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An Analysis of Dung Beetle (Coleoptera: Scarabaeidae: Scarabaeinae & Aphodiinae) Attraction to Small Mammal Carrion

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An Analysis of Dung Beetle (Coleoptera: Scarabaeidae: Scarabaeinae & Aphodiinae) Attraction to Small Mammal Carrion HEADS OR TAILS: AN ANALYSIS OF DUNG BEETLE (COLEOPTERA: SCARABAEIDAE: SCARABAEINAE & APHODIINAE) ATTRACTION TO SMALL MAMMAL CARRION A Thesis by Rachel Stone Bachelor of Science, Wichita State University, 2013 Submitted to the Department of Biological Sciences and the faculty of the Graduate School of Wichita State University in partial fulfillment of the requirements for the degree of Master of Science May 2018 © Copyright 2018 by Rachel Stone All Rights Reserved HEADS OR TAILS: AN ANALYSIS OF DUNG BEETLE (COLEOPTERA: SCARABAEIDAE: SCARABAEINAE & APHODIINAE) ATTRACTION TO SMALL MAMMAL CARRION The following faculty members have examined the final copy of this thesis for form and content, and recommend that it be accepted in partial fulfillment of the requirement for the degree of Master of Science with a major in Biological Sciences. __________________________________ Mary Jameson, Committee Chair __________________________________ Leland Russell, Committee Member __________________________________ Peer Moore-Jansen, Committee Member iii DEDICATION To all who have an appreciation for the industriousness, efficiency, and high moral integrity of the humble dung beetle iv “If we and the rest of the backboned animals were to disappear overnight, the rest of the world would get on pretty well. But if they were to disappear, the land's ecosystems would collapse. The soil would lose its fertility. Many of the plants would no longer be pollinated. Lots of animals, amphibians, reptiles, birds, mammals would have nothing to eat. And our fields and pastures would be covered with dung and carrion. These small creatures are within a few inches of our feet, wherever we go on land – but often, they're disregarded. We would do very well to remember them.”—David Attenborough v ACKNOWLEDGEMENTS This project could not have been possible without the contributions of Emmy Engasser (with whom I’m honored to share the esteemed title of Carrion Queen), the best co-investigator I could have ever hoped for and a person who exemplifies hard work and determination in everything she sets her mind to, as well as Dr. Mary Liz Jameson, my mentor extraordinaire, who has unwaveringly provided valuable knowledge, support, guidance, friendship, and even chocolates in desperate times. I am deeply inspired by the enthusiasm you both have for the natural world and the spirit of generosity you spread. I am truly privileged to have learned from you both. I would like to thank Dr. Peer Moore-Jansen for his generous monetary support and access to Skeleton Acres Research Facility. I would also like to thank Dr. Leland Russell for his statistical prowess and willingness to share in his knowledge. Thank you to Ranger Randy Just and Seth Turner (Kansas Department of Wildlife, Parks and Tourism) for access to El Dorado State Park, and to Joyce Dudeck, Kim and Scott Bays for sharing their beautiful 80-acre plot. Thanks also to Larry Slayton at the Sedgwick County Zoo for his ability to provide us with a seemingly unending supply of frozen rats. I am so deeply grateful to the many helpful research assistants both in the field and in the lab, who spent their time contributing to this research: Breanna Sayers, Morgan Trible, Brandon Hein, Niall Horton, Ethan Grennan, Hannah Hoetmer, Jacqueline Nascimento- Odenheimer, and Jacqueline Baum. I am humbled by your generosity and dedication to this ambitious project and I am so thankful for the friendships this work has fostered. Thanks also to my dear old dad, Brian Stone, a constant source of encouragement and sincere belief in my ability; everybody needs someone in their corner, and I am so glad that you are in mine. It takes a village to tackle such a project, to all the others who have in any way aided in the development and execution of this project: Thank YOU! vi ABSTRACT Necrophilous insects occupy a biologically interesting ecological niche because carrion is a highly desirable but ephemeral food source. Insects that feed on carrion are widely studied in forensic and entomological disciplines, but many taxa attracted to decomposition are often overlooked. Dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae and Aphodiinae) are frequently found at carrion, but very little is known about their attraction to this resource. Are dung beetles attracted to the carrion itself or are they attracted indirectly because the gastrointestinal contents of the animals are exposed? This research attempts to disentangle the association between dung beetles and carrion by examining the distribution of dung beetles on the head- and tail-end of rat carrion, delimiting a resource more attractive to necrophagous insects (head-end) and a resource more attractive to coprophagous insects (tail-end). Comparisons were made between dung beetle distributions on rat carrion with carrion beetle (Coleoptera: Silphidae) distributions, a model of distribution patterns for a taxon known to target carrion. A total of 25,081 dung beetle individuals from 21 species and 3,333 individual carrion beetles from 9 species were collected in our year-long study. Results indicate that dung beetles show higher attraction to the head-end of rat carrion than the tail-end. This distribution pattern is also found in carrion beetles, suggesting that similar resources are being targeted. When dung beetles are grouped by behavioral guilds, rollers and tunnellers also share this pattern of greater abundance at the head-end rather than the tail-end, but dwellers show no discernable difference between the head- and tail-end. This research indicates that dung beetle interactions with carrion that are more complex than previously understood. Our results suggest that scarabaeine dung beetles target carrion preferentially, challenging the long-held belief that, within temperate regions, dung beetle necrophagy is rare and unimportant to the decomposition of carrion. vii TABLE OF CONTENTS Chapter Page 1. INTRODUCTION…………………………….……………….………………….............1 1.1 Introduction……………….………………………….…………………………....1 1.2 Questions and Significance……………..…………………………………….…...7 2. MATERIALS AND METHODS………………………..………………………..……...11 2.1 Study Sites……………………….……….……………………………………....11 2.2 Insect Sampling……………………..…………………………………………....13 2.3 Abiotic Measurements…………….……………………………………….…….15 2.4 Laboratory Methods……...……………………..………………………………..16 2.5 Data Analyses…………..………………………………………………………...17 3. RESULTS…………………………………..…………………………………………....24 3.1 Diversity Results………………………..……………………………..………....24 3.2 Phenology Results…………………………………..………………..…………..26 4. DISCUSSION………..…………………………………………………………….…….34 4.1 Discussion………………………………………..……………………………....34 4.2 Significance…………..……………………………………………………..…....39 REFERENCES…………………………………………………………………………………..42 APPENDICES……………………………………………………………………….…………..52 viii LIST OF TABLES Table Page 1. Research site locations…………………………………………….……………………..19 2. Collection episode by date range and season…………………………………………….23 3. Dung beetle species and their abundances……………………………………………….28 4. Carrion beetle species and their abundances…………………………………………….28 5. Biodiversity metrics for dung beetles and carrion beetles……………………………….29 6. Mixed model ANOVA results…………………………………………………………...31 7. Abiotic factors……………………………………………………………………………33 ix LIST OF FIGURES Figure Page 1. Illustration of dung beetle guilds…………………………………...…………...……….10 2. Overview of transect design……………………………………………………………...22 3. Overview of pit fall trap design……………………………………………...…………..22 4. Wire exclosure design……………………………………………………………………23 5. Biodiversity profiles of dung beetle communities………………………...……………..29 6. Biodiversity profiles of carrion beetle communities…………...………………………...29 7. Average dung beetle and carrion beetle abundances………….…………...…………….30 8. Average abundances of dung beetle guilds………………………………………………30 9. Dung beetle phenology………………………………………...………………………...31 10. Carrion beetle phenology………………………………………………………………...32 x LIST OF MAPS Map Page 1. Physiographic map of Kansas……………………...………………………………...…..19 2. El Dorado State Park……………………………………………………………………..20 3. Skeleton Acres Research Facility………………………………...……………………...20 4. The 80 Acres……………………………………………………………………………..21 5. View of all research sites…………………………………...……………………………21 xi LIST OF PLATES Plate Page 1. Exemplar Scarabaeidae of Kansas……………………………………………………..….9 2. Dung beetle roller behavior……………………………………………………………...10 xii CHAPTER 1 INTRODUCTION 1.1 Introduction The vast majority of Scarabaeidae are either phytophagous or coprophagous, but many scarab beetles, particularly in the dung-feeding guild (Scarabaeinae and Aphodiinae: Scarabaeidae: Coleoptera) (Plate 1), are regularly represented in carrion-baited traps (Braack 1986; Ratcliffe and Paulsen 2008; Villet 2011; Whipple et al. 2012; Ratcliffe 2013). Researchers have previously hypothesized that their attraction is not to carrion itself, but to the contents within the gastrointestinal tract that become exposed during carcass decomposition (Midgley et al. 2012). However, the mechanisms of scarab attraction to carrion are not well understood. In fact, even the components of excrement that adult dung beetles utilize for food is poorly understood, except that it is sourced from fresh dung. The inspection of adult dung beetle gut contents reveals a liquid but viscous suspension of microscopic particles (Madle 1934; Miller 1961). More recent evidence indicates these fine particles are primarily bacteria and dead epithelial cells from the herbivore’s gut, indicating that tiny particles are preferentially selected while larger
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