THERMOREGULATION, WATER TURNOVER AND ENERGETICS OF FREE-LIVING KOMODO DRAGONS,
VARANUS KOMODOENSIS
BRIAN GREEN,* DENNIS KING,t MICHAEL BRAYSHER~ and ACI=IMAD SAIM§ *Division of Wildlife and Ecology, CSIRO, P.O. Box 84, Lyneham, A.C.T., 2602, Australia;
tc/o Western Australian Museum, Francis Street, Perth, W.A., 6000, Australia; 3;A.C.T. Parks and Conservation Service, P.O. Box 1119, Tuggeranong, A.C.T. 2901, Australia;
§Division of Zoology, Centre of Research and Development for Biology, Institute of Indonesian Science, Jl. Ir. H. Juanda 3, Bogor, 16122, Indonesia
(Received 8 August 1990)
Abstract--1. Body temperatures, water influxes and metabolic rates were determined for free-living Komodo Dragons (Varanus komodoensis) on Komodo Island, Republic of Indonesia.
2. Body temperatures, daily activity patterns and variations in water influx rates were similar to those of other species of varanid lizards.
3. Field metabolic rates were higher than predicted values.
INTRODUCTION
Since the Komodo dragon (V. komodoensis) was first described by Ouwens in 1912, a number of short-term expeditions have been made to study various aspects of its biology (de Jong, 1927; Dunn, 1927; Burden, 1927; Broughton, 1936; Hoogerwerf, 1954; Darevsky and Kadarsan, 1964). There has also been one longer study (Auffenberg, 1981). Even so, there is little information available on the environmental physi- ology of this animal, the largest extant lizard in the world.
A reasonable amount of data is now available on thermoregulation in varanid lizards (Sokolov et al., 1975; King, 1980; Weavers, 1983; Vernet et al., 1988; King et al., 1989; Wikramanayake and Green, 1989), but data for the largest species in the family are limited. Most data which are available consist of single cloacal temperatures taken from 10 individuals immediately after they were captured (McNab and Auffenberg, 1976). No indication of the times of capture is given by these authors, and these specific values are not separated from those taken from animals which had been held for undetermined periods in live traps. McNab and Auffenberg (1976) also presented "continuous" temperature data that consists of only six cloacal temperatures determined over approximately 18 hr for one animal, which was apparently held in captivity. Other body tem- peratures which are available were obtained in the morning from animals which had been held captive overnight in traps (Darevsky and Kadarsan, 1964).
The water fluxes and metabolic rates of a broad range of lizards have been studied by means of isotope turnover techniques and the influences of body size and habitat have been assessed (Nagy, 1982a,b). The water influx rates of reptiles from semi-arid and arid regions are generally lower than those of tropical forms, although the published data
97
base for tropical lizards is scanty. The Komodo dragon occupies a tropical equatorial habitat that is subjected to a well-defined monsoon season (November-April) followed by a long period of hot dry weather (May-October). There are no published data which could be used to determine whether V. komodoensis is a "tropical" or "semi-arid" species with respect to its water flux rates.
An attempt has been made to assess the food consumption rates of Komodo dragons in the wild by direct observation and an estimated rate of 3.56% of body mass/day has been given (Auffenberg, 1981, p. 292). However, there are no other published data to support this estimate.
The present study was undertaken to assess the water, energy and food requirements and thermo- regulation of free-living V. komodoensis during the dry season on Komodo Island. At the time of this study, there were about 10 very large Komodo dragons at Banu Ngulung, a site where large numbers of tourists are taken to observe them feeding. This group of animals was provided with large numbers of freshly killed goats for the entertainment of the tourists, with the result that these dragons led an inactive existence and were very obese. We could not see any point in studying animals leading such arti- ficial lives and made every effort to capture animals which were living in a natural state. This did not prove to be easy since free-ranging V. komodoensis are very nervous and wary despite their large size (Auffenberg, 1981).
MATERIALS AND METHODS
The field data were obtained between 25 August and 7 September 1987 in the vicinity of Loho Liang, Komodo Island. Data were obtained from four lizards which had snout-vent lengths of 535, 550, 1270 and 870 mm and body masses of 2.4, 2.2, 45.2 and 13.3 kg, for animals A, B, C and D respectively.
98 BRIAN GREEN e t al.
The animals were captured by noosing and their cloacal temperatures were taken immediately with a Schultheis thermometer. They were then fitted with harnesses (Green and King, 1978) containing temperature-sensitive trans- mitters .(Biotrak) with cloacal probes inserted approximately 5cm into the cloaca (King, 1980). The harnesses were cemented to the skin of the animals with epoxy resin (Araldite) and contact cement.
A background blood sample was obtained from each animal by caudal veni-puncture (Green e t al . , 1986) and all animals were then injected with 1 ml of tritiated water (185 M Bq). The two smaller animals were also injected with 0.5 ml and the largest with 2.5 ml of H2IsO (95% atoms excess). All injections were intraperitoneal. The animals were restrained overnight to allow equilibration of the isotopes in the body water pool and to allow the harness cement to completely harden.
The animals were then bled and released at their points of capture. During the release periods the body tempera- tures of the animals were monitored by radio-telemetry using a receiver (Custom electronics) and a stopwatch to time the duration of 20 consecutive radio pulses. Few visual observations were made of the animals as varanids are easily disturbed (King, 1980).
Animals A, B and C (Table 1) were recaptured 12, 10 and 10 days respectively after release. They were re-weighed and a final blood sample was obtained. All blood samples were frozen until required for water extraction and isotope analyses. Water was extracted from the whole blood samples by vacuum sublimation (Vaughan and Boling, 1961).
The tritiated water contents of extracted water samples were determined by counting 100pl aliquots in 3ml of cocktail (PCS, Amersham) with a Beckman 2800 L.S.C. The '60: lSO ratios in blood samples were determined by Urey exchange of 500 #1 of extracted water with a standard charge of CO2 at 80°C overnight. The equilibrated CO2 was drawn off and assayed in a VG Isogas 903 Isotope ratio mass spectrometer. Standard dilutions of the injection solutions were assayed for isotope concentration in the same way as blood extracts.
Water influx and metabolic rates were determined from the decline in 3H and tsO activities during the release periods and from the total body water pool (Lifson and McClin- tock, 1966). The latter was determined by comparison of the equilibration blood samples with standard dilutions of the injected isotopes. It was assumed that the mass specific water pool was constant during the release period so the final absolute body water pool was estimated from the body mass at recapture. It was also assumed that any changes in body mass and absolute pool size were linear during the release period.
Komodo dragons are completely carnivorous (Auffen- berg, 1981) and so their diet is predominantly protein with some fat. Therefore an energy equivalent of 26 k J/1 CO2 was assumed to estimate metabolised energy.
No official meteorological data were recorded on the island during the study period, however shaded air tem- perature was recorded approximately I m above the ground with a Schultheis thermometer at irregular intervals (no less than 15 min apart) during the collection of body temperature records. All mean values in the text are given __+1 SD.
RESULTS
There was no rainfall during the study period and the daily range of ambient temperatures was low, ranging from 21.4 to 31.9°C, but it was generally between 24 and 30°C. Overnight minima (~ =24.1, 21.4-26.1°C, n = 6) were reached between 0600-0700 hr and daily maxima (~ = 29.4, 27.2-31.9°C, n = 12) occurred between 1300-1400 hr.
The body temperatures of three animals at the time of their capture (all in the afternoon) were 36.4°C (A), 35.6°C (C) and 36.9°C (D). After their release the animals could not be located on every day, and after 6, 9 and 6 days respectively, animals A, B and C expelled their cloacal probes so that body tempera- ture recordings were not obtained over the entire release periods. Radio contact with animal D was lost after only one day. These four animals provided comprehensive body temperature data for 6, 7, 4 and 1 days respectively, representing 129, 101, 43 and 17 individual body temperature determinations for the animals while they were active. The numbers of daily temperature determinations for individuals ranged from 8 to 35. Fifty-five body temperatures were recorded from animals outside their activity periods, including values obtained when animals were basking during the mornings.
The lowest cloacal temperatures were measured at about sunrise. The temperatures of all animals then began to rise (Fig. 1) and had reached approximate activity levels by 0800-1000 hr. The cloacal tempera- ture of the largest animal (C) rose more slowly than did those of animals A and B, and maximum activity temperatures were reached in mid-to-late afternoon. (Fig. l).
The mean body temperatures of all animals remained high during their activity periods and were variable within and between individuals, with overall daily mean values of 37.67 + 1.58°C, 33.26 + 0.87°C, 32 .69+ 1.67°C and 34.38°C for animals A - D respectively.
Heating rates during basking ranged from 0.06-0.20°C/rain for A, 0.08~).19°C/min for B and 0.03-0.06°C/min for C. The time of onset and duration of periods of basking is not known precisely for any individual.
Cloacal temperatures began to decline between 1445 and 1800hr (~ = 1643, n = 15) and at rates of 0.01-0.45°C/min in the first 165-280 min after dark. Of 12 early morning (0610-0710 hr) determinations of cloacal temperature, one was below and one was equal to air temperature; all other daily minimum cloacal temperatures were above the minimum air temperature. Those of animal A, which was known to have sheltered inside hollow trees during at least two nights, showed the greatest differences between body temperature and ambient temperature ( + 3.6 to
Table 1. Field metabolic rates and water influxes of Varanus komodoensis
Animal Mass TBW H20 in CO 2 M.E. (kg) (ml/kg) (ml/kg/day) (ml/g/hr) (kJ/kg/day)
A 2.42 763 19.7 0.140 87 B 2.24 758 43.5 0.161 100 C 45.20 727 13.2 0.087 54 D 13.35 749 - - - - -- Mean + SD 749 -t- 16 25.5 _+ 16.0 0.129 +_ 0.038 80 + 24
4O
j. 20
Thermoregulation, water turnover and energetics of Komodo dragons
V komodoermls A, 28 Sept
! g ! 0 600 1200 1800 2400
t i m e
V komodoensis B, 29 Sept
! !
40
0 600 1200 1800 2400
tlme
V komodoensls C, 31 Sept
99
35
' 2'00 ' 0 600 I 1800 2400
Time Fig. 1. Cloacal temperature [] (°C) for individual V. komodoensis: A on 28 September 1987; B on 29 September
1987; C on 31 September 1987.
+7.1°C), while B ranged from - 0 . 8 to +2.1°C and C ranged between + 1.3 and + 1.8°C above ambient.
When the animals were recaptured early in the morning, animal A was sheltering within a hollow tree and B was under fallen branches and leaves. The overnight location of C prior to its recapture was not determined.
During the release period, animal A increased in body mass by 50g (3.1%) while animals B and C decreased by 80 g (3.6%) and 750 g (1.7%) respect- ively. Body mass changes of this order are not considered to be of any biological significance and therefore the dragons can be regarded as having
maintained water and energy balance during the study period.
The tritiated water spaces of the dragons were similar despite the wide range in body mass (Table 1). However, the water influx rates of the three animals that were recaptured varied substan- tially, with a coefficient of variation of 63% (£ = 2 5 . 5 + 16.0ml H20/kg/day ). The CO 2 pro- duction rates were also variable although to a lesser extent than was found with water influxes (.~ = 0.129 _+ 0.038 ml CO2/g/hr, CV = 29%). The smallest dragon (B) had the highest water influx and metabolic rate, while the largest animal (C) had the lowest rates (Table 1).
DISCUSSION
Despite the narrow range of ambient temperatures the mean values and range of the cloacal tempera- tures of V. komodoensis during their activity periods were very similar to those of other terrestrial varanids (Sokholov et al., 1975; King, 1980; Weavers, 1983; Pianka, 1986; Vernet et al., 1988; King et al., 1989; Wikramanayake and Green, 1989). They are also similar to the values given for captive animals, for which cloacal temperatures were independent of air temperature (McNab and Auffenberg, 1976). There was a high degree of variability in cloacal tempera- tures, both within and between active individuals (Fig. 1), which is similar to the situation in other varanids (King, 1980; King et al., 1989).
The daily activity patterns were also similar to those of other varanids in moderate climatic conditions (King, 1980; Weavers, 1983; King et al., 1989; Wikramanayake and Green, 1989).
The heating rates of the smaller individuals during basking were similar to those reported by Stebbins and Barwick (1968) for V. varius (0.4°C/min), by King (1980) for V. rosenbergi (0.10-0.28°C/min) and by King et al. (1989) for V. giganteus (0.09°C/min). The heating rates of the largest individual (C) were much lower than those of the juveniles which was probably due to its greater body mass (Brattstrom, 1973).
Very few observations were made of the behaviour of the animals in order to minimise disturbing them during their normal activities. Size differences be- tween individuals could account for some of the difference in their thermoregulatory patterns, but individual behavioural differences seem likely to be of greater importance in this regard.
Overnight cooling rates were highly variable, as were the daily minimum cloacal temperatures of individuals, but these were probably determined more by the nature of the selected shelter sites than by differences in body size. The use of shelter sites by varanids to ameliorate the effects of changes in ambient temperatures on body temperature have been discussed by Cowles (1930), Stebbins and Barwick (1968), King (1980), Auffenberg (1981) and King et al. (1989).
The water flux and metabolic rates of some varanids and other carnivorous lizards are shown in Table 2. The high coefficient of variation (C.V.) associated with the mean water influx of V. komod- oensis is greater than that found in most other field
100 BRIAN GREEN et al.
Table 2. Variations in field water influx and metabolic rates of carnivorous lizards
Species H20 In W CO2 C.V. (ml/kg/day) % (ml/g/hr) % Reference
Lacerta viridis 120 24.7 0.425 37.6 Bradshaw et al. (1987) Eremias lugubris 74.4 23.8 0.339 38.1 Nagy et al. (1984) Eremias lineoocellata 47.7 20.5 0.270 49.1 Nagy et aL (1984) Sceloporus graciost~ 25.0 48.3 0.26 41.0 Congdon and Tinkle (1982) Sceloporus (Fall) -- 0.198 54.3 Bennet and Occidentalis (Sp) -- 0.220 27.3 Nagy (1977) Cnemidophorus tigris 36.8 23.4 0.34 17.6 Anderson and Karasov (1981) Callisaurus draconoides 17.1 22.8 0.22 18.2 Anderson and Karasov (1981) Eremias olivieri 174 -- 0.41 -- Vernet et al. (1988b) Acanthodactylus pardalus 70 -- 0.08 -- Vernet et al. (1988b) Varanus acanthurus 15.9 42.8 0.10 31.7 Dryden et al. (in press) Varanus griseus 28.3 19.8 -- -- Vernet et al. (1988a) Varanus (gouldii) rosenbergi 22.0 25.5 -- -- Green (1972) Varanus varius 24.6 37.8 -- -- Weavers (1983) Varanus giganteus 22.3 58.7 0.17 36.3 Green et al. (1986) Varanus komodoensis 25.5 62.8 0.13 29.5 Present study
studies of reptiles and is due in part to the small sample size. However, the C.V. values for varanid water influxes are generally higher than those for other carnivorous lizards and that probably reflects the variability in the activity patterns of individuals (Green, 1972; Vernet et al., 1988a). The C.V. associ- ated with field metabolic rate in V. komodoensis is similar to the values for other carnivorous lizards (Table 2).
Young V. komodoensis are active foragers which are predominantly arboreal, whereas adults are less active and are carrion feeders or ambush predators (Auffenberg, 1981). Lizards that utilise ambush (sit- and-wait) predatory techniques have lower metabolic and water flux rates than active foragers (Anderson and Karasov, 1981; Vernet et al., 1988b).
Thus the lower water influx and metabolic rates of the largest dragon in this study can be explained in part by individual differences in hunting strategy, partly by the lower active body temperature main- tained by the largest animal and in part by the higher food and energy requirements of growing animals.
The precise nature of the diet of the study animals is not known, but by assuming a conservative metab- olisable energy content of 4 kJ/g prey a maximum rate of food consumption required to maintain en- ergy balance can be calculated. The two juvenile animals metabolised about 95 kJ/kg/day equivalent to 220 k J/day and requiring the ingestion of about 55 g food/day to cover this energy expenditure. The adult dragon would expend 2440 kJ and require 610 g of food each day. These daily rates of food consump- tion are equivalent to 2.4% of body mass for juveniles and 1.3% for the adult, both of which are lower than the daily rate of 3.6% estimated by Auffenberg (1981) for large V. komodoensis.
The prey of carnivorous animals has a high free water content. When metabolic water is taken into account, the total water available to a predator represents about 85% of the fresh mass of prey (Schmidt-Nielsen, 1964). Assuming this to be the case with the prey of V. komodoensis, the estimated food intake of animal A would provide 94% of the measured water influx, while that of animal C would provide 87%. The remaining water fraction is probably derived from the exchange of water vapour between the animals and the atmosphere or from drinking. In the case of juvenile B, the water influx
rate was so high compared to its metabolic rate and estimated food intake that it must have had access to drinking water. If the metabolisable energy content of prey was higher than the assumed value, then the estimated rates of food intake would obviously be lower and the estimated magnitude of water intake by vapour exchange and drinking would increase.
Nagy (1982a) has proposed predictive equations for water influx rates of reptiles inhabiting different environments;
Semi-arid/arid H20 influx (ml/day)= 20.5 kg °'91
Tropical H~O influx (ml/day)= 45.0 kg °'~.
These expressions predict water influxes of 43.7 and 78.0 ml/day respectively for a 2.3 kg juvenile dragon (19 and 34ml/kg/day respectively) and 658 and 55 ml/day respectively for a 45 kg adult (14.5 and 12.3ml/kg/day). The recorded water influx rates for V. komodoensis are intermediate between the predicted values, so the animals cannot be clearly ascribed to either the semi-arid or the tropical category.
Nagy (1982b) has also formulated a predictive expression for field metabolic rates in iguanid lizards;
Metabolised energy (k J/day) = 0.224 g0.S0.
The field metabolic rates of all three V. komodoensis were approximately double the values predicted by this equation.
The small sample size obtained in the present study renders the data on water fluxes and metabolic rates of preliminary value only. There is a need for further, more comprehensive studies to be made on the ecophysiology of this interesting species. It is hoped that more detailed information on the behaviour and activity patterns of varanids will facilitate an assess- ment of the relative importance of morphological, physiological and behavioural parameters in the ther- moregulation and metabolism of free-ranging lizards.
Acknowledgement--We are grateful for the assistance of Toni Lumsden in the preparation of the figures.
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