Ecological and physiological determinants of dive ... - CiteSeerX

Functional Ecology 2010, 24, 103–111

doi: 10.1111/j.1365-2435.2009.01599.x

Ecological and physiological determinants of dive duration in the freshwater crocodile Hamish A. Campbell*,1, Scott Sullivan2, Mark A. Read2, Mathew A. Gordos3 and Craig E. Franklin1 1

School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia; 2Queensland Parks and Wildlife, Marlow Street, Townsville, Queensland 4810, Australia; and 3Department of Primary Industries, 1243 Bruxner Highway, Wollongbar, New South Wales 2477, Australia

Summary 1. Body mass is a key determinant of diving performance in endotherms. In air-breathing ectotherms however, this paradigm occurs with considerably less force. Here, through remote recordings of dive behaviour over a wide size range (5–42 kg body mass, n = 17) of freshwater crocodiles (Crocodylus johnstoni), we demonstrate why body mass is such a poor determinant of dive duration for ectothermic divers. 2. Crocodiles were released into the wild with a time-depth-recorder attached to their dorsal scutes, and a movement activated radio-tag attached to their tail. Over 15 days, 652Æ6 ± 58Æ4 (mean ± SE, n = 17) dives were recorded, with all individuals exhibiting two specific divetypes. These were, a resting-dive (62Æ7 ± 5Æ4% of total dive no.), where no activity occurred during the dive, and an active-dive (37Æ1 ± 6Æ3% of total no.) associated with swimming. 3. The durations of resting-dives (12 min) were similar for all crocodiles. Smaller crocodiles (6Æ3 ± 0Æ7 kg, mean ± SE, n = 9) exhibited a significant correlation between dive duration and post-dive surface-interval, whilst larger crocodiles (17Æ9 ± 3Æ75 kg, mean ± SE, n = 8) did not. This demonstrated that aerobic dive duration was mass-specific during resting-dives, but other mass specific factors, presumably ecological, determined dive duration. 4. The durations of active-dives were never >1 min, showed no relationship with body mass and no correlation with the post-dive-surface interval. In crocodiles, aerobic metabolic scope is independent of body mass but anaerobic capacity is mass dependent, suggesting that active-dive duration was determined by sustained activity and dives were terminated before anaerobic metabolism became significant. 5. All individuals showed similar diel phase shifts in dive duration, type and depth, illustrating the overwhelming influence of the external environment on dive behaviour. Dive durations which resulted in significant anaerobic debt occurred rarely, but were undertaken in response to a potential threat. 6. Body mass was a poor predictor of diving in C. johnstoni because the external environmental and ecological factors exerted a greater influence on dive duration than oxygen reserves. Key-words: crocodylus johnstoni, ectotherm, diving behaviour, aerobic dive limit, body size

Introduction The length of time that an air-breathing animal can remain submerged is determined by the amount of stored oxygen and the rate it is utilized (Butler & Jones 1982). This has led to the application of the ‘aerobic dive limit’ (ADL), defined experimentally as, the dive *Correspondence author. E-mail: [email protected]

duration beyond which lactate levels rise above resting levels (Kooyman et al. 1980, 1983). Diving beyond ADL requires anaerobiosis, and whilst the diver may increase the duration of a single dive, the total accumulated time spent underwater is reduced because post-dive-surfacetime is extended to clear body lactic acid (Costa et al. 2004). In most air-breathing vertebrates oxygen stores scale isometrically with body mass, whereas metabolic rate scales

2009 The Authors. Journal compilation 2009 British Ecological Society

104 H. A. Campbell et al. allometrically with an exponent 0Æ1 m during the dive (active-dive). Dive parameters were calculated on an hourly basis and examined for diel phase shifts by power spectral analysis (PSA). The dive parameters for each crocodile were assessed independently. A purpose-written program in MATLAB R2008a generated a Lomb-Scargle periodogram from the dive data and applied the discrete Fourier transform. The results were defined graphically, and a peak significance (PS) value produced if oscillatory components were present in the data (PS < 0Æ05). If the period of the oscillation was between 23 and 25 h then it was considered to represent a diel rhythm. To calculate mean differences in dive variables, data were grouped and significant differences between hours over the diel cycle determined using repeated-measures ANOVA and Dunnet’s post-hoc tests. To examine the effect of body mass on dive duration and depth, crocodiles were separated into three groups determined by mass (Table 1), and the Kruskal–Wallis test with Dunn’s post-hoc multiple sample comparison was used to determine whether the medians were significantly different between the three groups. The Kolmogorov–Smirnoff test was used to determine whether the distribution between the groups was significantly different. The Mann–Whitney U-test was also used on one occasion to test for significant difference in median dive duration between two size class groups. All data were considered significant if P < 0Æ05.

Results After 20 days of free-ranging activity, 17 C. johnstoni were recaptured, and provided detailed depth information. The immediate 5 days after release were not included in the final analysis, to ensure conclusions were made from nondisturbed free-diving crocodiles. This produced a total of 6936 h of depth recordings and 13 389 individual dives, ranging from 315 to 967 dives per crocodile.

PHYSIOLOGICAL EFFECTS ON DIVE DURATION

All 17 C. johnstoni undertook two distinct types of dive (Fig. 2). A resting-dive, defined by an extended bottom phase with no change in depth, and an active-dive, defined by no extended bottom phase at a single depth. The median duration of the resting-dive was 12 min, but was 17Æ3, P > 0Æ05). Although larger crocodiles participated in more dives than smaller crocodiles, the total duration spent underwater was offset by the relatively

2009 The Authors. Journal compilation 2009 British Ecological Society, Functional Ecology, 24, 103–111

Determinants of dive duration in C. johnstoni

ENVIRONMENTAL AND ECOLOGICAL EFFECTS ON DIVE DURATION

The diving behaviour of C. johnstoni changed throughout the diel cycle with shared traits between individuals. The depth of dives began to increase around 04.00 h, and reached the daily maximum between 08.00 and 10.00 h (Fig. 4a). This correlated with an increase in submergence time. After 11.00 h, mean dive depth progressively shallowed and the amount of time that the crocodiles were submerged decreased. Throughout the evening and night, dives remained shallow and the crocodiles spent 0Æ05) in the number of dives exhibited each hour (period 12Æ2–26Æ2 h). *Hours when mean data were significantly different from mean data at 08.00 h. The proportion of the total number of dives that were active-dives throughout the diel cycle (white circles, mean ± SE, N = 17, n = 289). There was significant rhythmicity (PS < 0Æ05) in the proportion of activedives for all C. johnstoni (period 23Æ2–24Æ7 h). +Hours when mean data were significantly different from mean data at 18.00 h. (c) The maximum dive duration throughout the diel cycle (black triangles, mean ± SE, N = 17, n = 289). There was significant rhythmicity (PS < 0Æ05) in maximum dive duration for all C. johnstoni (period 23Æ1–25Æ2 h). *Hours when mean data were significantly different from mean data at 07.00 h. The mean dive duration throughout the diel cycle (black circles, mean ± SE, N = 17, n = 289). There was significant rhythmicity (PS < 0Æ05) in mean dive duration for all C. johnstoni (period 22Æ1–24Æ9 h). +Hours when mean data were significantly different from mean data at 07.00 h. The median dive duration for each hour over the diel cycle (white circles, mean ± SE, N = 17, n = 289). There was significant rhythmicity (PS < 0Æ05) in median dive duration for all C. johnstoni (period 21Æ8–25Æ2 h). #Hours when mean data were significantly different from mean data at 07.00 h.

Proportion of hour submerged

greater number of active-dives undertaken by larger crocodiles. This resulted in no significant difference in the proportion of the observational period that each size class group was submerged underwater. Larger crocodiles had significantly deeper dives compared with the smaller size groups (KW = 9Æ2, P = 0Æ027); active-dive depth however, was not mass dependent, and the smallest size class of crocodiles exhibited a deeper mean depth for active-dives than the medium size class (KW = 13Æ2, P = 0Æ047). The correlation between dive duration and the post-divesurface-interval was assessed from within a bout of three or more resting-dives, using Spearman-rank order correlation. The correlation coefficient was only significant (rs > 0Æ1 < 0Æ37, P < 0Æ02) for animals with a body mass of 5Æ0, 5Æ1, 5Æ1, 5Æ6,6Æ0, 6Æ1, 6Æ2, 6Æ4 and 11Æ6 kg, (6Æ3 ± 0Æ7 kg, mean ± SE, n = 9), and crocodiles of body mass, 8Æ6, 9Æ7, 13Æ1, 15Æ6, 22 and 42Æ4 kg (17Æ9 ± 3Æ75 kg, mean ± SE, n = 9) showed no significant correlation (rs < )0Æ009, P > 0Æ05). The surface interval duration between active-dives was substantially greater than the surface interval duration between restingdives, and no relationship existed between body size and the surface interval duration between active-dives for any size class.

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108 H. A. Campbell et al.

DIVE DURATION IN RESPONSE TO A PERCEIVED THREAT

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Surface water temperature (°C)

LTB (h–1)

In response to human presence on the banks of the waterhole 11 of the 17 crocodiles exhibited dives that were 1Æ86- to 3Æ9fold longer than the individuals maximum dive duration under routine diving (Fig. 6), and between 11Æ1- and 33Æ5-fold greater than the median resting-dive duration. The other six

500

400 Length of dive (min)

of dives undertaken from 13.00 to 16.00 h, and then 19.00 to 21.00 h, were significantly less than at other times of the diel cycle, but only three of the seventeen crocodiles showed a significant diel phase shift in the number of dives undertaken each hour. All crocodiles however, showed a significant circadian rhythm for specific dive-type (Fig. 4b). Restingdives were primarily occurred between 04.00 and 09.00 h, with active-dives making up 65% of all dives were active-dives (Q < 2Æ99, P < 0Æ05). Throughout the night the dive-type gradually shifted from the active to the resting-dive, and this can be observed with the increase in maximum, median and average dive duration (Fig. 4c). The mean number of LTB expressed each hour showed a significant circadian rhythm (Fig. 5). From 04.00 to 15.00 h activity was 30 LTB h)1, and remained elevated until 00.00 h. Between 00.00 and 04.00 h, activity was >20 LTB h)1. The temperature of the waterhole during the study period was consistently 23Æ5 ± 0Æ1 C at 1Æ5 m depth. Surface waters fluctuated daily between 19Æ3 ± 0Æ3 and 25Æ1 ± 0Æ1 C. The surface water was at its daily minimum between 03.00 and 06.00 h, and at the daily maximum between 13.00 and 15.00 h (Fig. 5).

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Fig. 6. The maximum routine dive duration (black circles) and avoidance dive duration (white circles) for the same Crocodylus johnstoni (indicated by body mass, n = 11).

crocodiles swam horizontally through the water hole in reaction to human disturbance and did not undergo a dive of lengthy duration. The crocodile with the greatest body mass showed the longest voluntary dive duration and the longest avoidance dive duration. Considerable variability in the maximum dive duration did occur for some of the other crocodiles, with a 5-kg animal diving for 344 min, resulting in no significant relationship between body mass and maximum dive duration. We tried to sample blood in all crocodiles when surfacing from a dive, but due to the problems associated with removing a blood sample within 1 min of surfacing and the rapid build-up of lactate due to handling, only data from six animals were included in the final analysis. All crocodiles, even after relatively short dives, showed elevated blood lactate, indicating a stress response induced by human presence (Table 2). Blood lactate was 2-fold and pH reduced by 0Æ3, in those crocodiles that had dived in excess of 187 min.

Discussion Previous modelling exercises have found that the widely accepted body mass dependency of dive duration in endotherms applies with significantly less force in air-breathing ectotherms (Brischoux et al. 2008). Calling into question the notion that body size was a general feature of diving evolution (Halsey, Butler & Blackburn 2006a,b). Body mass was a poor predictor of dive duration in the air-breathing ectotherm Crocodylus johnstoni. However, the results show that the limit

0

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Fig. 5. The number of lateral tail beats expressed per hour throughout the diel cycle (black circles, mean ± SE, N = 3, n = 45), and the mean hourly water temperature at 0Æ15 m depth (white circles, mean ± SE, n = 45). There was significant rhythmicity (PS < 0Æ05) in lateral tail beat activity (period 22Æ8–25Æ2 h). *Hours when mean data were significantly different from mean data at 07.00 h. The hourly water temperature at 0Æ15 m depth over the 15-day recording period (white circles, mean ± SE, n = 45).

Table 2. Blood pH and lactate sampled from six Crocodylus johnstoni immediately after surfacing from a dive. Dive duration was provided by attached time-depth-recorders Dive length (min)

13

18

45

187

237

344

Lactate (mmol L)1) pH Body mass (kg)

14Æ16 6Æ94 5Æ0

13Æ19 6Æ97 19

13Æ60 6Æ95 9Æ5

23Æ00 6Æ62 22Æ0

22Æ37 6Æ87 6Æ5

24Æ30 6Æ78 5Æ0


Determinants of dive duration in C. johnstoni of the aerobic dive duration did allometrically scale with body mass but external factors resulted in the observed allometric differences in dive behaviour. The substantial influence of the environment on the diving behaviour of C. johnstoni was made apparent by the diel phase shifts in dive depth, duration and underwater activity. The amount of time C. johnstoni was submerged was significantly elevated between 04.00 and 11.00 h, and was associated with a daily minimum in LTB activity. We disagree with the interpretation by Seebacher, Franklin & Read (2005) that these periods of high submergence represent foraging or social activity. Instead, our results show that the crocodiles maintained a constant depth at the bottom of the dive, and because of the high sensitivity of the TDR (0.04 m) and the uneven waterhole substratum, the crocodiles must have been sedentary on the substratum for the duration of the dive. This was supported by remote recordings of tail beat activity, which showed this type of dive was characterized by a single tail movement at the start of the dive, with no lateral tail movement occurring throughout the bottom phase. The crocodiles remained immobile in the deepest sections (>2Æ5 m) of the waterhole, and the turbid water would have resulted in zero visibility at this depth. Although prey items may have been taken if they came into contact with the crocodile, it appears unlikely that these dives functioned to capture prey. Resting-dives accounted for 62Æ7 ± 5Æ4% of the total number of dives and 97Æ2 ± 4Æ3% of the time spent underwater. They were on average between 11 and 13 min in duration with no significant correlation across the wide range of body sizes used in this study. The relationship between dive duration and the post-dive-surface-interval did however show an allometric component. A high proportion of resting-dives, undertaken by smaller crocodiles (6Æ3 ± 0Æ7 kg, mean ± SE, n = 9) required adjustment of the post-dive-surface-interval, presumably to clear an anaerobic debt (Costa et al. 2004). Crocodiles with a larger body mass (17Æ9 ± 3Æ75 kg, mean ± SE, n = 8) did not show a correlation between dive duration and the post-dive-surface-interval, suggesting that a large majority of their resting dives terminated before any significant lactate debt occurred. The physiology underpinning this behavioural response may be explained by calculations based on metabolic rate and oxygen stores in Crocodylus porosus, which showed that aerobic dive time increased with body size to an allometric exponent between 0Æ15 and 0Æ25 (Wright & Kirshner 1987). This would result in the aerobic dive duration increasing by 1Æ7-fold across the 5–42 kg body mass range in this study. The reason smaller crocodiles maintain dive duration similar to larger crocodiles, whilst enduring an anaerobic debt remains speculative, but strongly suggests conspecific pressure. Groups of C. johnstoni within a single waterhole have been shown to exhibit a strong social hierarchy with individuals eliciting dominance and submissive behaviours (Seebacher & Grigg 1997). The depth of resting-dives showed a positive association with body mass, and the largest crocodiles occupied the deepest sections of the waterhole. The relationship between body mass and the depth of rest-

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ing-dives suggests that the deep water served as a refuge for C. johnstoni, and pressure by conspecifics resulted in smaller subordinate crocodiles being forced to refuge in shallower locations. On one occasion during the study we observed a large (+3 m) adult C. porosus within the waterhole, which would have been a potential predator of C. johnstoni (Webb & Manolis 1989). Evasion of predators and conspecific aggression may be the reason C. johnstoni refuge during the early morning, as low air and surface water temperatures would have resulted in suboptimal muscle performance (Seebacher & Grigg 1997; Elsworth, Seebacher & Franklin 2003). Long-dives with a resting phase on the substratum have also been observed in some marine turtles (Van Dam & Diez 1996; Houghton et al. 2008), and may represent a common behavioural strategy for diving reptiles, enabling them to conserve energy costs whilst at the same time reducing the risk of predation. Over the day time period, air and surface water temperature at the waterhole warmed by 6 C. This was associated with a gradual increase in short-shallower dives, which were associated with swimming activity (active-dives). The depth varied constantly throughout the duration of these dives, illustrating that the crocodiles were moving through the water column or across the substratum. Crocodiles have an inability to sustain exercise for prolonged periods (Bennett et al. 1985; Baldwin, Seymour & Webb 1995), and this may have contributed to the very short duration of these activedives (21Æ5 C) and the small body mass; a 5-kg crocodile dived for 344 min and a 42-kg crocodile dived for 402 min. During these very long dives the attached TDR recorded very little change in depth, suggesting that the crocodiles remained completely sedentary on the substratum and invested virtually no metabolic resources into activity during these submergence periods. They may have also initiated physiological responses such as cardiac shunting to assist in extending dive duration (Grigg 1989; Axelsson & Franklin 1997). We hypothesized that these long dives with no investment in activity would have shown a strong positive correlation between body mass and dive duration. The largest crocodile did exhibit the longest dive but no significant allometric correlation was observed because of the large inter-individual variability and low sample size. Possible reasons for the interindividual variability may have occurred, because dives were initiated at different times of the diel cycle, and therefore, recent dive history would have significantly varied between individuals. This would have resulted in differences in body temperature and stored oxygen. A larger sample size under better controlled conditions may show a clearer allometric response. Logistical difficulties in acquiring a blood sample within 1 min of the crocodiles surfacing resulted in a low number of post-dive plasma lactate samples. The significant aspect of these results was that C. johnstoni showed a lactate debt after 187, 237 and 344 min of submergence similar to an equally sized C. porosus after only 2 min of exhaustive exercise (Bennett et al. 1985; Seymour, Bennett & Bradford 1985; Baldwin, Seymour & Webb 1995), thus illustrating the remarkable ability of crocodilians, and perhaps all reptiles, to extend dive duration far beyond the realm of endothermic divers by invoking hypometabolic processes. To answer, why body mass was such a poor predictor of dive duration in C. johnstoni, we need to examine the adaptive ecological significance of the dive behaviour. Foraging or other high-activity behaviours were not associated with long dives, presumably because of the reduced aerobic scope in reptiles. Their low metabolic rate and high capacity for anaerobic debt however, allowed very long inactive dives. This type of diving functioned as a low-cost energetic strategy to refuge from potential threats. Smaller crocodiles were required to go beyond aerobic dive durations more frequently than larger crocodiles, as conspecific and predation threats were size specific. Endothermic divers may show a much stronger correlation between dive duration and body mass, because they primarily undertake diving to forage for food and larger animals will require more food, and foraging time, than smaller animals.

Acknowledgements This project was funded by the Australian Research Council-Linkage scheme, with Australia Zoo as funding partners and Queensland Parks and Wildlife providing infrastructure and logistics. All research was undertaken with The University of Queensland, Animal Welfare Unit approval and a Queensland Environment Protection Agency Eco-Access permit. We thank Paul O’Callaghan, Annabelle Olsson, Dave Leyland, Mariana Micheli-Campbell, Lakefield National Park Rangers and QPWS Wildlife Services staff for their help during field work.

References Axelsson, M. & Franklin, C.E. (1997) From anatomy to angioscopy: 164 years of crocodilian cardiovascular research, recent advances, and speculations. Comparative Biochemistry and Physiology A, 118, 51–62. Baldwin, J., Seymour, R.S. & Webb, G.J.W. (1995) Scaling anaerobic metabolism during exercise in the estuarine crocodile (Crocodylus porosus). Comparative Biochemistry and Physiology A, 112, 51–62. Bennett, A.F. (1982) The energetics of reptilian activity. The Biology of the Reptilia (eds C. Gans & W. R. Dawson), Vol. 13, pp. 148–183, Academic Press, New York. Bennett, A.F. & Dawson, W.R. (1976) Metabolism. The Biology of the Reptilia (eds C. Gans & W. R. Dawson), Vol. 5, pp. 127–223, Academic Press, New York. Bennett, A.F., Seymour, R.S., Bradford, D.F. & Webb, G.J.W. (1985) Massdependence of anaerobic metabolism and acid-base disturbance during activity in the salt-water crocodile, Crocodylus porosus. Journal of Experimental Biology, 118, 161–171. Brischoux, F., Bonnet, W., Cook, T.R. & Shine, R. (2008) Allometry of diving capacities: ectothermy vs. endothermy. Journal of Evolutionary Biology, 21, 324–329. Butler, P.J. & Jones, D.R. (1982) The comparative physiology of diving in vertebrates. Advances in Comparative Physiology and Biochemistry, 8, 179–364. Carr, A., Ogren, L. & McVea, C.J. (1980) Apparent hibernation by the Atlantic loggerhead turtle off Cape canaveral, Florida. Biological Conservation, 19, 7–14. Costa, D.P., Kuhn, C.E., Weise, M.J., Shaffer, S.A. & Arnold, J.P.Y. (2004) When does physiology limit the foraging behaviour of freely diving mammals? International Congress Series, 1275, 359–366. Elsworth, P.G., Seebacher, F. & Franklin, C.E. (2003) Sustained swimming performance in crocodiles (Crocodylus porosus): effects of body size and temperature. Journal of Herpetology, 37, 363–368. Gleeson, T.T. (1980) Lactic acid production during field activity in the Galapagos marine iguana, Amblyrhynchus cristatus. Physiological Zoology, 53, 157– 162. Gordos, M.A., Franklin, C.E. & Limpus, C.J. (2003) Seasonal changes in the diel surfacing behaviour of the bimodally respiring turtle Rheodytes leukops. Canadian Journal of Zoology, 81, 1614–1622. Grigg, G.C. (1989) The heart and patterns of cardiac outflow in crocodilia. Proceedings of the Australian Physiology and Pharmacology Society, 20, 43–57. Grigg, G.C., Farwell, W., Kinney, J.L., Harlow, P., Taplin, L.E. & Johansen, K.W. (1985) Diving and amphibious behavior in a free-living Crocodylus porosus. Australian Zoologist, 21, 599–606. Halsey, L.G., Butler, P.J. & Blackburn, T.M. (2006a) A phylogenetic analysis of the allometry of diving. The American Naturalist, 167, 276–285. Halsey, L.G., Butler, P.J. & Blackburn, T.M. (2006b) A comparative analysis of the diving behaviour of birds and mammals. Functional Ecology, 20, 889– 899. Heatwole, H. (1975) Voluntary submergence times of marine snakes. Marine Biology, 32, 205–213. Heusner, A.A. (1991) Size and power in mammals. Journal of Experimental Biology, 160, 25–54. Hochscheid, S., Bentivegna, F. & Hays, G.C. (2005) First, records of dive durations for a hibernating sea turtle. Biology Letters, 1, 82–86. Hochscheid, S., McMahon, C.R., Bradshaw, C.J.A., Maffucci, F., Bentivegna, F. & Hays, G.C. (2007) Allometric scaling of lung volume and its consequences for marine turtle diving performance. Comparative Biochemistry and Physiology A, 148, 360–367. Houghton, J.D.R., Cedras, A., Myers, A.E., Liebsch, N., Metcalfe, J.D., Mortimer, J.A. & Hays, J.C. (2008) Measuring the state of consciousness in a free-living diving sea turtle. Journal of Experimental Marine Biology and Ecology, 356, 115–120.


Determinants of dive duration in C. johnstoni Kooyman, G.L., Wahrenbrock, E.A., Castellini, M.A., Davis, R.W. & Sinnett, E.E. (1980) Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: evidence of preferred pathways from blood chemistry to behaviour. Journal of Comparative Physiology A, 138, 335–346. Kooyman, G.L., Castellini, M.A., Davis, R.W. & Maue, R.A. (1983) Aerobic dive limits of immature Weddell seals. Journal of Comparative Physiology, 151, 171–174. Mathie, N.J. & Franklin, C.E. (2006) The influence of body size on the diving behaviour and physiology of the bimodally respiring turtle, Elseya albagula. The Journal of Comparative Physiology B, 176, 739–747. McKechnie, A.E. & Wolf, B.O. (2004) The allometry of avian basal metabolic rate; good predictions need good data. Physiological and Biochemical Zoology, 77, 502–521. Moberly, W.R. (1968) The metabolic responses of the common Iguana Iguana iguana, to walking and diving. Comparative Biochemistry and Physiology, 27, 21–32. Papastamatiou, Y.P., Meyer, C.G. & Holland, K.M. (2007) A new acoustic pH transmitter for the studying the feeding habits of free-ranging sharks. Aquatic Living Resources, 20, 287–290. Pough, F.H. (1980) The advantages of ectothermy for tetrapods. The American Naturalist, 115, 92–112. Rubinoff, I., Graham, J.B. & Motta, J. (1986) Diving of the sea snake Pelamis platurus in the Gulf of Panama. I Dive depth and duration. Marine Biology, 91, 181–191. Schreer, J.F. & Kovacs, K.M. (1997) Allometry of diving capacity in air-breathing vertebrates. Canadian Journal of Zoology, 75, 339–358. Seebacher, F., Franklin, C.E. & Read, M. (2005) Diving behaviour of a reptile (Crocodylus johnstoni) in the wild: interactions with heart rate and body temperature. Physiological and Biochemical Zoology, 78, 1–8. Seebacher, F. & Grigg, G.C. (1997) Patterns of body temperature in wild freshwater crocodiles, Crocodylus johnstoni: thermoregulation versus thermocon-

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formity, seasonal acclimatization, and the effect of social interactions. Copeia, 3, 549–557. Seymour, R.S., Bennett, A.F. & Bradford, D.F. (1985) Blood gas tensions and acid-base regulation in the salt-water crocodile, Crocodylus porosus, at rest and after exhaustive exercise. Journal of Experimental Biology, 118, 143–159. Tucker, A.D. (1997) Ecology and demography of freshwater crocodiles (Crocodylus johnstoni) in the Lynd River north Queensland. PhD Thesis, University of Queensland, Australia (THE12677). Ultsch, G.R. (1989) Ecology and physiology of hibernation and overwintering among freshwater fishes, turtles, and snakes. Biological Reviews, 64, 435– 516. Van Dam, R.P. & Diez, C.E. (1996) Diving behaviour of immature hawksbill turtles (Eretmochelys imbricata) in a Caribbean cliff-wall habitat. Marine Biology, 127, 171–178. Wallace, B.P. & Jones, T.T. (2008) What makes a turtle go: a review of metabolic rates and their consequences. Journal of Experimental Marine Biology and Ecology, 356, 8–24. Webb, G. & Manolis, C. (1989) Crocodiles of Australia. Reed, French Forest, NSW. White, C.R. & Seymour, R.S. (2005) Allometric scaling of mammalian metabolism. Journal of Experimental Biology, 208, 1611–1619. Wright, J.C. (1986) Effects of body mass, temperature and activity on aerobic and anaerobic metabolism in the juvenile crocodile, Crocodylus porosus. Physiological Zoology, 59, 505–513. Wright, J.C. & Kirshner, D.S. (1987) Allometry of lung volume during voluntary submergence in the saltwater crocodile Crocodylus porosus. Journal of Experimental Biology, 130, 433–436. Received 24 February 2009; accepted 21 May 2009 Handling Editor: Daniel Costa
