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Growth and metabolism of leatherback sea turtles (Dermochelys coriacea) in their first year of life Hastings, Mervin Derick 2006

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GROWTH AND METABOLISM OF LEATHERBACK SEA TURTLES (Dermochelys coriacea) IN THEIR FIRST YEAR OF LIFE by Mervin Derick Hastings B.Sc, University of the Virgin Islands, 1998 A THESIS SUBMITTED IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in THE FACULTY OF GRAUATE STUDIES (Zoology) The University of British Columbia October 2006 © Mervin Derick Hastings, 2006. ABSTRACT Oxygen consumption (VO2 ) was monitored in six juvenile leatherback turtles (Dermochelys coriacea) imported from the Virgin Islands (UK) and kept in a covered outdoor facility at the University of British Columbia. Growth data suggest that leatherbacks can attain a mature size in as little as 5 1/4 to 6 years, much faster than other sea turtles, and reach 90 kg (> 100 cm) in as little as 3 years when they may be thermally capable of venturing into temperature zones for greater resource availability. Animals were held at 24 °C and their Routine Metabolic Rate (R0MR)was measured during the first year at 24 °C as well as after acute exposure to 14, 19, 29 and 34 °C at four different body masses (0.1, 0.5, 1 and 10 kg). Increasing temperature, as well as body mass, significantly increased V 0 2 . Maximum flipper stroke rate occurred at the acclimation temperature (24 °C), falling with exposure to lower and higher temperatures. In contrast, breathing frequency (fR) was unaffected by changes in temperature across all size classes. The intraspecific scaling exponent for V0 2 over an order of magnitude change in body mass at 24 °C was 0.88, very similar to allometric scaling exponents of other reptiles. The scaling exponent increased at 14 °C and decreased at 34 °C. Intraspecific scaling exponents are temperature dependent in leatherback turtles and this may also be the same in other reptiles. ii TABLE OF CONTENTS ASBTRACT ii TABLE OF CONTENTS iii LIST OF TABLES iv LIST OF FIGURES v ACKNOWLEDGEMENT vi INTRODUCTION 1 METHODS 10 Rearing 10 Somatic Growth Measurements 13 Oxygen Consumption and Q10 Measurements 13 Breath and Stroke Frequency 15 Data Analysis 16 RESULTS 19 Growth 19 Oxygen Consumption, Temperature and Q10 20 Allometry of Oxygen Consumption Rate with Mass 21 Stroke and Breath Frequency 22 DISCUSSION 23 Growth 23 Allometry of Oxygen Consumption Rate 29 Oxygen Consumption, Temperature and Activity 34 CONCLUSION 38 BIBLIOGRAPHY 56 iii LIST OF TABLES Table 1.1 Intraspecific exponents for leatherback turtles (Dermochelys coriacea) between 14 and 34 °C 53 Table 1.2 Qi 0 s of leatherback turtles 54 Table 1.3 Strokes per Minute (SPM) and Breaths per Minutes (BPM) of juvenile leatherbacks from 14 - 34 °C 55 iv LIST OF FIGURES Figure 1.1 Tethered leatherback hatchlings in tank 39 Figure 1.2 Carapace length measurements of leatherback turtles (Dermochelys coriacea) 40 Figure 1.3 Closed-System Respirometer 41 Figure 1.4 Daily variations in growth in leatherbacks turtles {Dermochelys coriacea) during development 42 Figure 1.5 Increase in mass of leatherback turtles {Dermochelys coriacea) with development. 43 Figure 1.6 Increase in carapace length of leatherback turtles {Dermochelys coriacea) with development 44 Figure 1.7 Log relationship between mass and carapace length of leatherback turtles {Dermochelys coriacea) 45 Figure 1.8 Effects of temperature on oxygen consumption (v0 2 ) 46 Figure 1.9 Log v 0 2 and mass relationship of leatherback turtles (Dermochelys coriacea) at 24 °C 47 Figure 1.10 Mean log v 0 2 a r | d mass relationship of leatherback turtles {Dermochelys coriacea) 48 Figure 1.11 Growth rate of leatherback turtles {Dermochelys coriacea) compared with some extant vertebrate and dinosaurs 49 Figure 1.12 Increases in body mass of leatherback turtles {Dermochelys coriacea) as compared with previous studies 50 Figure 1.13 Increase in carapace length of leatherbacks {Dermochelys coriacea) as compared with previous studies. . . . 51 Figure 1.14 Relationship between scaling exponent and temperature 52 v ACKNOWLEDGEMENTS First and foremost I would like to thank my advisor Dr. David R Jones for having confidence in me, as it was well known from the beginning that this project would be costly and uncertain since leatherback turtles before now were thought to be impossible to maintain in captive conditions. His guidance and wisdom throughout the project was invaluable. I would also like to give thanks to Manuela Gardener, Brian Bostrom and Andreas Fahlman of the Jones lab for help in animal care, data entry, analysis and editing of my thesis. I am grateful to Charles Darveau for guidance through all the statistical analyses. I would like to give special appreciation to Heather Flanagan, Jada Hastings and Seth Hastings for providing stability and balance in my life outside the walls of academia. They are the ones that gave me inspiration when I needed it the most. I cannot express enough appreciation to T.Todd Jones as he has been a mentor, a best friend, a brother, a lab mate, an office mate, a roommate, as well as my main research partner in this endeavour. A great extent of this work would not have been possible without his assistance and guidance as his background with rearing leatherbacks in the past was a key component of the success of this project. Also, this project would not have been possible without the help of numerous undergraduate volunteers for the tedious but thorough care of the leatherback turtles over the past two years. I thank UBC, NSERC, NMFS and the government of the British Virgin Islands for assistance in funding the project. Last, I would like to give special thanks to Arthur Vanderhorst and Sam Gopaul (for their assistance in animal husbandry and care); Bruce vi Gillespie and Vincent Grant (for providing mechanical help) and Chris Harvey-Clark for all his veterinary assistance. vii INTRODUCTION The leatherback turtle (Dermochelys coriacea) diverged from the lineage that gave rise to cheloniid marine turtles during the Cretaceous Period, some 100 -150 million years ago (Zangerl 1980; Pritchard 1997). Leatherbacks are the only living member of the family Dermochelyidae and the largest of all marine turtles, averaging 300 to 600 kg in body mass (Pritchard 1971) with some specimens weighing over 800 kg. Unlike the 6 other extant marine turtle species in the family Cheloniidae, the leatherback lacks a bony carapace, possessing instead a leathery outer skin with seven prominent longitudinal ridges. This leathery shell is about 4 cm thick in adults and made primarily of a cartilaginous matrix of connective tissue (Pritchard 1971). The non-keratinized shell, which allows the lungs to collapse when diving, is one of many adaptations that allow leatherbacks to be among the deepest diving air-breathing vertebrates, capable of dives exceeding 1000 meters in depth (Eckert et al. 1989). Cheloniid sea turtles are for the most part coastal-benthic dwellers where they feed primarily on sea grasses, marine invertebrates and crustaceans. Leatherbacks on the other hand feed primarily on pelagic gelatinous prey (Salmon et al. 2004) and are oceanic-pelagic throughout their lives (Bolten 2003). They undertake long-distance migrations and have the largest global range of all sea turtles, stretching from the tropics to the Arctic Circle (Standora et al. 1984) encompassing the two major oceans (Atlantic and Pacific). Dutton et al. (1999) using analyses of mitochondrial DNA control region 1 sequences determined that leatherback nesting populations in the Atlantic and Pacific have haplotype frequencies that are strongly subdivided, thus they are considered two distinct populations. A decline in numbers of adults as a result of fishing practices in both populations is now apparent. Over two decades ago (1982), there were 115,000 adult female leatherbacks worldwide; one decade later (1996) numbers had dropped to 34,500 worldwide (Spotila et al. 1996). It is estimated that there are fewer than 5000 nesting females remaining in the Pacific and that the population may be facing extinction (Spotila et al. 2000). The dramatic decline in the Pacific leatherback population is likely due to incidental by-catch by the.sword fishing industry along the South American coast (Eckert and Sarti 1997). Although numbers are higher in the Atlantic (-30,000), that population is also threatened as a result of fishing practices and by damage to natal beaches e.g. beach erosion, installation of artificial lighting, beach armoring, beach nourishment and beach cleaning as well as natural predation on hatchlings and human poaching of eggs and nesting females to obtain meat and oil. These activities led the 2000 IUCN Red List of Threatened Species to classify leatherbacks as "critically endangered". With perhaps only one out of every thousand hatchlings surviving to adulthood (Frazer 1986), the outlook for this species seems quite grim if better conservation efforts are not introduced in the near future. 2 Sea turtles disperse from nesting beaches after hatching and do not return to their natal beach until they are sexually mature adults. We have very little information about where they go or habitat utilization during the first few years of development, and this period is consequently referred to as the "Lost Years" (Carr 1982; Bolton 1995). The paths taken by leatherback hatchlings after they leave the beach are uncharted, but those of other species of sea turtles are linked to major ocean currents/gyres. After leaving their natal beach cheloniid hatchlings entrain in oceanic currents and feed on organisms in sargassum drifts for an estimated 10 years (Brongersma 1968; Carr 1986 & 1987; Bolten 1995). There has been no direct evidence that links leatherback hatchlings to oceanic gyres, which may indicate that they do not enter these currents like other sea turtle hatchlings. Since the hatchling and juvenile distribution as well as habitat requirements are virtually unknown for leatherbacks, it makes conservation efforts extremely difficult. Limited knowledge of distribution of juveniles has come from a handful of chance encounters/sightings at sea by fishermen, marine mammal stranding coordinators and sea turtle biologists (Eckert 2002). How can you protect a species that you have very little information about? Further frustrations exist in trying to conserve this fascinating species as growth rate data for juvenile leatherbacks in the wild are not available due to the fact that their distribution is unknown, making capture-recapture methods for measurements of growth impossible. Capture-recapture data in other marine turtles have shown that they reach sexual maturity between 20 - 30 years of age (Chaloupka and Musick 1997). Results from limited captive rearing 3 studies suggest that leatherbacks mature much more rapidly. Extremely rapid growth rate in captive leatherbacks have led to the speculation that these animals reach sexual maturity as quickly as 2-3 years (Deraniyagala 1936; Birkenmeier 1971; Witham 1977; Bels etal. 1988). Rhodin (1985) predicted an age at maturity of 3 - 6 years based on chondro-osseous morphology of leatherbacks, but more recent skeletochronological analyses suggest that leatherbacks could take as long as 13 -14 years (Chaloupka and Musick 1997). Obviously, more data is needed as age at maturity estimates are widely scattered. Rearing studies may help us clarify this important aspect of leatherback life history. Unfortunately, leatherback hatchlings are extremely difficult to maintain in captivity; for the following reasons; 1) failure to recognize physical barriers due to their ocean- pelagic lifestyle; 2) diet limitation, being exclusively gelativorous; 3) their high susceptibility to bacterial and fungal infections (Birkenmeier 1971; Foster and Chapman 1975; Bels et al. 1988). However, a few investigators have been successful in maintaining leatherback hatchlings in captivity (Deraniyagala 1936; Birkenmeier 1971; Foster and Chapman 1975; Phillips 1976; Witham 1977; Bels etal. 1988; Chan 1988; Jones etal. 2000), but any success in rearing leatherbacks beyond the post-hatchling stage has been limited to only one or two individuals. Growth of animals reared in captivity tends to be higher than those of their wild counterparts obviously due to an increase in resource availability (Avery 4 1994). Nonetheless, the unavailability of juvenile leatherbacks in the wild makes captive growth studies the only option for growth studies. Because of the difficulties in rearing leatherbacks, very little is known about their nutritional requirements. Past studies have fed animals anywhere from once daily to ad libitum on a variety of diets including squid, beef heart, French bread, jelly fish (Cassiopeia xamachana), fish, scallops and mussels, leading to much scatter in growth rate curves. Growth for the majority of vertebrates over time follows an S - shaped curve (sigmoidal; Erickson et al. 2001). The first stage, which is usually slow is referred to as the lag stage and is followed by a rapid growth stage at which maximal slope is observed until it plateaus terminating with the stationary stage (Erickson et al. 2004). The ultimate form of the S- shaped curve varies depending on the length of the three specific stages of development. However, in some ectothermic vertebrates a simple sigmoidal curve is not always seen, as unfavorable temperatures affect growth rates (Case 1978). However, rearing ectotherms under rigorously controlled conditions should allow us to see whether a sigmoid growth curve is expressed in leatherback turtles. As a result of their migratory pelagic existence, juvenile leatherback turtles may find themselves exposed to waters of widely varying temperatures and one obvious question is how smaller leatherbacks (hatchling and juveniles) deal with the effects of these changes in temperature. Larese-Casanova and Penick (1998) showed that day old leatherback hatchlings exhibited the typical 5 ectothermic vertebrate response of increasing metabolism with acute exposure to a range of temperatures from 20 - 35 °C (Q-io= 0.98 - 3.21). Interestingly, however, whole-animal metabolism was unaffected over the range of 20 - 35 °C, 5 days after nest emergence (Q10 = 0.80 -1.43), which may indicate some form of adaptation to the temperature range they are likely to encounter in their pelagic phase. On the other hand, Eckert (2002) used reports of visual sightings and incidental captures to show that leatherbacks do not move above ~30° latitude until they are > 80 cm in carapace length and do not move into water < 26 °C until larger than 100 cm in carapace length. This suggests that juvenile leatherback turtles are unable to venture into temperate waters despite a degree of thermal independence of metabolism suggested by Larese-Casanova and Penick (1998). On the other hand, are they restricted by their smaller body size? As part of my research, I helped develop techniques to rear leatherback hatchlings, so that investigation of critical aspects of energetics (growth, metabolic rate, thermal dependence of metabolism) could be measured. My research investigated the changes in routine metabolic rate in leatherbacks over two orders of magnitude in body size (0.1 -10 kg) at their acclimation temperature (24 °C), as well as after acute exposure to a much larger temperature range (14 - 34° C). 6 Previous investigators (Lutcavage and Lutz 1986; Wyneken 1997) have published metabolic rates on frenzy and post-frenzy leatherback hatchlings at 24 - 26 °C. Jones et al. (in press) looked at the changes in oxygen consumption, aerobic scope and energetic reserves at 24 - 26 °C from frenzy to > 1 - month of age and found RMR decreased significantly one week after emergence, but was unchanged to 4 weeks of age. However, there have been no measurements of oxygen consumption in leatherback hatchlings or reports of the effects of temperature change on oxygen consumption beyond the first four weeks after hatching. This study provides the first look at the effects of temperature on whole-body metabolism of juvenile leatherback sea turtles during growth. It also permits an investigation of the effects of size on metabolic rate of leatherbacks. Biological scaling can be described by the allometric equation MR = aM b (where MR = metabolic rate, a = y intercept, M = mass and b= mass exponent). A 3/4 power scaling of metabolic rate has been identified in several organisms (Kleiber 1932, Kleiber 1961; Schmidt-Nielson 1984). However, a lively debate still exists in the literature on the true value of b. Rubner in 1883 found that metabolic rate in dogs was proportional to body surface area and proposed that metabolism was confined by surface heat loss and therefore should scale with body mass raised to the power of 2/3 (Schmidt-Nielson 1984; White and Seymour 2002). A 2/3 power does not seem to be the value for homeotherms, however, and a 3/4 b value has been more widely accepted, as initially shown in the mouse to elephant curve of Brody et al. (1934). Additionally, recent work by West et al. 7 (1999) found supporting evidence for the 3/4 exponent was based on the fractal-like design of exchange surfaces and distribution networks found in plants and animals. On the other hand, consensus around the value of b does not appear to have been reached for studies on ectothermic vertebrates. In reptiles, for instance, an interspecific mass exponent of 0.80 or higher seems more usual (Bennett and Dawson 1976; Nagy 1982; Andrews and Pough 1985), but studies have reported mass exponents ranging from 0.43 -1.20 (Thompson and Withers 1997). It has been suggested that ectothermic vertebrates should have interspecific scaling exponents closer to 1 and not 0.75 because of thermoregulatory mechanisms or lack there of (Kooijman 1993). There has been very little done on the effects of temperature on the b value in reptiles and the present experiments looked into whether the b value changes with growth and development. This study provides us with the first look at intraspecific allometric scaling of V 0 2 in juvenile leatherbacks over two orders of magnitude in body mass as well as the effects of growth and temperature shock on the allometric relation. Until now, growth data in leatherbacks has been limited to N = 1 with growth estimates to maturity being vastly scattered. By making weekly measurements of body mass and carapace length, this study provides an estimate of time to maturity in leatherback turtles as well as an estimate of the age and body mass that they possibly venture into colder waters. Additionally, it 8 provides a new tool which will aid in calculating the mass of nesting adult leatherback turtles in the field, something that up until now has been very difficult to calculate. 9 METHODS Rearing Twenty hatchlings were collected from the island of Tortola in the British Virgin Islands (UK) and transported to the University of British Columbia, Vancouver, British Columbia, Canada in April of 2004 and 2005. All procedures were approved by the University of British Columbia's Animal Care Committee in accordance with guidelines set by the Canadian Committee on Animal Care. The appropriate import and export permit/certifications for the Convention on International Trade in Endangered Species (CITES) for the two countries (Canada and the British Virgin Islands) were obtained. Animals were reared at the South Campus Animal Care facility using protocols developed by Jones et al. (2000). Hatchlings were kept in 3 elliptical pools (5m long x 1.5 m wide x 0.3 m deep) filled with - 2500 L of seawater. The water was heated by eight water heaters and supplemented by a thermostatically controlled freshwater heat exchanger connected to the hot water supply of the building. Temperature was maintained at 24 ± 1 °C. Water quality for each pool was maintained by three systems: a biological filter (0.75m long x 0.75m wide x 0.75 deep), an ultraviolet filter (Aqua Ultraviolet 114 W UV water sterilizer) and a Red Sea Berlin Turbo XXL protein skimmer. Four (40 W UVA/B) fluorescent fixtures (Repti-Glow 8) suspended 0.5 m above each pool provided full spectrum radiation on a 12/12 cycle. The tanks also received ambient light. Tank water 10 was changed weekly with fresh sterilized seawater from the Vancouver Aquarium that was delivered to the facility by the City of Vancouver's Sanitation Department in an 8000 L water truck. Tanks were emptied, washed and disinfected with Quatricidep v before a water change. Water quality limits (pH = 8.0 to 8.3; salinity = 28 -33 ppt; and ammonia < 0.1 mg /1) were monitored daily. If pH or ammonia limits were exceeded, water was replaced immediately. If salinity levels were too high, fresh water was added to reduce salinity and if too low, sea salt was added to raise it. A small (1-cm2) piece of hooked Velcro™ was attached to the posterior portion of the hatchling's carapace with a few drops of cyanoacrylate cement (as the animals increased in body mass, so did the size of their Velcro™ patch). The corresponding piece of felt Velcro™ served as an attachment to a monofilament line (-20 cm long) on a swivel, fixed to a bar across the tank -10 cm above the water surface. Attaching the felt Velcro™ on the line to the patch on a hatchling's carapace, made a tether that confined the turtle to a proscribed section of the tank (Figure 1.1). Each hatchling could swim or dive in any direction, but was unable to contact other turtles or the tank bottom and walls. Leatherback hatchlings swim continuously and fail to recognize physical barriers (Birkenmeier 1972; Phillips 1976; Witham 1977; Davenport 1986) so repeated contact with tank walls abrades their skin which leading to infections and usually death (Foster and Chapman 1975; Jones et al. 2000). 11 Turtles began feeding 5-8 days after hatching (Jones et al. 2000; personal observations in this study). Animals were hand-fed strips of formulated food, underwater, three to four times daily to satiation from 1 to 5 cm below the water surface. The depth at which food was presented increased with body mass. The diet consisted of squid, vitamins (Reptavite™) and calcium (Rep-Cal™), blended with flavorless gelatin and hot water. Hatchlings were left undisturbed except during V 0 2 measurements, or while being weighed and measured (weekly), or treated (daily) for any external infections. Hatchlings with sores and bacterial/fungal infections were treated with povidone iodine (10 %) solution. If bacterial/fungal infections increased, antibiotics, (enrofloxacin 5 mg / kg; or amikacin 2.5 mg / kg) were administered daily until the infections had resolved. 12 Somatic Growth Measurements Carapace length, the distance from the center of the nuchal notch to the caudal peduncle (posterior of the carapace), was measured weekly using a digital caliper to the nearest 0.1 mm (Figure 1.2). Body mass was measured using electronic balances. An Ek-1200 A (Stites Scale Inc., 3424 Beekman Street, Cincinnati, OH 45223) was used to measure animals from birth to 1.2 kg to the nearest 0.1 g, while an ADAM CPW-60 (Dynamic Scales, 1466 South 8th StreetTerre Haute, IN 47802) was used to measure animals from 1.2 kg and above to the nearest 0.02 kg. Oxygen Consumption and Qi0 Measurements Routine metabolic rates (R0MR) were measured with a closed-system respirometer using methods described by Jones et al. {in press). The respirometer consisted of a large acrylic aquarium with a smaller acrylic aquarium fitted upside down inside the first creating a water sealed air space (Figure 1.3). The air space inside the square respirometer box was measured using a ruler and the volume calculated. The calculated volume was periodically verified by nitrogen dilution. As turtles increased in body mass, larger inner aquariums were used. Air was pumped through the oxygen analyzing equipment and back into the chamber at 300 cc per/min. 13 The inverted chamber was isolated from ambient air. The change in oxygen in levels starting from ambient air (20.94%) was determined continuously by pumping air through an oxygen analyzer (Beckman paramagnetic oxygen analyzer) and then back into the respirometry box. Water and C O 2 were scrubbed from the recirculating air by drierite and soda lime/ seawater, respectively, so C O 2 did not accumulate in the chamber during trials. Animals were tethered inside the respirometer box and thus were free to swim or bask inside the respirometer without hitting the tank bottom or walls. Smaller turtles 0.1 -1 kg were placed in the chamber for 30 minutes to acclimate to each acute temperature change (14-34 °C) before 30 minutes of measurements were started. Larger turtles (10 kg) were allowed up to 5 hours for acclimation. V 0 2 was only measured in 5 kg individuals at the acclimation temperature. Body temperature of 10 kg animals was measured intragastrically using a thermometer. Rates of heating and cooling of 10 kg leatherbacks with an initial body temperature of 24 °C and moved into water temperatures 10 degrees above (34 °C) or below (14 °C) were within 1 °C of water temperature within 2 hours for an increase and 5 hours for a decrease in water temperature. The temperature of the water in the respirometer was maintained using an electronic water heater in conjunction with a cooler, both regulated by an electronic thermometer that measured to the nearest 0.1 °C. Turtles were not fed upto 3 hours before starting a trial. Measurements occurred during daylight hours (9 am - 5 pm) to avoid any possible diurnal patterns/shifts. Trials were performed at four 14 different masses (0.1, 0.5,1 and 10 kg) encompassing a 2 order of magnitude change in body mass. Oxygen consumed was calculated as V 0 2 = ((((%02i - %O2f)/100)*VA)/to-te). Where % 0 2 i = percentage of oxygen in respirometer pre-trial, % 0 2 f = percentage of oxygen in respirometer at the end of the trial, VA = volume of air inside the respirometer and associated tubing, t0 = time at start of trial and te = time at end of trial. Breath and Stroke Frequency During the trials, breath and flipper stroke rates were recorded visually as an indication of activity. At the onset of a trial, breath and fore-flipper stroke rates were recorded for 1-minute and then for 1-minute at 5-minute intervals during the 30 minute trial. A flipper stroke was counted when the animal did a complete fore flipper limb cycle (downward and upward stroke; Davenport 1986). 15 DATA ANALYSIS Growth Body mass measurements were used to calculate a mean daily growth rate (% of body mass) for the previous seven days. Growth rate was calculated using the formula g = (M t - M 0 / Mo*t)*100, where g = mean daily growth rate as percent body mass, t = elapsed time between body mass measurements (days), Mo = initial mass, M t = mass after time t. Regression equations of carapace length and mass against time in weeks as well as a correlation of mass gain with carapace length were obtained. Oxygen Consumption and Qw JMP IN Version 4 Statistical Package (SAS Institute Inc. 2001) was used to carry out all statistical analyses. I used a One-Way repeated measure Analysis of Variance (ANOVA) to determine the effects of temperature (14, 19, 24, 29 and 34 °C) on routine metabolism (R0MR ml OVmin). Tukey test, with alpha value set at 0.05, was used to determine where the statistically significant differences occurred within significant effects having more than two levels. The same statistical protocol was used to determine if temperature (14, 19, 24, 29 and 34 °C) had an effect on both breath and flipper stroke rate. All One-Way ANOVAs were performed at 4 mass categories (0.1, 0.5, 1 and 10 kg) for all main effects (VO2, fa and flipper stroke rate). Body mass could not be tested as a 16 covariate as its distribution was discontinuous and non-normal. Therefore, I compared the changes in metabolism, breath and flipper stroke rate at each temperature for each mass category. N = 6 animals in all cases. I used simple linear regression to determine if relationships existed between V0 2 and increasing mass (as turtles aged) for all temperatures (14, 19, 24, 29 and 34 °C; n = 18 at all temperatures). An ANOVA was used to determine if differences existed in the slope (b) of the lines at the five temperatures (14, 19, 24, 29 and 34 °C) and when regressions were not found to have statistically different slopes (b) an ANOVA was used to determine if there were significant differences in elevation (y- intercept [a]) of the regressions. Again, a Tukey test (alpha value 0.05) was used to determine where significant differences lay in the slope (b) or elevation (a) among the regressions at the 5 temperatures. Also I looked at whether the (a) and (b) values were influenced by increasing maturity by using the values (at the acclimation temperature only) for size ranges from 0.1 -1 kg, 0.5 - 5 kg and 1 -10 kg. Once again, an ANOVA was used to determine if differences existed in the slope (b) and elevation (a). The change in rate of metabolism over a 10 °C change in temperature is defined as Qi 0 . Qio= (R2/ R1) 1 0 / V i , where R 2 and R1 are the rates at two temperatures T 2 and T-i. Q10 values were calculated over 5 °C increments along with an overall Q10 value from 14 - 34 °C. An ANOVA was used to determine if differences existed across both temperature ranges and size classes. Once 17 again, Tukey test (alpha value 0.05) was used to determine where significant differences lay in temperature ranges or size classes. 18 RESULTS Growth (Body mass and Carapace length) Only the 4 animals that survived for 1 year were used in the growth data analysis, so N = 4 for the data set. Body mass of leatherbacks emerging from the nest was 0.047 kg ± 0.01 (N = 4) and increased in mass by 4 + 0.34 % a day over the first week dropping to 2 + 0.07 % per day after 10 -15 weeks and settling around 0.75 + 0.11 % a day, through 52 weeks (Figure 1.4). Leatherbacks at the end of 12 months averaged 8.76 + 0.33 kg (N = 4). The relationship for mass gain (kg) over age (weeks) is shown in Figure 1.5 and is described by the equation y = 0.0043x2 - 0.0673x + 0.4352 (R2 = 0.99, F = 323.72, p < 0.001), where y = mass and x = time (weeks). Newly hatched leatherbacks had an average carapace length of 6.6 + 0.04 cm (N = 4). At the end of 12 months, animals had a mean length of 41.3 cm + 0.64 (N = 4) and had increased on average 0.63 + 0.031 cm per week over the entire period. The relationship between carapace length (cm) and age (weeks) is shown in Figure 1.6 and is described by the equation y = 0.668x + 5.3208 (R2 = 0.99, F = 2030.79, p < 0.001), where y = carapace length and x = time (weeks). The logarithmic relationship between mass (kg) and carapace length (cm) is given by the power equation y = 0.0002x2 8 4 4 (F = 1680.33, p < 0.001) (Figure 1.7), where y = mass (kg) and x = carapace length (cm). 19 Oxygen Consumption, Temperature and Q10 Mean oxygen consumption (Vo2) rate ranged from 0.34 to 25.68 ml 02/min for animals from 0.1 to 10 kg (at the acclimation temperature, 24 °C). As expected, there was a significant increase in Vo 2 with mass (F = 314.88, p < 0.001) (Figure 1.8 a-d). Vo 2 decreased with a fall in temperature to 14 °C and 19 °C from 24 °C for all mass classes 0.1, 0.5, and 1 kg, but only the rate at 14 °C was significantly lower, (p < 0.05) than at 24 °C. All turtles (0.1, 0.5,1 and 10 kg) showed no significant change in oxygen consumption between 19 and 24 °C (F = 20.828, p < 0.001: F = 15.902, p < 0.001: F = 17.045, p < 0.001, F = 11.289, p < 0.001 respectively). Increasing temperature from 24 °C to 29 °C resulted in a significant increase in Vo 2 for 0.5 and 1 kg animals, but not for 0.1 and 10 kg turtles. Further increases in temperature (29 °C to 34 °C) had no effect on the larger individuals (0.5, 1 and 10 kg); however, the smallest turtles (0.1 kg) had a significant increase in Vo 2. These relationships are shown in Figure 1.8 a - d. Significant differences for Q i 0 values only occurred at the 29 - 34 °C temperature range for the larger individuals (0.5, 1 and 10 kg) (F = 6.669, p < 0.05) (Table 1.1), in which the temperature increase had no, or even a retarding effect, on Vo 2. 20 Allometry of Oxygen Consumption Rate with Body mass The scaling of metabolic rate with mass (0.1-10 kg) varied with temperature (F = 17.83, p < 0.001). At 24 °C, metabolism scaled with body mass by the following equation y = 0.0058x 0 8 8 (R2= 0.99, F = 137.036, p < 0.001), where y = oxygen consumption and x = mass and 0.83 (b-value) represents the power or slope (on a log-log scale) and 0.0077 (a-value) is the y-intercept or elevation (Figure 1.9 a). The slope for 14, 19, 29 and 34 °C was significantly different than that for the scaling of metabolism with body mass at 24 °C (Figure 1.10; Table 1.2). The scaling of metabolic rate with body mass (0.1-10 kg) was broken into three sections at the acclimated temperature (24 °C); 0.1 -1 kg, y = 0.0079x 0 8 2(R 2 = 0.99, F = 74.75, p< 0.001), 0.5 - 5 kg, y = 0.0091x 0 8 3(R 2 = . 0.97, F= 143.57, p< 0.001) and 1 -10 kg, y = 0.0026x 0 9 8 (R2 = 0.99, F = 96.91, p < 0.001) (Figure 1.9 b,c, and d). Over the largest size range, the slope increased and the intercept fell accordingly. 21 Stroke and Breath Frequency Flipper stroke rate for leatherbacks (0.1, 0.5, 1 and 10 kg) was significantly influenced by temperature (14 - 34° C; F = 18.303, p < 0.001; F = 23.249, p < 0.001; F = 25.428, p < 0.001; F = 14.821, p < 0.001 for mass classes respectively). Tukey test (alpha level 0.05) showed that stroke rate increased significantly in the 0.1 kg animals from 14 -19 °C peaking at 56.1 strokes»min"1 at 24 °C and then decreased significantly with increasing temperature to 17.6 strokes-min"1 (29 °C) and 3.3 strokesvnin"1 (34 °C), (Figure 1.8 a). At 0.5 and 1 kg, animals showed similar results with the exception that stroke rate was not significantly different between 19 - 24 °C (Table 1.3; Figure 1.8 b and c). 10 kg individuals showed no significant change in stroke frequency from 14-24 °C. Stroke rate peaked at 36.1 strokes*min"1 at 24 °C and then decreased significantly with increasing temperatures to 25.3 strokes»min"1 (29 °C) and 12.4 strokes'min"1 (34 °C), (Figure 1.8 d). fa in leatherbacks (0.1, 1 and 10 kg) remained stable with increasing temperatures from 14 - 34 °C (F = 1.385, p = 0.268, F = 2.408, p = 0.077, F = 0.83, p = 0.523 respectively) (Figure 1.8 a, c and d; Table 1.3). The 0.5 kg leatherbacks showed significant differences in fa with an increase in temperature (14-34 °C) (F = 9.191, p < 0.001), but Tukey test (alpha level 0.05) revealed that fa was only significantly higher at 24 °C with no differences across the other temperatures (14, 19, 29 and 34 °C) (Table 1.3; Figure 1.8 b). 22 DISCUSSION Growth Leatherbacks are critically endangered with current population trends in the Pacific indicating that they are nearing extinction (Spotila era/. 2000). Measurements of somatic growth in leatherbacks in the laboratory could help in our understanding of their growth and population dynamics in the wild (Chaloupka and Musick 1997). The validity of captive growth data in the past has been questionable as many researchers have been unsuccessful in maintaining N > 1 for more than 100 days (Deraniyagala 1939, 662 days; N = 1; Birkenmeier 1971, 203 days; N = 1; Phillips 1976, 136 days; N = 1; Witham 1977, 642 days; N = 1 and Bels era/. 1988, 1200 days; N = 1) whereas, this research has allowed successful rearing of 4 animals through their first year of life. All vertebrates usually display a S-shaped curve (sigmoidal) growth patterns during neonatal development (Erickson et al. 2001). The first stage, which is usually slow, is referred to as the lag stage and is followed by a linear exponential growth stage at which maximal slope is observed until the curve plateaus in what is termed as the stationary stage (Erickson et al. 2004). The shape of the S-curve varies depending on the length of the 3 stages of development. Some animals may have a long lag stage followed by a rapid exponential stage. Conversely, others may have a short lag and exponential phase attaining maturity much faster. As mentioned earlier, leatherbacks remain 23 entirely pelagic throughout their development which increases the risk of predation, thus it would be advantageous for leatherbacks to have a short lag and exponential stage to reach mature size as quickly as possible. Growth data for the current study only encompassed the first year of development, but it is quite apparent that leatherbacks grow at a very rapid rate (Figure 1.5). Extrapolation of the data beyond recorded data has determined that captive reared leatherbacks could possibly reach mature size (~250 kg) in as little as 5 1/4 to 6 years (5000-fold increase from birth). Results here show that leatherbacks do not grow like other reptiles (which grow slowly and gradually, through life), but grow to adult size rather quickly, similar to altricial birds and mammals (Figure 1.11) and much faster than current estimates for hard shell turtles (~20 years) (Chaloupka and Musick 1997). Erickson et al. 2001 using bone histology and scaling principles estimated that dinosaurs (100 - 1000 kg) grew at rates (93 - 786 g day"1) typical of precocial birds. The daily growth rate (117 g day"1) derived for leatherback during the current study is toward the low end but nonetheless within this range. Skeletochronological analyses of sclerotic ossicles (a bony element in the sclera of the eye) have shown that leatherbacks may reach maturity in 13 -14 years with a minimum age to maturity of 5 - 6 years (Chaloupka and Musick 1997). However, the current estimation of age for leatherbacks to reach maturity, obtained by this study," fits incredibly well with Chaloupka and Musick (1997) minimum value. However, a validation study of age and growth using 24 skeletochronology conducted in green turtles (Chelonia mydas) by Bjorndal etal. (1998) concluded that this was not a valid technique for estimating age in sea turtles as bone growth (humerus) was not significantly correlated with carapace length growth. Swingle etal. (1993) observed rapid growth rates in captive reared loggerhead sea turtles (Caretta careatta) (mean weight of 10.3 to 17.6 kg at 1.5 years of age with one exceptional turtle reaching 20 kg) and estimated a potential age to maturity of 6 to 7 years. Loggerhead sea turtles, Caretta caretta, average mass at maturity is 65 - 75 kg (Spotila 2004) compared with approximately 250 kg in leatherbacks (Eckert and Eckert 1985). Therefore leatherbacks are growing at a much higher rate to reach maturity in 5 Yz to 6 years. In general, reptiles in captivity tend to grow at much faster rates than their wild counterparts (Avery 1994), so age at maturity for leatherbacks in this study is almost certainly to be an underestimate of time to maturity in the wild. Figure 1.5 shows that leatherback hatchlings increase from an average size of 0.05 kg to 8.76 kg in 12 months which represents a 180 - fold increase in body mass. The lone surviving leatherback during 2005 survived for 1 Vz years and at a year had increased approximately 150 - fold in mass (Figure 1.12). Previous rearing studies (Birkenmeier 1971; Phillips 1976 and Witham 1977) have all reported rapid growth (4.7 kg in 203 days, 1 kg in 136 days, 27.7 kg in 642 days, respectively). 25 Body mass and carapace length data from this study were compared with published literature values and with the exception of Witham (1977), were very similar (Figures 1.12 and 1.13). Witham's hatchling was approximately 900 g by week 5, compared with 120 g in my study, and by week 25 approximately 10.5 kg (compared with 1.47 kg in this study). Growth at 52 weeks (8.76 kg) for the current study has yet to surpass the mass of Witham's animal at 25 weeks (10.5 kg). Witham fed his turtles ad libitum jellyfish (Cassiopeia) fortified with vitamins and minerals, but the growth rate observed is questionable. It is unlikely that any animal could increase in mass that quickly from birth under any conditions, particularly during the first few weeks of development when animals are going through chemical and biological changes. Birkenmeier (1971) showed that captive reared turtles reared on mussels exhibited daily percent increase in body mass of 2.75 % M b/d, and possessed a carapace length of 40 cm at 30 weeks of age. This rate is slightly higher than that of the current study (2.01% Mb/d and 28 cm) at week 30 (Figure 1.13). Nutrition may have contributed to the difference as Birkenmeier used a diet consisting of mussels which has a much higher kilocalorie (Kcal), fat and carbohydrate content (100, 300 and 400 % more, respectively) as compared to the squid and gelatin based diet used in the current study. Northern temperate zones and even sub polar temperate regions have long been known to be major feeding grounds for adult leatherbacks that forage primarily on gelatinous zooplankton (Ernest and Frazer 1983; Davenport and 26 Balazs 1991). Eckert (2002) using sighting data hypothesized that leatherbacks do not venture into temperature zones until they are at least 100 cm in carapace length. The data in Figures 1.5 and 1.6 show that leatherbacks would reach 100 cm carapace length in approximately 3 years and would have a body weight of approximately 90 kg (value based on extrapolating curves beyond recorded data). If my extrapolations are correct about the length of time to maturity in leatherbacks (6-7 years) then, from a conservation view point this would be extremely useful in trying to save this species from extinction. Having such a rapid growth to maturity compared with other sea turtles, which take 20 - 25 years, would allow leatherback populations to rehabilitate much faster. Consequently, a short term moratorium on egg harvesting, development of nesting beaches and the sword fishing industry would jump start the process of replenishing leatherback populations. As a result of the leatherbacks' rapid growth, moratoriums or any other conservation strategies could be implemented on a short term basis which would meet much less resistance from the community or commercial operations that would be directly affected by new laws or regulations. The current study also highlighted the current belief that it is difficult, if not impossible, to successfully rear more than one leatherback hatchling in captivity as four leatherbacks hatchlings have been reared for a year. Leatherback hatchlings can be collected on nesting beaches, or hatched in the laboratory and 27 after a year can be released into the environment. Hopefully, this would reduce the high levels of predation in early life stages giving leatherbacks a much higher change of attaining adulthood. Captive reared animals are prone to grow faster than their wild counterparts, but nevertheless, the log relationship for mass and carapace length (Figure 1.7) scaled to the power equation y = 0.0002x2 8 4 4 . Scaling to the power of almost 3 (2.844) is what one would expect to find in growing animals. Any three dimensional object is expected to scale to length as M 1 / 3 , surface area as M 2 / 3 and volume as M 1 °, where M = mass (Damuth 2001). Mass is proportional to volume, and volume is proportional to length3 thus mass is proportional to length3. The relationship for mass and length obtained during the current study fits extremely well to this relatively simple mathematical formulation. Oxygen Consumption: effects of body mass and temperature It has been a central assumption in my study of the effects of temperature shock that the acclimation time was adequate for the animal's body temperature to reach that of the experimental temperature. I assumed that a 30 minute exposure period for 0.1 -1 kg turtles was sufficient for the turtle's core body temperature to attain that of the acutely applied temperature. Seebacher and Shine (2004) using a theoretical model for reptiles showed that a 1 kg animal in air would take approximately 30 minutes to reach equilibrium for a 20 °C change 28 in temperature, whereas my animals were in water and were only exposed to a maximum temperature change of 10 °C. Body temperatures of the 10 kg animals were measured intragastrically using a thermometer so their body temperatures were at the water temperature before trials began. The relationship of metabolism to body mass to in ectotherms is reasonably well established (Bennett and Dawson 1976): The intraspecific mass scaling exponent obtained in this study at the acclimation temperature (24 °C) was 0.88 and is within the range described by several previous investigators on reptiles (Hughes et al. 1971, aldabra giant tortoise (Geochelone gigantean) - 0.82, 21-26 °C; Bennett and Dawson 1976, 10 species of aquatic turtles and 26 species of lizards - 0.86, 20° C and 0.83, 30 °C respectively; Prange and Jackson 1976, green sea turtles (Chelonia mydas) - 0.83, 23 - 27 °C; Southwood etal. 2006, green sea turtles (Chelonia mydas) - 0.89, 25 - 28°C). It is interesting to note that when the relationship between V 0 2 and body mass (0.1 -10 kg) at 24 °C was broken down into different sections, each encompassing an order of magnitude increase in body mass (0.1 -1 kg, 0.5 - 5 kg and 1-10 kg), the scaling exponent was higher for the largest range then for the two smaller size ranges (0.83 - 0.98, Figures 1.9b- d). The increase in slope was dominated by an almost 3 times decline in the intercept which was much larger than the 1.2 times increase in the exponent. Obviously it is crucial for allometric determinations to be made in the next mass range (0.5 - 50kg) before an explanation can be attempted. 29 Several studies of interspecific and intraspecific allometry of metabolic rates in reptiles have reported mass exponents ranging from 0.43 -1.20 (Bartholomew and Tucker 1964; Wood et al. 1978; Andrews and Pough 1985; Thompson and Withers 1992; Thompson and Withers 1997; Maxwell era/. 2003; Zaidan 2003). Reasons for the variability in mass scaling exponents in reptiles are unclear. As seen above, scaling exponents change depending on the developmental stage measured, increasing as animals mature. Sample size, limited range of body masses studied as well as the distribution of data selected (i.e. if more smaller animals are used compared with larger animals) have all been known to affect the regression curve by increasing or decreasing the exponent value (Maxwell et al. 2003). When determining scaling exponents it is extremely important to take all the above factors into consideration to avoid reporting values that may not be accurate. Predictions of energy requirements of animals are determined by scaling exponents and differences could have large impacts on these estimates. Intraspecific scaling exponents have been reported for three other species sea turtles. Prange and Jackson (1976) reported an exponent of 0.83 (minimum metabolic rate) and 0.94 (maximal metabolic rate) in green sea turtles (Chelonia mydas) (0.3 -141.2 kg) at temperatures 23 - 27 °C, Southwood et al. (2006), an exponent of 0.89 in green sea turtles (Chelonia mydas) (0.03 -15.3 kg) at 25 -28 °C and Hochscheid et al. (2003) an exponent of 0.35 for loggerhead turtles (Caretta caretta) (2 - 60 kg) seasonally acclimated to temperatures of 27.1 to 15.3 °C. Results presented here (0.88) are similar to Prange and Jackson 30 (1976) and Southwood et al. (2006), but much higher than that reported by Hochscheid etal. (2003). As suggested by Hochscheid etal. (2003) it is possible that there are real species differences in the metabolic consequences of growth and body size for V 0 2 . Heusner (1982 a&b) suggested that the constitution of the allometric equation was a product both of changes in the intercept and exponent. During the current study, acute changes in temperature (14-34 °C) affected both the intercept and exponent of V 0 2 - body mass regression curves (Figure 1.10) but only at the temperature extremes. Over the temperature range from 19 to 29 °C the scaling exponents and intercepts were simi;lar. However, the values recorded at 14 and 34 °C did not follow that trend. The exponent declined from 0.93 to 0.77 while the intercept increased by almost an order of magnitude (Figure 1.14). The explanation lies in the effects of extreme temperatures (14 and 34 °C) on metabolism. In the smallest animals, Q-inof 3.3 was observed in the 14 to 19 C temperature range while in the largest animals Qi 0 was only 2.3. Similarly, in the smallest creatures, Q i 0 was 3.4 in the 29-34 range while it fell to 0.5 in the largest. Obviously these effects on metabolism at the extremes of the temperature ranges can be explained by influences on both the intercept and exponent. For instance, the relatively greater fall in metabolism in the smallest animals compared with the larger will decrease the intercept and increase the slope at the lowest temperature. At the highest temperature, the relatively greater increase in metabolic rate in the smallest animals compared with the marked decline in the largest will raise the intercept and thereby decrease the 31 slope. In some respects, therefore, the changes in the allometric relation may be more a product of discontinuous nature of the data than a description of God's purpose. The effects of temperature on scaling exponents have not been well studied and the few investigations there are have given highly variable results. Dmi'el (1972) found that the mass exponent (b) was temperature dependent in snakes (acclimated at 29 °C, measurements between 20 - 30 °C), but Chappell and Ellis (1986) who also worked on snakes (acclimated at 30 °C, measurements at 20, 30 and 34 °C) found no such evidence. This discrepancy further highlights the paucity of information on the effects of temperature on scaling exponents in reptiles which is surprising since temperature is a major determinant of metabolism rate in ectotherms. Temperature effects add to an already great variation among allometric relationships in reptiles so it would be foolhardy to attempt to derive a universal mass exponent for all reptiles (Andrews and Pough 2003). Accurately determining the metabolic rates of the individuals in one species from the data derived from another species due to species-specific differences in the mass exponent and intercept cannot be done (Jacobson 1996); hence one should be only use an intraspecific mass exponent when extrapolating allometric data to determine energetics or antibiotic dosages. 32 It is well established that reptiles are highly temperature dependent (Schmidt-Nielsen, 1997), and oxygen consumption levels in reptiles increase with temperature as it directly affects metabolism through its effects on the rates of biochemical reactions (Gillooly et al. 2001) yet little is known about temperature effects on oxygen consumption in sea turtles. Only, two studies have directly looked at the relationship between temperature and metabolic rate in immature animals (Lutz et al. 1989; Hochscheid etal. 2003). Lutz etal. (1989) found a Q 1 0 of 2.4 in loggerhead turtles acclimated for two days to temperatures ranging from 10 - 30 °C and Hochschied etal. (2003) reported an overall Q-io of 5.4 in loggerhead turtles that were acclimated seasonally from summer to winter (25.4 -15.7 °C). My leatherbacks (0.1-10 kg) acutely exposed to temperatures from 14 - 34 °C had an overall Q10 of 2.0 -1.4, with the highest value at the smallest mass (Table 1.2). . Q10 values have been reported to be in the range of 2-3 for reptiles (Bennett and Dawson 1976; Glass and Wood 1983). In the current study, Q i 0 values (14 - 34 °C) for the current study are slightly lower than reported for reptiles with the highest levels occurring in the smallest subjects. Nevertheless, it is perhaps foolhardy to use a global value for Q i 0 when tests may be being perfomed outside of the animals tolerable limits. For instance, a Q10 of 3.3 occurred in the smallest animals over the temperature range from 14 -19 °C implying an extreme depression of metabolism at 14 °C similarly, in the largest animals, Q i 0 of 0.5 occurred over the range from 29 - 34 °C again indicative of pronounced metabolic depression. Over the temperature range from 19-29 °C, 33 Qio were in a much more restricted range from 1.4 to 2.8 which suggests that this range encompasses the tolerable limits for juvenile leatherbacks. Nevertheless, the current data suggests a thermal dependence of temperature from 14 - 34 °C in juvenile leatherbacks (0.1 -10 kg). Although is has been suggested by Larese-Casasnova and Penick (1998) that 5 day old hatchlings express thermally independent metabolism from 20 to 35 °C (Qio= 0.80 - 1.43) that is not supported by the present data. 5-week old hatchlings (0.1 kg, current study) displayed a thermal dependence of metabolism across a similar temperature range of 14 to 34 °C (global Q1 0= 2.0 ±0.1) and it seems unlikely that 5 day old hatchlings could have displayed independence of metabolism. It is possible that juvenile leatherbacks may develop an enzyme (or isozymes) that functions widely across temperatures, but the current data suggests a thermal dependence of temperature from 14 - 34 °C at least until animals are 22 weeks of age. Evidence presented by Eckert (2002) showed that juvenile leatherbacks are > 100 cm before venturing into colder waters, so it is fair to assume that a 10 kg leatherback would not be capable of maintaining a significant thermal gradient at lower temperatures. Estimations derived during the current study show that at a carapace length of > 100 cm (possible length when they show up in temperate waters), leatherbacks are approximately 90 kg. This mass (90 kg) may be the key size at which leatherbacks are thermally capable of venturing into colder waters by maintaining a thermal gradient over that of T a. It is interesting to note 34 that the mass of all leatherback turtles in studies showing that leatherbacks could thermally elevate T b gradients over T a in temperate waters (Friar et al. 1972 = 18 °C above T a; James and Mrosovsky 2004 = 8.2 °C above T a; Standora et al. 1984 = 3.4 and 8.3 °C above Ta) have all been 100 kg or greater. Lutz et al. (1989) acclimated animals for two days prior to measurements and still had values similar to this study (Qi 0 = 2.4). Bennett and Dawson (1976) reported that the estimated duration time necessary to induce acclimation in reptiles is 2 - 3 weeks and in many cases longer. It is very difficult to speculate what the results would have yielded if the animals were acclimated for > 3 -weeks to each temperature, although we can get some idea from the results of Southwood et al. (2003). Southwood et al. (2003) showed that there was no significant difference in V 0 2 between summer (26 °C) and winter (17 °C) conditions, but there was a moderate 24 - 27 % decrease in oxygen consumption during winter conditions compared with summer conditions suggesting acclimation possibly through increased levels of pyruvate kinase and lactate dehydrogenase. Stroke frequency for all size classes across the temperature range (14 -34 °C) showed stroke rates to be highest at 24 °C "acclimation temperature. Deviations above or below the acclimated temperature resulted in a decrease in stroke frequency (Figure 1.8 a - d, Table 1.3). There was no correlation between stroke frequency and V0 2 . 35 Sea turtles increase oxygen uptake at the lungs through an increase in respiratory frequency, tidal volume and increased oxygen extraction efficiency. (Lutcavage and Lutz 1997). Sea turtles are known to have highly variable tidal volumes which are strongly influenced by the physical conditions under which they are measured (Lutcavage et al. 1989). Figure 1.8 a - d, shows the relationship for /R»min"1 and V 0 2 across all temperatures at each mass class. Although breathing frequency remained unchanged as temperature increased V0 2 values increased suggesting that individuals may possibly be using tidal volume or oxygen extraction efficiency to change V 0 2 with increasing temperature. By increasing their heart rate, it is possible that the animals are able to maximize gas exchange and O2 loading during ventilation (Southwood 1997). Unfortunately, tidal volume was not recorded for the current study. As mentioned previously, leatherback hatchlings swam continuously during trials, which is why I used R 0MR rather than RMR as animals were not as rest. Once entering the ocean newly emerged leatherbacks are in a highly energetic phase termed a frenzy (Carr and Hirth 1961) which typically lasts for about 24 hours (Wyneken and Salmon 1992). Beyond the frenzy period leatherbacks enter a post frenzy state (routine swimming) during which they swim continuously with activity being more prevalent during the day (Wyneken and Salmon 1992). Wyneken 1997, Lutcavage and Lutz 1986 and Jones et al. (in press) reported post frenzy mass specific metabolic rates between 24 - 26 °C for leatherback hatchlings of 0.0040, 0.0047 and 0.0041 ml/g.min respectively. The mass specific metabolic rate in the current study at 24 °C (0.0035 ml/g*min) 36 was slightly lower. This minimal difference may be a result of animals reducing their activity (swimming) as they get older as the metabolic rate derived for the current study are for 5 week old individuals. Additionally, there may be scaling differences, as 5 week old hatchlings are approximately 100g compared with 60g at 1 week. When comparisons were made with the only known FMR recorded leatherback turtles by Wallace et al. 2005 (0.20 - 0.74 W kg"1), the current study's extrapolated (Figure 1.9 a) metabolic rate for an adult leatherback (250 kg)was 0.81 W kg"1, is slightly higher than the highest value reported by Wallace et al. 2005. Extrapolation beyond the recorded data can be misleading as an animal's biochemistry can change as they develop, but nevertheless, although slightly higher, the extrapolated values are in the same range. Lutcavage and Lutz (1986) using their leatherback V O 2 data along with the calorific content of jellyfish calculated that an adult leatherback (~250 kg) would have to consume its body mass in jellyfish to satisfy its daily energy requirement; however this assumed scaling hatchling metabolism to 1. Using the intraspecific scaling exponent of 0.88 derived in the current study and using the same computation as Lutcavage and Lutz (1986) for caloric content of jellyfish, an adult leatherback (~250 kg) would only require the energetic equivalent of approximately 74 kg (-1/3 its body mass) of jellyfish daily to satisfy energy requirements. Nevertheless, as pointed out earlier, the exponent was increasing througout development although the intercept was falling. Obviously, a re-37 examination of leatherback energy expenditure in the field is required before conservation measures are put into effect to ensure the survival of this species with respect to resource availability and energy allocation (growth, fecundity) (Jones et al. 2004). Conclusion For many years, researchers have and still consider leatherbacks unique among all other sea turtles and reptiles because of their larger global ventures into temperate waters. The current study has demonstrated that thermal dependence of metabolism is still apparent in leatherbacks at 10 kg and that 90 kg may be the key size at which leatherbacks are thermally capable of venturing into colder waters. The results also suggest that leatherbacks are capable of achieving maturity within 5 Vz to 6 years increasing their body mass 5000 - fold from birth. So are leatherbacks just another sea turtle? Yes! They just grow faster and are much larger. 38 Tethered leatherback hatchlings in the holding tank. 39 Figure 1.2 Carapace length measurements of leatherback turtles (Dermochelys coriacea). 40 Figure 1.3 Closed-System Respirometer. 41 Figure 1.4 Variation in daily growth rate (% of body mass) in leatherbacks during development [Dermochelys coriacea) at 24 °C. (N=4) 42 Figure 1.5 Increase in mass of leatherbacks (Dermochelys'coriacea) with development. (N=4) 43 50 -, 5 0 1 • , , , , , 0 10 20 30 40 50 60 Age (weeks) Figure 1.6 Increase in carapace length of leatherbacks (Dermochelys coriacea) with development. (N=4) 44 Figure 1.7 Logarithmic relationship between mass and carapace length of leatherbacks (Dermochelys coriacea). (N=4) 45 fR • mirr1 Strokes • mirr1 (Flipper) fR • min-1 Strokes • min-1 (Flipper) o 7a a s 01 a (u|ui/!o It") Z 0 A fR • mirr1 Strokes • mirr' (Flipper) o 2 D. E (u|ui/ !o |UJ) Z 0 A fR • mirr1 Strokes • mirr1 (Flipper) (UIUI/*O |iu) J 0 A (u!Ui/Jo |w) z OA Figure 1.8 a - d Effects of temperature on Oxygen consumptions ( v 0 2 ) i n leatherback turtles (Dermochelys coriacea) at 0.1, 0.5,1 and 10 kg with Strokes*min"1 (flipper) and fR'min"1 as an indicator of activity. 46 O T~ T-Figure 1.9 a - d Log - mass relationship of leatherback turtles (Dettmchelys coriacea) at 24 °C 47 Figure 1.10 Mean log metabolism - mass relationship of leatherback turtles (Dermochelys coriacea) at 14,19,24,29 and 34 °C. * Regression curve power equations and R 2 are based on scatter plot and not the mean data displayed on graph. 0 48 10000 1000 100 10 0.1 0.01 • A • Dinosaurs Leatherbacks Precocial birds Reptiles Eutherians Altricial birds 10 100 1000 10000 Body Mass (g) 100000 1000000 Figure 1.11 Growth rate of leatherback turtles (Dermochelys coriacea) compared with some extant vertebrates and dinosaurs. Data for dinosaurs and extant vertebrates are modified from Erickson et al. (2001). 49 Figure 1.12 Increases in body mass of leatherback turtles [Dermochelys coriacea) as compared with previous studies. 50 50 n E o 45 40 35 30 -| 3 25 o> o « o. 2 ra O 20 15 -10 -5 0 • CD CCD oca ,ooco • Current Study (2005-2006) N=4 • Birkenmeier (1971) N=1 O Current Study (2004-2005) N=1 10 20 30 40 Age (weeks) 50 60 70 Figure 1.13 Increases in carapace length of leatherback turtles (Dermochelys Coriacea) as compared with previous studies. 51 1.00 0.95 g 0 9 0 c o Q . UJ 0.85 H J> 0.80 0.75 0.70 — i — 14 19 24 Temperature (°C) 29 — i — 34 Figure 1.14 Relationship between scaling exponent and temperature in Leatherback turtles (Dermochelys Coriacea). 52 Qio Temperature Range (°C) 0.1kg 0.5 kg 1kg 10 kg 14-19 3.3 ± 1.7 3.3 ±0.5 1.6 ±0.2 2.3 ±0.5 19-24 1.8 ±0.4 1.5 ±0.2 1.9 ± 0.1 2.7 ±0.5 24-29 1.6 ±0.5 2.8 ± 1.0 2.4 ±0.4 1.4 ±0.2 29-34 3.4 ±0.8 *1.1 ±0 *1.1± 0.2 *0.5±0.1 14-34 2.0 ±0.1 1.8± 0.1 1.7 ± 0.1 1.4 ±0.1 Table 1.1 Qio of leatherback turtles (Dermochelys coriacea) exposed to sudden temperature shock at 5 °C increments. * (indicates areas of significance across both temperature range and size class). 53 Temperature (°C) a-value b-value R2 F-value P-value 14 0.0019 0.93 0.97 490.19 < 0.001 19 0.0047 0.86 0.98 109.18 < 0.001 24 0.0058 0.88 0.99 137.04 < 0.001 29 0.0055 0.92 0.97 181.90 < 0.001 34 0.0163 0.77 0.99 83.11 < 0.001 Table 1.2 Intercepts (a-value) and the exponents (b-value) for the allometric analysis of V02 & M b between 14 and 34 °C. 54 Strokes* min"1 Temp. 0.1 kg 0.5 kg 1 kg 10 kg 14 °C 24.1 ±5.2 32.5 ±2.3 29.4 ±3.1 28.3 ± 1.1 19 °C 40.8 ±2.3 44 ± 1.6 42.6 ± 1.4 33.2 ±2.2 24 °C 56.1 ±3.4 53.3 ± 1.1 45.7 ±3.4 36.1 ±2.5 29 °C 17.6 ±7.9 30.6 ±7.9 17 ±3.8 25.3 ±3.7 34 °C 3.3 ±2.9 3.7 ± 1.8 8 ±3.9 12.4 ± 1.7 fR» min'1 Temp. 0.1 kg 0.5 kg 1 kg 10 kg 14 °C 1.5 ±0.4 1.5 ±0.3 2.3 ±0.2 2.4 ±0.5 19 °C 2.3 ±0.6 2.9 ±0.4 1.9 ±0.3 3.2 ±0.6 24 °C 2.1 ±0.6 4.2 ±0.6 2.3 ± 0.3 3.8 ± 1.0 29 °C 1.4 ±0.2 1.8 ±0.3 1 ±0.1 2.8 ±0.2 34 °C 1.1 ±0.1 1.8 ±0.1 2 ±0.2 2.8 ±0.5 Table 1.3 Influence of temperature (14 - 34 °C) & M b on Strokesmin"1 and fRmin" 1 (+ S.D.) of juvenile leatherback turtles. 55 BIBLIOGRAPHY Andrews, R.M. and Pough, H. 1984. Metabolism of squamate reptiles: Allometric and ecological relationships. Physiological Zoology 58(2): 214-231. Avery, R.A. 1994. Growth in Reptiles. Gerontology 40:193-199. Bartholomew, G.A. and Tucker, V.A. 1964. Size, body temperature, thermal conductance, and heart rate in Australian varanid lizards. Physiological Zoology 37: 341-354. Bels, V., Rimblot-Baly, F. and Lescure, J. 1988. Croissance et maintain en captivity de la torte luth, Dermochelys coriacea (Vandelli 1761). Revue Francaise d'Aquariologie 15(2): 59-64. Bennett, A. F. 1988. Structural and functional determinates of metabolic rate. American Zoologist 28: 699-708. Bennett, A. F. and Dawson, W.R., 1976. Metabolism. In: Biology of the Reptilia. Physiology A. Vol. 5 (eds. C. Gans and F.H. Pough), New York Academic Press, pp. 127-223. Birkenmeier, E. 1971. Juvenile leatherback turtles, Dermochelys coriacea (Linnaeus), in captivity. Museum Journal 3(1): 160-172. Bjorndal, K. A., Bolten, A. B., Bennett, R. A., Jacobson, E. R., Thomas, J. , Baleski, J . J . and Eliazar, P. J. 1998. Age and growth in sea turtles: Limitation of skeletochronology for demographic studies. Copeia 23-30. Bolten, A. B. 1995. Biology of the early pelagic stage the 'lost year'. Biology and Conservation of Sea Turtles. (Revised Edition). Smithsonian Institution Press. Washington, D.C. and London, pp. 579 -581. Bolten, A.B. 2003. Variation in sea turtles life history patterns: neritic vs. oceanic development stages. In: The Biology of Sea Turtles Volume II. (ed. P. Lutz, J. Musick , J Wyneken). CRC Press, Boca Raton, pp. 243-257. Bostrom, B. and Jones, D.R. 2006. Exercise keeps adults leatherbacks warm. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology. In Press. Brody, S. Procter, R.C., and Ashworth U.S. 1934. basal metabolism, endogenous nitrogen, creatinine and neutral sulfur excretions as functions of body weight. University of Missouri Agric. Exp. Sta. Res. Bull. 220: 1-40. 56 Brongersma, L. D. 1968. Notes upon some turtles from the Canary Islands and from Madiera. Koninkl. Nederl. Akademie van Wetenschappen Proceeding Series C71: 128-136. Carr, A., 1986. Rips, fads and little loggerheads. Bioscience 36(2): 92-110. Carr, A., Hirth, H. 1961. Social facilitation in green turtle hatchlings. Animal Behavior 9: 68-70. Cartland, L.K. and Grimmond N.M. 1994. The effect of temperature on the metabolism of juveniles tuatara, Sphenodon punctatus. New Zealand Journal of Zoology 21: 373-378. Chan, E. H. 1988. A note on the feeding of leatherback Dermochelys coriacea hatchlings. Pertanika 11(1): 147-149. Chaloupka, M.Y. and Musick, J.A. 1997. Age, Growth, and Population Dynamics, In: The Biology of Sea Turtles, (ed. P. Lutz, J , Musick). CRC Press, Boco Raton, FL. pp. 233-276. Chappell, M.A. and Ellis, T.M. 1987. Resting metabolic rates in boid snakes: allometric relationships and temperature effects. Journal of Comparative Physiology B 157: 227-235. Davenport, J . 1986. Locomotion in hatchling leatherback turtles Dermochelys coriacea. Journal of Zoology London 212: 85-101. Davenport, J. , Holland, D. L., and East, J. 1990. Thermal and biochemical characteristics of the lipids of the leatherback turtle Dermochelys coriacea: Evidence of endothermy. Journal of Marine Biological Association UK: 70. Davenport, J. , Ingle, G. and Hughes, A.K. 1982. Oxygen uptake and heart rate in young green turtles Chelonia mydas. Journal of Zoology (London) 198: 399-412. Deraniyagala, P.E.P. 1936. Some postnatal changes in the leathery turtle Dermochelys coriacea. Ceylon Journal of Science 19B: 225-239. Dorcas, M.E., Hopkins, W.A. and Roe. J.H. 2004. Effects of body mass and temperature on standard metabolic rate in the eastern diamondback rattlesnake (Crotalus adamanteus). Copeia 145-151. Dmi'el, R. 1971. Relation of metabolism to body weight in snakes. Copeia 179-181. Eckert, K. L., and S. A. Eckert. 1985. Tagging and nesting research of leatherback sea turtles Dermochelys coriacea on Sandy Point, St. Croix, 1985. 57 Annual report. U.S. Virgin Islands Division of Fish and Wildlife, U.S. Fish Wildlife Reference Service MIN 54-8680431. Laurel, Maryland. Eckert, S.A., Eckert, K.L., Ponganis, P. and Kooyman, G.L. 1989. Diving and foraging behavior of leatherback sea turtles (Dermochelys coriacea). Canadian Journal of Zoology 67: 2834-2840. Eckert, S. A. and Sarti, L.M. 1997. Distant fisheries implicated in the loss of the world's largest leatherback nesting population. Marine Turtle Newsletter 78: 2-7. Erickson, G.M., Makovicky, P.J., Currie, P.J., Norell, M.A., Yerby, S.A. and Brochu, C.A. 2004. Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430: 772-775. Erickson, G.M., Rogers, K.C. and Yerby, S.A. 2001. Dinosaurian growth patterns and rapid avian growth rates. Nature 412: 429-433. Ernest, J. and Frazer, J . 1983. A leatherback turtle Dermochelys coriacea feeding in the wild. Journal of Herpetology 17: 81-81. Foster, P. and Chapman C. 1975. The care and maintenance of young leatherback turtles, Dermochelys coriacea. International Zoo Yearbook 15: 170-171. Frair, W., Ackman, R. G. and Mrosovsky, N. 1972. Body temperatures of Dermochelys coriacea: warm turtle from cold water. Science 177: 791-793. Frazer, N.B. 1986. Survival from egg to adulthood in a declining population of loggerhead turtles, Caretta caretta. Herpetologica 42(l):47-55 Frayr, W. (1970). The world's largest living turtle. Salt Water Aquarium (5): 235-241. Greer, A.E., Lazell, J.D., Jr. and Wright, R.M. 1973. Anatomical evidence for a counter-current heat exchanger in the leatherback turtle (Dermochelys coriacea). Nature 244:181 Glass, M.L. and Wood, S.C. 1983. Gas exchange and control of breathing in reptiles. Physiological Review 63: 232-260. Hochscheid, S., Bentivegna, F. and Speakman, J.R. 2003. Long-term acclimation leads to high Q10 effects on oxygen consumption of loggerhead turtles Caretta caretta. Physiological and Biochemical Zoology 77 (2): 209-222. 58 Hughes, G.M., Gaymer, R., Moore, M. and Woakes, A.J. 1971. Respiratory exchange and body size in the Aldabra giant tortoise. Journal of Experimental Biology 55: 651-665. Jacobson, E.R. 1996. Metabolic scaling of antibiotics in reptiles: basis and limitations. Zoological Biology 15: 329-239. James, M.C. and Mrosovsky, N. 2004. Body temperatures of leatherback turtles (Dermochelys coriacea) in the temperate waters off Nova Scotia, Canada. Canadian Journal of Zoology 82: 1302-1306. Jones, D.R., Southwood, A.L., Andrews, R.D. 2004. Energetics of Leatherback Sea turtles. In: Experimental Approaches to Conservation, (ed: M.S. Gordon and S.M. Barton) University if California Press Ltd, London England. Jones, T. T., Salmon, M., Wyneken, J. , and Johnson, C , 2000. Rearing leatherback hatchlings: protocols, growth and survival. Marine Turtle Newsletter 2000 (90): 3-6. Jones, T.T., Reina, R.D., Darveau, C.A., and Lutz, P.L. 2006. Ontogeny of Energetics in Leatherback, Dermochelys coriacea and Olive Ridley, Lepidochelys olivacea Sea Turtle Hatchlings. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology. In Press. Hayes, J. P., 2001. Mass-specific and whole-animal metabolism are not the same concept. Physiological and Biochemical Zoology 74: 147-150. Heusner, A. A., 1982. Energy Metablosim and Body Size. I. Is the 0.75 Mass Exponent of Kleiber's Equation a Statistical Artifact? Respiration Physiology 48:1-12. Heusner, A. A., 1982. Energy Metablosim and Body Size. II. Dimensional Analysis and Energetic Non-Similarity. Respiration Physiology 48:13-25. Hochscheid, S., Bentivegna, F. and Speakman, J.R. 2002. Regional blood flow in sea turtles: Implications for heat exchange in an aquatic ectotherm. Physiological and Biochemical Zoology 75(1): 66-76. Hughes, G. M., Gaymer R, Moore, M. and Woakes, A.J. 1971. Respiratory exchange and body size in the Aldabra tortoise. Journal of Experimental Biology 55: 651-665. IUCN (2004) 2004 IUCN red list of threatened species, 59 Kleiber, M. 1932. Body size and metabolic rate. Halgardia 6: 315-353. Kleiber, M. 1962. The Fire of life; an introduction to anima energetics. Wiley, New York. Kooijman S.A.L.M. 1993. Dynamic energy budgets in biological systems. Cambridge University Press, Cambridge. Larese-Casanova, M. and Penick, D.N. 1998. Ontogeny of temperature independent metabolism in leatherback sea turtle hatchlings, Dermochelys coriacea. American Zoologist 38(5): 178. Litzgus, J.D. and Hopkins W.A. 2003. Effect of temperature on metabolic rate of the mud turtle (Kinostenon subrubrum). Journal of Thermal Biology. 28: 595-600. Lutz, P.L., Bergey, A. and Bergey, M. 1989. Effects of temperature on gas exchange and acid-base balance in the sea turtle Caretta caretta at rest and during routine activity. Journal of Experimental Biology 144: 155-169. Lutcavage, M.E. and Lutz, P.L. 1986. Metabolic rate and food energy requirements of the leatherback sea turtle, Dermochelys coriacea. Copeia 3: 796-798. Maxwell, L.K., Jacobson, E.R. and Mc Nab, B.K. 2003. Intraspecific allometry of standard metabolic rates in green iguanas, Iguana iguana. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 136(2): 301-310. Paladino, F. V., O'Connor, M. P. and Spotila J.R. 1990. Metabolism of leatherback turtles, gigantothermy, and thermoregulation of dinosaurs. Nature 344: 858-860. Penick, D. N., Spotila, J . R., O'Connor, M. P.,Steyermark A C - , George, R.H., Salice, C.J. and Paladino, F.V. 1998. Thermal independence of muscle tissue metabolism in the leatherback turtle, Dermochelys coriacea. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 120(3): 399-403. Phillips, E. J. 1976. Raising hatchlings of the leatherback turtle, Dermochelys coriacea. British Journal of Herpetology 5: 677-678. Prange, H.D. and Jackson, D.C. Ventilation, gas exchange and metabolic scaling of a sea turtle. 1976. Respiration Physiology 27: 369-377. Pritchard, P. C. H. 1997. Evolution, phylogeny and current status, In: The Biology of Sea Turtles, (eds. Lutz, P. L. and Musick, J. A.). CRC Press, Boco Raton, FL. pp. 1-28. 60 Rhodin, A. G. J. , 1985. Comparative chondro-osseous development and growth of marine turtles. Copeia 752-771. Salmon, M., Jones, T. T. and Horch, K., 2004. Ontogeny of diving and feeding behavior in juvenile sea turtles: A comparison study of green turtles Chelonia mydas and leatherbacks Dermochelys coriacea in the Florida current. Journal of Herpetology 38:36-43. Schmidt-Nielson, K. 1984. Scaling: Why is Animal Size so Important? Cambridge University Press, Cambridge, pp 56-73. Schmidt-Nielson, K. 1997. Animal Physiology - Adaptation and environment. Cambridge University Press, Cambridge, pp 217-240. Seebacher, F. and Shine, R. 2004. Evaluating thermoregulation in reptiles: The fallacy of the inappropriately applied method. Physiological and Biochemical Zoology 77 (4): 688-695. Seebacher, F., Grigg, G.C., and Beard, L.A. 1999. Crocodiles as dinosaurs: Behavioral thermoregulation in very large ectotherms leads to high and stable body temperatures. Journal of Experimental Biology 202: 77-86. Southwood, A.L., Darveau, C.A., and Jones, D.R. 2003. Metabolic and cardiovascular adjustments of juvenile green turtles to seasonal changes in temperature and photoperiod. Journal of Experimental Biology 206: 4521-4531. Southwood, A.L. 1997. Heart rates and dive behaviour of the leatherback turtle {Dermochelys coriacea). Master Thesis. University of British Columbia. Spotila, J . R. 2004. Sea turtles: A complete guide to their biology, behaviour and, conservation. Baltimore, The Johns Hopkins University Press, pp 160-177. Spotila, J. R., R. D. Reina, Steyermark, A.C. and Paladino, F.V. 2000. Pacific leatherback turtle face extinction. Nature 405: 529-530. Standora, E. A., J . R. Spotila, Keinath, J. A. and Shoop, C. R. 1984. Body temperatures, diving cycles, and movement of a sub adult leatherback turtle, Dermochelys coriacea. Herpetologica 40: 169-176. Swingle M.W., Warmolts, D.I., Keinath, J.A. and Musick, J.A. 1993. Exceptional growth rates if captive loggerhead seat turtles, Caretta caretta. Zoological Biology 12: 491-497. 61 Thompson, G.G. and Withers P.C. 1992. Effects of body mass and temperature on standard metabolic rates for two Australian varanid lizards {Varanus gouldii and V. panoptes). Copeia 343-350. Thompson, G.G. and Withers P.C. 1997. Standard and maximal metabolic rates of goannas (Squamata: Varanidae). Physiological Zoology 70: 307-323. West, G.B., Brown, J.H. and Enquist B.J. 1999. The fourth dimensional of life: Fractal geometry and allometric scaling of organisms. Science 284: 1677-1679. White, C.R., Seymour, R.S. 2003. Mammalian basal metabolic rate is proportional to body mass 2 / 3. Proceedings of the National Academy of Sciences 100 (7): 4046-4049. Willme, P., Graham, S., and Johnston, I. 2000. Environmental Physiology of Animals. Blackwell Science Ltd, Oxford, pp 124-154. Witham, R. 1977. Dermochelys coriacea in captivity. Marine Turtle Newsletter 3: 6. Wood, R. C , Johnson-Gove, J. , Gaffney, E.S. and Maley, K.F. 1996. Evolution and phylogeny of leatherback turtles (Dermochelyidae), with description of new fossil taxa. Chelonia Conservation Biology 2: 266-286. Wood, S.C., Johansen, K., Glass, M.L. and Malioy, G.M.O. 1978. Aerobic metabolism of the lizard Varanus exanthematicus: effects of activity, temperature and size. Journal of Comparative Physiology B 127: 331-336. Wyneken, J . 1997. Sea turtle locomotion: mechanisms, behavior, and energetics, pp. 165-198 in. The Biology of Sea Turtles, (eds. P. Lutz, J , Musick). CRC Press, Boca Raton. Wyneken, J. and Salmon, M. 1992. Frenzy and Postfrenzy Swimming Activity in Loggerhead, Green, and Leatherback Hatchling Sea Turtles. Copeia 2: 478 -484. Zaidan, F. 2003. Variation in cottonmouth (Agkistrodon piscivorus leucostoma) resting metabolic rates. Comparative Biochemistry and Physiology A 134: 511 -523. Zangerl, R. 1980. Patterns of phylogenetic differentiation in the Toxochelyid and Chelonid sea turtles. American Zoologist 20: 585-596. 62 


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