MIGRATION AND HABITAT UTILIZATION IN LAMNID SHARKS A DISSERTATION SUBMITTED TO THE DEPARTMENT OF BIOLOGICAL SCIENCES AND THE COMMITTEE ON GRADUATE STUDIES OF STANFORD UNIVERSITY IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Kevin Chi-Ming Weng May 2007 © Copyright by Kevin Chi-Ming Weng 2007 All Rights Reserved ii Abstract Understanding the movements, habitat utilization, and life history of high trophic level animals is essential to understanding how ecosystems function. Furthermore, large pelagic vertebrates, including sharks, are declining globally, yet the movements and habitats of most species are unknown. A variety of satellite telemetry techniques are used to elucidate the movements and habitat utilization of two species of lamnid shark. Salmon sharks used a subarctic to subtropical niche, and undertook long distance seasonal migrations between subarctic and subtropical regions of the eastern North Pacific, exhibiting the greatest focal area behavior in the rich neritic waters off Alaska and California, and showing more transitory behaviors in pelagic waters where productivity is lower. The timing of salmon shark aggregations in both Alaska and California waters appears to correspond with life history events of an important group of prey species, Pacific salmon. The enhanced expression of excitation-contraction coupling proteins in salmon shark hearts likely underlies its ability to maintain heart function at cold temperatures and their niche expansion into subarctic seas. Adult white sharks undertake long distance seasonal migrations from the coast of California to an offshore focal area 2500 km west of the Baja Peninsula, as well as Hawaii. A full migration cycle from the coast to the offshore focal area and back was documented. During the offshore migration, white sharks frequently swam at the surface. Sharks remained in the offshore focal area for up to 167 d, where they exhibited a broad depth distribution with intensive oscillatory behavior, possibly associated with feeding or mating. Young-of-the-year sharks remained south of Point Conception whereas one three-year-old shark moved north to Point Reyes, California. All juvenile white sharks displayed a diel change in behavior, with deeper mean positions during dawn, day and dusk than during night. Juvenile white sharks are captured as bycatch in both US and Mexican waters, suggesting that management of fishing mortality should be of increased concern. The ability of lamnid sharks to undertake rapid long distance migrations is essential in enabling them to integrate the productivity of distant regions. iv Acknowledgements I would like to thank my advisor, Barbara Block, for making all of this work possible and for keeping me motivated through the varied terrain of a PhD. I would like to thank George Somero for his advice, support and moral compass; as well as my other committee members Fiorenza Micheli, Mark Denny, Peter Vitousek, Stuart Thompson and Alexandria Boehm. The wonderful community of Hopkins Marine Station made my time here very rewarding and enjoyable, and I am very grateful to the students, postdocs, faculty and staff who make it a great place to work. I would also like to thank present and past members of the Block Lab, Jason Blank, Andre Boustany, Steve Teo, Andreas Walli, George Shillinger, Chris Perle, Heidi Dewar, Andy Seitz, Dan Dau, Jeff Morissette, Shana Beemer, Carol Reeb, Tim Sippel, Jean de Marignac, Robbie Schallert, Mathew Price, Alex Norton, James Ganong, Alan Swithenbank, Pedro Castilho, Ana Landeira- Fernandez, Don Kohrs, Glenn Strout, Robyn Matteson, Mike Castleton, Sal Jorgensen, Gareth Lawson, Mike Stokesbury and Jake Noguiera. During my graduate work I had the pleasure of collaborating with the Monterey Bay Aquarium, and I would like to thank Chuck Farwell, John O’Sullivan, Tom Williams, Randy Hamilton, Jim Hekkers, Julie Packard, Chris Harold, Randy Kochevar, Manny Ezcurra, Joe Welsh, Scott Reid, Mike Murray, Gil Falcone, George Peterson, Tiffany Davies, Scott Greenwald, Jon Hoech, Kevin Lewand, Jeannette Post, Freya Singer, Jonelle Verdugo, Chad Widmer, Alan Young, Randy Wilder, Paul Sund, Diane Richards and Eric Nardone. I also had the great pleasure of working with Peter Pyle, Scot Anderson, Adam Brown, Ken Goldman, Chris Lowe and his group, Chuck Winkler, Ken Bates, Carolina Espinoza, Oscar Sosa-Nishizaki, Dave Holts, Dave Foley, Daniel Palacios, Steve Bograd and Lynn DeWitt. My work would not have been possible without the captains and crews of research vessels at Alaska Fish and Game, and the Southern California nearshore gillnet fleet, to whom I am extremely grateful. v I thank my friends for their support and companionship, particularly Carl Palmer, Carrie Kappel, Charlie Palmer, Cheryl Logan, Will Ludington, Patrick Martone, Rebecca Martone, Caroline Clabaugh, Jeannie Stamberger, Stephen Porder and Ernest Daghir. Finally, I would like to thank my family, Carolyn, Byron, Keith and Philein Weng for their love and support throughout my life. vi Contents 1 INTRODUCTION ............................................................................................................. 1 1.1 Endothermic fishes.................................................................................1 1.2 The phylogeny of the order Lamniformes..............................................2 1.3 The biology of lamnid sharks.................................................................3 1.3.1 Lamna .................................................................................................4 1.3.2 Carcharodon .......................................................................................5 1.3.3 Isurus ..................................................................................................6 1.4 Endothermy ............................................................................................7 1.4.1 Endothermy in distant lineages ..........................................................7 1.4.2 Endothermy in fishes..........................................................................9 1.4.3 Cardiac function...............................................................................11 1.4.4 The evolution of endothermy ...........................................................12 1.5 Electronic tagging technologies...........................................................14 2 SATELLITE TAGGING AND CARDIAC PHYSIOLOGY REVEAL NICHE EXPANSION IN SALMON SHARKS................................................................................. 19 2.1 Introduction ..........................................................................................19 2.2 Materials and methods..........................................................................19 2.3 Results and conclusions........................................................................24 3 MOVEMENTS OF A HIGH TROPHIC LEVEL PREDATOR BETWEEN DISTANT ECOREGIONS .................................................................................................... 41 3.1 Introduction ..........................................................................................41 3.1.1 Migration in pelagic marine vertebrates...........................................41 3.1.2 Studying animal movement in the marine environment...................42 3.1.3 The Lamnidae – endothermic sharks................................................46 3.1.4 Ecoregions of the eastern North Pacific ...........................................48 3.1.5 Habitat use in a highly migratory marine vertebrate ........................49 3.2 Methods ................................................................................................50 3.2.1 Satellite telemetry.............................................................................50 vii 3.2.2 Environmental data...........................................................................51 3.2.3 Analysis ............................................................................................51 3.3 Results ..................................................................................................53 3.3.1 Salmon shark movements.................................................................53 3.3.2 Habitation utilization of major ecoregions within the eastern North Pacific 60 3.3.3 Weaknesses and biases in the data ...................................................62 3.4 Discussion.............................................................................................63 3.4.1 Sources of bias..................................................................................63 3.4.2 Nature and repeatability of seasonal migrations ..............................64 3.4.3 Utilization of ecoregions vs. productivity ........................................66 3.4.4 Life history functions of migration...................................................73 4 MIGRATION AND HABITAT OF WHITE SHARKS (CARCHARODON CARCHARIAS) IN THE EASTERN NORTH PACIFIC OCEAN.................................. 118 4.1 Introduction ........................................................................................118 4.2 Materials and methods........................................................................120 4.2.1 Satellite telemetry of sharks ...........................................................120 4.2.2 Data recovery..................................................................................121 4.2.3 Analysis ..........................................................................................122