How Behavior and Anatomy Affect Resource Use by Snakes
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How Behavior and Anatomy Affect Resource Use by Snakes A thesis submitted to the Graduate School of the University of Cincinnati in partial fulfillment of the requirements for the degree of Master of Science in the Department of Biological Sciences of the College of Arts and Sciences by Noah D. Gripshover B.S. Biology, University of Louisville, April 2017 Committee Chair: Bruce C. Jayne, Ph.D. May 2020 ABSTRACT The physical structure of animals and their environment are two obvious factors that can limit what animals do. However, the behaviors of animals and the choices they make can result in animals doing things that are only a small subset of what is physically possible. I used two systems to gain insights into the role of behavior in affecting resource use by snakes. First, I studied how varying the darkness, shape, and locations of artificial branches affected where snakes chose to go. Second, I studied two species of snakes to test how diet and feeding behavior were affected by the size of prey relative to the snakes’ anatomical constraints on prey size. Variation in the environment can affect the mechanical demands of locomotion as well as influence where animals choose to go. Arboreal habitats facilitate studying path choice by animals because variable branch structure has known mechanical consequences and different branches create discrete choices. Recent studies found that arboreal snakes can use vision to select shapes and locations of destinations that mechanically facilitate bridging gaps. However, the extent to which the appearance of objects unrelated to biomechanical demands affects the choice of destinations remains poorly understood for most animal taxa including snakes. Hence, I manipulated the intensity (black, gray or white), contrast, structure, and locations of destinations to test for their combined effects on perch choice during gap bridging of brown tree snakes and boa constrictors. The results presented herein provide a striking example of how visual cues unrelated to the physical structure of surfaces, such as contrast and intensity, can bias choice and, in some cases, supersede a preference for mechanically beneficial surfaces. Snakes consume their prey whole. Consequently, variation in the anatomy of the trophic apparatus of snakes directly affects gape and limits maximal prey size. However, for the foraging ecology of snakes and other systems, scant data exist regarding how often maximal capacities are ii taxed in nature. Hence, I quantified: 1) maximal gape, 2) the size of prey relative to maximal gape, and 3) how the type and relative size of prey affected behavior and prey handling times for two species of natricine snakes that primarily eat soft- (Regina septemvittata) or hard-shell (Liodytes alleni) crayfish. Several of the differences between the crayfish-eating snakes including maximal gape, prey size, prey handling times and behavior resemble those between two phylogenetically distant species of homalopsid snakes that consume either hard- or soft-shell crabs. In both groups of crustacean-eating snakes, the decreased prey capture success in captivity and the rare consumption of relatively large hard-shell crustaceans in the field suggest that the ability to capture this type of prey constrains prey size more commonly than maximal gape. Regina septemvittata was superior to the other species based on new metrics of potential feeding performance that integrated snake size and gape with the relative mass of prey. iii iv ACKNOWLEDMENTS First and foremost, I would like to thank my advisor, Dr. Bruce Jayne, for the support, opportunities, and advice during my three years at the University of Cincinnati. I have learned so much about how to conduct high quality research in both laboratory and field studies. I greatly appreciate all your support in my efforts to collect snakes in Kentucky and Florida. I will always remember biking through the everglades to collect pythons and wading through the mud and water hyacinths looking for Liodytes. I thank my committee members, Dr. Takuya Konishi and Dr. Daniel Buchholz, for their insightful comments on my thesis and discussions during our committee meetings. Thank you for taking the time to meet with me and help me with my projects. I thank all of the undergraduate students that have assisted me with my research and animal care. I especially thank Miranda Rodgers, Curran Bobbitt, Trey Saunders, and Brittany Fithen who assisted with the gap bridging experiments and Lily Bischoff, Nicole Addison, and Trey Saunders who assisted with the collection and experiments of the crayfish-eating snakes. I have enjoyed working with all of you and you have made my time here at the University of Cincinnati much more enjoyable and fulfilling. Last but certainly not least, I would like to thank my family for their continued support throughout my graduate career. Thank you for teaching me that hard work pays off and allowing me to follow my passion in studying the animals that I was never allowed to bring into the house. v TABLE OF CONTENTS Abstract……………………………………………………………………………………..……ii Acknowledgments………………………………………………………………………….……v List of Tables and Figures……………………………………………………………….....…viii Chapter 1: Visual Contrast and Intensity Affect Perch Choice of Brown Tree Snakes (Boiga irregularis) and Boa constrictors (Boa constrictor)………………………………………...….…1 Abstract…………………………………………………………………………...……….2 Introduction………………………………………………………………………………..3 Materials and Methods…………………………………………………………………….5 Results……………………………………………………………………………………10 Discussion………………………………………………………………………………..11 References……………………………………………………………………………….20 Chapter 2: Crayfish Eating in Snakes: A Model System for Testing How Anatomy, Behavior and Performance Affect Foraging Ecology……………………………………………………...31 Abstract…………………………………………………………………………………..32 Introduction………………………………………………………………………………33 Materials and Methods…………………………………………………………………...36 Results……………………………………………………………………………………40 Discussion………………………………………………………………………………..44 vi References………………………………………………………………………………..53 Supplemental Information.………………………………………………………………66 vii LIST OF TABLES AND FIGURES Chapter 1 Table 1.1. Mean + s.e.m. preference for destination perches……………………………………27 Figure 1.1. Overhead view of the experimental apparatus………………………………………29 Figure 2.1. Schematic views of the destinations showing the manipulations of destination intensity and structure……………………………………………………………………………30 Chapter 2 Figure 2.1. Simplified phylogeny of Natricine and Homalopsid snakes based on Figueroa et al. (2016)…………………………………………………………………………………………….59 Figure 2.2. Scaling relationships for morphological data………………………………………..60 Figure 2.3. Computed tomography scans of R. septemvittata and L. alleni……………………..61 Figure 2.4. Relationships between the absolute and relative sizes of prey………………………62 Figure 2.5. Prey handling behaviors and prey handling times…………………………………...63 Figure 2.6. Constraints of gape on feeding performance for four species of crustacean-eating specialists………………………………………………………………………………………...64 Figure 2.7. Three-dimensional maximal feeding performance spaces for four species of crustacean-eating snakes…………………………………………………………………………65 Table S2.1. Regression analyses of morphology and handling time……………………….……66 Table S2.2. Summary of prey handling behaviors during laboratory trials..…………………….67 viii Table S2.3. Mean values of prey handling times during laboratory trials.………………………68 Table S2.4. Final multiple regression models for total handling time and the occurrence of some behaviors....………………………………………………………………………………………69 Table S2.5. Univariate regressions for behavior and handling times……………………………70 Table S2.6. ANCOVA results for morphology and behaviors comparing the two species and sexes within a species……………………………………………………………………………72 ix CHAPTER ONE Visual Contrast and Intensity Affect Perch Choice of Brown Tree Snakes (Boiga irregularis) and Boa Constrictors (Boa constrictor) Noah D. Gripshover and Bruce C. Jayne* Department of Biological Sciences University of Cincinnati Cincinnati, OH, 45221 USA *The work presented here, as well as the preparation and completion of the narrative for this manuscript, was principally composed by Noah D. Gripshover with the assistance of Bruce C. Jayne. The manuscript can be viewed in its published form, in the journal Zoology: Gripshover, N. D., and B. C. Jayne. 2020. Visual Contrast and Intensity Affect Perch Choice of Brown Tree Snakes (Boiga irregularis) and Boa Constrictors (Boa constrictor). Zoology 139:DOI 10.1016/y.zool.2020.125744 1 ABSTRACT Habitat structure can affect animal movement both by affecting the mechanical demands of locomotion and by influencing where animals choose to go. Arboreal habitats facilitate studying path choice by animals because variation in branch structure has known mechanical consequences and different branches create discrete choices. Recent laboratory studies have found that arboreal snakes can use vision to select shapes and locations of destinations that mechanically facilitate bridging gaps. However, the extent to which the appearance of objects unrelated to biomechanical demands affects the choice of destinations remains poorly understood for most animal taxa including snakes. Hence, we manipulated the intensity (black, gray or white), contrast, structure, and locations of destinations to test for their combined effects on perch choice during gap bridging of brown tree snakes and boa constrictors. For a white background and a given perch structure and location, both