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Title of Thesis Or Dissertation 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... Predator-induced behavioral and morphological plasticity in marine snails, Nucella spp. A Dissertation Presented by Paul Eugene Bourdeau 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 2009 Copyright by Paul Eugene Bourdeau 2009 Stony Brook University The Graduate School Paul Eugene Bourdeau We, the dissertation committee for the above candidate for the Doctor of Philosophy degree, hereby recommend acceptance of this dissertation. Dianna K. Padilla – Dissertation Advisor Professor, Ecology and Evolution Jeffrey S. Levinton - Chairperson of Defense Distinguished Professor, Ecology and Evolution Massimo Pigliucci Professor, Ecology and Evolution Geerat J. Vermeij Geology, University of California, Davis This dissertation is accepted by the Graduate School Lawrence Martin Dean of the Graduate School ii Abstract of the Dissertation Predator-induced behavioral and morphological plasticity in marine snails, Nucella spp. by Paul Eugene Bourdeau Doctor of Philosophy in Ecology and Evolution Stony Brook University 2009 Predator-induced changes in the defensive traits of prey organisms are widespread in nature and have important ecological consequences. Currently, our understanding of inducible defense comes from studies focused on single trait responses to single predators that often fail to link traits to patterns of co- occurrence with predators in nature. Consequently, we have poor understanding of how prey express multivariate phenotypes in the presence of multiple predators and which traits are important for allowing prey to coexist with predators. This dissertation explores the ecology and evolution of inducible defenses, using marine snails as a model system. Specifically I investigate predator-induced behavior and morphology in three sympatric intertidal snails, (Nucella spp.) in response to the presence of two predators with different attack modes (crab and seastar). My objectives were to determine: 1) whether snails exhibit adaptive responses to different types of predation risk, 2) how prey respond to combined predators, 3) what mechanisms underlie inducible morphological defenses, and 4) whether snails in the genus Nucella exhibit species-specific responses to predators. Snails were extremely plastic in their ability to respond to different predator cues. Responses to a given predator were dependent on the predatorʼs diet and prey prioritized their response to the most dangerous predator when exposed to multiple predators simultaneously. I also found that consideration of single traits alone can lead to erroneous interpretations about how prey respond to combined predators. Growth rates were slowed in the presence predators indicating that snails are paying a cost for defending themselves. However, reduced feeding activity rather than an active iii physiological response appears to be the mechanism underlying predator- induced shell thickening, suggesting that the cost is associated with lost feeding opportunity rather than the production of structural defenses. Statistical analyses of shell strength indicate that the accumulation of new shell material, rather than architectural or material properties changes in the shell was responsible for increased structural strength. Lastly, all species altered their feeding behavior and shell morphology in the presence of predators, but exhibited species-specific differences that can be linked to their distribution across a predation gradient. iv To the little breeze off the water (or the little bird that sings) that helped me along the way Table of Contents List of Tables……………………………………………………………………. ...viii List of Figures…………………………………………………………………….. x Acknowledgements………………………………………………………………. xii Chapter 1: Introduction…………………………………………………………... 1 References……………………………………………………………………….. 5 Chapter 2: Cue reliability, risk sensitivity and inducible morphological defense in a marine snail Abstract……………………………………………………………………………. 9 Introduction……………………………………………………………………….. 10 Materials and methods…………………………………………………………... 13 Results…………………………………………………………………………….. 16 Discussion………………………………………………………………………… 17 Tables……………………………………………………………………………... 24 Figures…………………………………………………………………………….. 26 References……………………………………………………………………...... 29 Chapter 3: Specificity of cues that induce shell defenses in marine snails: Is a crab just a crab? Abstract…………………………………………………………………………… 35 Introduction……………………………………………………………………….. 35 Methods…………………………………………………………………………… 37 Results…………………………………………………………………………….. 41 Discussion………………………………………………………………………… 42 Figures…………………………………………………………………………….. 48 References……………………………………………………………………….. 49 Chapter 4: Prioritized phenotypic responses to combined predators in a marine snail Abstract……………………………………………………………………………. 56 Introduction……………………………………………………………………….. 57 Methods…………………………………………………………………………… 60 Results…………………………………………………………………………….. 68 Discussion………………………………………………………………………… 71 Figures…………………………………………………………………………….. 81 References………………………………………………………………………... 85 Chapter 5: An inducible morphological defence is a passive by-product of behaviour in a marine snail Abstract……………………………………………………………………………. 92 Introduction……………………………………………………………………….. 93 Methods…………………………………………………………………………… 96 Results…………………………………………………………………………….. 101 vi Discussion………………………………………………………………………… 104 Figures…………………………………………………………………………….. 108 References………………………………………………………………………... 113 Chapter 6: Variation in inducible defenses in a marine snail from habitats with different predation regimes Introduction……………………………………………………………………….. 118 Methods…………………………………………………………………………… 120 Results…………………………………………………………………………….. 125 Discussion…………………………………………………………………………127 Tables…………………………………………………………………………….. 132 Figures……………………………………………………………………………. 136 Refereces ………………………………………………………………………… 142 Chapter 7: Predator-induced plasticity and habitat partitioning in congeneric marine snails distributed along a vertical intertidal gradient. Introduction………………………………………………………………………. 147 Materials and methods………………………………………………………….. 149 Results……………………………………………………………………………. 155 Discussion………………………………………………………………………… 160 Tables………………………………………………………………………………166 Figures…………………………………………………………………………….. 174 References……………………………………………………………………….. 179 Chapter 8: Conclusions…………………………………………………………. 184 References……………………………………………………………………….. 186 Bibliography………………………………………………………………………. 187 Appendices Appendix 1…………………………………………………………………………227 Appendix 2…………………………………………………………………………228 Appendix 3…………………………………………………………………………229 Appendix 4…………………………………………………………………………230 Appendix 5…………………………………………………………………………231 Appendix 6…………………………………………………………………………232 vii List of Tables Chapter 2: Table 1. Analyses of defensive shell responses and linear shell growth of Nucella lamellosa to the presence of injured con- and hetero-specific snails and Cancer productus fed different diets……………………………….. 24 Chapter 6: Table 1. Factorial ANCOVA for the effects of origin, treatment, size and their interactive effects on Nucella lamellosa shell shape…………………… 132 Table 2. Factorial ANCOVA for the effects of origin and treatment and their interactive effects on Nucella lamellosa apertural lip thickening ………133 Table 3. Factorial ANCOVA for the effects of origin and treatment and their interactive effects on Nucella lamellosa shell mass gain……………… 134 Table 4. Factorial ANCOVA for the effects of origin and treatment, and their interactive effects on Nucella lamellosa shell strength change……….. 135 Chapter 7: Table 1. Results of factorial ANOVA on activity of three species of Nucella raised in the presence and absence of cues associated with the risk of predation……………………………………………………………………. 166 Table 2. Analysis of growth of three species of Nucella raised in the presence or absence of cues associated with the risk of predation….. 167 Table 3. Results of nested analyses of covariance on morphological traits for three species of Nucella raised in the presence or absence of cues associated with the risk of predation …………………………………… 168 Table 4. Differences in the allometeric growth rates of three species of Nucella raised in the presence or absence of cues associated with the risk of predation………………………………………………………………… 170 Table 5. Analyses of allometric scaling relationships among three species of Nucella………………………………………………………………………. 171 Table 6. Results of nested analyses of covariance on shell strength for three species of Nucella raised in the presence or absence of cues associated with predation risk…………………………………………………………. 173 Appendix 2: Analyses of morphological responses to predators by Nucella lamellosa after 70 days of exposure to experimental conditions………………… 228 Appendix 3: Results of MANCOVA on shell shape variables in Nucella lamellosa ……………………………………………………………………………….. 229 Appendix 4: Analysis of shell and body growth variation in Nucella lamellosa ……………………………………………………………………………….. 230 Appendix 5: Final size ranges of reference samples of Nucella species raised in the viii presence or absence of chemical cues from crabs……………………. 231 Appendix 6: Results of analyses of covariance on shell strength for experimental and
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