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The Pelagic Propagule's Toolkit The pelagic propagule’s toolkit: An exploration of the morphology, swimming capacity and behaviour of marine invertebrate propagules by © Emaline M. Montgomery A Dissertation submitted to the School of Graduate Studies in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Marine Biology, Department of Ocean Sciences, Faculty of Science, Memorial University of Newfoundland June 2017 St. John’s, Newfoundland and Labrador Abstract The pelagic propagules of benthic marine animals often exhibit behavioural responses to biotic and abiotic cues. These behaviours have implications for understanding the ecological trade-offs among complex developmental strategies in the marine environment, and have practical implications for population management and aquaculture. But the lack of life stage-specific data leaves critical questions unanswered, including: (1) Why are pelagic propagules so diverse in size, colour, and development mode; and (2) do certain combinations of traits yield propagules that are better adapted to survive in the plankton and under certain environments? My PhD research explores these questions by examining the variation in echinoderm propagule morphology, locomotion and behaviour during ontogeny, and in response to abiotic cues. Firstly, I examined how egg colour patterns of lecithotrophic echinoderms correlated with behavioural, morphological, geographic and phylogenetic variables. Overall, I found that eggs that developed externally (pelagic and externally-brooded eggs) had bright colours, compared to the typically pale colour intensity of internally-brooded eggs. Additionally, my analysis suggested geographic location as a potential driver of the evolution of colour diversity through the selection of better-adapted pigments in response to ecological pressure. I then undertook a critical assessment of swimming capacity and sensory ability in propagules from four co-occurring North Atlantic echinoderms with two different types of pelagic development: the sea stars Asterias rubens (planktotrophic) and Crossaster papposus (lecithottrophic), the sea urchin Strongylocentrotus droebachiensis (planktotrophic), and ii the sea cucumber Cucumaria frondosa (lecithotrophic) at two different temperatures. Propagule swimming speed increased with ontogeny in two of the four species (the sea stars A. rubens and C. papposus) but did not uniformly increase with temperature. Contrary to initial assumptions, some lecithotrophic propagules emerged as the fastest swimmers (e.g., 1.2 mm s-1 in the brachiolaria of C. papposus). Lastly, in a study of phototaxis involving the same focal species, variation in swimming speed and trajectory were detected when propagules were exposed to three different light colours. Taken together, the data generated by my PhD work provide a framework to assess the adaptive value of pelagic propagules to benthic animals, to examine the trade-offs of complex life- history strategies, and to enhance modeling of larval dispersal in the marine environment. iii Acknowledgements Firstly, I would like to express my sincerest appreciation to my supervisor, Annie Mercier for the tireless dedication and mentorship she provided during this PhD. I have learned much from our work together, and her attention to detail and success in the field continues to be an inspiration. My sincere thanks also goes to my collaborator, Jean-Francois Hamel, for his motivation and passion for natural history. I will always remember to tell a story through my publications, not just a list of numbers. I would also like to thank my committee members: Kurt Gamperl, Garth Fletcher and Don Deibel, for their insightful comments and encouragement, but also for their questions that helped me tackle my research from different perspectives. I would also like to acknowledge the support and encouragement of Chris Parrish, who provided guidance and a sounding board like I was one of his own students. Many thanks to Don Stansbury (DFO) and the crew of the CCGS Teleost for the opportunity to study the deep sea on a research cruise, and to Memorial field services and the Ocean Sciences Centre’s workshop for their invaluable assistance with animal collections and experimental logistics. I thank my fellow labmates, past and present, for all the late nights in the lab and all the fun of the last four years. Special thanks to Katie Verkaik, Camilla Parzanini and Justine Ammendolia for their help with raising thousands of baby echinoderms and staring at dots in a dish. Finally, I would like to thank my parents for their encouragement and advice (from one island to another), and my good friends Nathan Gentry and Tyler Brown for always being there when I needed it most. iv Table of Contents Abstract ................................................................................................................................ ii Acknowledgements ............................................................................................................. iv Table of Contents ................................................................................................................. v Lists of Tables ..................................................................................................................... xi List of Figures .................................................................................................................... xii List of Appendices ............................................................................................................ xiv Co-Authorship Statements ................................................................................................ xvi Chapter 1. General Introduction........................................................................................... 1 1.1. Life-History Strategies .............................................................................................. 1 1.2. Origins of Marine Propagules ................................................................................... 2 1.3. Importance of Marine Propagules: Ecology, Aquaculture, Conservation ................ 5 1.4. Current State of Knowledge in the Larval Ecology of Benthic Invertebrates .......... 7 1.5. Echinodermata: A Focal Phylum for Comparative Study ........................................ 8 1.6. Main Objectives and Thesis Structure .................................................................... 12 1.7. References ............................................................................................................... 14 1.8. Tables and Figures .................................................................................................. 20 Chapter 2. Propagule Ecology from Egg to Juvenile ......................................................... 25 2.1. Classification of Marine Propagules ....................................................................... 25 2.2. Importance of Cilia ................................................................................................. 28 2.3. Sensory Behaviour .................................................................................................. 29 v 2.4. Types and Mechanisms of Sensory Detection ........................................................ 30 2.4.1. Photosensitivity ................................................................................................ 31 2.4.2. Chemosensitivity .............................................................................................. 32 2.4.3. Gravisensitivity ................................................................................................ 34 2.5. Measuring Behavioural Responses ......................................................................... 35 2.6. Practical Applications of Sensory Behavioural Responses..................................... 37 2.6.1. Dispersal models .............................................................................................. 37 2.6.2. Ecotoxicology ................................................................................................... 38 2.6.3. Climate change ................................................................................................ 39 2.7. References ............................................................................................................... 42 2.9. Tables and figures ................................................................................................... 51 Chapter 3. Patterns and Drivers of Egg Pigment Intensity and Colour Diversity in the Ocean: A Meta-Analysis of Phylum Echinodermata ......................................................... 54 3.1. Abstract ................................................................................................................... 54 3.2. Introduction ............................................................................................................. 56 3.3. Study of Egg Metrics, and Biotic and Abiotic Factors ........................................... 60 3.3.1. Dataset collection ............................................................................................ 60 3.3.2. Standardization of variables for colour assessment ........................................ 61 3.3.3. Subset generation and data analysis ................................................................ 63 3.4. Drivers of Egg Pigmentation Intensity and Diversity ............................................. 64 3.4.1. Overall patterns of egg colour relative to development site
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