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 References ...... 7
2 Exercise Warms Adult Leatherback Turtles ...... 10
2.1 Introduction ...... 10 2.2 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 2.3 Discussion ...... 23 2.3.1 Test of the model ...... 27 2.4 Figures ...... 31 2.5 References ...... 36
iv
3 Behaviour & Physiology: The Thermal Strategy of Leatherback Turtles ...... 41
3.1 Introduction ...... 41 3.2 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 3.3 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 3.4 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 3.5 Tables ...... 60 3.6 Figures ...... 61 3.7 References ...... 66
4 General Discussion ...... 68
4.1 Other Sea Turtles ...... 73 4.2 Final Conclusions ...... 75 4.3 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 (Q 10 = 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 Q 10 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, non- avian 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
3 2 2/3 to LB . Surface area scales to LB and therefore surface area scales with mass as MB . 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 TURTLES 1
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 300-
500 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
2 balance the drag force on its body. The Fdrag (N) on an object with frontal area A (m ) moving through a fluid of density ρ (kg m -3) at a speed U (m s -1) is:
1 = 2 (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,