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Cognitive and Magnetosensory Ecology of the Yellow Stingray, Urobatis Jamaicensis

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COGNITIVE AND MAGNETOSENSORY ECOLOGY OF THE YELLOW STINGRAY, UROBATIS JAMAICENSIS by Kyle C. Newton A Dissertation Submitted to the Faculty of The Charles E. Schmidt College of Science In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Florida Atlantic University Boca Raton, FL August 2017 Copyright by Kyle C. Newton 2017 ii ACKNOWLEDGEMENTS This dissertation research would not have been possible without the guidance and encouragement from my committee chair, Steve Kajiura, and my dissertation committee, Sarah Milton, Ken Dawson-Scully, and Bob Stackman. Ed Gerstein, Mike Salmon, and Korey Sorge were reliable sources of help on experimental design; Mark Royer and Fred Knapp let me use their machine shops and tools during the construction of experimental apparatuses; Neal Tempel, Mark Scales, and Corey Jasper lended facilities support and helped me solve the world’s problems; Michelle Cavallo, Becky Dixon, Sharon Ellis, and Jenny Govender helped me navigate an incredible amount of university bureaucracy. Chris Bedore, Matt Kolmann, Dovi Kacev, Kady Lyons let me complain about my situation for two years; my labmates Eloise Cave, Beth Bowers, Kier Smith, Lindsay Harris, Theresa Gunn, Jessica Noble, Tanner Anderson, and Shari Tellman let me vent and rant some more; volunteers Shelby Creager, Celina Prince, Lisa Celano, Katie Kramer, and Gabriela Gil, took care of my stingrays; Stephen Ramirez and Anthony Radzins built custom electronic gadgets; and Adam Summers, Dean Grubbs, Joe Sisneros, Donovan German, Kathryn Dickson, Sean Walker, Chris Lowe, Yannis Papastamatiou, Jeremy Vaudo, Derek Burkholder, Phil Motta, Colin Hughes, Marianne Porter, and iv Jeanette Wyneken gave me excellent advice when times were dark and encouraged me to stay the course. Last but not least, I’m thankful for the continuous love and support from Mom and Dad as I returned to graduate school after a long hiatus. My best friend, Ben Smith, always encouraged me to seek out the adventurous road and helped me return to my true path when I strayed. The patience, kindness, and love of Shelby Creager helped me survive three of the hardest years I have ever experienced. And of course, Walter, who taught me patience and acceptance – you’re the best damn cat ever! v ABSTRACT Author: Kyle C. Newton Title: Cognitive and magnetosensory ecology of the yellow stingray, Urobatis jamaicensis Institution: Florida Atlantic University Dissertation Advisor: Dr. Stephen M. Kajiura Degree: Doctor of Philosophy Year: 2017 Elasmobranchs (sharks, skates, and rays) migrate across a wide range of spatiotemporal scales, display philopatry, seasonal residency, and maintain home ranges. Many animals use the Earth’s magnetic field to orient and navigate between habitats. The geomagnetic field provides a variety of sensory cues to magnetically sensitive species, which could potentially use the polarity, or intensity and inclination angle of the field, to derive a sense of direction, or location, during migration. Magnetoreception has never been unequivocally demonstrated in any elasmobranch species and the cognitive abilities of these fishes are poorly studied. This project used behavioral conditioning assays that paired magnetic and reinforcement stimuli in order to elicit behavioral responses. The specific goals were to determine if the yellow stingray, Urobatis jamaicensis, could detect magnetic fields, to quantify the nature of the magnetic stimuli it could detect, and to quantify the learning and memory capabilities of this species. The vi results supported the original hypotheses and demonstrated that the yellow stingray could: discriminate between magnetic and non-magnetic objects; detect and discriminate between changes in geomagnetic field strength and inclination angle; and use geomagnetic field polarity to solve a navigational task. The yellow stingray learned behavioral tasks faster and retained the memories of learned associations longer than any batoid (skate or ray) to date. The data also suggest that this species can classify magnetic field stimuli into categories and learn similar behavioral tasks with increased efficiency, which indicate behavioral flexibility. These data support the idea that cartilaginous fishes use the geomagnetic field as an environmental cue to derive a sense of location and direction during migrations. Future studies should investigate the mechanism, physiological threshold, and sensitivity range of the elasmobranch magnetic sense in order to understand the effects of anthropogenic activities and environmental change on the migratory ability of these fishes. vii COGNITIVE AND MAGNETOSENSORY ECOLOGY OF THE YELLOW STINGRAY, UROBATIS JAMAICENSIS LIST OF FIGURES ............................................................................................... XI CHAPTER 1. INTRODUCTION ............................................................................ 1 Orientation and Navigation ............................................................................. 2 Magnetoreception .......................................................................................... 3 Mechanisms of Magnetoreception ................................................................. 7 Research Goals ........................................................................................... 10 CHAPTER 2. MAGNETIC FIELD DISCRIMINATION, LEARNING, AND MEMORY…. ..................................................................................................... 12 ABSTRACT ..................................................................................................... 12 INTRODUCTION ............................................................................................. 13 METHODS ....................................................................................................... 20 Husbandry .................................................................................................... 20 Behavioral Considerations ........................................................................... 20 Training ........................................................................................................ 21 Memory Probes ............................................................................................ 24 Behavioral Data Collection and Analysis ..................................................... 24 RESULTS ........................................................................................................ 26 Overall Results ............................................................................................. 26 Individual Results ......................................................................................... 27 viii DISCUSSION .................................................................................................. 30 Magnetoreception in Elasmobranchs ........................................................... 32 Learning and Memory in Elasmobranchs ..................................................... 33 CHAPTER 3. DETECTION OF THE GEOMAGNETIC CUES NEEDED TO DERIVE A SENSE OF LOCATION .................................................................. 42 ABSTRACT ..................................................................................................... 42 INTRODUCTION ............................................................................................. 43 METHODS ....................................................................................................... 47 Subjects ....................................................................................................... 47 Apparatus ..................................................................................................... 47 Pretraining .................................................................................................... 49 Experiment #1 – Magnetic Stimulus Detection by Naïve Stingrays ............. 51 Experiment #2 – Magnetic Stimulus Discrimination by Experienced Stingrays ...................................................................................................... 52 Experiment #3 - Magnetic Stimulus Discrimination by Naïve Stingrays ....... 52 Data Collection and Analysis ....................................................................... 53 RESULTS ........................................................................................................ 54 DISCUSSION .................................................................................................. 56 CHAPTER 4. THE USE OF MAGNETIC FIELD POLARITY AS A CUE TO SOLVE A SPATIAL TASK ................................................................................ 70 ABSTRACT ..................................................................................................... 70 ix INTRODUCTION ............................................................................................. 71 METHODS ....................................................................................................... 76 Experimental Set Up .................................................................................... 76 Pretraining .................................................................................................... 77 Behavioral Conditioning ............................................................................... 78 Reversal Training ......................................................................................... 81 Data Collection and Analysis ......................................................................
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