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Electroreception in the Euryhaline Stingray, Dasyatis Sabina

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Electroreception in the Euryhaline Stingray, Dasyatis Sabina ELECTRORECEPTION IN THE EURYHALINE STINGRAY, DASYATIS SABINA by David W. McGowan A Thesis Submitted to the Faculty of The Charles E. Schmidt College of Science In Partial Fulfillment of the Requirements for the Degree of Master of Science Florida Atlantic University Boca Raton, Florida May 2008 ELECTRORECEPTION IN THE EURYHALINE STINGRAY, DASYATIS SABINA by David W . McGowan This thesis was prepared under the direction of the candidate's thesis advisor, Dr. Stephen M. Kajiura, Department of Biological Sciences, and has been approved by the members of his supervisory committee. It was submitted to the faculty of The Charles E. Schmidt College of Science and was accepted in partial fulfillment of the requirements for the degree of Master of Science. SUPERVISORY COMMITTEE Thes1s A v1sor ~~ ii. ACKNOWLEDGEMENTS I would like to thank my committee members Dr. Mike Salmon of Florida Atlantic University and Dr. Joseph Sisneros of the University of Washington for their time and invaluable input throughout the length of this project. This study would not have been possible without the support of my colleagues at the Florida Fish & Wildlife Research Institute's Tequesta and Deleon Springs Field labs in collecting and transporting the stingrays. My fellow lab mates in the FAU Elasmobiology Lab, Chris Bedore, Laura Macesic, Mikki McComb, Tricia Meredith, and Anthony Cornett, were of such great support throughout this endeavor, as well the numerous undergraduate volunteers. They constantly assisted me with husbandry, transportation of animals and supplies, and in the trials and tribulations of graduate school. Special thanks to my amazing wife, Veronica, for her unconditional love and support, and limitless patience over these past four years. Finally, I would like to thank my advisor and mentor, Dr. Stephen Kajiura, for accepting such an untraditional student and tolerating all of my distractions (as important as they were). He has opened my eyes to another side of science that I had taken for granted, and for that I am forever grateful. lll ABSTRACT Author: David W. McGowan Title: Electroreception in the euryhaline elasmobranch, Oasyatis sabina Institution: Florida Atlantic University Thesis Advisor: Dr. Stephen M. Kajiura Degree: Master of Science Year: 2008 This study determined the electrosensitivity of a euryhaline elasmobranch, the Atlantic stingray, Dasyatis sabina, throughout the range of salinities that it would naturally encounter. It quantified the behavioral response of the stingrays . to prey-simulating electric stimuli in freshwater, brackish, and full strength seawater. The electroreceptive capability of stingrays from a permanent freshwater population in the St. Johns River system was also compared with stingrays that inhabit the tidally-dynamic Indian River Lagoon in east Florida. This study demonstrated that D. sabina can detect prey-simulating electric fields in freshwater, but the function of its electrosensory system is significantly reduced. The SJR stingrays did not demonstrate an enhanced electrosensitivity in freshwater, nor did they have reduced sensitivity when introduced to higher salinities. The reduction in electrosensitivity and detection range in freshwater is attributed to both an environmental factor (electrical resistivity of the water) and the physiological limitations of the ampullary canals. IV TABLE OF CONTENTS LIST OF TABLES ........................................................................................................... vi LIST OF FIGURES ........... ....... ....... ..... .. .................. .. .. ....... .. ... ..... ... ... .................... .... .. vii ELECTRORECEPTION IN THE EURYHALINE STINGRAY, DASYATIS SABINA INTRODUCTION .... ... .. ....... ... ... .. .... .......... .... ...... .... ................ ............................. 1 MATERIALS AND METHODS ............................................................................. 4 Study area .. ................. .. ........ .. ... .. ........ ................................. .. .... ............. 4 Stingray collection and maintenance .................................................... .... 4 Experimental apparatus ........... .......... ...... ... .. ...... ... .... .... ............ .. ... .... ..... 5 Experimental protocol ... ... ....... ....... .. ...... ... ......... ................................. ...... 6 Data analysis ............................................................................................ 7 RESULTS ..... .... .................. .... ...... ....... .. .... .... ....... .... ... ............. .. ............. .... ... .. 13 DISCUSSION .... ............................. ................. .. ...... ............. .. ... ............. ...... ... .. 19 LITERATURE CITED ......................................................................................... 27 v LIST OF TABLES TABLE 1. Stingray disc width and observed electric field intensities that resulted in initiation of a feeding response by treatment.. ....... ... .... ...... ............ .. .. .. ... ..... 15 Vl LIST OF FIGURES FIGURE 1. Map of the two sample areas: Lake Harney in the St. Johns River system and the southern half of the Indian River Lagoon system .................... .. .... 10 FIGURE 2. The experimental apparatus used to measure the electrosensitivity of the stingrays .. .... ...... .. .. .. ....... .. ...... ... ... ....... ... ..... ... ... ... .. .......... ..... .. .. ............... 12 FIGURE 3. Electric field intensities for each stingray's best response to the prey simulating dipole ..... ....... ................... ........... .. ... ..... ....... .... ................. ..... .. 16 FIGURE 4. Empirical orientation distances and derived detection ranges for brackish- saltwater and freshwater groups ... ..... ...... ... ...... .... .. .. .. .. ... ... .... .... ... ... ..... ... 17 FIGURE 5. The distribution of voltage equipotentials produced by a prey-simulating electric dipole in an electrically conductive marine environment and a resistive freshwater environment.. ..... ... ........ .. ..... ... .. .. .. .... ................. ........ 25 Vll ELECTRORECEPTION IN THE EURYHALINE STINGRAY, DASYATIS SABINA INTRODUCTION All elasmobranchs (sharks, skates, and rays) possess an extremely sensitive electrosensory system that enables them to detect weak extrinsic electric fields in their environment. This sensory capability has been demonstrated to function in the detection and localization of weak bio-electric fields of less than 0.5 nV generated by prey (Kalmijn, 1971; Tricas, 1982; Haine et al., 2001; Kajiura and Holland, 2002) and con specifics (Tricas et al., 1995). It has also been shown to detect the relatively low frequency electric fields produced by predators, triggering a defensive response (Sisneros et al., 1998), and theorized to aid in geomagnetic orientation and navigation (Kalmijn, 1974; Paulin, 1995). The elasmobranch electrosensory system consists of hundreds to thousands of bulb-like electroreceptive organs known as the ampullae of Lorenzini. These ampullae are grouped into 3 to 5 subdermal clusters that are distributed over the head of galeoids and also the body of batoids (Chu and Wen, 1979; Zakon, 1988). A single ampulla consists of multiple alveolar sacs continuous with a narrow canal that terminates in a pore on the skin surface (Waltman, 1966). The canal is filled with a low-impedance glycoprotein gel and the cells comprising the canal wall are bound by tight junctions that form a high impedance electrical barrier (Murray and Potts, 1961; Waltman, 1966). The lumen of the ampulla is lined by a single-layer epithelium that is comprised of sensory and support cells (Waltman, 1966; Zakon, 1988; New and Tricas, 2001 ). The elasmobranch electrosensory system evolved in a highly conductive seawater environment. However, there are several elasmobranch species that have subsequently transitioned to a freshwater environment. The high impedance freshwater environment presents a challenge to their electrosensory system. The ampullary 1 electroreceptors of obligate freshwater elasmobranchs, such as the South American freshwater stingrays (Potamotrygonidae), have undergone substantial morphological adaptations to compensate for their high impedance environment. The ampullae are significantly smaller "microampullae", individually distributed in the dermis rather than in subdermal clusters, and the canals are much shorter (Raschi and Mackanos, 1989; New and Tricas, 2001 ). To aid in osmoregulation, the skin is thicker, enabling the animal to maintain an internal ionic concentration that is greater than that of the surrounding freshwater (New and Tricas, 2001 ). The thicker skin increases transcutaneous electrical resistance, forming a high impedance barrier that results in the greatest voltage change occurring across the skin (Kalmijn, 1974; Raschi and Mackanos, 1989; New and Tricas, 2001 ). Thus, the microampullae are ideally located in the dermis to detect these voltage changes (Kalmijn, 197 4; Zakon, 1988; New and Tricas, 2001 ). Whereas the electrosensory systems of freshwater elasmobranchs have evolved to function in a high impedance environment, the electroreceptors of euryhaline elasmobranchs remain morphologically similar to those of marine species {Whitehead, 2002). Nonetheless, euryhaline species retain electroreceptive capabilities in freshwater, as demonstrated in the bull shark (Carcharhinus leucas) {Whitehead, 2002). How the function of the elasmobranch electric sense is affected when euryhaline species
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