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Reproduction and Early Life of the Humboldt Squid

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REPRODUCTION AND EARLY LIFE OF THE HUMBOLDT SQUID A DISSERTATION SUBMITTED TO THE DEPARTMENT OF BIOLOGY AND THE COMMITTEE ON GRADUATE STUDIES OF STANFORD UNIVERSITY IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Danielle Joy Staaf August 2010 © 2010 by Danielle Joy Staaf. All Rights Reserved. Re-distributed by Stanford University under license with the author. This work is licensed under a Creative Commons Attribution- Noncommercial 3.0 United States License. http://creativecommons.org/licenses/by-nc/3.0/us/ This dissertation is online at: http://purl.stanford.edu/cq221nc2303 ii I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. William Gilly, Primary Adviser I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Mark Denny I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. George Somero Approved for the Stanford University Committee on Graduate Studies. Patricia J. Gumport, Vice Provost Graduate Education This signature page was generated electronically upon submission of this dissertation in electronic format. An original signed hard copy of the signature page is on file in University Archives. iii Abstract Dosidicus gigas, the Humboldt squid, is endemic to the eastern Pacific, and its range has been expanding poleward in recent years. It is a voracious predator of small fish and invertebrates and prominent prey for large fish and mammals, including humans. Very little is known about Humboldt squid reproduction, development, and early life stages. To study the behavior, including dispersal capabilities, of paralarval D. gigas, I analyzed video of animals swimming in the laboratory, and determined that paralarvae are active swimmers that engage in hop-and-sink behavior. Control of the mantle aperture allows them to engage in slow swimming, in which water is leaked through the mantle aperture, and fast jetting, in which the mantle aperture is tightly closed and all water is expelled through the siphon—as is typical of adult jetting. A theoretical model of squid swimming was built to study the importance of aperture control during the jet cycle. This model predicts that active reduction of the aperture during jetting increases hydrodynamic efficiency, and that squid of large sizes can constrain the risk of embolism by increasing aperture size and decreasing jet frequency to values comparable to empirical measurements. Connectivity among populations of D. gigas throughout the range of this species was assessed with a population genetic approach, in which D. gigas was compared to the co-occurring squid Sthenoteuthis oualaniensis. In D. gigas, only two weakly differentiated populations were evident, with a biogeographic break at 5-6° N. I uncovered four deeply divergent clades in S. oualaniensis, including one which aligns with previous descriptions in the literature of Sthenoteuthis sp. nov. Breaks between clades of S. oualaniensis also occurred at 5-6° N. Range overlap between these two species occurs in the eastern tropical Pacific (ETP), a region both are believed to use as spawning grounds. I looked for paralarvae of D. gigas and S. oualaniensis in surface and subsurface net tows taken in the ETP from 1998 to 2006, and found that abundance was much greater in surface than subsurface tows. I then used a Generalized Linear Model approach to assess the importance of in situ oceanographic variables as predictors of paralarval incidence. iv Sea surface temperature was found to be a strong predictor of incidence in both surface and subsurface tows, with the probability of paralarval capture rising monotonically from near zero at 15 °C to 0.9 at 30 °C. The apparent lack of paralarvae at surface temperatures below 15 °C raises a question of whether D. gigas can spawn in the temperate and even subpolar waters of its expanded range. I conducted in vitro fertilization studies and found the optimal temperature range for successful laboratory development of D. gigas is 15-25° C. v Acknowledgements Many squid were sacrificed for this research, and I only hope that the science presented here will serve to make the world a better place for their descendants, as well as my own. For support and guidance over the last six years I am grateful to all my mentors, especially my advisor, William Gilly. I’ve learned so much from six hilariously unpredictable years in his lab. Mark Denny was an endless source of advice and encouragement, and conversations with George Somero continually invigorated my work. Collaborating with John Field has always been an education and a pleasure. Rob Dunbar served as a kind and thoughtful committee chair. I truly don’t know what would have become of this thesis if not for my labmates. Ashley Booth and Julie Stewart, with their boundless generosity and good humor, made the lab a place to call home. Lou Zeidberg gave freely of his time, supplies, and sarcastic wit, and Charles Hanifin dispensed tall tales and scientific wisdom. Alex Norton has been rooting for me since day one, and Carl Elliger was always happy to process “just one more sample.” Zora Lebaric was my lab mother, and Judit Pungor my new little lab sister. Hopkins Marine Station is such a character that I want to thank it as one entity, but the individuals who make it run deserve personal mention. Judy Thompson, Doreen Zelles, Chris Patton, John Lee, Freya Sommer, Joe Wible, and Jim Watanabe have all solved problems and opened doors for me. Equally worthy of gratitude is our umbilical cord to main campus, the wonderfully friendly and competent biology student services staff: Valerie Kiszka, Jennifer Mason, and Matt Pinhiero. Eternal thanks go to all my fellow grad students, with whom I have laughed, cried, ranted and celebrated. Monthly progress meetings with Cheryl Logan kept me motivated, and spontaneous field trips with Alison Haupt always improved my mood and perspective. For taking me to the Monterey Bay Aquarium at a malleable age, and for their subsequent tolerance of pet octopuses, I am grateful to my parents, Ben and Sue vi Shulman. A special shout-out to my father for learning to scuba dive just so I would have a buddy. To my older brother Michael, whom I’ve always looked up to, even when we were the same height, and to his lovely wife Megan, thanks for getting your PhDs so I had to get mine. To my in-laws--Carmen, Carl, Diana and Clint--thanks for adopting me so readily, and being so understanding of my tilting at the PhD windmill for the entire time you’ve known me. That also goes for my husband. Anton, this thesis is for you. vii Table of Contents Abstract..........................................................................................................................iv Acknowledgements .......................................................................................................vi Table of Contents.........................................................................................................viii List of Tables ...............................................................................................................xiv List of Figures..............................................................................................................xvi Chapter 1 ........................................................................................................................ 1 INTRODUCTION 1.1. Figures.................................................................................................................. 7 Chapter 2 ........................................................................................................................ 9 THE LITTLEST SQUID: LOW REYNOLDS NUMBERS AND FUNNEL APERTURE MODIFICATION 2.1. Abstract ................................................................................................................ 9 2.2. Introduction.......................................................................................................... 9 2.3. Methods.............................................................................................................. 12 2.3.1. Animal collection ........................................................................................ 12 2.3.2. Video recording........................................................................................... 12 2.3.3. Kinematic measurements ............................................................................ 13 viii 2.3.4. Modeling ..................................................................................................... 14 2.3.5. Parameterization.......................................................................................... 19 2.4. Results................................................................................................................ 21 2.4.1. Behavior...................................................................................................... 21 2.4.2. Kinematics .................................................................................................. 22 2.4.3. Model .......................................................................................................... 24 2.5. Discussion.........................................................................................................
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