SSStttooonnnyyy BBBrrrooooookkk UUUnnniiivvveeerrrsssiiitttyyy The official electronic file of this thesis or dissertation is maintained by the University Libraries on behalf of The Graduate School at Stony Brook University. ©©© AAAllllll RRRiiiggghhhtttsss RRReeessseeerrrvvveeeddd bbbyyy AAAuuuttthhhooorrr... The effect of parasitism and predation on phenotypically plastic traits of the marine gastropod Tritia obsoleta A Dissertation Presented by Mica McCarty-Glenn to The Graduate School in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in Ecology and Evolution Stony Brook University May 2017 Copyright by Mica McCarty-Glenn 2017 Stony Brook University The Graduate School Mica McCarty-Glenn We, the dissertation committee for the above candidate for the Doctor of Philosophy degree, hereby recommend acceptance of this dissertation. Dr. Dianna K. Padilla – Dissertation Advisor Professor, Ecology and Evolution Dr. Ross H. Nehm - Chairperson of Defense Associate Professor, Ecology and Evolution Dr. Glenn R. Lopez Professor, School of Marine and Atmospheric Sciences Dr. April M. H. Blakeslee Assistant Professor, Biology East Carolina University This dissertation is accepted by the Graduate School Charles Taber Dean of the Graduate School ii Abstract of the Dissertation The effect of parasitism and predation on phenotypically plastic traits of the marine gastropod Tritia obsoleta by Mica McCarty-Glenn Doctor of Philosophy in Ecology and Evolution Stony Brook University 2017 Interactions among species have important influences on the structure and function of the communities in which they reside. Much is known about interactions involving two species, but little is known about the potential synergistic or antagonistic effects when a species is confronted with multiple types of interactions. Organisms may respond to species interactions through phenotypic plasticity, where the same genotype can produce different phenotypes depending on the environment. Many aquatic gastropods are known to have phenotypically plastic behavior and shell morphology in response to two common interactions, parasitism and predation. However, few studies have examined the synergistic effects of both predation and parasitism on gastropod plasticity. This dissertation uses the marine snail Tritia (Ilyanassa) obsoleta to answer the following questions: Do predators and parasites alter the feeding behavior of T. obsoleta? Do parasites alter the antipredator behavior of their gastropod host? Do parasites and predators alter the shell morphology of T. obsoleta? Do juvenile and adult T. obsoleta respond similarly to risk of predation? I found that neither predators nor parasites altered the feeding rates of juvenile or adult T. obsoleta. Adult snails did exhibit antipredator behaviors when exposed to risk of predation, but juvenile snails did not. Generally, parasitized snails exhibited the same antipredator behaviors as unparasitized individuals, but snails infected with certain species of parasites altered their behavior in both the laboratory and in the field. Although snails from different sites had different shell morphologies, long-term exposure to risk of predation did not alter shell morphology, but gastropods infected with certain parasite species did have different shell morphologies than unparasitized snails. There appeared to be no interaction between parasitism and predation with regards to feeding behavior, antipredator behavior, or shell morphology, which was counter to my predictions. The lack of synergism is probably due to few impacts of either predation or parasitism separately on T. obsoleta phenotypes, which is counter to results in other gastropods. Tritia obsoleta exhibits both thick shells and high density population, which both decrease predation risk and may explain lack of its responses to predators. iii I dedicate this to my parents, Mark and Tricia. iv Table of Contents List of Tables………………………………………………………………………………...…..vii List of Figures……………………………………………………………………..………….…...x Acknowledgements……………………………………………………………………….…..….xii Chapter 1: Introduction…………………………………………………………………………..1 Chapter 2: The effect of parasitism, predation and ontogeny on the feeding rates of a marine snail………………………………………………………………………………………………..7 Abstract…………………………………………………………………………………………....8 Introduction……………………………………………………………………………………..…9 Methods…………………………………………………………………………………………..11 Results……………………………………………………………………………………………16 Discussion………………………………………………………………………………………..17 Tables…………………………………………………………………………………………….21 Figures……………………………………………………………………………………………24 Chapter 3: Phenotypic plasticity of antipredator behavior across ontogeny………………..…..27 Abstract…………………………………………………………………………………………..28 Introduction………………………………………………………………………………………29 Methods…………………………………………………………………………………………..31 Results……………………………………………………………………………………………36 Discussion………………………………………………………………………………………..39 Tables…………………………………………………………………………………………….45 Figures……………………………………………………………………………………………46 Chapter 4: The effect of parasitism on the movement of marine snail Tritia obsoleta in the laboratory and field……………………………………………………………………..………..48 Abstract…………………………………………………………………………………………..49 Introduction………………………………………………………………………………………50 Methods…………………………………………………………………………………………..52 Results……………………………………………………………………………………………57 Discussion………………………………………………………………………………………..59 Tables…………………………………………………………………………………………….64 Figures……………………………………………………………………………………………68 Chapter 5: Morphological plasticity in response to the environment, but not in response to predators………………………………………………………………………………………….70 Abstract…………………………………………………………………………………………..71 Introduction………………………………………………………………………………………72 Methods…………………………………………………………………………………………..73 Results……………………………………………………………………………………………78 Discussion………………………………………………………………………………………..80 Tables………………………………………………………………………………………….....84 Figures……………………………………………………………………………………………89 v Chapter 6: The impact of parasites on the size and morphology of a marine gastropod…….....94 Abstract………………………………………………………………………………………......95 Introduction……………………………………………………………………………………....96 Methods…………………………………………………………………………………………..97 Results…………………………………………………………………………………………..102 Discussion………………………………………………………………………………………104 Tables…………………………………………………………………………………………...108 Figures…………………………………………………………………………………………..113 Chapter 7: Conclusions…………………………………..…………………………………....117 Bibliography……………………………………………………………………………………128 Appendices Appendix 1……………………………………………………………………………………...147 Appendix 2………………………………………………………………………………….…..153 Appendix 3……………………………………………………………………………………...170 Appendix 4……………………………………………………………………………………...171 Appendix 5……………………………………………………………………………………...173 vi List of Tables Chapter 1: Table 1-1. Interactions between both predation and parasitism in gastropods…………………...3 Chapter 2: Table 2-1. The total number of T. obsoleta from each snail category that was tested in each experimental treatment………………………………………...…………………………………21 Table 2-2. Permutation test results demonstrating the effect of treatment (predator chemical cues, control) and life history stage (juvenile, adult) on the feeding coefficients (mass consumed/ snail shell length) of T. obsoleta……………..…………………………………...……...………22 Table 2-3. Permutation test results demonstrating the effect of treatment (predator chemical cues or control) and infection category (unparasitized, L. setiferoides infected, or S. dentatum infected) on the feeding rate of adult T. obsoleta.…………………………………………….…23 Chapter 3: Table 3-1. Number of T. obsoleta examined in each experiment by treatment and collection site.……...…………………………………………………………………………...…………...45 Chapter 4: Table 4-1. The behavior of T. obsoleta seen in the laboratory and field experiments by parasite species, and the next hosts for these parasites…………..………………………………….……64 Table 4-2. Number of T. obsoleta infected with each species of parasite at each site.……....….65 Table 4-3. The average shell lengths (± standard error) of parasitized and unparasitized T. obsoleta from each collection site.…………………………………………………..…..……….66 Table 4-4. Odds ratios were used to test for interactions between collection site and infection status on T. obsoleta behavior in the laboratory and field experiments..………………….….….67 Chapter 5: Table 5-1. MANOVA table for analysis of initial shell morphologies of juvenile T. obsoleta from three sites.……………..………………………….…………………………………..….....84 Table 5-2. MANOVA table from analysis of the effects of treatment and site on shell morphology of T. obsoleta.…………………………...…..…………………………...………....85 Table 5-3. MANOVA table for the analysis of shell morphology of juvenile T. obsoleta at the beginning and the end of the experiment..……………………...………..………………..…..…86 Table 5-4. ANOVA tables of the growth data of juvenile T. obsoleta before (initial shell length) and after the experiment (all other dependent variables)…………….…………………….….....87 Table 5-5. Pairwise comparisons (Tukey’s HSD) to determine differences in initial shell lengths and final growth measurements that were collected at the end of the experiment among sites.…………………………..………………………..……………….…………………..…....88 Chapter 6: Table 6-1. Infection status of Tritia obsoleta collected during the summer of 2014…….….…108 Table 6-2. ANOVA table of results indicating how the shell lengths of snails differed by parasite species and collection site.……………………………….………………………..……...….…109 Table 6-3. Average shell length of T. obsoleta by parasite species and by collection site….…110 vii Table