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Anti-Predator Responses of Squid Throughout Ontogeny

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Anti-Predator Responses of Squid Throughout Ontogeny Old Dominion University ODU Digital Commons Biological Sciences Theses & Dissertations Biological Sciences Spring 2016 Anti-Predator Responses of Squid Throughout Ontogeny Carly Anne York Old Dominion University, [email protected] Follow this and additional works at: https://digitalcommons.odu.edu/biology_etds Part of the Biology Commons, and the Physiology Commons Recommended Citation York, Carly A.. "Anti-Predator Responses of Squid Throughout Ontogeny" (2016). Doctor of Philosophy (PhD), Dissertation, Biological Sciences, Old Dominion University, DOI: 10.25777/twms-7w98 https://digitalcommons.odu.edu/biology_etds/9 This Dissertation is brought to you for free and open access by the Biological Sciences at ODU Digital Commons. It has been accepted for inclusion in Biological Sciences Theses & Dissertations by an authorized administrator of ODU Digital Commons. For more information, please contact [email protected]. ANTI-PREDATOR RESPONSES OF SQUID THROUGHOUT ONTOGENY by Carly Anne York B.S. December 2007, Elon University M.S. August 2011, Western Kentucky University A Dissertation Submitted to the Faculty of Old Dominion University in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY ECOLOGICAL SCIENCES OLD DOMINION UNIVERSITY May 2016 Approved by: Ian Bartol (Director) Lisa Horth (Member) Kent Carpenter (Member) Sara Maxwell (Member) Paul Krueger (Member) Joseph Thompson (Member) ABSTRACT ANTI-PREDATOR BEHAVIOR OF SQUID THROUGHOUT ONTOGENY Carly Anne York Old Dominion University, 2016 Director: Dr. Ian K. Bartol Multiple sensory modalities and a complex array of escape behaviors have evolved as components of anti-predator responses in squids. The goals of this study include: (1) examine the role of the lateral line analogue and vision in successful predator evasion; (2) measure kinematics of escape jetting; (3) document how chromatic patterning, posturing and inking in squid change in response to predators; and (4) investigate escape jet hydrodynamics of squid. Given that squids undergo considerable morphological, ecological, and behavioral changes throughout ontogeny, the goals above were all investigated across different life history stages. To test the respective roles of vision and the lateral line analogue, squid of different life stages were recorded in the presence of natural predators under light and dark conditions with their lateral line analogue intact and ablated via a pharmacological technique. Anti-predator behaviors of squid throughout ontogeny were studied in a series of predator-prey trials using high-speed videography. Additionally, the hydrodynamics and kinematics of high velocity escape jets in squid were examined using a combination of 2D/3D velocimetry. The lateral line analogue played a role in initiation of an escape response at the earliest life stages, and continued to contribute to successful evasion by aiding visual cues in juvenile/adult squid. Paralarvae relied heavily on stereotyped swimming behaviors and translucent coloration to avoid capture, while juvenile and adults used multiple cues associated with the predator’s approach to determine whether posturing or inking and escape jetting is the most suitable anti-predator behavior. Throughout ontogeny, squid produced two escape jet patterns: (1) escape jet I characterized by short rapid pulses resulting in vortex ring formation and (2) and escape jet II characterized by long high volume jets, often with a leading edge vortex ring. Paralarvae exhibited significantly higher propulsive efficiency (94.55%) than adult squid (87.71%) during jet ejection. These results indicate that all life stages of squid are well adapted for predator avoidance; they employ multiple sensory modalities for predator detection, use a variety of anti-predator behavioral responses, and utilize a highly efficient and flexible escape jet to maximize escape from predation. iii Copyright, 2016, by Carly A. York and Ian K. Bartol, All Rights Reserved. iv “Jetting animals are just hearts set free…” O’Dor and Webber, 1991 v ACKNOWLEDGMENTS I owe a debt of gratitude to my advisor Dr. Ian Bartol for his patience and guidance through this program. It has truly been a pleasure to be a part of his lab family for the past five years. I am also very thankful for the input of all my committee members: Dr. Lisa Horth, Dr. Kent Carpenter, Dr. Joseph Thompson and Dr. Sara Maxwell. Dr. Paul Krueger was especially helpful in providing code for my analysis and answering an excessive number of email inquiries. I thank the crew of VIMS ESL, principally Captain Sean Fate, for assistance in trawling for squid and for not letting me fall off the boat. Thanks also go to the Society of Integrative and Comparative Biology for awarding me the Grant-in-Aid of Research and National Science Foundation grant IOS 1115110, which contributed to the funding of this work. Eternal appreciation goes to my fellow graduate students with whom I have laughed, whined, raged and celebrated. My lab mate Rachel Jastrebsky, in particular, has been a wonderful friend and colleague through all of our squid adventures. I thank Tripp York for happily allowing me to uproot our lives so I could be a grumpy graduate student for five more years. Most of all, I thank my overly generous parents for their love and support. Without them I would surely be doing something less interesting with my life. vi TABLE OF CONTENTS Page LIST OF TABLES ............................................................................................................ vii LIST OF FIGURES ......................................................................................................... viii Chapter I. INTRODUCTION ...........................................................................................................1 II. LATERAL LINE ANALOGUE AIDS VISION IN SUCCESSFUL PREDATOR EVASION FOR BRIEF SQUID LOLLIGUNCULA BREVIS ........13 INTRODUCTION .................................................................................................13 MATERIALS AND METHODS ...........................................................................14 RESULTS ..............................................................................................................18 DISCUSSION ........................................................................................................21 III. MULTIPLE SENSORY MODALITIES USED BY SQUID IN SUCCESSFUL PREDATOR EVASION THROUGHOUT ONTOGENY. .........23 INTRODUCTION .................................................................................................23 MATERIALS AND METHODS ...........................................................................27 RESULTS .............................................................................................................34 DISCUSSION ........................................................................................................43 IV. ANTI-PREDATOR BEHAVIOR OF SQUID THROUGHOUT ONTOGENY .........................................................................................................52 INTRODUCTION .................................................................................................52 MATERIALS AND METHODS ...........................................................................55 RESULTS ..........................................................................................................64 DISCUSSION ........................................................................................................74 V. HYDRODYNAMICS AND KINEMATICS OF ESCAPE JETS THROUGHOUT ONTOGENY.............................................................................83 INTRODUCTION .................................................................................................83 MATERIALS AND METHODS ...........................................................................86 RESULTS ..............................................................................................................97 DISCUSSION ......................................................................................................105 VI. CONCLUSIONS ......................................................................................................114 REFERENCES ................................................................................................................119 VITA ................................................................................................................................128 vii LIST OF TABLES Table Page 1. Descriptive information for each treatment group. ............................................... 19 2. Descriptive measurements of escape jet I and escape jet II in paralarvae, juveniles and adults ............................................................................................... 100 viii LIST OF FIGURES Figure Page 1. SEM images of the lateral line analogue shown on a Doryteuthis pealeii .......... 16 paralarvae. 2. Comparison of the proportion of interactions survived (a) and number of interactions survived (b) in each treatment group. ........................................... 20 3. Angular orientation of squid during interactions with predator............................ 33 4. Mean proportion of escape responses (A) and surviving individuals (B) for paralarval and juvenile/adult squid for non-ablated and ablated squid during light and dark conditions ........................................................................... 36 5. Kinematics of the paralarval escape
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