The Ecology of Carrion Decomposition: Necrophagous Invertebrate
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THE ECOLOGY OF CARRION DECOMPOSITION: NECROPHAGOUS INVERTEBRATE ASSEMBLY AND MICROBIAL COMMUNITY METABOLIC ACTIVITY DURING DECOMPOSITION OF SUS SCROFA CARCASSES IN A TEMPERATE MID-WEST FOREST Thesis Submitted to The College of Arts and Sciences of the UNIVERSITY OF DAYTON In Partial Fulfillment of the Requirements for The Degree Master of Science in Biology By Andrew Joseph Lewis UNIVERSITY OF DAYTON Dayton, OH December, 2011 THE ECOLOGY OF CARRION DECOMPOSITION: NECROPHAGOUS INVERTEBRATE ASSEMBLY AND MICROBIAL COMMUNITY METABOLIC ACTIVITY DURING DECOMPOSITION OF SUS SCROFA CARCASSES IN A TEMPERATE MID-WEST FOREST Name: Lewis, Andrew Joseph APPROVED BY: ________________________________________________________ M. Eric Benbow, Ph.D. Faculty Advisor ________________________________________________________ Carl Friese, Ph.D. Committee Member ________________________________________________________ Ryan McEwan, Ph.D. Committee Member ________________________________________________________ Jayne Robinson, Ph.D. Department Chairperson ii ABSTRACT THE ECOLOGY OF CARRION DECOMPOSITION: NECROPHAGOUS INVERTEBRATE ASSEMBLY AND MICROBIAL COMMUNITY METABOLIC ACTIVITY DURING DECOMPOSITION OF SUS SCROFA CARCASSES IN A TEMPERATE MID-WEST FOREST Name: Lewis, Andrew Joseph University of Dayton Advisor: Dr. M. Eric Benbow Decomposition is a fundamental process to ecosystem function and energy flow where nutrients are recycled and reintroduced into food webs. Vertebrate carrion decomposition can provide significant resource pulses for habitats and can range from large whale carcasses to small rodents. Necrophagous invertebrates have been documented to be a predominant driver of vertebrate carrion decomposition. However, microorganisms also participate in the utilization of this common food fall, microorganisms. Little is known about the structure and composition of the microbial communities associated with carrion, or if they follow a pattern of succession as decomposition progresses, although this process is important for nutrient and energy cycling in ecosystems. The objective of this study was to evaluate both the microbial and invertebrate community succession during iii carrion decomposition. It was hypothesized that microbial and invertebrate communities on decomposing carcasses would vary both over decomposition time and between seasons, as well demonstrates inter-carcass variation among the replicates. To test these hypotheses, Sus scrofa carcasses (N=3-6) were placed in a forested habitat near Xenia, OH during spring (15 March – 8 June 2009) summer (23 July – 31 August 2009), autumn (11 November 2009 – 1 May 2010) and winter (2 February – 1 May 2010). For the microbial sample collections skin biopsies and swabs of the anus and buccal of each carcass along with cores of soil underneath and 1m away were collected to compare with microbial community metabolic succession during decomposition. Biolog EcoPlates, phenotypic microarray 96 well plates were used to monitor the differential use of 31 different carbon sources to provide a community level physiological profile (CLPPs) as a measure of microbial community metabolic activity. In addition, standardized insect samples involving aerial sweep nets, pitfall traps and hand collections were used to evaluate the arthropod communities through the entire process of carrion decomposition. One and two-way ANOVA with Bonferroni Post-tests, non-metric multidimensional scaling (NMDS), multi-response permutation procedure (MRPP) and indicator species analysis (ISA) were employed to evaluate the microbial community metabolic activity and invertebrate community change over decomposition, between replicates, and between seasons. For the microbial communities, there were significant differences (p<0.001) between seasons for both carrion and soil samples. Carrion samples were significantly different from soil samples (p<0.001), but the control and soil under body were not (p=0.271). For the invertebrates, iv while most taxa remained constant among seasons, five taxa demonstrated significant differences (One-way ANOVA; p<0.05) in presence across seasons. Necrophagous insect communities had significant differences across the different stages of decomposition (MRPP; p<0.001) for each season in multivariate analyses. According to pairwise comparisons while there were significantly different necrophagous insect communities between summer and fall (p=0.001) and summer and winter (p< 0.001), the communities were similar between fall and winter trials (p=0. 073). Another observation was a undocumented phenomenon concerning en masse larval dispersal of the blow fly Phormia regina.. We highly recommend that future studies related to carrion decomposition increase replication of carcasses and make comparisons across seasons and year. v DEDICATION To my mother and father for showing me the way. To my brothers and sister for pushing me in the right direction. To my grandparents for providing guidance. To my wife for keeping me going when times get rough. To my friends who help make sure I stay sane. And lastly to my advisor, who gave me the chance to prove myself. vi ACKNOWLEDGEMENTS I would like to thank my advisor, Dr. Eric Benbow for providing me with the chance to go to graduate school and receive my Master’s. Thank you to my committee members, Dr. Carl Friese and Dr. Ryan McEwan for providing guidance and figuring out the best course I should take to reach my goals with school. Thanks to all of the undergraduates who helped out with the research; Tiffany Blair, Maureen Berg, Allison Gansel, Elizabeth Gazdick, An Lai, Jessica Teater, Carolyn Teter, Sandra Tilton, and Jon White. Thanks as well to the past and present graduate students that aided me as well; Meg Shoda, Kathy Gorbach, Ryan Kimirakaus, Jen Lang, Mollie MacIntosh, Jennifer Pechal, and Jennifer Rosati. I greatly appreciate all the other professors and graduate students for teaching me and lending a helping hand or sound advice when needed. Thanks to my parents Alice and Kevin Lewis and my wife Caitlin Powell for going out into the field with me when I needed help and for always being willing to do some proof reading. I am also grateful to the Greene County Parks District for allowing me to use the Morris Bean Reserve for my research. Lastly, thanks to the University of Dayton for providing me with the education and ability to perform this research and obtain my degree. vii TABLE OF CONTENTS ABSTRACT………………………………………………………………………………………………………….iii LIST OF ILLUSTRATIONS……………………………………………………………………………………..ix LIST OF TABLES…………………………………………………………………………………………………xii CHAPTER 1: Microbial Metabolic Community Change During Vertebrate Carrion Decomposition……………………………………………………………………………………………………..1 ABSTRACT……………………………………………………………………………………..........1 INTRODUCTION…………………………………………………………………………………...2 METHODS……………………………………………………………………………………………8 RESULTS……………………………………………………………………………………………15 DISCUSSION……………………………………………………………………………………….18 CHAPTER 2: Necrophagous Insect Community Assembly During Vertebrate Carrion Decomposition: Seasonal and Inter-Carcass Variation..………………...................................34 ABSTRACT………………………………………………………………………………………...34 INTRODUCTION…………………………………………………………………………………36 METHODS………………………………………………………………………………………….39 RESULTS……………………………………………………………………………………………44 DISCUSSION……………………………………………………………………………………….47 CHAPTER 3: When Entomological Evidence Crawls Away: Phormia regina En Masse Larval Dispersal..………………………………………………………………………………………………..62 ABSTRACT…………………………………………………………………………………………62 INTRODUCTION…………………………………………………………………………………63 METHODS………………………………………………………………………………………….66 RESULTS……………………………………………………………………………………………68 DISCUSSION……………………………………………………………………………………….71 BIBLIOGRAPHY………………………………………………………………………………………………….84 viii LIST OF ILLUSTRATIONS Chapter 1 Figure 1: Mean (SD) non-normalized (A) and normalized (B) carrion microbial metabolic community activity during each season compared to non-normalized (C) and normalized (D) activity for soil underneath (Under) and 1 m away from the carcass (Control). Each figure shows the overall microbial community metabolic activity for each date, standardized for ADH, through the process of decomposition in each season. In Figure 1A, the number beside each point represents the number of days since death for each sampling date in each season. ………………………………….22 Figure 2: Non-metric multidimensional scaling ordinations of microbial community level physiological profiles for carrion communities (A) during decomposition time is represented by ADH ranges and among seasons (B), and soil communities during decomposition (C) represented by ADH ranges and among seasons (D). The MRPP statistics indicate significant differences where p<0.05, and the amount of variation explained by each axis is also provided in the axes labels…………………………………….23 Figure 3: Non-metric multidimensional scaling ordinations of microbial community level physiological profiles for carrion communities over decomposition time represented as ADH during each season: A) spring, B) summer, C) autumn, and D) winter. The MRPP statistics indicate significant differences where p<0.05, and the amount of variation explained by each axis is also provided in the axes labels……...24 Figure 4: Non-metric multidimensional scaling ordinations of microbial community level physiological profiles for soil communities over decomposition time represented as ADH during each season; A) spring, B) summer, C) autumn, and D) winter. The MRPP statistics indicate significant differences