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Visual Adaptations in Sharks, Skates and Rays

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Visual Adaptations in Sharks, Skates and Rays VISUAL ADAPTATIONS IN SHARKS, SKATES AND RAYS by Dawn Michelle McComb 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 2009 ACKNOWLEDGEMENTS This work would not have been possible without financial support from the Florida Atlantic University Graduate Fellowship for Academic Excellence, FAU Newell Doctoral Fellowship, PADI Project AWARE Foundation Grant, Junior Women’s Club of Boca Raton Scholarship Award and the National Science Foundation. Obtaining a PhD is never a solitary experience, but rather a process that takes you down unexpected paths leading to wonderful discoveries, experiences and relationships. So many people have entered my life as a result of this work and made the journey all the more amazing. The members of my dissertation committee have provided extensive personal and professional guidance, support and encouragement. With great respect, I thank my advisor, Steve Kajiura, who allowed incredible freedom, yet was there for me when I needed help with experiments, field work, electronics debugging and interpreting results. He improved my analytical and writing skills, and provided so much opportunity while teaching me the importance of having fun along the way. My research took me to many distant places and I am grateful to everyone who helped me while I was away from home. At Mote Marine Laboratory, I thank Dr. Bob Hueter for making my research possible, Dr. Carl Luer for clearnose skates, Jack Morris for collecting and housing animals, and Dr. Jim Gelsleichter and John Tyminski for shark transport. At the University of Hawaii at Manoa, thanks goes to Dr. Tim Tricas and Dr. Kim Holland for use of their laboratories and to Yannis and Ariel for the logistical assistance. iii Daniel Kimberly at the Charles Darwin University in Darwin, Australia has my gratitude for the day and nighttime fishing trips during the monsoon, for helping me catch a barramundi and the lectures on crocodile safety. Gumbo Limbo Research Station housed many of my research animals and thanks to Dr. Kirt Rusenko, Judy Gire and all the staff for their invaluable help. At Florida Atlantic University, I am ever grateful to Dr. Michael Salmon and Dr. Jeanette Wyneken for support and encouragement. Thank you Neil Temple for saving the day more than once! The technical genius of Mark Royer created many versions of the devices used during experimentation, while Mary Morris designed my shutter motor. I cannot thank members of the shark lab enough for everything they have done for me. From field work on the high seas and back waters, assistance and company in the dark rooms, lively manuscript discussions, to coffee trips and friendship: Laura, Dave, Tricia, Anthony, Chris, Audrey, Kier, Gabby, Joey, Faydra, Evan, Garth, and Jodi, you were indispensible and kept my sanity in check. Laura thanks for always being there for me and for the chocolate. I particularly thank Dr. Ivan Schwab (University of Davis) for inspiring me, believing in me, and mentoring me. Richard Brinn for the trip to the Amazon and that amazing research opportunity. Tim Rahn for all the fishing trips in the Florida Keys, knowing so much about bonnetheads, and being my number one fan. Lastly, I thank my family for all of the love and support you have given me. You introduced me to the wonder of the ocean at an early age and sparked my love of nature. I would not have been able to pursue this dream without you. Finally, I thank my husband, Mac, for making all my dreams come true and for giving me our first son, Nicholas. iv ABSTRACT Author: Dawn Michelle McComb Title: Visual Adaptations in Sharks, Skates and Rays Institution: Florida Atlantic University Dissertation Advisor: Dr. Stephen M. Kajiura Degree: Doctor of Philosophy Year: 2009 The central importance of vision to an organism is evident in the anatomical and physiological adaptations within the eye that can be correlated to the organism’s behavior and ecology. The goal of this study was to perform a functional analysis of adaptations within the elasmobranch visual system. An integrative approach was used to examine morphological and physiological adaptations in several species and link these adaptations to phylogeny, locomotion, habitat, behavior and ecology. Functional aspects investigated were eye position, pupil shape, spectral sensitivity, temporal resolution, the extent of the visual field and ultimately the integration of the visual and electrosensory systems. The elasmobranch eye adapts to the light environment of its habitat. Sharks from similar habitats had similar spectral sensitivities such as the bonnethead and blacknose sharks, both maximally sensitive to blue light of 480 nm. The spectral sensitivity of the scalloped hammerhead, which lives in a different environment, was maximally sensitive v to green light (530 nm). The temporal characteristics of the eye also matched habitat and lifestyle. Species experiencing variable light conditions exhibited increased critical flicker-fusion frequencies, such as the bonnethead (31 Hz) and scalloped hammerhead (27 Hz), in contrast to deeper or more nocturnal species such as the blacknose shark (18 Hz). Elasmobranch visual fields correlated to each species’ lifestyle, habitat and foraging strategy. Expansive monocular views, including a 360º panoramic view in the yellow stingray, were measured in species that rely on vision for vigilance against predators. The Atlantic stingray possessed large binocular overlaps (72º), which provided depth perception useful for tracking prey. By comparison, the frontal binocular overlaps of hammerhead species were larger than sharks with a more conventional head shape. This study quantified the range of the electrosensory system and the extent of the visual field of several shark species, confirming both systems overlap around the head facilitating near seamless visual and electrosensory sensory function relevant to prey detection. The findings of this study indicate that ambient environmental light strongly influenced the function of the elasmobranch eye and that the extent of species’ visual fields correlated with aspects of their morphology, locomotion and ecology. vi VISUAL ADAPTATIONS IN SHARKS, SKATES AND RAYS LIST OF TABLES. ............................................................................................................x LIST OF FIGURES ......................................................................................................... xi CHAPTER 1: INTRODUCTION.....................................................................................1 VISUAL SYSTEM EVOLUTION.................................................................................1 VISUAL SYSTEM OF ELASMOBRANCH FISHES...................................................2 VISUAL SYSTEM ADAPATATIONS .........................................................................5 Spectral sensitivity .....................................................................................................6 Temporal resolution...................................................................................................8 Visual field .................................................................................................................9 Sensory integration ..................................................................................................11 RESEARCH SUMMARY............................................................................................12 CHAPTER 2: TEMPORAL RESOLUTION AND SPECTRAL SENSITIVITY OF THE VISUAL SYSTEM OF THREE COASTAL SHARKS SPECIES FROM DIFFERENT LIGHT ENVIRONMENTS ....................................................................14 ABSTRACT..................................................................................................................14 INTRODUCTION ........................................................................................................15 METHODS ...................................................................................................................17 Specimen collection .................................................................................................17 Pupil shape and dilation ..........................................................................................18 Experimental setup...................................................................................................19 Temporal resolution.................................................................................................20 Spectral sensitivity ...................................................................................................21 RESULTS .....................................................................................................................22 Pupil shape and dilation ..........................................................................................22 Temporal resolution.................................................................................................23 Spectral sensitivity ...................................................................................................23 DISCUSSION...............................................................................................................24 Pupil shape and dilation ..........................................................................................24 Temporal resolution.................................................................................................25
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