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Thermoregulation in the leatherback sea turtle (Dermochelys coriacea) Bostrom, Brian Lee 2009

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Thermoregulation in the leatherback sea turtle (Dermochelys coriacea) by  Brian Lee Bostrom  B.Sc., The University of British Columbia, 2005  A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF  MASTER OF SCIENCE  in  THE FACULTY OF GRADUATE STUDIES  (Zoology)  THE UNIVERSITY OF BRITISH COLUMBIA  (Vancouver)  August 2009 © Brian Lee Bostrom, 2009  ABSTRACT Adult leatherback turtles (Dermochelys coriacea) exhibit thermal gradients between their bodies and the environment of ≥ 8 °C in sub-polar waters and ≤ 4 °C in the tropics. There has been no direct evidence for thermoregulation in leatherbacks although modelling and morphological studies have given an indication of how thermoregulation may be achieved. Using a cylindrical model of a leatherback I investigated the extent to which heat production by muscle activity during variation of swim speed could be used in a leatherback’s thermal strategy. Drag force of a full scale cast of a leatherback was measured in a low velocity wind tunnel to obtain an estimate of the metabolic cost needed to offset drag. It is apparent, from this modelling, that heat flux from the body and flippers, activity and body and water temperatures are important variables to measure in order to fully classify the thermoregulatory response of live leatherbacks. Using captive juvenile leatherbacks of 16 and 37 kg I show for the first time that leatherbacks are indeed capable of thermoregulation. In cold water (< 25 °C), flipper stroke frequency increased, heat loss through the plastron, carapace and flippers was minimized, and a positive thermal gradient of up to 2.3 °C was maintained between body and environment. In warm water (25 – 31 °C), turtles were inactive and heat loss through their plastron, carapace and flippers increased, minimizing the thermal gradient (0.5 °C). In juvenile leatherbacks, heat gain is controlled behaviourally through activity while heat flux is regulated physiologically, presumably by regulation of blood flow distribution. Using a scaling model, I show that a 300 kg adult leatherback is able to maintain a maximum thermal gradient of 18.2 °C in cold sub-polar waters. Thus, by employing both physiological and behavioural mechanisms, adult leatherbacks are able to  ii  keep warm while foraging in cold sub-polar waters and to prevent overheating in a tropical environment, greatly expanding their range relative to other marine turtles.  iii  TABLE OF CONTENTS Abstract ................................................................................................................................... ii Table of Contents .................................................................................................................. iv List of Tables ......................................................................................................................... vi List of Figures ....................................................................................................................... vii List of Abbreviations ............................................................................................................ ix Acknowledgements ............................................................................................................... xi Co-authorship Statement ................................................................................................... xiii  1  General Introduction ............................................................................... 1 1.1  2  References ....................................................................................................... 7  Exercise Warms Adult Leatherback Turtles ......................................10 2.1 2.2  2.3 2.4 2.5  Introduction .................................................................................................. 10 Materials and Methods ................................................................................ 14 2.2.1 Heat production .................................................................................. 14 2.2.1.1 Parameters and variables of the heat gain equation ............. 15 2.2.1.1.1 Resting metabolic rate .............................................. 15 2.2.1.1.2 Aerobic efficiency .................................................... 16 2.2.1.1.3 Drag force ................................................................. 16 2.2.1.1.4 Propeller efficiency .................................................. 17 2.2.2 Heat loss ............................................................................................. 18 2.2.2.1 Parameters and variables of the heat loss equation .............. 18 2.2.2.1.1 Surface area .............................................................. 18 2.2.2.1.2 Insulation .................................................................. 19 2.2.2.1.3 Cost of ingesting gelatinous prey ............................. 19 2.2.3 Results ................................................................................................ 20 2.2.3.1 Turtle drag ............................................................................ 20 2.2.3.2 Surface area .......................................................................... 21 2.2.4 Predictions from the model ................................................................ 21 2.2.4.1 Metabolic rate ....................................................................... 21 2.2.4.2 Temperature gradient ........................................................... 22 Discussion ...................................................................................................... 23 2.3.1 Test of the model ................................................................................ 27 Figures ........................................................................................................... 31 References ..................................................................................................... 36 iv  3  Behaviour & Physiology: The Thermal Strategy of Leatherback Turtles .........................................................................41 3.1 3.2  3.3  3.4  3.5 3.6 3.7  4  Introduction .................................................................................................. 41 Materials and Methods ................................................................................ 43 3.2.1 Materials ............................................................................................. 43 3.2.1.1 Animals and husbandry ........................................................ 43 3.2.2 Methods .............................................................................................. 44 3.2.2.1 Temperature regime ............................................................. 44 3.2.2.2 Instrumentation ..................................................................... 45 3.2.2.2.1 TB and TW recording ................................................. 45 3.2.2.2.2 Heat flux recording ................................................... 45 3.2.2.2.3 Activity recording ..................................................... 46 3.2.3 Data recording and analysis................................................................ 46 3.2.3 Calculations ........................................................................................ 47 3.2.4.1 Surface area .......................................................................... 47 3.2.4.2 Total heat transfer rate .......................................................... 48 3.2.4.3 Thermal admittance of the plastron ...................................... 48 Results ........................................................................................................... 49 3.3.1 Thermal gradient ................................................................................ 49 3.3.2 Swimming activity.............................................................................. 49 3.3.3 Heat loss ............................................................................................. 50 3.3.4 Surface area ........................................................................................ 51 3.3.5 Total heat loss ..................................................................................... 51 3.3.6 Fraction of heat loss through the body and carapace ......................... 52 Discussion ...................................................................................................... 52 3.4.1 Physiological and behavioural responses to warm and cold water .... 53 3.4.2 Effect of body mass on thermal gradients .......................................... 57 Tables............................................................................................................. 60 Figures ........................................................................................................... 61 References ..................................................................................................... 66  General Discussion.................................................................................68 4.1 4.2 4.3  Other Sea Turtles ......................................................................................... 73 Final Conclusions ......................................................................................... 75 References ..................................................................................................... 77  Appendix A ........................................................................................................................... 80  v  LIST OF TABLES Table 3.1  Recorded values and calculated values of heat loss and production at each water temperature for two leatherback turtles weighing: (A) 37 kg (B) 16 kg........................................................................................................ 60  vi  LIST OF FIGURES  Figure 2.1  Drag of a full scale cast of a 340 kg leatherback. (a) The measured drag force and the line derived from CDA and Eq. 2.1 vs wind speed. (b) CDA calculated from drag vs Reynolds number. ...................................... 31  Figure 2.2  Metabolic rate predictions from the model. (a) Metabolic rate for a fasting leatherback at different swimming speeds. (b) The cost of transport at different swimming speeds. ................................ 32  Figure 2.3  The predicted achievable temperature gradient (TB – TW) that a leatherback can maintain above ambient is plotted against swim speed for turtles varying in size from 100 to 500 kg. ............................................................. 33  Figure 2.4  Metabolic rates (both fasting and feeding) are plotted against TB – TW for 100, 300 and 500 kg leatherbacks. ................................................................. 34  Figure 2.5  Water temperature (TW), sub-carapace temperature (TSC) and depth experienced by a leatherback in the tropics during a long dive. ................... 35  Figure 3.1  (A) An illustration of the turtles harnessed in their tanks. (B) The placement of the HFT’s on the animals. ........................................... 61  Figure 3.2  The complete water temperature profile for the experiment performed on the 37 kg leatherback. .......................................................................................... 62  Figure 3.3  Activity, water and body temperature and heat fluxes recorded simultaneously from the 37 kg leatherback during stepwise increases in water temperature. .......................................................................................... 63 vii  Figure 3.4  A 3D image showing how activity and thermal admittance affect the thermal gradient held by juvenile leatherbacks. .......................................................... 64  Figure 3.5  The affect of mass and heat production on the thermal gradient held by leatherbacks. ................................................................................................. 65  viii  LIST OF ABBREVIATIONS A  frontal area  AB  body surface area (plastron and carapace)  ADL  aerobic dive limit  AF  flipper surface area  CD  drag coefficient  CG  specific heat capacity of prey  COT  cost of transport  EG  energy gained per mass of prey  ηa  aerobic efficiency  ηp  propeller efficiency  Fdrag  drag force  FMR  field metabolic rate  ГTot  total metabolic rate (fasting)  Γo  resting metabolic rate  ГLoco  metabolic cost of locomotion  ΓTot,G  total metabolic rate (feeding)  HFT  heat flux transducer  k  thermal conductivity  L  insulation thickness  LB  body length  MB  body mass  MG  mass of prey ix  v  kinematic viscosity  qT  total rate of heat transfer  QP  plastron heat flux  QF  flipper heat flux  rC  radius of core  rT  total radius  Re  Reynolds number  ρ  density  SPM  flipper strokes per minute  Tamb  ambient temperature  TB  body temperature  TB – TW  thermal gradient  TS  skin temperature  TSC  sub-carapace temperature  TW  water temperature  U  swimming speed  Uair  air speed  x  ACKNOWLEDGEMENTS First, I would like to thank my supervisor Dr. David R. Jones CM for guidance both in and out of the lab. In the lab, Dave’s confidence in me and my ideas allowed me to push myself and to accomplish more than I thought possible. It was actually Dave’s enthusiasm that made me finally enjoy Biology! Before I joined the Jones lab I drank Budweiser, had never been to an opera, an art museum, a professional sporting event, or met someone who could not safely blow out a candle. Thanks Dave I couldn’t imagine a better, more interesting supervisor and mentor.  I thank my initial lab mates Todd Jones, Andreas Fahlman, Mervin Hastings and Manuela Gardner. Merv is the only person I know who could win a rib eating contest with the smallest pile of bones on his plate. I thank Andreas for teaching me that there is more to zoology than leatherback turtles. Todd, I can’t say enough about someone who was willing to throw away half their chimichunga, just because you wanted to make me feel better about dropping mine. Our adventures led to many memories such as “shark attack”, “the trapeze” and most recently to “why thank you, that’s all I wanted anyway”. Thanks Todd, I couldn’t have got through it without your help, encouragement and advice.  I would like to thank Dr. Chris Harvey Clark for the support with the turtles as well as all the good times out of the lab and for getting me interested in diving again. I thank Dr. Colin Brauner for keeping me on track and acting as close to a committee as I had. Dr. Bob Shadwick we held those South campus BBQ’s for you! Art Vanderhorst made South  xi  campus interesting and had a seemingly endless supply of different “anti-dentite” jokes. I thank old friends Damian, Josh and Daniel for allowing me to escape from university and Vancouver for a few days at a time to keep up with old hobbies. I thank my parents Mike and Sue for the advice, keeping me up on the latest fishing news and for the constant reminders that university isn’t so bad. Jaclyn Bowers - thank you for the love and support. You gave me something to look forward to everyday for the past few years.  xii  CO-AUTHORSHIP STATEMENT  Chapter two:  Exercise warms adult leatherback turtles.  Authors:  Bostrom BL and Jones DR  Date Accepted: October 20, 2006 Journal:  Comparative Physiology and Biochemistry A147: 323-331  Comments:  The research was designed and performed by BLB. The mathematical modelling, data analysis and preparation of the manuscript was conducted by BLB. DRJ provided supervision.  Chapter three:  Behaviour & Physiology: The thermal strategy of leatherback turtles.  Authors:  Bostrom BL, Jones TT and Jones DR  Date Accepted: A version of this chapter will be submitted for publication. Journal: Comments:  This research was designed and performed by BLB. The data analysis and preparation of the manuscript was conducted by BLB. TTJ provided technical assistance. DRJ provided supervision.  xiii  1  GENERAL INTRODUCTION  The leatherback (Dermochelys coriacea) is unique among sea turtles and is the sole member of the family, Dermochelyidae. Leatherbacks have a soft carapace that is covered in a layer of “leathery” skin as opposed to all other sea turtles which have a keratinized / bony carapace and plastron, i.e. a “hard shell”. Leatherbacks are the largest (up to 917 kg, Eckert and Luginbuhl 1988), deepest diving (recorded to 1280 m depth, Doyle et al. 2008) and the only sea turtle to sustain itself completely on calorie poor gelatinous zooplankton. Despite these differences, the leatherback sea turtle has a life history strategy that shares similarities with the six other species of sea turtle. Both males and females of all species spend the breeding season near-shore at tropical and sub-tropical beaches and females venture on land to nest several times during the 2 to 5 month breeding season (Miller 1997). The adult turtles then migrate to foraging grounds and will return to nest 2 to 8 years later (Miller 1997). When foraging, hard shelled sea turtles are mainly confined to tropical and subtropical waters, approximately the 20 °C isotherm, and remain on the continental shelf (Davenport 1997). If exposed to water 10 °C or lower hard shelled turtles enter a coma like state known as “cold shock” and frequently die (Davenport 1997). In sharp contrast, leatherbacks have an oceanic-pelagic lifestyle and habitat that extends over a much larger range of latitudes. As a result leatherbacks experience waters temperatures (TW) ranging from 30 °C in the tropics (Southwood et al. 2005) to 0 °C in cold northern waters (James et al. 2006). Leatherbacks must have a unique thermal strategy that allows them to spend long periods of time in waters that would surely kill all other sea turtles and yet still allows them to enter much warmer tropical seas.  1  Various physiological mechanisms have been suggested that set leatherbacks apart from other turtles and allow them to spend long periods of time in near freezing waters. A unique suggestion is that leatherback metabolic rates and thus physiological processes are unaffected by changes in temperature (Penick et al. 1998). Penick et al. (1998) showed that the metabolism of isolated leatherback muscle is thermally independent from 5 to 38 °C (Q10 = 1). As well, in unpublished preliminary data, Penick et al. (1998) claimed that when a live adult leatherback was cooled by 5 °C no change in metabolic rate occurred. This was taken as evidence of whole body thermal independence in leatherbacks. However, body temperature (TB) has a pronounced affect on many metabolic processes of all other animals and consequently animals have evolved means to maintain their TB within a certain range (Avery 1982). As well, leatherbacks of 10 kg had a Q10 of 1.4 between 14 and 39 °C (Hastings 2008). Thermal independence has never been confirmed in the leatherback or even given much thought since Penick et al. (1998).  A more plausible explanation for the ability of leatherbacks to venture into cold water is that they maintain their body temperature (TB) within a tolerable range. As the body temperature of reptiles decreases the metabolic rate follows (Avery 1982). The argument is easily made that a minimum preferred TB must exist if only to maintain a metabolic rate high enough to support maintenance processes and growth. For example, hard shelled sea turtle physiology is highly temperature linked and these species will generally stop feeding in water less than 20 °C (Birse and Davenport 1987) and show severe locomotor deficiencies in water less than 15 °C (Davenport et al. 1997) becoming comatose when water temperature falls below 10 °C.  2  Considerable evidence suggests that leatherbacks maintain body temperatures above ambient in cold water. Adult leatherbacks captured off Nova Scotia, Canada had an average TB of 24 °C in water that was 16 °C at the surface and likely much colder at depth (James and Mrosovsky 2004). As well, an injured adult leatherback vigorously swimming in a tank had a difference between body and water of 18 °C (Frair et al. 1972). The next question is how are leatherbacks able to hold such magnificent temperature gradients, TB – TW, despite being submerged in water and being a reptile which, as a group, are normally considered “cold blooded”.  To maintain a constant TB-TW the rate heat is lost to the environment must balance the rate heat is gained or produced. Most mammalian and avian species have high metabolic rates that are precisely regulated and they hold elevated thermal gradients despite losing considerable amounts of heat (McNab 1978). Reptiles, on the other hand, have metabolic rates an order of magnitude lower (Kleiber 1961) and this heat is usually not sufficient to play an important role in their thermal biology. Instead, most reptiles rely on external sources of heat energy and use behavioural means such as shuttling between microclimates to regulate TB (Avery 1982). Leatherbacks have been considered endothermic, since they do hold large thermal gradients and this energy must have come from metabolism. From a limited number of studies leatherbacks appear to have metabolic rates comparable to other hard shelled turtles (Wallace and Jones 2008) and therefore heat production has not focused on the mechanism by which leatherbacks thermoregulate. The understanding of heat loss, rather, has received more scrutiny.  Most completely aquatic species cannot maintain TB above the temperature of the surrounding water (TW) due to high convective heat loss. A high rate of heat transfer can work to the  3  advantage of many animals, however. Hard shelled sea turtles only hold thermal gradients between body and water (TB-TW) of 1 – 2 °C (Sato et al. 1994) and therefore simply stay in tropical and subtropical waters. Arctic and tropical fish are homeotherms because their TB is effectively coupled to water which is at a constant temperature. In fact, leatherbacks only hold TB-TW of 1-4 °C in the tropics (Southwood et al. 2005) and do not overheat, likely due to the high capacity for water to pull heat away from a body. Maintaining elevated thermal gradients in water is a significant challenge which is beyond the capabilities of most non-mammalian, nonavian species. As well, an oceanic-pelagic lifestyle means a leatherback cannot rely on an external source of heat since the ocean is relatively homogenous in temperature and is not conducive to rapidly shuttling to a new microclimate. Furthermore, notwithstanding possible cloudy conditions, solar radiation is not a reliable heat source for about half of every day in the tropics.  A physical property that would appear to help leatherbacks maintain their thermal gradient is their large body mass and cylindrical shape. The majority of heat lost to the environment occurs over the body surface. A cylindrical shape endows leatherbacks with one of the geometric shapes with the lowest possible surface area for a given mass. As well, most animals retain proportionate relationships as they grow in length, LB, body mass, MB, increases proportionally to LB3. Surface area scales to LB2 and therefore surface area scales with mass as MB2/3. Hence, mass increases at a greater rate than surface area and since each unit of mass has less surface area exposed to the environment, larger animals lose less heat proportionally and naturally will hold larger thermal gradients. This idea is supported by the fact that leatherbacks do not show up in waters colder than 26 °C until they are >100 cm in carapace length (Eckert 2002). In fact a  4  proposed thermal strategy named “gigantothermy” suggested adult leatherbacks were large enough to easily hold the thermal gradients needed to venture to northern foraging grounds, even at low metabolic rates (Paladino et al. 1990).  The layer of insulation surrounding a leatherback may also be a crucial aspect of its ability to venture into cold northern waters. A green turtles carapace is a poor insulator (Heath and McGinnis 1980). Could this be the difference between hard shelled turtles and leatherbacks? An in depth study into leatherback insulation has never been carried out but it has been suggested that the outer layers of tissues surrounding the body core of the leatherback such as fat and the carapace and plastron may act as sufficient insulation to hold measured TB-TWs (Paladino et al. 1990). This would especially be true if the tissues were not perfused and heat was transferred solely by conduction. By perfusing these layers a leatherback could increase heat loss in warm waters.  Leatherbacks have anterior flippers with a large surface area and very little insulation that could act as a major source of heat loss. There is anatomical evidence that heat exchangers exist in the very large front flippers of leatherbacks (Greer et al. 1973). These heat exchangers could further aid in controlling heat exchange. Green turtles have never been shown to possess heat exchangers but they do decrease blood flow to their flippers in cold water (Hochscheid et al. 2002) Although it seems likely that leatherbacks limit heat loss from their flippers in cold waters it has never been shown either in the laboratory or field.  5  This thesis attempts to further the understanding of leatherback thermal biology. In particular I want to ascertain if leatherbacks thermoregulate and if so, how. To accomplish this I have two main objectives that comprise the research of my thesis. The first objective is to create a mathematical model that predicts the rate heat energy is gained and lost by a leatherback (Chapter 2). This model will be used as a tool to isolate the variables that influence TB in leatherbacks. Specifically, I will explore if heat production per se, an overlooked variable, could be important in a leatherback thermal strategy. The second objective is to expose captive juveniles to different TW‘s and measure the variables isolated from the model (Chapter 3). Captive animals should provide a means to quantify the thermoregulatory response that allows leatherbacks to cope with changing thermal environments.  6  1.1 References  Avery RA (1982) Field studies of body temperatures and thermoregulation. In (Gans C, Pough FH eds.), Biology of the Reptilia. volume 12. Academic Press, New York, 93-166 Birse R, Davenport J (1987) Gut action in young loggerhead turtles Caretta caretta L. Herpetological Journal 1: 170-175 Davenport J (1997) Temperature and the life-history strategies of sea turtles. Thermal Biology 22: 479-488 Doyle TK, Houghton JD, Suilleabhain PF, Hobson VJ, Marnell F (2008) Leatherback turtles satellite-tagged in European waters. Endangered Species Research 4: 23-31 Eckert KL, Luginbuhl C (1988) The death of a giant. Marine Turtle Newsletter 43: 2-3 Eckert SA (2002) Distribution of juvenile leatherback sea turtle Dermochelys coriacea sightings. Marine Ecology Progress series 230: 289-293 Frair W, Ackman RG, Mrosovsky N (1972) Body temperature of Dermochelys coriacea: warm turtle from cold water. Science 177: 791-793 Greer AE, Lazelle JD, Wright RM (1973) Anatomical evidence for a countercurrent heat exchanger in the leatherback turtle (Dermochelys coriacea). Nature 244: 181 Hastings MD (2006) Growth and metabolism of leatherback sea turtles (Dermochelys coriacea) in their first year of life. MSc thesis, University of British Columbia, Vancouver Heath ME, McGinnis SM (1980) Body temperature and heat transfer in the green sea turtle, Chelonia mydas. Copeia 4: 767-773  7  Hochscheid S, Bentivegna F, Speakman JR (2002) Regional blood flow in sea turtles: implications for heat exchange in an aquatic ectotherm. Physiological and Biochemical Zoology 75: 66-76 James MC, Mrosovsky N (2004) Body temperatures of leatherback turtles (Dermochelys coriacea) in temperate waters off Nova Scotia, Canada. Canadian Journal of Zoology 82: 1302-1306 James MC, Davenport J, Hays GC (2006) Expanded thermal niche for a diving vertebrate: a leatherback turtle diving into near-freezing water. Journal of Experimental Marine Biology and Ecology 335: 221–226 Kleiber M (1961) The fire of life: an introduction to animal energetic. John Wiley and Sons, Inc., New York McNab BK (1978) The evolution of endothermy in the phylogeny of mammals. The American Naturalist 112: 1-21 Miller JD (1997) Reproduction in sea turtles. In (Lutz P, Musick J eds.) The biology of sea turtles. CRC Press, Boca Raton, 51-81 Penick DN, Spotila JR, O’Connor MP, Steyermark AC, George RH, Salice CJ, Paladino FV (1998) Thermal independence of muscle tissue metabolism in the leatherback turtle, Dermochelys coriacea. Comparative Biochemistry and Physiology A120: 399-403 Sato K, Sakamoto W, Matsuzawa Y, Tanaka H, Naito Y (1994) Correlation between stomach temperatures and ambient water temperatures in free-ranging loggerhead turtles, Caretta caretta. Marine Biology 118: 343-351  8  Southwood AL, Andrews RD, Paladino FV, Jones DR (2005) Effects of diving and swimming behavior on body temperatures of Pacific leatherback turtles in tropical seas. Physiology and Biochemical Zoology 78: 285-297 Wallace BP, Jones TT (2008) What makes marine turtles go: A review of metabolic rates and their consequences. Journal of Experimental Marine Biology and Ecology 356: 8-24 Paladino FV, O’Connor MP, Spotila JR (1990) Metabolism of leatherback turtles, gigantothermy, and thermoregulation of dinosaurs. Nature 344: 858-860  9  2  EXERCISE WARMS ADULT LEATHERBACK TURTLES1  2.1 Introduction  Leatherback sea turtles (Dermochelys coriacea) have the greatest global distribution of all sea turtles. Not only are they the deepest diving, having been recorded diving to depths over 1200 m (Hays et al. 2004), but they also have the largest global range. Leatherbacks migrate thousands of kilometers from tropical nesting beaches to distant foraging grounds (Morreale et al. 1996; Hughes et al. 1998). As a result, leatherbacks experience ambient water temperatures (TW) ranging from 0 °C in the high latitudes to 30 °C in the tropics (Goff and Lien 1988). Impressively, they do not cool down to the point of becoming lethargic when foraging on gelatinous zooplankton in temperate waters, or overheat when venturing into warm tropical waters. Obviously, leatherbacks’ thermal biology is an integral part of their ability to venture into regions that are out of reach of other marine turtles.  In the tropics, female leatherbacks maintain body temperatures (TB) 1.2 to 4.3 °C higher than TW (Southwood et al. 2005). Recently, foraging leatherbacks captured off the coast of Nova Scotia had an average TB 8.2 °C above surface water that was at 15 °C (James and Mrosovsky 2004). This is an amazing feat considering the leatherback may spend up to 40 % of the time foraging at depth in water much colder than at the surface. Ingestion of large volumes of prey offers a substantial thermal challenge due to the high heat capacity and cold temperature of gelatinous zooplankton (Davenport 1998). 1  A version of this chapter is published. Bostrom BL, Jones DR (2007) Exercise warms adult leatherback turtles. Comparative Physiology and Biochemistry A129: 323-331  10  Many reptiles use behavioural means to regulate TB. When faced with changes in ambient temperature they vary body position and/or move between thermal environments to keep TB in an optimum range (Avery 1982). Crocodiles, when faced with seasonal or daily changes in ambient temperature, vary the time spent on land and in water to regulate a high and stable TB (Seebacher et al. 1999). Marine iguanas (Amblyrhynchus cristatus) spend a large percentage of time basking on shore to counteract the heat they lose to the ocean during foraging excursions (Trillmich and Trillmich 1986).  Such behavioral strategies, however, are not feasible for ectotherms continually roaming a marine environment. They are unable to escape the high convective heat loss of water and, in higher latitudes, large thermal gradients. In addition, relying on solar energy for heat is not a viable option due to the rapid absorption of infrared radiation by sea water and possible cloudy conditions. Metabolic heat is thus particularly important in a marine reptile’s thermal biology. Loggerhead turtles maintain TB above TW without staying near the surface and basking (Sato et al. 1995). Sato et al. (1995) found no correlation between TB and light intensity. This suggests the loggerheads’ elevated TB came purely from metabolic processes. A thermal gradient of up to 8 °C has been measured between TW and the pectoral muscles of a vigorously swimming green turtle (Chelonia mydas) compared with only 1 - 2 °C when at rest (Standora et al. 1982). In the tropics, leatherbacks do not spend time near the surface basking, again suggesting that heat production is purely metabolic (Eckert 2002).  11  For marine animals to maintain large temperature gradients, retaining metabolic heat is essential. Some tunas are able to maintain regions in their body 10 °C above TW by using counter-current heat exchangers to control heat loss (Brill et al. 1994).  Another important physical attribute for heat retention is large size. Larger animals have a lower surface area to volume ratio than smaller animals. Since heat energy is lost through an animal’s surface there is an effective dampening effect on changes in TB in large animals. This phenomenon is referred to as thermal inertia. The amplitude of fluctuations in crocodile TB as a result of changing ambient temperatures decreases with an increase in body mass (MB) (Seebacher et al. 1999).  Due to large thermal gradients (TB – TW) in cold water leatherbacks must be particularly efficient at retaining metabolic heat. They are the largest sea turtle (nesting adults typically weigh 300500 kg), which gives them a large thermal inertia. They also have heat exchangers which enable them to maintain their flippers at TW to further aid in heat retention (Greer et al. 1973). Currently a thermal strategy termed “gigantothermy” is thought to be employed whereby large body size, insulating peripheral tissues, and circulatory changes enable leatherbacks to regulate TB in the face of low metabolic rates (Paladino et al. 1990). Paladino et al. (1990) suggested that a leatherbacks large size sets it apart from other marine turtles in the latitude ranges it can explore although effects of MB were not explicitly explored in their model. By varying the rate of heat loss through circulatory changes they suggested a leatherback could theoretically thermoregulate. However, gigantothermy considers physiological mechanisms solely for thermal regulation despite the fact that many other reptiles use behavioural means.  12  Since reptiles commonly use behavioral adjustments to maintain high and stable TB’s, Southwood et al. (2005) hypothesized that behavioral control in leatherbacks may be important in their thermoregulatory technique i.e. depth and TW selection could be a way to control TB. Furthermore, there also appears to be a correlation between swim speed (U) and TB, with low average U’s corresponding to a decrease in TB, and TB increasing as U rises (see Fig. 7B from Southwood et al. 2005). These data suggest that the rate of production of metabolic heat in a leatherback directly affects its achievable TB – TW.  In this paper I attempt to further the understanding of leatherback thermal biology by looking at the rate metabolic heat is produced while overcoming hydrodynamic drag. Moreover, by estimating heat loss I can predict a leatherbacks’ achievable temperature gradient at different metabolic costs, i.e. swim speeds. In a heat flow model it is important to estimate where heat is produced and from where it is lost. I assume that in a leatherback heat production is the byproduct of resting metabolic rate (Γo) and the metabolic cost of locomotion (ГLoco). Heat loss depends on TB – TW, insulation thickness, thermal conductivity of the insulation (k) and the convection coefficient.  For a leatherback to maintain a certain TB – TW the rate at which heat is produced must be equal to the rate at which heat is lost to the surrounding water. With this assumption I can quantitatively predict the extent to which behavioral control of U could be used in a leatherback’s thermoregulatory strategy. I propose that metabolic heat produced as a byproduct of locomotion is crucial in maintaining a high TB. By keeping insulation thickness constant in  13  this model I highlight the effect that the behavioral control of swim speed has on generating a large thermal gradient. Overall, I hypothesize that behaviourally controlling the rate of heat production, through variation of swim speed, could be an equally effective way for a leatherback to thermoregulate as controlling the rate of heat loss, through circulatory adjustments and TW selecting.  2.2 Materials and Methods  2.2.1 Heat production  Any metabolic energy that does not perform a function or perform work external to the body must be released as heat energy. The portion of metabolic energy produced for locomotion that performs external work is the aerobic efficiency of the muscle, the rest is then released as heat. This can be summarized in the following equation, (1 – ηa) ГLoco = heat production rate; where ηa is the aerobic efficiency of muscle and ГLoco is the metabolic cost of locomotion. Resting metabolic rate Γo has been measured in leatherbacks (Lutcavage et al. 1990; Paladino et al. 1990; Lutcavage et al. 1992) and ГLoco can be estimated from the work a turtle expends in overcoming hydrodynamic drag forces (Fdrag).  For a turtle to swim at a constant speed the propulsive force the turtle produces must exactly balance the drag force on its body. The Fdrag (N) on an object with frontal area A (m2) moving through a fluid of density ρ (kg m-3) at a speed U (m s-1) is: ‫ܨ‬ୢ୰ୟ୥ = 1ൗ2 ߩ‫ܥ‬ୈ ‫ ܷܣ‬ଶ  (2.1)  14  where CD is the drag coefficient which accounts for the shape and boundary flow characteristics around the turtle. The work a turtle does while swimming is the product of Fdrag and U. ГLoco is the quotient of work and the efficiency at which the turtle converts biochemical energy into forward thrust. Efficiency includes converting chemical energy into muscular energy (ηa), and the propeller efficiency (ηp) of the flippers. Hence, the heat production rate by a swimming turtle can be written as, ܳ୮୰୭ୢ = Γ୭ +  (ଵିఎ౗ )ఘ஼ీ ஺௎ య ଶఎ౦ ఎ౗  (2.2)  with whole animal metabolic rate (ГTot) estimated as: Γ୘୭୲ = Γ୭ +  ఘ஼ీ ஺௎ య ଶఎ౦ ఎ౗  (2.3)  2.2.2.1 Parameters and variables of the heat gain equation  2.2.2.1.1 Resting metabolic rate  The metabolic rate of three undisturbed nesting female leatherbacks (average mass 305 kg) was 0.083 W kg-1 (Lutcavage et al. 1990). The leatherbacks were quiescent so this value is a good approximation of Γo. Scaling allometrically with body mass (MB) to the 0.83 power (Prange and Jackson 1976) gives Γo for leatherbacks as: Γ୭ = 0.22‫ܯ‬୆ ଴.଼ଷ  (2.4)  15  2.2.1.1.2 Aerobic efficiency  The best estimates of ηa come from the efficiency of excised muscle performing a complete contraction cycle. This is 25% in frogs (Heglund and Cavagna 1987) and 35% in tortoises (Woledge 1968). Leatherback muscle ηa has not been measured so I used 30% for ηa, midway between that of a frog and tortoise.  2.2.1.1.2 Drag force  Drag force was measured on a full scale leatherback turtle model borrowed from the Vancouver Aquarium and Marine Science Centre (Vancouver, B.C., Canada). This model was cast from a 340 kg leatherback that died around 30 years ago (Carla Sbrocchi, personal communication), and is very realistic, having most of the surface elements of the skin such as folds and wrinkles. The leatherback is fixed with its fore-arms pulled back in a gliding position.  The cast was tested in an open circuit, low velocity, wind tunnel in the Mechanical Engineering Department at the University of British Columbia. The working section of the tunnel is 1.6 m X 2.5 m in cross section and 23 m long. The leatherback cast was fixed to a force balance projecting through the floor of the wind tunnel. The leatherback cast was mounted upside down on the force balance by brackets on its dorsal carapace. The cast was positioned 30 cm above the floor to reduce boundary effects, and faced directly into the wind. The force balance measured drag force parallel to the wind direction.  16  A drag test was performed on the mount, before the turtle was attached, to determine its drag. The drag was tested on the mounting bracket at speeds ranging from 5.89 m s-1 to 17.0 m s-1, sampling 24 times in this range. Drag was then tested on the turtle at 24 speeds in a range of 6.63 to 17.1 m s-1 with each test speed close to speeds used for the mount drag test. The mount drag was subtracted from the drag of the mount and turtle together to estimate Fdrag.  Fluids at the same Reynolds number (Re) have similar flow patterns so wind speed was converted to water velocity by equating Re for each fluid. Re is expressed as LBU/v where v is the kinematic viscosity of the fluid and LB is the length of the object. Equating Re at v for air and water at 25 °C (1.56*10-5 m2 s-1 and 1.004*10-6 m2 s-1) showed an air speed of 15.5 m s-1 to be equal to water flowing at 1m s-1. Consequently, Fdrag was measured over a range of Re that turtles might experience in the ocean by measuring over a wind speed of 6 – 17 m s-1. 24 data points were taken over that range to ensure an accurate representation of the drag trend with each data point consisting of an average of 100 samples at a given wind speed.  2.2.1.1.4 Propeller efficiency  Propeller efficiency accounts for inefficient paddling techniques stemming largely from the added drag of the fins being moved through the water. The flippers were fixed in place on the turtle cast in the wind tunnel so the measured Fdrag was greater than that required for propulsion. I assumed that the extra drag of the flippers accounted for ηp.  17  2.2.2 Heat loss  I model a leatherback turtle as a cylinder, with a constant insulation thickness. I consider a turtle as two concentric cylinders. The inner cylinder represents the core of the turtle, where metabolic heat is produced. The core has radius rC and a constant temperature due to blood flow (Paladino et al. 1990; Hind and Gurney 1997). The outer cylinder has radius rT. The volume of the larger cylinder that lies outside the inner cylinder is the insulation layer of the turtle. No heat is produced in the insulation. Heat will be conducted from the warm core (TB) to the cool surface (TS) across the insulation layer. Heat conduction rate from the core to the surface of a cylinder (Kreith and Black, 1980) is given by:  ܳ௖௢௡ௗ =  ଶగ௞௅ా (்ా ି்౏ ) ୪୬ (௥౐ ⁄௥ి )  (2.5)  where k is thermal conductivity of the insulation (W m-1 °C-1) and LB is the length of the cylinder (m). The heat conducted to the surface of the cylinder will then be carried away by movement of the surrounding fluid with temperature TW, through convection. For simplicity, I assume that the convection coefficient is high enough that skin temperature equals TW.  2.2.2.1 Parameters and variables of the heat loss equation  2.2.2.1.1 Surface area  Surface area, AB, was measured by covering the head, neck, tail, and carapace of the cast with small pieces of paper of known area, and then counting the pieces of paper to give the area. I 18  assumed that heat exchangers kept the flippers at TW (Greer et al. 1973) so they did not contribute to heat loss or the surface area for heat exchange.  2.2.2.1.2 Insulation  The insulative layer is represented in my model as the ratio of the heated core radius (rc) to the whole body radius (rT) and was held constant at rC/rT = 0.85. In the cylinder that I use to describe a 300 kg turtle, this ratio is equivalent to an average thickness of insulation of 3.6 cm which makes up 28% of the volume of the cylinder.  2.2.2.1.3 Cost of ingesting gelatinous prey  As ingested gelatinous zooplankton works its way through a leatherback’s digestive system it will warm from TW to the core temperature of the turtle (TB). In doing so, energy is transferred from the turtle to the ingested prey. The amount of energy required to warm up a mass of zooplankton from TW to TB can be written as, MGCG(TB – TW); where MG is the mass and CG is the specific heat capacity of the prey consumed. Therefore, the turtle gains less energy from a mass of cold than from an equivalent mass of warmer jellyfish. The overall energy gained by a leatherback per mass of jelly eaten can be expressed as, EG = (134 -4.186(TB – TW)); where 134 kJ kg-1 is the total energy derived per mass of ingested jelly (Lutcavage and Lutz 1986) and assuming gelatinous zooplankton has a similar specific heat capacity to that of water (4.186 kJ kg-1 °C -1). Due to the added cost of warming ingested prey, the metabolic rate of an actively foraging leatherback (ΓTot,G) can be expressed as, ΓTot,G = 4.186*( TB – TW)*MG + ΓTot. The mass  19  of jellyfish that is needed to be consumed per second to cover ΓTot can be calculated as, MG = ΓTot / EG.  2.2.3 Results  2.2.3.1 Turtle drag  Drag force (turtle plus mount drag minus mount drag) against wind speed is shown in Fig. 2.1a. Drag force was converted to CDA using Eq. 2.1 (Fig. 2.1b). In laminar flow CD varies significantly with Re. However, when flow becomes turbulent dependence of Re on CD becomes weak (Tritton 1988). At Re greater than 1.85*106 (Uair =13.5 m s-1) CD is constant and flow is turbulent. I assume that flow around a turtle is turbulent and therefore that CD in the turbulent region (Fig. 2.1b) accurately represents turtle Fdrag. Hence CD of a turtle is invariant and is unaffected by the size of the turtle or density of the fluid so that drag force can be scaled from air to water.  I fit Eq. 2.1 to my drag data at wind speeds greater than 13.5 m s-1. This produced an average value of CDA equaling 0.31 m2. Since CD depends on the shape of leatherback and is a constant while drag scales proportionally to A, I can use CDA to scale drag between turtles of different MB. Assuming that A scales to the 2/3 power with MB, ‫ܥ‬ୈ ‫ = ܣ‬6.39 ∙ 10ିଷ ‫ܯ‬୆  ଶൗ ଷ  (2.6)  20  2.2.3.2 Surface area  The 340 kg turtle cast had a body surface area (AB) of 3.2 m2. Aquatic animals follow a certain aspect ratio that minimizes total drag (McMahon and Bonner 1983) which approximates as length / width = 4. Since AB scales to the 2/3 power with MB then a cylinder that matches the surface area of a turtle has dimensions described by 8rT = LB where rT = 0.036MB1/3.  Area across which heat is lost is of primary importance. A cylindrical model of a leatherback with AB = 3.2 m2 and having tissue the density of water, would weigh 390 kg. Therefore, a cylinder matching MB of a turtle actually underestimates AB from which heat is lost. Consequently, I matched the dimensions of the cylinders used in my model to AB and not MB.  2.2.4 Predictions from the model  2.2.4.1 Metabolic rate  The metabolic rate (ΓTot) is plotted against U in Fig. 2.2a for 100, 300, and 500 kg turtles. As U increases, ΓTot increases cubically with it. The metabolic rate of a 300 kg turtle swimming at 0.7 m s-1 is predicted therefore to be 0.65 W kg-1.  The cost of transport (COT) is ΓTot per unit mass divided by the swimming velocity: ‫= ܱܶܥ‬  Γ୘୭୲ ൗܷ‫ܯ‬ ୆  (2.7)  21  COT gives the energy requirements for a leatherback to swim a given distance. Fig. 2.2b is a graph of COT as a function of velocity for 100, 300, 500 kg turtles. At very low swim speeds the COT is high due to the dominance of Γo per meter traveled. As U increases, the influence of Γo falls but Fdrag increases, elevating ΓLoco. These two factors combine to give a minimum COT near 0.3 m s-1 for all sizes of leatherback.  2.2.4.2 Temperature gradient  For a leatherback to maintain a constant temperature gradient the rate at which heat is lost must equal the rate heat is produced. By equating Eq. 2.2 and 2.5, TB – TW can be solved as a function of swim speed. This relationship is graphed in Fig. 2.3. This model predicts that leatherbacks up to 500 kg can maintain a TB – TW gradient of < 2 °C while at rest. At a U of 0.7 m s-1, 100, 300, and 500 kg leatherbacks can maintain a TB – TW of 5.2, 7.7 and 9.3 °C, respectively.  The metabolic rate for fasting (ΓTot) and feeding (ΓTot,G) 100, 300 and 500 kg leatherbacks is plotted in Fig. 2.4 against TB – TW. ΓTot is proportional to heat production and is thus directly related to TB – TW. ΓTot,G is ΓTot with an added cost of warming the ingested mass of prey from TW to TB. Due to this added cost a lower TB – TW is achievable at a given metabolic rate for a feeding turtle than for one which is fasting. At a U of 0.5 m s-1 (ΓTot= 0.29 W kg-1, ΓTot,G= 0.33 W kg-1, TB – TW = 3.7 °C) a 300 kg leatherback would have to eat 63 kg day-1 of gelatinous prey, and at 0.7 m s-1 (ΓTot=0.65 W kg-1, ΓTot,G= 0.85 W kg-1, TB – TW = 7.7 °C) the animal would have to eat 165 kg day-1 to provide for ΓTot,G if it was to remain in neutral energy balance.  22  2.3 Discussion  I suggest that heat produced as a metabolic by-product of overcoming Fdrag while swimming is a crucial aspect of an adult leatherback’s ability to maintain a high and stable TB – TW gradient. Insulation was held constant in my model which provided evidence that large, stable TB – TW’s recorded in leatherbacks may be due to this behavioral temperature control mechanism. In conjunction with the ability of a leatherback to spend time at different TW’s, this could be a very effective way to control TB. I conclude that leatherback thermoregulation does not have to be achieved completely through physiological changes that vary the rate at which the turtle loses heat. In fact, my model provides quantitative evidence that leatherback TB could largely be behaviorally controlled through TW selection and by varying the rate of heat production through swim speed selection.  The achievable TB – TW for a leatherback scales cubically with swim speed (U) and with MB to approximately the 1/3 power. Fig. 2.3 shows that the same thermal gradient in a 500 kg animal swimming at 0.6 m s-1 can be achieved by a 300 kg animal with as little as an 8% increase in U. If a leatherback is behaviorally thermoregulating through variation of U and TW selection, it would be expected that a stronger correlation between U and TW would be seen than between U and MB. In fact, studies by Eckert (2002) and Southwood et al. (2005) found no correlation between curved carapace length (thus MB) and U.  As expected, leatherbacks encountered in northern waters are often larger animals (Eckert 2002). My model predicts that to maintain a TB – TW of 10 °C in northern waters a leatherback must be  23  fasting and at least 130 kg if maximum metabolic rate is 1.5 W kg-1. If a leatherback is constantly feeding my model predicts a minimum size limit of 226 kg. In fact, the smallest of 4 leatherbacks captured in Nova Scotia (TW =15 °C) was 315 kg (Eckert 2002).  Dive depth and duration and surface TW have been monitored for female leatherbacks foraging in northern waters by use of satellite telemetry devices (McMahon and Hays 2006). As surface TW cooled both dive depth and duration decreased. This was suggested to be a result of prey availability. However, since leatherbacks surface to breathe they are limited by their aerobic dive limit (ADL). My model suggests that turtles could be offsetting the high heat loss of the cold waters by increasing activity. Therefore, to maintain a constant TB as TW drops a leatherback must increase its metabolic rate which would shorten its ADL.  Heat loss in marine animals has been investigated on a number of occasions (Yasui and Gaskin 1986; Kshatriya and Blake 1988; Hokkanen 1990; Paladino et al. 1990; Worthy 1991; Watts et al. 1993; Kvadsheim et al. 1996; Hind and Gurney 1997; Ahlborn and Blake 1999) and, unfortunately, many models are flawed because of inaccurate values for insulation thickness and distribution (Kvadsheim et al. 1997). For lack of detailed data on blood flow and insulation thickness I chose an evenly distributed insulation layer in my model which therefore could be flawed. Fortunately, there is unpublished data from Southwood and colleagues which allows us to test my choice of rC/rT at least for tropical waters (Fig. 2.5). TB of a 244 kg turtle, resting on the shallow ocean floor at 22 °C, dropped from 30.2 to 29.1 °C over a period of 67 minutes. This cooling curve can be used to estimate the relative insulation thickness (rC/rT). Owing to blood flow, I assume that the whole core of the turtle (approximately half the turtle’s mass) dropped by  24  1.1 °C. Specific heat capacity of various human tissues varies from 3.6 to 3.9 kJ kg-1 °C -1 (Giering et al. 1995) and assuming that human tissue has a similar heat capacity to that of turtles I use a value that falls in the middle of the range (3.75 kJ kg-1 °C -1). While resting on the bottom the turtle lost 503 kJ of stored heat energy representing an average of 125 W over 67 minutes. Total heat lost to the water is from stores plus heat produced internally and for a resting turtle heat produced comes solely from resting metabolic rate (Γo). Γo for a 244 kg turtle is 21 W from Eq. 2.4, giving a power loss of 146 W. Assuming that k for leatherback insulation is the same as whale blubber (0.25 J s-1 K-1, Kvadsheim et al. 1996) and solving Eq. 2.5 gives rC/rT = 0.86 which is close to the value I used in my model (rC/rT = 0.85).  I assumed insulation thickness was constant in my model to highlight the effect U has on a leatherback’s achievable temperature gradient. It should be noted that insulation thickness will vary from turtle to turtle and even vary in a single turtle over time. Leatherbacks have been found to be fatter in northern foraging grounds than when on nesting beaches (James et al. 2005). If a leatherback’s insulation is thicker than the value used in my model, the rate of heat loss to the surrounding water will be less than predicted. Consequently, less metabolic heat will be needed to achieve a given temperature gradient and leatherbacks could swim at a slower rate.  The wind tunnel experiment gave CDA as 0.31 m2 with A being a constant to account for scaling with MB. Watson and Granger (1998) calculated CD = 0.339 for a green turtle cast using frontal area to scale with MB. The frontal area of the turtle cast, not including flippers (Watson and Granger 1998), was approximately 0.4 m2 giving a CD of 0.78. This is not unreasonable because the cast still had the flippers attached. The increase in Fdrag in the cast was accounted for in my  25  calculations by assuming ηp was 100%. Muscle ηa in the model presented in this paper is 30% which is the average value between ηa of frog and tortoise muscle. If ηp actually accounts for a 50% loss then overall metabolic efficiency is 15% which is slightly higher than the 10% estimated for green turtles (Prange 1976).  Leatherbacks appear to have a large thermal tolerance as they have been found in TW above 30 °  C in the tropics (Southwood et al. 2005) and near 0 °C off of Nova Scotia (Goff and Lien 1988;  James and Mrosovsky 2004). In this study I predict the largest internal heat gain comes from metabolic heat as a result of locomotion. I assume ηa will be unchanged at any given TB because the metabolic rate of leatherback pectoral muscles was found to be thermally independent from 5 - 38 °C (Penick et al. 1998). Therefore my model predicts heat produced at all TB‘s a leatherback experiences in the wild.  Other behavioural modifications may play a part in maintaining thermal balance in cold waters. In waters off Nova Scotia leatherbacks often appear to bring prey from depth to the surface before eating it (James and Mrosovsky 2004). By surfacing with gelatinous prey before ingesting it, the prey can warm to surface TW. A leatherback, maintaining TB 8 °C above surface TW of 15 °C and capturing prey in water at 10 °C by bringing it to the surface would realize a 25% gain in energy per mass of jellyfish consumed.  There is no doubt that physiological and/or behavioural strategies may be required in some situations to prevent overheating. Redistribution of blood flow to the body surface will bypass the insulative layer and greatly enhance heat loss. Also, I assumed that heat exchangers enabled  26  leatherbacks to maintain their flippers at TW (Greer et al. 1973) and thus they did not contribute to heat loss. However, the heat exchangers are likely not 100 % efficient and the possibility exists to greatly increase heat loss by pumping warm blood through the flippers and using them as cooling fins. Green and Loggerhead turtles have been found to vary circulation through their front flippers to control heat exchange (Hochscheid et al. 2002). I did not vary the leatherbacks’ insulation thickness or the efficiency of its heat exchangers in this model since I was interested in how different rates of heat production affect TB.  It has been suggested that leatherbacks dive to cold deep waters during their internesting intervals in order to use the water as a heat sink and cool off (Eckert et al. 1986; Wallace et al. 2005). Wallace et al. (2005) found that high metabolic rates positively correlated with the percentage of time spend in waters colder than 24 °C. They suggested that the leatherbacks were actively diving to deep cold waters in order to use the water as a heat sink and cool off. In contrast, my model predicts that in order to dump heat a leatherback is better off to rest and minimize metabolic heat production.  2.3.1 Test of the model  Southwood et al. (2005) showed temperature data for two turtles of 329 and 251 kg, respectively, in tropical waters. These data sets contain values for gastro-intestinal tract temperature, swim speed, and dive depth. TW and depth were measured on another turtle in the same area at the same time (Fig. 1 of Southwood et al. 2005), and the data were used to estimate water temperature as a function of depth in Southwood et al.’s Fig. 7 A&B.  27  In Fig. 7A, from 0:00 to 6:00 and from 18:00 to 21:00, the 329 kg leatherback was swimming in 26 °C water and maintaining TB of 32.8 °C. To maintain this TB – TW my model predicts that a leatherback must maintain a swim speed of U = 0.66 m s-1. The measured swim speed varies between 0.6 and 0.7 m s-1 during this time which supports results from my model. In Fig. 7B, from 0:00 to 4:00, the 251 kg turtle was swimming to a depth of around 20 meters (TW = 26 °C) and TB is stable at 31 °C. My model indicates an average U of 0.60 m s-1 is necessary to maintain this TB – TW. Actually, the turtle spent the majority of time at swim speeds oscillating between 0.4 and 0.7 m s-1, which would be close to my prediction. After 16:00 there are similar TW and TB and a similar U is predicted to produce this TB – TW, which is again supported by the data. Between 12:30 and 15:30 there is a TB gain of approximately 1 °C over 3 hours corresponding to an internal heat gain of 44 W. During this dive bout the turtle spent the majority of the time at depths of 30 m (TW = 22 °C). From my model, a U of 0.83 m s-1 is needed to achieve a 44 W surplus over heat being lost to the water. The data shows a swim speed between 0.8 and 0.9 m s1  . From 8:00 to 12:00 the leatherback spent the majority of the time not swimming and TB  dropped over this period. These data provide evidence that TB is a direct result of the heat produced as a byproduct of the metabolic cost of swimming.  Fig. 2.5 shows a 244 kg turtle’s TB falling while sitting on bottom (Southwood, personal communication). This is expected since there was a large TB – TW (8 °C). However, when the turtle rose to the surface after the dive, TB continued to fall although TB – TW at the surface was only a couple of degrees. My model predicts a TB – TW of around 1.2 °C at resting metabolic rate so the animal continued to lose heat. After 11:45 the turtle returned to an active dive cycle and  28  TB immediately began rising. This confirms that leatherbacks are not able to maintain more than a small thermal gradient in the absence of activity. A large thermal inertia will be useful in dampening out quick changes in ambient temperature but a continuously low TW will cause TB to fall. This agrees with research that suggests a crocodile needs a mass of 10,000 kg before it becomes thermally isolated from its environment (Seebacher et al. 1999). Furthermore, Eckert (2002) reported that leatherbacks swam constantly, day and night, while migrating. They swam about two meters under the surface suggesting they were selecting depth for drag reduction and were not basking. My model predicts that it is not possible for a leatherback to maintain an elevated TB – TW if it stops and rests while in cold water.  Leatherbacks captured off the coast of Nova Scotia had an average TB of 8 °C above surface TW (James and Mrosovsky 2004). To maintain this TB – TW I predict a 300 kg leatherback would need to maintain a U of 0.71 m s-1 and metabolic rate of 0.90 W kg-1 when ingesting food. This metabolic rate is higher than the maximum field metabolic rate of 0.74 W kg-1 recorded during the internesting interval (Wallace et al. 2005) but is not unexpected due to the added metabolic cost of maintaining a large TB – TW and warming ingested prey in cold water.  Field metabolic rate (FMR) of leatherbacks during the internesting interval in Costa Rica ranged from 0.2 – 0.74 W kg-1 (Wallace et al. 2005). Wallace et al. (2005) suggested that leatherbacks were unlikely to be feeding during this time. For 300 kg leatherbacks, measured FMR represents a range in U of 0.41 – 0.74 m s-1 and achievable fasting TB – TW of 2.7 – 8.7 °C. If they did happen to be feeding the model predicts ranges of 0.40 – 0.67 m s-1 and 2.5- 7.0 °C. These are certainly reasonable ranges for U and TB – TW (Southwood et al. 2005).  29  During the internesting interval, female leatherbacks outfitted with velocity data loggers had an average U of 0.7 m s-1 (Southwood et al. 2005). The turtles averaged 282 kg so this swimming velocity corresponds to a metabolic rate of 0.66 W kg-1 in a non feeding animal and 0.86 W kg-1 in one that is feeding. The FMR predicted here for a non feeding turtle is within the range measured by Wallace et al. (2005). My predicted metabolic rate for a feeding turtle is slightly greater than measured, but as noted by Reina et al. (2005) and suggested by Wallace et al. (2005) these leatherbacks may not be actively foraging during the internesting interval.  In conclusion, I created a quantitative model to predict the thermal gradient that a leatherback can sustain for a given level of activity. Using this model I was able to accurately replicate published TB, swim speed and metabolic rate data. I believe these data show the strong predictive power of the model and support the hypothesis that leatherbacks can behaviourally regulate their body temperature through variation in swim speed.  30  2.4 Figures  a) 60  50  Drag (N)  40  30  20  10  0 0  2  4  6  8  10  12  14  16  1.5e+6  1.8e+6  2.1e+6  -1  Wind Speed (ms )  b) 0.32  CDA (m2)  0.30  0.28  0.26  0.24  0.22 0.0  2.6e+5  5.1e+5  7.7e+5  1.0e+6  1.3e+6  Reynolds number  Figure 2.1 The results of a drag test performed in a wind tunnel on a full scale cast of 340 kg leatherback. (a) The measured drag force and the line derived from CDA and Eq. 2.1 are plotted against wind speed. (b) CDA is calculated from drag and is plotted against Reynolds number (Re). Past a Re of 1.85*106 or a wind speed of 13.5 m s-1 the air flow around the cast is turbulent and drag scales quadratically with wind speed. This turbulent region is represented in (b) by a constant CDA and in (a) by the measured data closely matching my fit.  31  Metabolic Rate (Wkg-1)  a) 1.5 1.4 1.3 1.2 1.1 1.0 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0  100 kg leatherback 300 kg leatherback 500 kg leatherback  0.0  0.1  0.2  0.3  0.4  0.5  0.6  0.7  0.8  0.9  1.0  0.6  0.7  0.8  0.9  1.0  b)  Cost of Transport (Jkg-1m-1)  2.5 100 kg leatherback 300 kg leatherback 500 kg leatherback  2.0  1.5  1.0  0.5  0.0 0.0  0.1  0.2  0.3  0.4  0.5 -1  Swim Speed (ms )  Figure 2.2 Metabolic rate predictions from the model. (a) Metabolic rate for a fasting leatherback is plotted against swim speed. Metabolic rate is initially resting metabolic rate and it then increases cubically with swim speed mirroring the work a turtle expends to overcome drag while swimming. (b) The cost of transport (COT) is plotted for leatherbacks against swim speed. The minimum COT occurs at 0.3 m s-1.  32  25.0 22.5 20.0 o T B-T W ( C)  17.5 15.0 12.5 10.0 7.5 5.0 2.5 0.0  B 400 od y 300 M as s 200 (k g) 100  0.0  0.1  0.2  0.3  Swim  0.4  0.5  e Spe  0.6  0.7  0.8  0.9  1.0  -1 )  s d (m  Figure 2.3 The predicted achievable temperature gradient (TB – TW) that a leatherback can maintain above ambient is plotted against swim speed for turtles varying in size from 100 to 500 kg. At a swim speed of 0 m s-1 all internally generated heat comes from standard metabolic rate and leatherbacks can only maintain a TB – TW of < 2 °C regardless of mass. As swim speed increases so does internally generated heat and TB – TW rises.  33  1.6  Metabolic Rate (W kg-1)  1.4 1.2 1.0 0.8 0.6 100 kg No feeding 100 kg feeding 300 kg No feeding 300 kg feeding 500 kg No feeding 500 kg feeding  0.4 0.2 0.0 0  2  4  6  8  10  12  14  16  TB-TW (oC)  Figure 2.4 Metabolic rates (both fasting and feeding) are plotted against TB – TW for 100, 300 and 500 kg leatherbacks. In fasting leatherbacks metabolic rate is directly proportional to TB – TW. Feeding leatherbacks have a lower TB – TW than fasting ones because some metabolic energy is used to warm ingested food.  34  Depth (m)  0 20 40 60  Temperature (oC)  30 28  TSC  26 24  TW  22 10:00  11:00  12:00  13:00  15 NOV 1996  Figure 2.5 An unpublished figure from Southwood and colleagues that shows the water temperature (TW), sub-carapace temperature (TSC) and depth experienced by a leatherback in the tropics during a long dive. The leatherback stayed at a depth near 40 m for 67 minutes returning to the surface for 30 minutes before resuming an active dive cycle. The leatherbacks TB decreased throughout the whole dive and continued decreasing during the surface interval despite a TB – TW of only a couple degrees. TB only started climbing once an active bout started suggesting metabolic heat from muscle activity is crucial in maintaining a high TB – TW.  35  2.5 References  Ahlborn BK, Blake RW (1999) Lower size limit of aquatic mammals. American Journal of Physics 67: 920-922 Avery RA (1982) Field studies of body temperatures and thermoregulation. In (Gans C, Pough FH eds.), Biology of the Reptilia. volume 12. Academic Press, New York, 93-166 Brill RW, Dewar H, Graham JB (1994) Basic concepts relevant to heat-transfer in fishes, and their use in measuring the physiological thermoregulatory abilities of tunas. Environmental biology of fishes 40: 109-124 Davenport J (1998) Sustaining endothermy on a diet of cold jelly: energetics of the leatherback sea turtle Dermochelys coriacea. British Herpetological Society Bulletin 62: 4-8 Eckert S A (2002) Swim speed and movement patterns of gravid leatherback sea turtles (Dermochelys coriacea) at St Croix, US Virgin Islands. Journal of Experimental Biology 205: 3689-3697 Eckert SA, Nellis DW, Eckert KL, Kooyman GL (1986) Diving Patterns of two leatherback sea turtles (Dermochelys coriacea) during internesting intervals at Sandy Point, St Croix, U.S. Virgin Islands. Herpetologica 42: 381-388 Giering K, Lamprecht I, Minet O, Handke A (1995) Determination of the specific-heat capacity of healthy and tumorous human tissue. Thermochimica Acta 251: 199-205 Goff GP, Lien J (1988) Atlantic leatherback turtles, Dermochelys coriacea, in cold water off Newfoundland and Labrador. Canadian Field Naturalist 102: 1-5 Greer AE, Lazell JD, Wright RM (1973) Anatomical evidence for a countercurrent heatexchanger in leatherback turtle (Dermochelys coriacea). Nature 244: 181  36  Hays GC, Houghton JDR, Myers AE (2004) Endangered species - Pan-Atlantic leatherback turtle movements. Nature 429: 522 Heglund NC, Cavagna GA (1987) Mechanical work, oxygen-consumption, and efficiency in isolated frog and rat muscle. Americal Journal of Physiology 253: 22-29 Hind AT, Gurney WSC (1997) The metabolic cost of swimming in marine homeotherms. Journal of Experimental Biology 200: 531-542 Hochscheid S, Bentivegna F, Speakman JR (2002) Regional blood flow in sea turtles: Implications for heat exchange in an aquatic ectotherm. Physiology and Biochemical Zoology 75: 66-76 Hokkanen JEI (1990) Temperature regulation of marine mammals. Journal of Theoretical Biology 145: 465-485 Hughes GR, Luschi P, Mencacci R, Papi F (1998) The 7000-km oceanic journey of a leatherback turtle tracked by satellite. Journal of Experimental Marine Biology and Ecology 229: 209-217 James MC, Mrosovsky N (2004) Body temperatures of leatherback turtles (Dermochelys coriacea) in temperate waters off Nova Scotia, Canada. Canadian Journal of Zoology 82: 1302-1306 James MC, Ottensmeyer CA, Myers RA (2005) Identification of high-use habitat and threats to leatherback sea turtles in northern waters: new directions for conservation. Ecology Letters 8: 195-201 Kreith F, Black WZ (1980) Basic Heat Transfer. Harper & Row, New York. Kshatriya M, Blake RW (1988) Theoretical-model of migration energetics in the blue whale, Balaenoptera musculus. Journal of Theoretical Biology 133; 479-498  37  Kvadsheim PH, Folkow LP, Blix AS (1996) Thermal conductivity of minke whale blubber. Journal of Thermal Biology 21: 123-128 Kvadsheim PH, Gotaas ARL, Folkow LP, Blix AS (1997) An experimental validation of heat loss models for marine mammals. Journal of Theoretical Biology 184: 15-23 Lutcavage M, Lutz PL (1986) Metabolic-rate and food-energy requirements of the leatherback sea-turtle, Dermochelys coriacea. Copeia. 3: 796-798 Lutcavage ME, Bushnell PG, Jones DR (1990) Oxygen-transport in the leatherback sea-turtle Dermochelys coriacea. Physiological Zoology 63: 1012-1024 Lutcavage ME, Bushnell PG, Jones DR (1992) Oxygen stores and aerobic metabolism in the leatherback sea-turtle. Canadian Journal of Zoology 70: 348-351 McMahon TA, Bonner JT (1983) On Size and life. Scientific American Library, New York. McMahon CR, Hays GC (2006) Thermal niche, large-scale movements and implications of climate change for a critically endangered marine vertebrate. Global Change Biology 12: 1330-1338 Morreale SJ, Standora EA, Spotila JR, Paladino FV (1996) Migration corridor for sea turtles. Nature. 384: 319-320 Paladino FV, O’Connor MP, Spotila JR (1990) Metabolism of leatherback turtles, gigantothermy, and thermoregulation of dinosaurs. Nature 344: 858-860 Penick DN, Spotila JR, O'Connor MP, Steyermark AC, George RH, Salice CJ, Paladino FV (1998) Thermal independence of muscle tissue metabolism in the leatherback turtle, Dermochelys coriacea. Comparative Biochemistry and Physiology A 120: 399-403 Prange HD (1976) Energetics of swimming of a sea turtle. Journal of Experimental Biology 64: 1-12  38  Prange HD, Jackson DC (1976) Ventilation, gas exchange and metabolic scaling of a sea turtle. Respiratory Physiology 27: 369-377 Reina RD, Abernathy KJ, Marshall GJ, Spotila JR (2005) Respiratory frequency, dive behaviour and social interactions of leatherback turtles, Dermochelys coriacea during the inter-nesting interval. Journal of Experimental Marine Biology and Ecology 316: 1-16 Sato K, Sakamoto W, Matsuzawa Y, Tanaka H, Minamikawa S, Naito Y (1995) Bodytemperature independence of solar-radiation in free-ranging loggerhead turtles, Caretta caretta, during internesting periods. Marine Biology 123: 197-205 Seebacher F, Grigg GC, Beard LA (1999) Crocodiles as dinosaurs: behavioural thermoregulation in very large ectotherms leads to high and stable body temperatures. Journal of Experimental Biology 202: 77-86 Southwood AL, Andrews RD, Paladino FV, Jones DR (2005) Effects of diving and swimming behavior on body temperatures of Pacific leatherback turtles in tropical seas. Physiology and Biochemical Zoology 78: 285-297 Standora EA, Spotila JR, Foley RE (1982) Regional endothermy in the sea turtle, Chelonia mydas. Journal of Thermal Biology 7: 159-165 Trillmich KGK, Trillmich F (1986) Foraging strategies of the marine iguana, Amblyrhynchus cristatus. Behavioural Ecology and Sociobiology 18: 259-266 Tritton DJ (1988) Physical fluid dynamics. Oxford University Press, Oxford, England. Wallace BP, Williams CL, Paladino FV, Morreale SJ, Lindstrom RT, Spotila JR (2005) Bioenergetics and diving activity of internesting leatherback turtles Dermochelys coriacea at Parque Nacional Marino las Baulas, Costa Rica. Journal of Experimental Biology 208: 3873-3884  39  Watson KP, Granger RA (1998) Hydrodynamic effect of a satellite transmitter on a juvenile green turtle (Dermochelys coriacea). Journal of Experimental Biology 201: 2497-2505 Watts P, Hansen S, Lavigne DM (1993) Models of heat-loss by marine mammals thermoregulation below the zone of irrelevance. Journal of Theoretical Biology 163: 505525 Woledge RC (1968) Energetics of tortoise muscle. Journal of Physiology 197: 685 Worthy GAJ (1991) Insulation and thermal balance of fasting harp and gray seal pups. Comparative Biochemistry and Physiology A100: 845-851 Yasui WY, Gaskin DE (1986) Energy budget of a small cetacean, the harbor porpoise, Phocoena phocoena. Ophelia 25: 183-197  40  3  BEHAVIOUR & PHYSIOLOGY: THE THERMAL STRATEGY OF LEATHERBACK TURTLES2  3.1 Introduction  Body temperature (TB) has a pronounced effect on all metabolic processes and it is usually advantageous to maintain TB within a certain temperature range. To regulate TB animals employ a thermal strategy that has both physiological and behavioural components which alter the rate of heat loss or gain. Most non-mammalian and non-avian species are ectothermic so metabolic heat is not integral to their thermal biology. Due to the lack of an internal heat source most reptiles and fish maintain optimum physiological performance across a narrow range of ambient temperatures. Nevertheless some animals, such as the leatherback sea turtle, can maintain TB near optimum over a large range of ambient temperatures which expands their thermal niche and increases their global range.  Leatherback sea turtles are large oceanic pelagic reptiles that nest in the tropics where the water temperature (TW) can be as high as 30 °C (Southwood et al. 2005) and spend extended periods of time foraging in cold northern waters that approach 0 °C (James et al. 2006). No other known reptile inhabits such a large ambient temperature range. Southwood et al. (2005) reported leatherbacks swimming in tropical waters have body temperatures (TB) 1.2 – 4.3 °C above ambient TW. In contrast, James and Mrosovsky (2004) captured leatherbacks in foraging grounds off of Nova Scotia (Canada) where the turtles typically maintained TB of 24.3 °C in  2  A version of this chapter will be submitted for publication. Bostrom BL, Jones TT, Jones DR. Behaviour & Physiology: the thermal strategy of leatherback turtles.  41  surface water of 16.1 °C for a thermal gradient (TB - TW) of at least 8.2 °C. Unfortunately, the precise mechanisms involved in the leatherbacks’ thermoregulatory ability are poorly understood.  Leatherbacks are thought to draw on a suite of physiological and behavioral adaptations to regulate their rate of heat loss and gain. Based on biophysical modeling, Paladino et al. (1990) concluded that large body size and use of peripheral tissues as insulation coupled with the ability to control heat flux via circulatory adjustments would allow leatherbacks to regulate TB in both warm and cold waters. Importantly, leatherbacks are thought to possess counter-current heat exchangers in the anterior flippers (Greer et al. 1973) as well as peripheral layers of fat which includes deposits of brown adipose tissue (Goff and Stenson, 1988). However, the TB – TW a leatherback maintains not only depends on the rate of heat loss, but also on the rate of heat production. Bostrom and Jones (2007; Chapter 2) demonstrated the importance of behavioral adjustments (i.e. swimming activity) as a further thermoregulatory mechanism to maintain preferred TB – TW in different thermal environments. Taken together, results of previous studies have suggested integrated roles of large body size and physiological and behavioral adjustments in leatherback thermoregulation.  While different components of leatherback thermal biology have been measured and/or modelled in several studies, a holistic approach to quantifying the collective leatherback thermoregulatory response is lacking. In this study, I report the first empirical observations of the physiological and behavioral responses of leatherbacks to controlled variations in thermal environment. I apply  42  my results to thermoregulation of leatherbacks, from juveniles to adults, in their natural environment, from tropical to polar seas. 3.2 Materials and Methods  3.2.1 Materials  3.2.1.1 Animals and husbandry  Leatherback hatchlings were transported from nesting beaches on the British Virgin Islands to the Animal Care Centre, University of British Columbia, Vancouver, B.C., Canada, and raised for a two year period. The experiments reported here were performed on two animals, one weighed 16.1 kg at the start of the experiment and the other weighed 36.7 kg. Both animals were raised in TW = 25 °C. Throughout the experiment the animals were held in a cylindrical holding tank 2 m in diameter and 1.5 m deep, filled with seawater supplied from the Vancouver Aquarium and Marine Sciences Centre (Vancouver, B.C., Canada). Leatherback turtles were obtained on Canada CITES Import permit CA05CWIM0039 and British Virgin Islands CITES Export certificate CFD062005. These animals were held for research purposes and all animal care/research standards of the Canadian Council for Animal Care (CCAC) and the UBC Animal Care Committee (UBC Animal Care Protocol: A04-0323) were met.  Leatherbacks swim continuously and have an oceanic-pelagic lifestyle with the result that they do not recognize barriers, consequently, they repeatedly collide with the sides of the tanks. To prevent this, the animals were tethered to the centre of their housing tank by a short length of  43  monofilament fishing line attached to a custom made harness (Fig. 3.1A). The animals could swim or dive without touching the walls or bottom of the tank. The animals were exposed to a 12 hour light/dark cycle. Water quality was maintained by a biological filter, UV sterilization and a protein skimmer. A reservoir tank of equal volume was plumbed into the holding tank. Water temperature of the reservoir was varied and mixing the water in the two tanks allowed TW to be changed rapidly. TW was maintained within ± 0.25 °C in the holding tank by a thermostat that controlled hot or cold water flow through a stainless steel heat exchanger. The animal was instrumented and put in the tank at the beginning of the experiment and was disturbed only to repair instruments or for feeding which was attempted twice a day.  3.2.2 Methods  3.2.2.1 Temperature regime  TW was changed in a stepwise manner by 3 °C increments or decrements starting from 25 °C. Water was cooled to 16 °C and then warmed from 16 to 31 °C and cooled back to 25 °C over several days (Fig. 3.2). TW was changed by mixing the water in the holding tank with the reservoir tank and the change was completed within 20 minutes of commencing the mix. The water was maintained at each temperature for 11 – 22 hours for the 37 kg turtle and for 7 – 24 hours for the 16 kg turtle, long enough for TB to become stable (i.e. TB change < 0.1 °C hr-1). In total, the experiment with the 16 kg leatherback took 6 days and the experiment with the 37 kg leatherback took 8 days.  44  3.2.2.2 Instrumentation  3.2.2.2.1. TB and TW recording  A thermocouple (90104, Mon-a-therm® General Purpose, Mallinckrodt Medical, St. Louis, MO, USA) was mounted 5 cm into the housing tank and connected to an electronic thermometer (Physitemp BAT – 12, Sensortek Inc., Clifton, NJ, USA). TW was recorded every second. At the beginning of the experiment each animal was given a thermometer pill that was 2.5 cm in length and 1.0 cm in diameter (HT150036, CorTempTM Equine EXSM Temperature Sensor, HQ Inc., Palmetto, FL, USA). The signal from the pill was picked up by a receiver (HT150001, CorTempTM Data Recorder, HQ Inc.) housed in a waterproof container suspended 15 cm above the center of the tank. TB was recorded every 10 seconds. The thermometer pill had a lifespan of around 3 days after which I briefly removed the turtle from the water and gave the animal a new pill. The electronic thermometer and thermometer pill were calibrated against a mercury thermometer (14-985B, FISHERbrand, Fisher Scientific Ltd., Nepean, ON, Canada).  3.2.2.2.2 Heat flux recording  Heat flux, Q (W m-2), was recorded with heat flux transducers (HFT’s; Thermonetics Corp., La Jolla, CA, USA). HFT’s are rectangular flat pads that produce a voltage directly proportional to the heat flux through the pad. I attached the transducers to the animals with a thin layer of  45  cyanoacrylate glue. A 3.9 x 1.9 cm HFT was attached 1/3 of the way along the left front-flipper at the point of largest flipper width (see Fig. 3.1B for placement of HFT’s). A 5.7 x 5.7 cm HFT was attached to the plastron 10 cm distally from the anterior edge and 2.5 cm to the right of each animal’s center line. A 3.9 x 1.9 cm HFT was attached only to the carapace of the 16 kg turtle. The HFT wires ran from the turtle, along the bottom of the tank and then out of the tank to a multiple channel signal conditioner (CyberAmp 320, Axon Instruments) and, after amplification, the signals were A – D converted and recorded at a rate of 1 Hz. HFT’s were attached so that a positive value of heat flux represented heat transferring from the turtle to the water.  3.2.2.2.3 Activity recording  A wooden plank with a short section of 14 mm (internal diameter) PVC pipe inserted through it was placed across the tank. A length of monofilament fishing line attached to the animal’s harness (figure 3.1A) passed through the PVC pipe to a force transducer (FT03C, Grass Instrument Co., Quincy, MA, USA). The PVC pipe redirected the force exerted by the turtle vertically so that recorded force was unaffected by the direction in which the animal was swimming. The signal from the force transducer was A-D converted and recorded at a rate of 5 Hz. Flipper strokes per minute (SPM) were used as an index of activity.  3.2.3 Data recording and analysis  All analog signals were digitized with an analog to digital (A-D) converter (USB – 1208LS, Measurement Computing, Norton, MA, USA) and recorded on a notebook computer with  46  TracerDAQ® (Measurement Computing). Data was discarded during all feeding events and when an animal had been disturbed due to re-instrumentation. Heat flux data was calibrated using calibration curves provided by the manufacturer. AcqKnowledge® software (version 3.7.5, BIOPAC Systems Inc., Santa Barbara, CA, USA) was used to detect peaks in the data from the force transducer. Each peak corresponded to a flipper stroke. This force data was then converted to strokes per minute (SPM) and averaged over the period the animal was held at a given temperature. All other data were taken when the animal was close to steady state which was considered to be when TB was changing at a rate < 0.1 °C hour-1. Therefore, in the 16 kg animal no data was included that was < 6 hours after the water change, and in the 37 kg animal no data < 7.5 hours was included. Water temperature in the holding tank fluctuated by ± 0.25 °C and all heat fluxes as well as the thermal gradient fluctuated in time with TW oscillations (Figure 3.2). To get the steady state heat flux and thermal gradient maintained for a given TW I averaged that small section of the data when TW was ± 0 0.075 °C around the mean value for that trial. The actual period averaged was usually about 30 minutes.  3.2.4 Calculations  3.2.4.1 Surface area  Surface area of both leatherbacks was measured post-mortem. When the large and small animals died of natural causes their masses were 42.0 and 22.3 kg, respectively. Half the carapace, half the plastron, the ventral side of the left front and rear flipper of each animal was covered in paper. The paper was then removed, laid flat and the area was determined by creating geometric  47  shapes with an easily measured area. Total body area (AB) was twice the measured area of plastron and carapace and total flipper area (AF) was four times the measured area of both front and rear flippers.  3.2.4.2 Total heat transfer rate  The total rate of heat transfer, qT (W), from the turtle to the tank was estimated as ABQP+AFQF where QP and QF are heat flux (W m-2) from the plastron and flipper, respectively. The fraction of qT that was lost through the flippers is AFQF / qT. The remaining heat loss was from the body.  3.2.4.3 Thermal admittance of the plastron  The rate of heat transfer (W) across an insulation layer of thermal conductivity k (W m-1 °C-1) and thickness L (m) is given by: q = A k (TB - TW) / L  (3.1)  where TB – TW is the thermal gradient from one side of the layer of insulation to the other, and A (m2) is the area over which heat is lost. To give an index of the regulation over heat loss through the plastron exhibited by the turtles I divided measured QP from the HFT (ie., q /A) by the measured TB – TW. This gives a rate at which heat energy transfers across a given insulator of area 1 m2 driven by a thermal gradient of 1 °C and is referred to as the thermal admittance (W m-2 °C-1).  48  3.3 Results  3.3.1 Thermal gradient  As tank water was cooled stepwise from the acclimation temperature of 25 °C (for TW change protocol see Fig. 3.2) both study animals maintained a progressively larger thermal gradient between their body and the water (Table 3.1 A and B). Initially, the 37 kg turtle maintained a TB – TW of 0.9 °C at TW 25°C which increased to 2.3 °C in TW of 16 °C. The 16 kg animal started off with a gradient of 1.2 °C which increased to 2.0 °C in the coldest water. The 37 kg animal’s thermal gradient decreased to 0.5 °C and the 16 kg turtle’s gradient was 0.8 °C in water at 31 °C. Overall a trend was found in both leatherbacks where cooler water led to the maintenance of larger thermal gradients, but TB – TW gradients in both animals were greater when water temperature was stepped down to a given TW compared with being raised to the same TW. Additionally, the larger turtle displayed a larger variation in thermal gradients (0.5 to 2.3 °C) when compared with the smaller turtle (0.8 to 2.0 °C) over the TW range tested.  3.3.2 Swimming activity  In tank water of 22 °C and higher, the 37 kg leatherback was nearly inactive swimming at a flipper stroke frequency ranging between 2 and 8 SPM (Table 3.1A). The 16 kg leatherback on the other hand maintained 13 SPM in 22 °C water although the animal became nearly inactive in water that was any warmer (Table 3.1B). Stroke frequency greatly increased in both  49  leatherbacks after a drop in temperature from 22 °C. After each reduction in TW the animals stroked at an increased rate, which was maintained over the entire time the turtle was in that TW. In the coldest water (16 °C), the 37 and 16 kg leatherbacks maintained their highest average activity rates at 29 and 36 SPM, respectively.  3.3.3 Heat loss  When TW was 25 °C or less the 37 kg leatherback lost < 7 W m-2, through the front flippers except when cooled to 19 °C when heat loss rose to 11.0 W m-2 (Table 3.1A). When warmed to 28 °C heat flux increased substantially to 16 W m-2. A similarly high QF was maintained until the animal was re- cooled to 25 °C. The 16 kg leatherback lost < 4 W m-2 through its flippers when tank water was 22 °C and below (Table 3.1B). When in water of 25 °C, heat flux increased to 6.2 W m-2 and in 28 °C increased another 39 % to 8.6 W m-2. At 31 °C, QF of the smaller turtle dropped slightly to 7.4 W m-2.  The 37 kg leatherback lost 12.8 W m-2 through the plastron at the acclimation temperature and this value steadily rose to 26.2 W m-2 in the coldest water (Table 3.1). Upon re-warming to 19 °C QP dropped to 10.9 W m-2. This heat flux was maintained until 28 °C when it increased slightly to 13.8 W m-2 remaining stable until the turtle was returned to 25 °C when plastron heat flux dropped to 9.4 W m-2. The 16 kg leatherback followed a similar trend with heat flux highest in 15 °C water (15.7 W m-2) and a steady heat flux around 9 W m-2 from 19 through 28 °C. The rate of heat flux from the carapace of the 16 kg leatherback was nearly the same as QP at each TW tested.  50  When the 37 kg leatherback was in TW ≤ 25 °C , thermal admittance was between 10 and 14 W m-2 °C-1 (Table 3.1A). When °C was warmed to 28 °C, the thermal admittance nearly doubled to 20.6 W m-2 °C-1 and in 31 °C water reached 29.5 W m-2 °C-1, nearly triple the cold water value. On cooling the animal to its acclimation temperature of 25 °C thermal admittance fell to 10.4 W m-2 °C-1. The 16 kg turtle had a constant value for thermal admittance around 9 W m-2 °C-1 in all water temperatures tested. There was insufficient data, unfortunately, to calculate the thermal admittance in 31 °C TW for the smaller turtle.  3.3.4 Surface area  The total surface area of the plastron and carapace, AB, was 0.64 and 0.42 m2 for the 42.0 and 22.3 kg leatherback carcasses, respectively. AF was 0.25 and 0.15 m2 for the large and small turtle, respectively. Total body area (m2), was fitted to a power function and found to scale with MB (kg) as AB = 0.049 MB0.69 and the area of all four flippers scaled as AF = 0.014 MB0.77. Therefore at the time of the experiments, AB for the smaller 16 kg turtle was 0.33 m2 and the 37 kg turtle was 0.59 m2. AF was 0.12 m2 for the small and 0.22 m2 for the larger turtle.  3.3.5 Total heat loss  At 25 °C the 37 kg leatherback lost 0.24 W kg-1 from the body and flippers, and this heat loss rose steadily to 0.44 W kg-1 in the coldest water (Table 3.1A). When warmed to 19 °C, qT dropped to 0.19 W kg-1 and this value varied little until 28 °C when it rose to 0.32 W kg-1. This  51  qT was held steady until the animal was again cooled to 25 °C. The smaller turtle at 25 °C had a qT of 0.35 W kg-1 which fell to 0.28 W kg-1 in 22 °C water but increased to 0.35 W kg-1 in 16 °C TW. Upon re-warming to 19 °C, qT dropped to 0.20 W kg-1 and then slowly increased to 0.24 W kg-1 at 28 °C.  3.3.6 Fraction of heat loss through the body and carapace  In the coldest water (16 °C) both turtles lost about 7% of qT through their flippers with the remaining 93 % being lost through the body (ie. plastron and carapace, Table 3.1 A and B). The proportion of heat lost from the flippers increased as TW rose in both turtles. In 28 and 31 °C TW around 30 % of qT was lost from the flippers compared with 70 % from the plastron and carapace.  3.4 Discussion  There has been considerable speculation that leatherbacks are endothermic and able to thermoregulate based upon the fact that their global range spans from cold northern foraging grounds to tropical nesting beaches. In the coldest water (16 °C) both the 16 and 37 kg leatherback maintained a thermal gradient of 2.0 and 2.3 °C, respectively, while in the warmest water (31°C) the thermal gradient was reduced to 0.5 and 0.8 °C (Table 3.1 A and B). Therefore, I have shown for the first time, using juveniles in a controlled temperature environment, that leatherbacks possess the ability to hold and regulate their thermal gradient. Furthermore, since  52  the heat energy to hold these thermal gradients is metabolically derived the animals are, by definition, endothermic. 3.4.1 Physiological and behavioural responses to warm and cold water  In water colder than their acclimation temperature (TW < 25 °C) the flipper stroke frequency of both leatherbacks increased as TW decreased (Table 3.1 A and B). Since each flipper stroke causes water movement the activity is proportional to expended energy and due to the inefficiency of metabolic processes, as TW gets colder, endogenous heat production increased. In the coldest water flipper stroke frequency was highest and the largest thermal gradient was maintained. TB – TW during cooling was different from that during re-warming and a similar hysteresis was seen in the relation between flipper stroke frequency and TW. Further, TB – TW varied in association with activity for TB – TW’s between 1 and 2.3 °C. Since both leatherbacks maintained a stable thermal admittance during those trials the TB – TW‘s were due largely to activity (Fig. 3.4). The potential to use behavioral control of activity to regulate heat production and therefore TB (Chapter 2) has been confirmed in my study. Eckert (2002) found leatherbacks swim continuously which shows their potential to maintain high activity rates over very long periods of time. Behavioral control of heat production has not been shown to be an integral thermoregulatory mechanism in any other reptile but it is probable that it may be used in other endothermic species such as lamnid sharks, tunas and billfish, especially when exposed to very cold waters. Behavioural control of heat production contrasts with other endotherms in which metabolic heat production is controlled autonomically.  53  Even though the surface area of the front and rear flippers combined represents 27 % of the total surface area of each turtle I found that only 6-7 % of total heat loss, qT, came from them in the coldest water (Table 3.1 A and B). Despite not having the ability to completely halt heat flux, the flippers are responsible for only a small fraction of total heat loss. In warm water heat flux increases substantially from the flippers to a rate nearly 3 times that in cold water and accounts for 30 % of qT. These observations suggest an effective control over flipper heat flux, either by utilization of counter-current heat exchangers or, at its simplest, a reduction in total blood flow to the flippers in cold water. Greer et al. (1973) described a dense, intertwining network of arteries and veins in both the anterior and posterior flippers of a leatherback and suggested these structures were anatomical evidence for heat exchangers. Heat exchangers have evolved independently in lamnid sharks and scombrids, underscoring the primary importance of heat retention in maintenance of elevated body temperatures in each lineage (Bernal et al. 2001). No evidence of heat exchangers in green and loggerhead sea turtles has been reported, but both turtles have been shown to greatly reduce blood flow to their flippers when exposed to TW lower than their acclimation temperatures (Hochscheid et al. 2002). In addition, thermal effects on the whole circulation could have an important influence on heat flux. Nonetheless, despite the lack of clarity on the precise mechanism controlling heat loss from the flippers there is no doubt that heat loss/gain via the flippers is an important part of a leatherbacks thermal arsenal.  In contrast to the flippers, leatherbacks lost a substantial amount of heat energy through the plastron at all water temperatures (Table 3.1 A and B). Since the body was always warmer than tank water, heat was conducted from the core of the animal to the water. If heat passed to the water solely by conduction, heat flux should be directly proportional to the thermal gradient  54  across the plastron (Eq. 3.1) with any deviation reflecting physiological changes such as a variation in blood flow. Therefore, the thermal admittance, the heat flux for a given thermal gradient, should be an accurate index of physiological blood flow changes a leatherback makes that affect QP. In TW ≤ 25 °C the 37 kg leatherback maintained a stable thermal admittance of around 12 W m-2 °C-1 (Table 3.1A) and at all temperatures tested the 16 kg leatherback also maintained a constant thermal admittance, although slightly lower at 9 W m-2 °C-1 (Table 3.1B). When in water colder than the acclimation temperature, little heat energy was lost through the flippers so physiologically their thermal insulation was at a maximum due to little blood flow to the skin surface. In contrast, in water above the acclimation temperature, thermal admittance nearly tripled so more heat was lost convectively and therefore blood flow to the skin must have increased. As well, TB – TW correlated closely with thermal admittance when TB – TW was below 1 °C (Fig. 3.4). Since activity was minimized the physiological changes affected the TB – TW confirming the suggestion that leatherbacks could control TB through blood flow (Paladino et al. 1990).  Interestingly, the large leatherback lost around 30 % more heat per unit area from its plastron than the small turtle, regardless of the gradient between body and water. I expected the smaller turtle to have a thinner layer of insulation and consequently a higher heat flux for a given TB – TW. This apparent discrepancy may be because the thermal conductivity, k, of the 16 kg turtle’s plastron was lower and a better insulator than that of the larger turtle. However, it is also possible that the thermal gradient I measured between the body and tank water did not truly represent the thermal gradient from one side of the plastron to the other. TB was measured as gastrointestinal tract temperature and although core body temperature is generally modelled as  55  being homogenous due to blood flow (Paladino et al. 1990; Chapter 2), this may not always be the case. Heat lost through the plastron could cause a temperature profile inside the turtle where the core of the animal is at TB and the temperature approaches TW closer to the plastron. If the insulating layer was thinner in the smaller animal the temperature on the inside of the plastron actually could be lower than TB measured in the core, reducing the thermal gradient across the plastron. As the animal grows and insulation thickens the sub-plastron temperature should more closely reflect core TB.  In cold water, heat flux from the carapace was the same as from the plastron in the 16 kg turtle which suggests the heat flux may be homogenous over the body surface, AB, if the skin is not perfused. This would be expected if TB was homogenous and there is an even layer of insulation over AB. Assuming the measured thermal gradient in the larger animal was a true representation of the thermal gradient directly across the plastron, the thermal conductivity, k, of leatherback shell can be estimated. The plastron of juvenile leatherbacks of similar size is around 0.02 m thick (unpublished results), so k is between 0.2 - 0.3 W m-1 °C-1, which is similar to the thermal conductivity recorded for whale blubber (Kvadsheim et al. 1996).  As the leatherbacks were in steady state at each TW and held a stable TB, the total rate of heat production must equal the total rate of heat loss. Therefore the sum of the heat lost from the plastron, carapace and flippers (ie. qT) will be an estimate of total heat produced (Table 3.1 A and B). A caveat is that heat loss is modelled to occur evenly over the entire surface. Total heat production was greatest when the animals were most active and therefore in the coldest water. Despite activity falling as water was warmed from 19 to 25 °C, heat loss was constant in both  56  animals and this was likely an expression of the thermal dependence on basal metabolic processes. In 28 and 31 °C TW the 37 kg leatherbacks heat production rate further increased despite having a very low activity rate, again due to temperature effects on basal metabolism. In adult leatherbacks that maintain stable TB’s the heat production rate is expected to more closely reflect the rate of activity because basal metabolic rate should be constant.  3.4.2 Effect of body mass on thermal gradients  At steady state TB – TW, the total rate of heat transfer, qT, to the environment equals the rate of heat gain. In leatherbacks, heat is produced endogenously so heat production must approximate the metabolic rate of the animal. Given that resting metabolic rate scales with body mass, MB (kg), to the 0.83 power in leatherback sea turtles (Wallace and Jones, 2008) and rate of heat transfer across an insulation layer is given by Eq. 3.1 then: (TB – TW) k A L-1 = a MB0.83  (3.2)  where a is the proportionality coefficient. The body shape of juvenile leatherbacks are similar to those of sub-adults and adults so A scales with MB to the 2/3 power and L will scale with MB to the 1/3 power since MB has dimensions of L3. Therefore if k is constant then the thermal gradient scales with MB to the 0.5 power as: (TB –TW) = b MB0.5  (3.3)  where b is a coefficient that is proportional to the energy expenditure of the animal (ie. doubling b corresponds to twice the heat production).  57  The thermal gradients that adult leatherbacks hold can be predicted by scaling the thermal gradient held by juveniles. At 25 °C the animals in this study maintained a low level of activity with TB – TW around 1 °C. I fitted these results to Eq. 3.3 to predict the TB – TW that animals of different MB could maintain with low endogenous heat production and found b = 0.21. Fig. 3.5 quantitatively shows the effect that varying heat production, changing b, has on the TB – TW achieved by leatherbacks with minimized heat loss in cold water. The thermal gradient is predicted to be 1.7 and 2.5 °C for juveniles of 16 and 37 kg with a heat production rate two times the resting level. This is close to the 2.0 and 2.3 °C thermal gradient my animals held when in 16 °  C tank water when heat loss was double that at 25 °C. An average thermal gradient of 8.2 °C,  measured for adults in 15 °C water off of Nova Scotia (James and Mrovosky 2004), occurs if heat production is double that of a resting animal.  Metabolic rate of active leatherbacks on a beach was 1.51 W kg-1 (Paladino et al. 1990), or five times resting metabolic rate (Wallace and Jones, 2008). If leatherbacks maintain such a high heat production rate, my model predicts that a 300 kg animal could hold a maximum TB – TW gradient of 18.2 °C. Therefore leatherbacks swimming in northern temperate waters must maintain substantially elevated metabolic rates to keep TB stable. The predictions in Fig. 3.5 assume a thickness of insulation which scales to the 1/3 power with MB. Animals fatten while foraging so if the insulation layer increases, then for a given heat production rate, a larger thermal gradient will be maintained. James et al. (2005) found leatherbacks off Nova Scotia, Canada to have a 33% greater mass than nesting animals of the same carapace length. If a substantial portion of this increased mass is sub-cutaneous fat, insulation will be improved.  58  Due to scaling effects, the achievable thermal gradient is predicted to scale with MB, at a given metabolic cost, to the 0.5 power (Eq. 3.3). Therefore if leatherbacks have to maintain their TB above a minimum value only larger animals should be found foraging in colder waters. Eckert (2002) noted that animals < 100 cm carapace length were not observed in TW < 26 °C. James et al. (2006) recorded a leatherback of 148 cm curved carapace length (around 500 kg) repeatedly diving into water of 0.4 °C! The model predicts that a 500kg leatherback would have to have a metabolic rate twice that of my swimming juveniles (four times resting) to keep a body temperature of 20 °C in these extremely cold waters.  In warm water my leatherbacks had a similar heat loss rate (Table 3.1 A and B) from the flippers as the plastron suggesting similar heat flux over their entire body surface when dumping heat in warm water. Presumably this was due to maximizing blood flow. When coupled with a minimization in flipper stroke frequency the 37 kg leatherback had a TB – TW of only 0.5 °C in the warmest water (31 °C). The 16 kg leatherback although having a similar flipper stroke frequency as the 37 kg animal did not increase heat loss as water temperatures rose so its thermal gradient was greater (TB – TW = 0.8 °C). Since surface area scales with MB to the 2/3 power and heat production scales to the 0.83, there is very little added heat production per surface area as an animal grows. Therefore, in the tropics, if an adult leatherback routed blood to its entire surface the potential for heat loss should be great enough that the animals will not be in danger of overheating, even when swimming. In the tropics, adult females had a TB 1 – 4 °C greater than ambient water (Southwood et al. 2005) and TB was correlated with TW, signifying high rates of heat loss in large leatherbacks.  59  3.5 Tables A 37 kg leatherback Water temperature (oC)  Thermal Gradient TB - TW (oC)  25 22 19 16 19 22 25 28 31 28 25  0.9 1.4 1.6 2.3 1.0 0.7 1.1 0.7 0.5 0.5 0.9  Flipper stroke frequency (SPM)  3 21 25 29 19 5 3 3 3 8 6  Flipper Heat Loss Rate (W m-2)  6.5 5.8 11.0 4.6 2.8 5.4 5.7 16.5 14.6 14.3 2.4  Plastron Heat Loss Rate (W m-2)  12.8 16.0 19.5 26.2 10.9 10.7 10.9 13.8 13.5 14.0 9.4  Thermal Admittance (W m-2 °C-1)  Total Heat Loss (W kg-1)  Flipper Heat Loss (% total heat loss)  14.4 11.4 12.0 11.5 10.4 14.4 10.4 20.6 29.5 26.9 10.4  0.24 0.29 0.38 0.44 0.19 0.20 0.21 0.32 0.30 0.31 0.16  16 12 18 6 9 16 17 32 29 28 9  Thermal Admittance (W m-2 °C-1)  Total Heat Loss (W kg-1)  Flipper Heat Loss (% total heat loss)  9.9 8.7 7.9 8.6 11.1 7.9 8.4 -  0.35 0.28 0.35 0.20 0.21 0.23 0.24 -  14 10 7 15 11 20 26 -  B 16 kg leatherback Water temperature (oC)  Thermal Gradient TB - TW (oC)  25 22 19 16 19 22 25 28 31 28 25  1.5 1.4 1.6 2.0 1.0 0.8 1.2 1.0 0.8 -  Flipper stroke frequency (SPM)  20 22 30 36 29 13 2 2 2 3 9  Flipper Heat Loss Rate (W m-2)  6.7 4.0 3.1 3.3 4.0 3.0 6.2 8.6 7.4 -  Plastron Heat Loss Rate (W m-2)  14.5 12.3 15.7 8.2 8.9 9.1 8.8 11.1 -  60  Table 3.1 Recorded and calculated values at each water temperature for the 37 kg (A) and 16 kg (B) leatherbacks.  3.6 Figures  Figure 3.1 A. An illustration of the turtles harnessed in their tanks. B. The placement of the HFT’s on the animals. 61  34 32  Water temperature (oC)  30 28 26 24 22 20 18 16 14 0  1  2  3  4  5  6  7  Time (days)  Figure 3.2 The complete water temperature profile for the experiment performed on the 37 kg leatherback.  62  Activity (SPM) o  Temperature ( C)  30 20  2D Graph 5  10 0 31 28 25 22  2D Graph 4  feeding TW  19  TB  Heat Loss (W m-2)  16 20  0  -20  Plastron Flipper 3.0  3.5  4.0  4.5  5.0  5.5  6.0  Time (days)  Figure 3.3 Activity, water and body temperature and heat fluxes recorded simultaneously from the 37 kg leatherback during stepwise increases in water temperature.  63  Figure 3.4 A 3D image showing how activity and thermal admittance affect the thermal gradient held by juvenile leatherbacks.  64  18 juvenile: TW = 25 oC 16  juvenile: TW = 15 oC adult: TW = 15 oC  14  low heat gain (b) 2b 3b 4b  TB - TW (oC)  12 10 8 6 4 2 0 0  100  200  300  400  Body Mass (kg)  Figure 3.5 The effect of mass and heat production on the thermal gradient held by leatherbacks.  65  3.7 References  Bernal D, Dickson KA, Shadwich RE, Graham JB (2001) Review: Analysis of the evolutionary convergence for high performance swimming in lamnid sharks and tunas. Comparative Physiology and Biochemisty A129: 695-726 Bostrom BL, Jones DR (2007) Exercise warms adult leatherback turtles. Comparative Physiology and Biochemisty A147: 323–331 Eckert SA (2002) Swim speed and movement patterns of gravid leatherback sea turtles (Dermochelys coriacea) at St. Croix, US Virgin Islands. Journal of Experimental Biology 205: 3689–3697 Frair W, Ackman RG, Mrosovsky N (1972) Body temperature of Dermochelys coriacea: warm turtle from cold water. Science 177: 791–793 Goff PG, Stenson GB (1988) Brown adipose tissue in leatherback sea turtles: A thermogenic organ in an endothermic reptile? Copeia 4: 1071-1075 Greer AE, Lazelle JD, Wright RM (1973) Anatomical evidence for a countercurrent heat exchanger in the leatherback turtle (Dermochelys coriacea). Nature 244: 181 Hochscheid S, Bentivegna F, Speakman JR (2002) Regional blood flow in sea turtles: implications for heat exchange in an aquatic ectotherm. Physiology and Biochemical Zoology 75: 66–76 James MC, Davenport J, Hays GC (2006) Expanded thermal niche for a diving vertebrate: a leatherback turtle diving into near-freezing water. Journal of Experimental Marine Biology and Ecology 335: 221–226  66  James MC, Mrosovsky N (2004) Body temperatures of leatherback turtles (Dermochelys coriacea) in temperate waters off Nova Scotia, Canada. Canadian Journal of Zoology 82: 102–106 James MC, Ottensmeyer A, Myers RA (2005) Identification of high-use habitat and threats to leatherback sea turtles in northern waters: new directions for conservation. Ecology Letters 8: 195-201 Paladino FV, Spotila JR, O'Connor MP, Gatten Jr RE (1996) Respiratory physiology of adult leatherback turtles (Dermochelys coriacea) while nesting on land. Chelonian Conservation Biology 2: 223–229 Southwood AL, Andrews RD, Paladino FV, Jones DR (2005) Effects of swimming and diving behavior on body temperatures of Pacific leatherbacksin tropical seas. Physiology and Biochemical Zoology 78: 285–297 Wallace BP, Jones TT (2008) What makes marine turtles go: A review of metabolic rates and their consequences. Journal of Experimental Marine Biology and Ecology 356: 8-24  67  4 General Discussion  By modelling thermal relationships (Chapter 2), I identified key variables that play an important role in the thermoregulatory ability of the leatherback sea turtle and may be important for extending the range of distribution of this most impressive animal. If body temperature (TB) is maintained above water temperature (TW) the rate the animal loses heat must equal the rate it is produced. Therefore the variables that influence these rates will be of primary importance in maintaining and/or regulating the thermal gradient between the body and water (TB – TW).  Body mass, MB, is important because surface area scales as MB2/3 so surface area from which heat is lost increases at a slower rate than MB. The thermal conductivity and thickness of the layer of insulation surrounding the turtle’s body affects heat loss by conduction. On the other hand, an increase in blood flow to the animal’s surface will result in an increase in convective heat loss and act as a means to by-pass the layer of insulation but allowing this layer to reach its full expression when blood flow is withdrawn. Regulation of blood flow to the surface of the animal was suggested previously as a means to regulate TB (Paladino et al. 1990). The flippers do not have a thick layer of insulation so heat loss, especially from the large surface area of the anterior flippers, would represent a massive source of heat loss. Heat loss from the flippers however can be controlled by either regulation of blood flow (Hochscheid et al. 2002) or use of counter-current heat exchangers (Greer et al. 1973).  Heat production is the other side of the coin to heat loss and I predicted that a by-product of heat energy released during locomotion would help maintain the thermal gradient, representing a 68  method to behaviourally control TB – TW (Chapter 2). I concluded from modelling that, in an experiment, the magnitude of heat loss from the animal would be the most important variable to measure. In steady state, heat loss will equal heat production so heat loss also can be used as an indicator of metabolic rate. Furthermore, heat loss divided by TB – TW is a variable termed thermal admittance that expresses the ease with which heat flows across an insulator (Chapter 3).  Consequently, in the third chapter, I measured heat flux and TB – TW as well as swimming stroke frequency as a proxy for rate of activity of captive juveniles in TWs ranging from 16 to 31 °C. Heat flux allowed calculation of heat production which, in combination with activity, provided an index of behavioural modifications made by the animal. Physiological blood flow changes were inferred from TB – TW and heat flux. I recorded juvenile leatherbacks holding larger gradients (up to 2.3 °C) in cold water (16 °C) compared to the gradients held when exposed to warm water (in 31 °C TB – TW = 0.5 °C). This confirmed that even juvenile leatherbacks possess the ability to influence their TB.  The key factors predicted to be responsible for maintenance of TB – TW are activity and thermal admittance. Activity is an index of heat production and is behaviourally controlled. Thermal admittance is a manifestation of blood flow and any other physiological changes or characteristics. When TB – TW was below 1 °C activity was minimized and higher thermal admittances were associated with lower TB – TWs (Fig. 3.4). This confirms the utility of using physiological adjustments for temperature regulation (Paladino et al. 1990). When TB – TWs rose above 1 °C thermal admittance was minimized and higher activities were associated with greater TB – TWs, confirming my hypothesis that control of thermogenesis through activity could be an  69  important part of the leatherbacks’ thermal strategy (Chapter 2). In juveniles either thermal admittance or activity changed but when investigated serially did not do so simultaneously (illustrated by the data hugging the “walls” in Fig. 3.4). Obviously, in the wild, animals have both physiological control of heat loss and behavioural control of heat production at their disposal.  In the juveniles, TBs were warmer than the water at every TW tested. Due to a lack of an extraneous heat source leatherbacks must therefore be endothermic. This kind of endothermy is unusual in the mammalian or avian sense but is undeniable. In an aquatic environment, where animals are plagued by high heat loss rates and unavoidable cold water temperatures, using activity as a means to regulate heat is not without precedent. Maintaining elevated activity rates to prevent cooling has been suggested to be important in lamnid sharks (Bernal et al. 2001, Goldman et al. 2004) and some tunas (Guppy et al. 1979, Dewar et al. 1994). This leads to the speculation that endogenously produced heat may be an important factor in the thermoregulatory response of other large reptiles such as salt water crocodiles venturing out to the Great Barrier Reef in Australia. Many claim dinosaurs also may have been endothermic (Paladino et al. 1990, Seebacher 2003). Endothermy in leatherbacks is unlike that found in mammalian and avian species; rather a simpler version consisting of behavioural changes to elevate metabolic rates and regulation of insulation abetted by their large size. A strategy similar to that found in leatherback turtles would be especially useful in smaller aquatic dinosaurs and seems plausible as leatherbacks have been titled the “last of the dinosaurs”.  70  As mentioned, mathematical models are only as good as the data on which they are based. In the model presented, heat production was probably overestimated by a factor of 2 as it was assumed to be the by-product of energy expended in overcoming hydrodynamic drag (Chapter 2) and drag was measured using a cast that had the anterior flippers still attached. Due to the complicated nature of drag and propulsion of oscillating bodies the flippers should have been removed leaving just the rigid body hull (Watson and Granger 1998). I assumed a propeller efficiency of 100 % in an attempt to isolate the body from the flippers. If propeller efficiency, in reality, is 50 % then the drag coefficient would be equivalent to 0.35 which is similar to a green turtle (Watson and Granger 1998). A water flume in Bamfield, Canada, was used to perform a pilot drag study on a leatherback carcass, with front flippers removed, and it appears leatherbacks have a drag coefficient closer to 0.15 (unpublished data). Therefore the heat production rate predicted in Chapter 2 is likely an overestimation on the order of 2-3 times. This explains why the predicted minimum cost of transport in Chapter 2 was 0.3 m s-1 when the animals usually swim closer to 0.7 m s-1 (Southwood et al. 2005). Recently the aerobic dive limit of adult leatherbacks was estimated from behavioural data and used to calculate a diving metabolic rate of 0.24 W kg-1 (Bradshaw et al. 2007). The model in Chapter 2 estimates the metabolic rate of a 300 kg leatherback swimming at 0.7 m s-1 to be 0.65 W kg-1, nearly three times greater than that inferred from studies on animals in the wild.  Interestingly, I ended up with a model that predicted thermal gradients at given swimming speeds fairly accurately. This leads to the suspicion that I overestimated heat production and heat loss by similar amounts. I used a single dive in which a leatherback rested on the sea floor in the tropics, with a rapidly decreasing TB, to model heat loss rate and predict the amount or  71  capabilities of the insulation (Chapter 2). In retrospect, it is possible that this animal may have had a greatly increased heat loss and minimized its activity in an attempt to dump heat (Chapter 3). Therefore, in the model, the insulation thickness of leatherbacks could have been underestimated. Juvenile leatherbacks in 31 °C water increased the thermal admittance threefold when compared with cold water and it seems possible that the adult would have done likewise.  Modelling from Chapter 2 and scaling of measured thermal gradients from Chapter 3 provide strong evidence that larger leatherbacks can hold greater thermal gradients than smaller turtles. The 37 kg leatherback in this study maintained a 2.3 °C TB – TW when exposed to 16 °C water. Since metabolic processes are temperature dependant the argument could be made that leatherbacks need to maintain TB at all costs. It is unclear what the minimum is that can be tolerated but at TB = 18.5 °C, the juvenile leatherback appeared to swim at a maximum rate and had stopped eating. It therefore seems unlikely that a leatherback of this size would venture in waters as cold as this in nature. As an animal grows and is able to hold larger TB – TWs, it can venture into colder water so a solid understanding of the TWs / MB relationship will allow predictions of where leatherbacks will be found geographically throughout their life history. Knowing the habitat space of leatherbacks could have major implications in terms of lowering the impact of fisheries by-catch and imposing moratoriums on the fishery (Jones 2009).  Although this research is a start, to fully characterize the thermal range available to leatherback turtles of different size classes more research needs to be done. One characteristic that is poorly understood is the minimum sustainable TB. This value may change in different situations as  72  there are tradeoffs to having a warm or cold TB. An elevated TB would increase metabolic efficiency, assimilation and growth rates. On the other hand a higher TB – TW means a greater rate of heat loss requiring a greater metabolic rate. This could lead to an inverse relationship between aerobic dive limit and foraging efficiency and TB. Dive depth and duration decreased as TW decreased in tagged adults (McMahon and Hays 2006). A possible strategy to overcome this is to lower TB while foraging, and then move to warm surface water and either bask or swim to warm up and digest the meal. Another variable not assessed in this thesis is the effect subcutaneous fat, put on while foraging (James et al. 2005), has on the thermal balance of leatherbacks. It takes time for leatherbacks to migrate to colder waters and, given sufficient resources during migration, their fat stores may build up. An expansion of dead zones in the ocean may, therefore, have a greater influence on leatherback survival than previously imagined. During migration leatherbacks may not have the resources to store the insulation needed to reach colder, resource rich, areas. Overall, the time spent without adequate insulation presents greater thermoregulatory costs to the animal which will limit dive depth and duration, overall foraging efficiency and reproductive output.  4.1 Other Sea Turtles  Sea turtles other than leatherbacks have never been shown to sustain TB – TWs that are large enough to allow migration to cold temperate waters. Free swimming adult loggerhead turtles, for example, generally hold thermal gradients between stomach and water of only 1-2 °C (Sato et al. 1994). A loggerhead’s TB thus closely reflects TW, and in fact in the Western Atlantic, loggerheads rely on warm waters of the Gulf Stream to overwinter (Hawkes et al. 2007). Kemp's  73  ridleys and green turtles cease to feed and become semi-dormant in water of 15 °C (Moon et al. 1997), whereas adult leatherbacks have been recorded actively feeding in waters as low as 0.4 °C (James et al. 2006). Hard shelled turtles are distributed throughout tropical and subtropical waters again suggesting an inability to maintain a homeostatic TB across a wide range of TWs. A lack of insulation and/or insufficient heat production must underlie the low TB – TWs held by these turtles.  Green turtles do seem to be capable of substantial heat production, at least in the short term, and can maintain pectoral muscles 8 °C above TW while actively swimming (Standora et al. 1982). However, activity in green turtles is unpredictable and when a juvenile was exposed to water at 20 °C it remain inactive for 30 minutes before starting swimming (Heath and McGinnis 1980). Green turtles of 7 – 11 kg decrease activity when TW is below 20 °C and are quiescent in water of 15 °C (Moon et al. 1997). This does not seem to be the appropriate behaviour for keeping warm in cold water! Juvenile leatherbacks, on the other hand, increase activity as water temperature decreases to at least 16 °C and at each TW activity levels were constant (Chapter 3). In a similar study to the one presented in Chapter 3 juvenile green turtles appear to use a thermal strategy much like leatherbacks and accomplish similar TB – TWs (Heath and McGinnis 1980). Juvenile greens between 2 and 60 kg held a TB – TW of 2.2 °C in 20 °C water and a gradient of 1.7 °C in 30 °  C. The greens had a higher thermal admittance in warm water and were more active in cooler  water (20 °C) but, as shown above, activity declines below 20 °C. Despite superficial similarity between the data of Heath and McGinnis (1980) and that presented in Chapter 3, in reality, the data of Heath and McGinnis (1980) yield little insight into why leatherbacks are capable of traveling to sub-polar waters and greens are not because they did not expose their animals to low  74  temperatures. Due to constant swimming leatherbacks have a more reliable source of endogenous heat which is fuelled by their oceanic, pelagic lifestyle.  To maintain elevated thermal gradients retaining body heat is as important as producing it. Although the pectoral muscles of an actively swimming green sea turtle can be 8 °C above TW the rest of the body is only 1-2 °C above TW (Standora et al. 1982). This suggests a lack of suitable insulation to maintain large TB – TWs. The measurement of similar internal and external carapace temperatures in a green sea turtle being exposed to intense solar radiation confirms that their carapace is a very poor insulator (Heath and McGinnis 1980). Leatherbacks are able to hold a larger gradient than other sea turtles by a combination of large size, a more efficient insulative layer and better control of heat production. Controlling heat loss and gain concurrently is a thermal strategy that allows leatherbacks to exploit the rich foraging grounds of sub-polar waters while avoiding overheating while actively swimming in tropical reproductive zones.  4.2 Final Conclusions  Even though this research was carried out by modelling of adults and juveniles, rigorous scientific data was only obtained from juvenile leatherbacks. Nevertheless, I am confident that I have furthered the understanding and future of adult leatherback thermal biology. Chapter 2 is a mathematical model that estimates heat loss and production of animals of all size classes. It predicted heat production and behaviour as two important, yet previously overlooked, aspects of the thermoregulatory mechanism used by adult leatherbacks which I then confirmed with the juveniles. As well, by scaling our results on the juveniles we get similar results to adult studies,  75  providing support that the results and modelling are applicable to adults. Knowing the TWs that turtles of different masses can venture into is important for conservation efforts and now we can do better than simply noting that leatherbacks < 100 cm are not seen in temperate waters (Eckert 2002). Tagging events have been restricted to adults and mainly confined to either temperate (James et al. 2005) or tropical waters during the interesting interval (Southwood et al. 2005). Since leatherbacks are critically endangered and adults do poorly in captivity raising animals was the only feasible way to measure detailed behavioural and physiological responses to a wide range of TWs. Recently, with new GPS technologies it has become possible to record data from turtles migrating over a wide range of latitudes and for long periods of time. From this thesis the measurements needed to understand the thermal response of these migrating turtles is now evident. I have found that to understand a leatherbacks response to different TWs the thermal gradient needs to be measured as well as heat flux, as a proxy of skin perfusion, and swimming speed as an index of heat production. This research will hopefully be a spring board for future research into the thermoregulatory ability of adult leatherbacks.  76  4.3 References  Bernal D, Sepulveda C, Graham JB (2001) Water-tunnel studies of heat balance in swimming mako sharks. Journal of Experimental Biology 204: 4043-4054 Bradshaw CJA, McMahon CR, Hays GC (2007) Behavioral inference of diving metabolic rate in free-ranging leatherback turtles, Physiology and Biochemical Zoology 80: 209–219 Dewar H, Graham J, Brill R (1994) Studies of tropic tuna swimming performance in a large water tunnel – thermoregulation. Journal of Experimental Biology 192: 33-44 Eckert SA (2002) Distribution of juvenile leatherback sea turtle Dermochelys coriacea sightings. Marine Ecology Progress series 230: 289-293 Goldman KJ, Anderson SD, Latour RJ, Musick JA (2004) Homeothermy in adult salmon sharks, Lamna ditropis. Environmental Biology of Fishes 71: 403-411 Greer AE, Lazell JD, Wright RM (1973) Anatomical evidence for a countercurrent heatexchanger in leatherback turtle (Dermochelys-Coriacea). Nature 244: 181 Guppy M, Hulbet WC, Hockachka PW (1979) Metabolic sources of heat and power in tuna muscles: II. Enzyme and metabolic profiles. Journal of Experimental Biology 82: 303320 Hawkes LA, Broderick AC, Coyne MS, Godfrey MH, Godley BJ (2007) Only some like it hot – quantifying the thermal niche of the loggerhead sea turtle. Diversity and Distributions 13: 447-457 Heath ME, McGinnis SM (1980) Body temperature and heat transfer in the green sea turtle, Chelonia mydas. Copeia 4: 767-773  77  Hochscheid S, Bentivegna F, Speakman JR (2002) Regional blood flow in sea turtles: Implications for heat exchange in an aquatic ectotherm. Physiology and Biochemical Zoology 75: 66-76 James MC, Ottensmeyer A, Myers RA (2005) Identification of high-use habitat and threats to leatherback sea turtles in northern waters: new directions for conservation. Ecology Letters 8: 195-201 James MC, Davenport J, Hays GC (2006) Expanded thermal niche for a diving vertebrate: a leatherback turtle diving into near-freezing water. Journal of Experimental Marine Biology and Ecology 335: 221–226 Jones TT (2009) Energetics of the leatherback turtle, Dermochely coriacea. PhD thesis, University of British Columbia, Vancouver McMahon CR, Hays GC (2006) Thermal niche, large-scale movements and implications of climate change for a critically endangered marine vertebrate. Global Change Biology 12: 1330-1338 Moon D, MacKenzie DS, Owens DWM (1997) Simulated hibernation of sea turtles in the laboratory: I. Feeding, breathing frequency, blood pH, and blood gases. Comparative Physiology and Biochemistry A278: 372-380 Paladino FV, O’Connor MP, Spotila JR (1990) Metabolism of leatherback turtles, gigantothermy, and thermoregulation of dinosaurs. Nature 344: 858-860 Sato K, Sakamoto W, Matsuzawa Y, Tanaka H, Naito Y (1994) Correlation between stomach temperatures and ambient water temperatures in free-ranging loggerhead turtles, Caretta caretta. Marine Biology 118: 343-351  78  Seebacher F (2003) Dinosaur body temperatures: the occurrence of endothermy and ectothermy. Paleobiology 29: 105-122 Southwood AL, Andrews RD, Paladino FV, Jones DR (2005) Effects of diving and swimming behavior on body temperatures of Pacific leatherback turtles in tropical seas. Physiology and Biochemical Zoology 78: 285-297 Standora EA, Spotila JR, Foley RE (1982) Regional endothermy in the sea turtle, Chelonia mydas. Journal of Thermal Biology 7: 159-165 Watson KP, Granger RA (1998) Hydrodynamic effect of a satellite transmitter on a juvenile green turtle (Chelonia mydas). Journal of Experimental Biology 201: 2497-2505  79  APPENDIX A THE UNIVERSITY OF BRITISH COLUMBIA  ANIMAL CARE CERTIFICATE Application Number: A04-0323 0323 Investigator or Course Director: David R. Jones Department: Zoology Animals: Sea turtle 20  Start Date:  April 1, 1995  Approval Date:  December 8, 2006  Funding Sources: Funding Agency: Funding Title:  Natural Science Engineering Research Council Physiological adaptation of animals  Funding Agency:  Natural Science Engineering Research Council  Funding Title:  Ontogeny geny of Physiological Function in the Leatherback Sea Turtle (Dermochelys coriacea)  Unfunded title:  N/A  80  The Animal Care Committee has examined and approved the use of animals for the above experimental project. This certificate is valid for one year from the above start or approval date (whichever is later) provided there is no change in the experimental procedures. Annual review is required by the CCAC and some granting agencies.  A copy of this certificate must be displayed in your animal facility.  Office of Research Services and Administration 102, 6190 Agronomy Road, Vancouver, BC V6T 1Z3 Phone: 604-827-5111 Fax: 604-822-5093  81  

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