON HOST CONTEST BEHAVIOR OF THE TICK IXODES PACIFICUS ON THE LIZARD SCELOPORUS OCCIDENTALIS A Thesis presented to the Faculty of California Polytechnic State University San Luis Obispo In Partial Fulfillment of the Requirements for the Degree Master of Science in Biological Sciences by Dylan Michael Lanser August 2019 © 2019 Dylan Michael Lanser ALL RIGHTS RESERVED ii COMMITTEE MEMBERSHIP TITLE: Infestation Intensities, Attachment Patterns, and the Effect on Host Contest Behavior of the Tick Ixodes pacificus on the Lizard Sceloporus occidentalis AUTHOR: Dylan Michael Lanser DATE SUBMITTED: August 2019 COMMITTEE CHAIR: Gita Kolluru, Ph.D. Professor of Biological Sciences COMMITTEE MEMBER: Larisa Vredevoe, Ph.D. Professor of Biological Sciences COMMITTEE MEMBER: Emily Taylor, Ph.D. Professor of Biological Sciences iii ABSTRACT Infestation Intensities, Attachment Patterns, and the Effect on Host Contest Behavior of the Tick Ixodes pacificus on the Lizard Sceloporus occidentalis Dylan Michael Lanser Parasites often have profound effects on the survival and evolution of their hosts, and hence on the structure and health of entire ecosystems. Yet basic questions, such as the degree of virulence of a given parasite on its host, and factors influencing which hosts in a population are at the greatest risk of infection, are vexingly difficult to resolve. The western blacklegged tick-western fence lizard (Ixodes pacificus-Sceloporus occidentalis) system is important, primarily because I. pacificus, a vector of the Lyme disease spirochete Borrelia burgdorferi, is dependent on S. occidentalis for blood meals in its subadult stages, and this lizard possesses an innate immune response that removes the Lyme disease pathogen from attached ticks. My study focused on two aspects of the I. pacificus-S. occidentalis interaction. In Chapter 1, I investigated factors correlating with the intensity of I. pacificus infestations on S. occidentalis. Infection intensity (parasites per host) is often highly variable within a host population, though certain individuals, such as males, tend to be more heavily infected. Previous work in the I. pacificus-S. occidentalis system suggests that differences in behavior, such as the frequency of territorial patrols, may contribute to variation in tick intensity among lizards. I therefore hypothesized that lizard traits that correlate with dominance would also correlate with infestation intensity. Specifically, I predicted that larger and more colorful males would have higher infestation intensities than less impressive animals. In this chapter, I also focused on site selection by ticks infesting S. occidentalis. Skin folds on the necks of these lizards (nuchal pockets) may function to divert ectoparasites away from eyes, ears, and other potentially vulnerable structures. I therefore also looked for factors correlating with tick attachment in these pockets. I sampled ticks on adult male S. occidentalis in the spring and summer, which is the seasonal peak for both S. occidentalis territorial behavior and subadult I. pacificus abundance. After determining the site of infestation and intensity of ticks on these lizards, I re-infested lizards with laboratory-reared I. pacificus larvae, and again quantified tick intensity and attachment location. Contrary to expectation, no host traits correlated with tick intensity among ticks naturally infesting lizards, and lab-reared larval intensity was negatively correlated with lizard body size. As expected, ticks acquired by lizards naturally concentrated inside nuchal pockets, and I also observed this site preference among ticks in lab-based experimental infestations. Although the general pattern, lab- reared ticks were more varied in the sites on which they fed. There was a negative correlation between infestation intensity and the proportion of ticks attached in nuchal pockets. Unsurprisingly, the most reliable predictor of tick intensity and site selection was the season. In Chapter 2, I explored how tick attachment affects male S. occidentalis contest behavior. I. pacificus infestation has been shown to have negative physiological impacts on S. occidentalis, but mechanisms linking physiological changes to ultimate fitness consequences have been largely underexplored. I hypothesized that tick infestation iv reduces male S. occidentalis fighting ability by reducing O2 carrying capacity, or by obstructing or damaging vulnerable structures on their hosts. I held fifty half-hour trials between pairs of size- and ventral badge-matched male S. occidentalis, with one male in each pair infested with lab-reared I. pacificus larvae. I found that tick infestation negatively correlated with aggressive behavior in these staged contests. In support of reduced O2 capacity as the mechanism of reduced aggression, my ecologically relevant infestation intensities seemed to cause significant declines in hematocrit among experimentally infested lizards relative to controls. However, the site at which ticks attached did not significantly correlate with the aggressiveness of their lizard hosts. This is one of only a handful of studies to address the direct effect of I. pacificus on S. occidentalis. My study demonstrates that tick infestation can be detrimental to the fitness of their lizard hosts even without the transmission of pathogens. This insight may prove informative in future work on the ecology of I. pacificus-borne diseases in the western United States. This study is also one of only a few to use parasite infection to induce an asymmetry in fighting ability in intrasexual contests. v ACKNOWLEDGMENTS I am extremely grateful to my committee cochairs, Drs. Gita Kolluru and Larisa Vredevoe, for their extensive advice and support over the past few years. Many thanks to Dr. Emily Taylor for serving on my committee, and also for the insight on matters herpetological shared by her and her graduate students in the Physiological Ecology of Reptiles Laboratory, especially Heather Neldner for teaching me how to noose lizards. Thanks to the many undergraduates who worked on this project, including Rebeca Almeida, Eric Gonzales, Josh Hallmark, Teo Humkey, Kei Iemori, Fiona Kelly, Julius Larion, Connor Maldonado, Jamie Marcos, Laura Murray, Lucy Ramirez, Rachel Rivera, Jenna Van Mouwerik, and especially to Andrew Morris, for assistance during many critical phases of this project. Dr. Christy Strand loaned the security cameras used to record fights between lizards. Thanks to Dave Clendenen for lending equipment and assistance in numerous photography sessions. Amber Nichols facilitated the use of the roof of Science North for more than a year for this project. Thanks to Doug Brewster, for lending his expertise and assistance in the fabrication of arenas, and to Rob Brewster, for 3D printed mounts for surveillance cameras, as well as for his advice on animal enclosures. I am very grateful for the support provided by the rest of the faculty, staff, and graduate students of the Cal Poly Biological Sciences Department. Allan Hancock College and the NSF Bridges to the Baccalaureate program funded Esmeralda Sanchez to help with this project during summer 2016. Aaron Lazanoff and the students at the Cal Poly Beef Unit provided cattle for rearing ticks. Thanks to Sarah Bailey for providing samples of Plasmodium-infected reptile blood. Dr. John Walker provided input on statistical methods The Baker/Koob Endowment and Cal Poly Cal Poly College Based Fees provided funds. This research was conducted with Cal Poly IACUC and CDFW (SC-12412) approval. vi TABLE OF CONTENTS Page LIST OF TABLES…………………………………………………………………...…viii LIST OF FIGURES……………………………………………………………………….x CHAPTER 1. INFESTATION INTENSITIES AND ATTACHMENT PATTERNS OF IXODES PACIFICUS ON SCELOPORUS OCCIDENTALIS UNDER FIELD AND LABORATORY CONDITIONS…………..……...................................1 1.1 Introduction………...…………………………..……………………...1 1.2 Methods……..……………………………………………..…………13 1.3 Results………..…………………………………………..………..…26 1.4 Discussion…..……………………………………..…………………29 2. THE EFFECTS OF TICK PARASITISM ON CONTEST BEHAVIOR IN THE LIZARD SCELOPORUS OCCIDENTALIS……………………..………..…...46 2.1 Introduction……...……………………………………..…………….46 2.2 Methods ….……………………………..……………………………56 2.3 Results ….……………………………………………..……………..71 2.4 Discussion ….………………………………………..………………75 3. TABLES………………………………………………………..……………………86 4. FIGURES……………………………………...……………………………………101 REFERENCES…………………………………………………………………………138 vii LIST OF TABLES Table Page 1. Giemsa Staining Materials……………………….………………...……...…………86 2. Results of a Factor Analysis on Lizard Morphological Variable……………..……..87 3. Results of the Logistic Regression Model of the Relationship between the Odds of Wild-acquired Ticks Attaching in the Nuchal Pocket (Versus at Other Locations on Lizard Hosts) and Predictor Variables, Including the Day on which Lizards Were Collected, Factor 1 Body Size, Factor 2 Badge Color, S. (L.) occidentalis Coinfection, and Wild-acquired Tick Intensity………………..….....…88 4. Results of the Mixed Effects Logistic Regression Model of the Relationship between Lab-reared Ticks Attaching in the Nuchal Pocket (Versus at Other Locations on Lizard Hosts) and Predictor Variables, Including Factor 1 Body Size, Factor 2 Badge Color, S. (L.) occidentalis Coinfection, and Lab-reared Tick Intensity……………..………………………………………………………….89 5. Summary Statistics of Wild-acquired Tick Intensity……..………………………….90 6. Output from the Linear Mixed Model of the Relationship between Wild-