Body temperature and thermoregulation of Komodo dragons in the field
Introduction
There are about 50 species of varanid lizards that while similar morphologically, vary in mass by nearly 4 orders of magnitude (Pianka, 1994, Pianka, 1995). The Komodo dragon (Varanus komodoensis) is the largest of these carnivorous lizards, and is found only on 5 islands in the Lesser Sunda region of south eastern Indonesia (Ciofi and de Boer, 2004, Jessop et al., 2006). Dragons forage in three major habitat types on these islands; coastal mangroves, open savanna and broken shade forests (Auffenberg, 1981), which offer their own distinct prey abundance and thermal characteristics.
During growth from hatchlings (0.1 kg) to adults (maximum of 87 kg in this study), Komodo dragons express almost the entire range of body size distribution of the genus Varanus. Concomitant changes in predatory strategies and dietary niche breadth accompany this dramatic change in body size (Auffenberg, 1978, Auffenberg, 1981, Jessop et al., 2006). For example, juveniles (<4 kg) are predominantly arboreal and forage on lizards, birds and insects (Imansyah et al., 2008). Medium sized dragons are largely terrestrial and generalist predators, while larger dragons increasingly supplement their diet with large ungulate prey including Timor deer (Cervus timorensis), wild pigs (Sus scrofa), and to some extent water buffalo (Bubalus bubalis) (Auffenberg, 1981, Jessop et al., 2006). Diet undergoes an ontogenetic shift associated with differences in feeding strategy as dragons change from active foraging in small individuals, through a more sedentary sit and wait strategy in larger individuals (Auffenberg, 1978, Auffenberg, 1981, Ciofi and Bruford, 1999).
The ontogeny of growth may also be associated with altered thermoregulatory behavior. For example, small dragons are active sun shuttlers, while medium sized animals move less between sun and shade, and large dragons become sedentary throughout the afternoon (Auffenberg, 1981, Harlow et al., in press). Thus, each size group of dragons may be using selected microhabitats and interact with their thermal environment differently.
Terrestrial, diurnal lizards behaviorally regulate a plateau or preferred body temperature (Tb) range (Brattstrom, 1965, Diaz, 1994, Christian and Weaver, 1996, Tosini and Avery, 1996). Measurements of the Tb of lizards during daytime activity periods suggest that lizards have a single species-specific preferred Tb (Cowles and Bogert, 1944, Templeton, 1970), implying that the preferred temperature is the same for all size groups. However, it has also been suggested that larger reptiles (with smaller surface area to volume ratios) have a higher preferred body temperature with a greater thermal constancy (Spotila et al., 1973).
Huey (1982) presents a model for ectotherm thermoregulation based on the assumption that reptiles incur costs (energy loss, risk of predation) as well as derive benefits (energy gain; avoid overheating) from thermoregulation. Benefits of the mean selected (or preferred) temperature correlate with the optimal temperature of many tissue and cellular functions (Dawson, 1975). The range of Tb over which lizards are generally active tends to maximize the amount of assimilated energy (Angilletta, 2001). The broader the preferred temperature range, the more energy that can be utilized in growth and reproduction. On the cost side, the longer it takes to bask and reach the preferred Tb, the greater the risk. Indeed, body size influences the heat balance of ectotherms through varying behavioral and physiological mechanisms that control Tb (Heinrich, 1981, Bartholomew, 1982, Huey, 1982, Huey and Stevenson, 1979). For example, small ectotherms can heat up relatively quickly allowing them to take advantage of shorter intervals of time that are thermally favorable for daily activity (Cowles and Bogert, 1944, Grigg et al., 1979, Robertson and Smith, 1981, Diaz, 1997) while large ectotherms would be unable to show similar patterns because of their long thermal time constant (Stevenson, 1985, Grigg et al., 1998). However, the thermal inertia of large ectotherms may also have an advantage. These animals can potentially have less thermoregulatory constraints in their environment during a day because their mass buffers them from extreme Tb fluctuations (Spotila et al., 1973, McNab and Auffenberg, 1976, Stevenson, 1985), resulting in longer daily activity periods (Stevenson, 1985).
We first address the question of whether: (1) the preferred Tb of the Komodo dragon exhibits size group differences in both the extent and duration of their preferred Tb or (2) the size groups compensate for body mass differences in thermal conductance through thermoregulatory behavior and achieve a similar preferred Tb profile. To address this question, we non-invasively monitored continuous daily Tb and compared heating/cooling curves and preferred Tb profiles of free ranging dragons spanning a body mass of 5–80 kg.
By knowing the Tb activity range of Komodo dragons thermoregulating in a homogenous environment with an approximated thermal gradient (Phillips, 1984), referred to as TSET, and the operative environmental temperature (Te) of the major habitat types, we address a second question of how carefully dragons of varying body size regulate their body temperature. The Te can be determined by using microclimatic data (Tracy, 1982, Bakken, 1992, O’Conner and Spotila, 1992) or physical models with thermal properties similar to those of the animal (Bakken, 1992). For the latter, Crawford et al. (1983) defined Te as the temperature of an inanimate object of zero heat capacity with the same size, shape and radiative properties of the animal exposed to the same microclimate. In this study, we monitored copper cylinders representing the various size groups in each of the thermal habitats. These techniques allowed us to determine how well Komodo dragons can attain and maintain their preferred Tb while freely moving under natural field conditions in the given habitats (Christian et al., 1983, Christian et al., 1984, Tracy and Christian, 1986, Peterson, 1987, Grant, 1990).
Indices to evaluate how carefully an ectotherm thermoregulates and the relationship between Tb and Te have been presented by Hertz et al. (1993) and others (Christian and Weavers, 1996). For example, the index of average thermal quality of the habitat (d¯e) is the mean of deviations that Te is recorded to be above or below the range of TSET during the daily activity period. A small de implies that optimal microclimate conditions are abundant in the habitat while a large value suggests that the animal must thermoregulate carefully to stay within the TSET range. The index of closeness of thermoregulation (d¯b) is the mean of deviations of internal Tb that is recorded above and below the TSET range during the daily activity period. The direct comparison of db with de serves as an indicator of thermoregulation and is expressed as the index of effectiveness of thermoregulation ((E=1−(d¯b/d¯e)). This value generally ranges from 0 (indicating no thermoregulation) to 1 (indicating very acute thermoregulation). The index of exploitation (Ex) is the average time a lizard spends in the TSET range.
Previous studies on the thermobiology of dragons in the field (Darevasky and Kadarsan, 1964, McNab and Auffenberg, 1976, Auffenberg, 1981, Green et al., 1991, Wikramanayake et al., 1999) or in confinement (Walsh et al., 1999) have provided fragmented profiles taken on a limited size range of animals (only up to 45 kg), by variable means of capture as well as monitoring. As a result, no accumulated data provides a sufficient basis upon which to assess Komodo dragon’s precision of thermoregulatory ability or habitat selection.
The specific objectives of this study are to compare small, medium and large dragon in terms of (1) extent and duration of the preferred Tb, heating and cooling rates and cooling constant, (2) operative environmental temperature (Te) using copper cylinder models in the forest, mangrove and savanna habitats, (3) percent of observations the Tb was found within the TSET range (Ex) while in the forest, mangrove and savanna habitats, (4) the mean of deviations that Te and Tb of small, medium and large dragons (db) and cylinders (de) were outside of the TSET range and from this (5) calculate the index of effective thermoregulation ((E=1−(db/de)) for different size groups of dragons.
Section snippets
Study area
Free ranging Komodo dragons were investigated within a 500 km2 study area within La Buaya Valley (8°39′S; 119°43′W) on the island of Rinca within Komodo National Park, Indonesia during the late dry season (October/November). All animal handling procedure and experimental design were approved by Komodo National Park authorities and the animal welfare committee of the Zoological Society of San Diego.
Animal capture and monitoring
Dragons ranging from 5 to 70 kg were captured in 0.5 m×0.5 m×3 m aluminum traps with a sliding door
Results
Body temperature transmitters remained within the gastrointestinal track for an average of 3.5 (±1.2 SE) days. Dragons reached their lowest body temperature between 0600 and 0700 h and their highest Tb during mid-afternoon (Fig. 1). All animals, regardless of size, achieved a preferred body temperature during the day that was relatively constant (Fig. 1). There was no significant difference between the extent (Fig. 2: 34–35.6 °C) nor the duration (Fig. 3: 5.1–5.6 h) of the preferred temperature of
Discussion
There are at least two interdependent influences on the thermoregulatory biology of Komodo dragons that span the full magnitude of varanid body size during ontogenetic growth. The first is the physical relationship of heat transfer as the surface-to-volume ratio decreases with increased body size. In an associated study (manuscript in press) we found that small dragons engage in greater sun shuttling behavior than large dragons and they continue this throughout the day while larger dragons show
Conclusions
Even though Komodo dragons can exhibit four orders of magnitude difference in body mass through development and growth, they thermoregulate the same species-specific preferred body temperature in extent and duration for all size groups (at least over the period of our study). They show physiological control by heating faster than they cool compared to non-thermoregulating copper models and large dragons cool slower than small dragons, but they retain the same duration of the preferred Tb
Acknowledgments
Special thanks are given to Cladio Ciofi for use of telemetry equipment, advice and assistance in the field. Appreciation is extended to Jeri Imansyah and to all of the Komodo National Park rangers on Rinca for their hospitality, hard work and enthusiastic participation on this project which was a collaborative effort between Komodo National Park and the Zoological Society of San Diego. Financial support for this study was provided by the Zoological Society of San Diego and the Offield Family
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