Body temperature and thermoregulation of Komodo dragons in the field

Body temperature and thermoregulation of Komodo dragons in the field

Journal of Thermal Biology 35 (2010) 338–347 Contents lists available at ScienceDirect Journal of Thermal Biology journal homepage: www.elsevier.com...

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Journal of Thermal Biology 35 (2010) 338–347

Contents lists available at ScienceDirect

Journal of Thermal Biology journal homepage: www.elsevier.com/locate/jtherbio

Body temperature and thermoregulation of Komodo dragons in the field Henry J. Harlow a,n, Deni Purwandana b, Tim S. Jessop c, John A. Phillips d a

Department of Zoology and Physiology, University of Wyoming, Laramie, WY 82071, USA Komodo Survival Program, Jalan Pulau Moyo, Komplek Karantina, Denpasar, Bali 80222, Indonesia Department of Zoology, University of Melbourne, Parkville 3010, Australia d Conservation and Research for Endangered Species, Zoological Society of San Diego, Escondido, CA 92027, USA b c

a r t i c l e in f o

a b s t r a c t

Article history: Received 22 September 2009 Accepted 5 July 2010

Komodo dragons from hatchlings ( E0.1 kg) to adults (r 80 kg) express the full magnitude of varanid species size distributions. We found that all size groups of dragons regulated a similar preferred body temperature by exploiting a heterogeneous thermal environment within savanna, forest and mangrove habitats. All dragons studied, regardless of size, were able to regulate a daytime active body temperature within the range 34–35.6 1C for 5.1–5.6 h/day. The index of effectiveness of thermoregulation (a numerical rating of thermoregulatory activity) was not different among size groups of dragons. However, the index of closeness of thermoregulation, which rates the variability of body temperature, suggests a greater precision for regulating a preferred body temperature for medium compared to small and large dragons. Reference copper cylinders simulating small, medium and large Komodo dragons heated and cooled at the same rate, whereas actual dragons of all size groups heated faster than they cooled. Larger dragons heated and cooled more slowly than smaller ones. The mean operative environmental temperatures of copper cylinders representing medium sized dragons were 42.5, 32.0 and 29.41 C for savannah, forest and mangrove habitats, respectively. The index for average thermal quality of a habitat as measured by the absolute difference between operative environmental temperature and the dragon’s thermal range suggests the forest habitat offers the highest thermal quality to dragons and the savannah the lowest. The percent of total daytime that the operative environmental temperature was within the central 50% of the body temperatures selected by dragons in a thermal gradient (Phillips, 1984) was 45%, 15%, and 9% for forest, mangrove and savannah, respectively. Forest habitat offers the most suitable thermal environment and provides the greatest number of hours with conditions falling within the dragon’s thermal activity zone. & 2010 Elsevier Ltd. All rights reserved.

Keywords: Komodo dragon Reptiles Thermoregulation Body temperature Body size

1. Introduction There are about 50 species of varanid lizards that while similar morphologically, vary in mass by nearly 4 orders of magnitude (Pianka, 1994, 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

n

Corresponding author. E-mail address: [email protected] (H.J. Harlow).

0306-4565/$ - see front matter & 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jtherbio.2010.07.002

dramatic change in body size (Auffenberg, 1978, 1981; Jessop et al., 2006). For example, juveniles (o4 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, 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.

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Terrestrial, diurnal lizards behaviorally regulate a plateau or preferred body temperature (Tb) range (Brattstrom, 1965; Diaz, 1994; Christian and Weavers, 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, 1984; Tracy and Christian, 1986; Peterson, 1987; Grant, 1990).

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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 ¼1 (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 ((E¼1  (db/de)) for different size groups of dragons.

2. Materials and methods 2.1. Study area Free ranging Komodo dragons were investigated within a 500 km2 study area within La Buaya Valley (81390 S; 1191430 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. 2.2. 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 that dropped when dragons pulled a release pin attached to bait within the trap. In addition, many dragons of all body sizes were hand captured by overpowering the animal with the aid of several skilled Park rangers. Monitored animals were categorized and subsequently analyzed as their size group consisting of small (5–20 kg; n ¼5), medium (20–40 kg; n ¼6) and large ( 440 kg; n¼7) dragons. VHF tracking transmitters (ATS Inc., North Isanti, Minnesota USA, model M1235; diameter 5.5 cm  11.2 cm length, 650 g weight) were placed on the hip of large dragons with nylon straps that went around their body and crossed their hind limbs, while

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custom built ATS transmitters (weight¼200 g) were placed on medium sized dragons and ATS Model M1235 (diameter 1.8 cm  7.9 cm length, 24 g weight) were placed on smaller dragons (20–5 kg). StowAway Tidbit temperature loggers (0.2 1C accuracy; Onset, Procasset, Massachusetts, USA) were attached to the top of the VHF tracking transmitters to record unshaded ambient temperatures (Ta) around the free ranging dragons without having contact with the skin. The temperature sensor in this model logger is embedded in a loop of resin that protrudes from the side of the unit. The thickness of the resin was reduced to less than 1 mm which provided similar absolute values and only a short thermal lag time when compared to an alcohol thermometer. Deep core body temperature (Tb) of dragons in each body mass group was measured with iButton temperature loggers (Model DS 1921; Maxim, Dallas Semiconductor Inc., Dallas, USA). These loggers were attached to ATS model M1235 telemetry transmitters (cylindrical with dimensions, 1.8 cm diameter  7.9 cm length, 24 g weight with extended range). The telemetry transmitter and attached iButton temperature logger were placed within a piece of meat and fed to dragons. All loggers were programmed to record and store temperatures every 20 min. Once the signal from the internal VHF transmitter did not coincide with the external tracking transmitter on the dragon, we assumed it had been defecated. The transmitter with attached iButton was then located, data down-loaded into a laptop computer with interpretative software (Maxim, Dallas Semiconductor Inc., Dallas, USA) for analysis of daily internal body temperature profiles over the duration of time the logger and transmitter were in the gastrointestinal track of the dragon (2–5 days). After 1–3 weeks of data collection, the VHF tracking transmitter and ambient temperature loggers were retrieved from dragons at night while the animals were sleeping. Data from the ambient temperature logger was down-loaded into a BoxCar Pro 4.0 software program for interpretation (OnSet, Pocasset, Massachustetts, USA). The extent and duration of the preferred Tb range was established as the beginning and end of a Tb plateau that remained within a 70.5 1C range over time. The cooling constant of dragons was calculated from the simultaneously collected Tb (iButton loggers) and Ta (OnSet loggers) by the formula: a ¼ (DTb/Dt)/Tb  Ta where a is the cooling constant and Dt the time difference between the monitoring intervals and is expressed in units on a per animal basis (Bartholomew and Tucker, 1964). It is preferable to take Te as the baseline to calculate the difference between ‘external’ temperature and body temperature (Bakken, 1976). However here we measure the rate of body cooling as a function of air temperature at night in the absence of solar radiation for an approximation of the cooling constant for different size groups of dragons.

2.3. Operative environmental temperature (Te): copper cylinder models To obtain abiotic reference heating and cooling rates in the three microhabitat types we employed three cylinders with sealed caps at both ends representing models of small (6280 cm3), medium (27,224 cm3) and large (67,824 cm3) dragons. The cylinders were constructed of 1-mm-thick copper roll stock and painted a dark gray color with approximately the same reflectivity and absorbance of dragon skin. We attempted to duplicate the spectral pattern of the skin by matching it with various paint combinations sprayed on to plastic squares placed into a spectrophotometer. However, given that carbon pigment paints have a flat spectral response and half the incident solar radiation is in the near-IR band compared to melanin which is

more reflective in the near-IR solar region, the color match is only an approximation. OnSet Temperature Sensor probes (Model S-THA-M006) were fastened into the center of the cylinders midway between each end. Temperatures were recorded every 20 min on a HOBO Weather Station data logger (model H21-001). No thermal gradient was observed along the length of the cylinder; however, we did not attempt to measure the presence of a gradient from the center to the periphery. Komodo dragons are mobile with large home ranges by reptilian standards that encompass many types of microhabitat (Ciofi et al., 2007; Imansyah et al., 2008). From our observations, dragons predominantly select mangrove, savanna or forest microhabitat throughout their daily foraging and thermoregulatory activities. Some studies have placed dozens of models throughout the activity area of their research animal to measure Te (Wouter et al., 1997; King et al., 1998). However, to subdivide further the microhabitats for the Komodo dragon on Rinca island would be difficult for several reasons: dragons have a very large activity range, there is considerable heterogeneity of microhabitats within this range, and dragons use burrows and other refugia, all of which deemed it necessary (Christian and Weaver, 1996) to restrict monitoring of Te and to calculate de on representative plots of mangrove, savanna and shade forest habitats. Even though this use of the de index does not have the same resolution of thermal microhabitat heterogeneity as originally described by Hertz et al. (1993), it is a functional index of thermal quality reflective of microclimatic conditions and the dragon’s behavior as well as physiology (Christian and Weaver, 1996). Small, medium and large cylinder models were placed together in the open savanna, coastal mangrove and shade forest for 24 h on three occasions over a ten day period to determine the Te for each of the thermal habitats. Climate conditions over this period were relatively constant thereby minimizing the variable of fluctuating ambient conditions that could potentially confound the comparison between habitats. Sites for the cylinders were selected based upon observed usage by dragons during days prior to their placement. Passive heating and cooling curves were also recorded for the three model sizes in each of the three thermal habitats. TSET is defined as the central 50% of the Tb’s selected by lizards in a thermal gradient (Hertz et al., 1993). Selected Tb ranges within a laboratory thermal gradient are not available for Komodo dragons. However TSET values for dragons have been determined by Phillips (1984) in an outdoor enclosure with a defined thermal gradient and without variables such as the need for foraging or influence of non-thermoregulatory demands like agonistic behavior or social interaction, which may alter daily movement activities from those of strict temperature selection. The index of the average thermal quality of a habitat (d¯e) was calculated as the mean of the absolute value of the deviations of Te’s in each of the 3 habitats from TSET and is expressed as 1C (Huey, 1982; Hertz et al., 1993). If daily Te values are below (or above) the TSET range, de is the difference between the Te’s and the lower (or upper) boundary of TSET. Readings of Te’s that are within the TSET range are assigned a deviation value of 0, but are included in the total P number of observations to calculate mean d¯e as de/number of observations made between 0600 and 1900 (Huey, 1982; Hertz et al., 1993). An index of the closeness of thermoregulation (d b) to TSET is calculated as the mean deviations of field active Tb’s from TSET in an analogous manner as described for d e made during the 0600–1900 activity period and is also expressed as 1C (Huey, 1982; Hertz et al., 1993). The index of effectiveness of thermoregulation (E) was determined by the formula: E¼1 (d b/d e) and is a scale between 0 and 1 with no units. The index for exploitation of the available time in the set-point range (Ex) was calculated as the % of total Tb’s of a dragon that are within the TSET.

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Body temperature transmitters remained within the gastrointestinal track for an average of 3.5 ( 71.2 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 1C) nor the duration (Fig. 3: 5.1–5.6 h) of the preferred temperature of dragons in all three body size groups. However, large dragons had a significantly smaller daily Tb change from morning to afternoon (5.170.38 1C) than medium (6.670.44 1C) and small dragons (7.370.61 1C). The rate of heating was significantly greater than the rate of cooling (as represented by examples in Fig. 4A) and by the positive and negative slopes for heating and cooling curves for lizards in all size groups (Table 1). Small dragons had a significantly greater heating slope than medium and large dragons (Table 1) and there was a linear relationship between the cooling constant (a) and body mass of dragons with large dragons exhibiting a greater thermal conductance when expressed on a per animal basis (Fig. 5). On the other hand, there was no significant difference between rates of heating and cooling of small, medium and large cylinder models; all showed similar positive and negative slopes as depicted for a representative dragon in Fig. 4B. The Te of savanna, forest and mangrove thermal habitats reached their peak values of 55, 35 and 32 1C, respectively, at approximately 1200 (Fig. 6A–C). However, the Tb profiles of dragons in all size groups were different from that of Te in each of the habitat types and they exhibited an approximate 1–2 h thermal lag between the peak Te and onset of their preferred Tb. The mean time of day for the beginning of the preferred Tb plateau (Fig. 6A–C) was mid afternoon (about 1300 h) with a greater delay from peak Te for

LARGE DRAGON

BODY TEMPERATURE (°C)

38 36 34 32 30 28 26 0600

0600

0600

0600

0600

TIME OF DAY (HOURS) Fig. 1. Deep core body temperature profile for a representative free ranging Komodo dragon (70 kg) over a four day period obtained from an ingested iButton logging Tb every 20 min.

36 BODY TEMPERATURE (°C)

3. Results

38

34 32 30 28 26 24 22 20 SMALL

MEDIUM

LARGE

Fig. 2. Mean preferred core body temperature of small (n¼ 5), medium (n¼ 6) and large (n¼ 7) free ranging Komodo dragons obtained from ingested iButton logging Tb every 20 min. Vertical bars represent 7 SE.

7 6 5 TIME (HOURS)

A similar protocol was used to determine the frequency for each Te of cylinder models in the savanna, forest and mangrove habitats that were within the TSET range. Analysis of variance (ANOVA) was conducted with a Tukey test for interaction when comparing the extent and duration of preferred Tb, slopes of heating and cooling curves, mean daily temperatures and de, db, E as well as Ex between animals within the different groups (Zar, 1999).

341

4 3 2 1 0

SMALL

MEDIUM

LARGE

Fig. 3. Mean duration (hours) that the core body temperature (obtained from iButton logging Tb every 20 min) was maintained within the preferred temperature range for small (n¼ 5), medium (n¼6) and large (n¼ 7) free ranging Komodo dragons. Vertical bars represent 7 SE.

large dragons (1.570.4 h) compared to medium and small dragons (0.5 70.1 and 0.470.2 h, respectively). The mean time for the Tb to begin declining from the preferred Tb plateau was late afternoon (about 1800 h) with larger dragons expressing later onset of decline than medium and small dragons. The mean daily active Tb calculated from the temperature frequency profiles between 0600 and 1900 h was 33.5 1C for small and medium sized dragons (Fig. 7A, B) with large dragons (Fig. 7C) significantly lower (32.5 1C). The temperature with the highest frequency during the activity period of 0600–1900 h was 34.5, 34 and 32.5 1C for small, medium and large dragons (Fig. 7A–C). The index for exploitation (Ex) which is defined as the % of time between 0600 and 1900 h a dragon spends within the TSET range was 66%, 82% and 64% for small, medium and large dragons, respectively. The mean daily Te between 0600 and 1900 h for a medium sized cylinder was 42.5, 32.0 and 29.4 1C for the savanna, forest and mangrove habitats, respectively (Fig. 8A–C), with concomitant values for the highest frequency of observed daily Te at 51, 34 and 29 1C, respectively (Fig. 8A–C). The percent of the total daytime (between 0600 and 1900 h) the Te was recorded to be within the dragon’s TSET for the mangrove,

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-1.4 LOG COOLING CONSTANT

LARGE DRAGON

40 35 TEMPERATURE (°C)

30 y = 0.3211x + 27.591 R2 = 0.9562

25 20

y = -0.1786 x + 41.831 R2 = 0.9742

15 10

-1.6 -1.8

a = - 1.23 M-0.766

-2

y = -0.7659x - 1.2315 R2 = 0.8452

-2.2 -2.4 -2.6 -2.8

5

0

0 0

5

15

10

20

25

TIME (HOURS)

100

Fig. 5. Log–log plot of cooling constant (a) and body mass (kg) where a ¼  (DTb/ Dt)/Tb  Ta. Body temperature (Tb) was obtained from recordings every 20 min on ingested iButton loggers and ambient temperature (Ta) recorded every 20 min from an OnSet logger attached to the external body of free ranging Komodo dragons. Change in Tb was expressed on a per animal basis.

LARGE CYLINDER IN SAVANNA

70

10 LOG BODY MASS (Kg)

TEMPERATURE (°C)

60 50

4. Discussion

40

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-tovolume 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 a progressive reduction in mid-day shuttling activity, perhaps as a result of greater thermal inertia. The second is related to transitional foraging and predatory behavior as dragons increase in size. Small dragons feed on insects, lizards, rodents and birds (and eggs) that are either on the ground or in trees (Auffenberg, 1981). The availability of food, constraints on prey size, and their higher mass specific metabolic rate may result in a more continuous foraging activity by small dragons throughout the day. Medium sized animals ( o40 kg) ingest larger prey such as nesting birds and juvenile ungulates, and they feed on carrion (Auffenberg, 1981). However, it is believed that only larger dragons in excess of 50 kg are capable of the more sedentary sit-and-wait ambush predation required to kill adult deer, pig and buffalo (Auffenberg, 1981). Transitions in predatory behaviors by dragons of varying size should influence their differential selection of habitat with concomitantly individualized exposure to sun, shade and wind that are the primary determinants of heat transfer and Tb. We set out to determine whether: (1) dragons of all body size effectively thermoregulate the same preferred Tb or (2) their thermoregulatory and foraging behaviors are so different that it results in a unique preferred Tb for each size class. Many previous studies have attempted to identify the range of preferred temperatures for different size groups of Komodo dragons in the field. McNab and Auffenberg (1976) report the Tb of four active dragons (7–35 kg) by telemetry to be in the range 35–40 1C. However the variability in these data was quite large and no association was made to mass specific Tb. Green et al. (1991) also monitored four animals by telemetry in a similar size group (2–45 kg) as McNab and Auffenberg (1976) and found their mean active Tb to be 32.7, 33.3, 34.4 and 37.7 1C. Again, no reference was made between the body mass and Tb of each animal. Wikramanayake et al. (1999) monitored three adult and three juvenile dragons and concluded that both groups of free ranging

30

y = 0.9857x + 26.959

20

y = -0.8382x + 87.109 R2 = 0.9776

R2 = 0.9136

10 0 0

5

10

15

20

TIME (HOURS) Fig. 4. (A) Heating and cooling curve for a representative free ranging Komodo dragon (obtained from ingested iButton logging Tb every 20 min). (B) Heating and cooling curves of a large copper cylinder (67,824 cm3) in the savanna, logged every 20 min.

Table 1 Slope for the regression lines through Tb’s obtained every 20 min from ingested iButton loggers during heating and cooling by free ranging small (n ¼5), medium (n¼ 6) and large (n¼ 7) Komodo dragons. Data is expressed as mean 7SE. Dragon group size

Heating slope

Cooling slope

Small Medium Large

0.424(7 0.090)a,b 0.270(7 0.030)a 0.230(7 0.025)a

0.181(7 0.065) 0.110(7 0.034) 0.139(7 0.043)

a

Represents heating significantly different from cooling. Represents small dragons significantly different from other size groups. Significance level is set at Po 0.05. b

savanna and forest habitats was 9%, 15%, and 45%, respectively (Fig. 8A–C). The index of closeness of thermoregulation (d b) was significantly lower (i.e. less deviation) for medium compared to small and large dragons while in the forest habitat (Table 2A). And the index of average thermal quality of a habitat (d e) for dragons was greatest (lowest number) for the forest habitat and lowest (highest number) for the savanna (Table 2B). The index of effectiveness of thermoregulation (E) was not significantly different between dragon size groups (Table 2A) but the value was lowest (less thermoregulation) in the forest for all size groups (Table 2B).

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SMALL CYLINDER (FOREST, MANGROVE AND SAVANNA) SMALL THERMOREGULATING DRAGON

60

55

50 45 SAVANNA (Te)

40 TSET

30

FOREST (Te)

SMALL DRAGON (Te) MANGROVE (Te)

25

TEMPERATURE (°C)

TEMPERATURE (°C)

MEDIUM CYLINDER (FOREST, MANGROVE AND SAVANNA) MEDIUM THERMOREGULATING DRAGON

60

55

35

343

50 45

SAVANNA (Te)

40

MEDIUM DRAGON

TSET

35

FOREST (Te) MANAGROVE (Te)

30 25

20 0600

1800 TIME (HOURS)

0600

20 0600

1800 TIME (HOURS)

0600

LARGE CYLINDER (FOREST, MANGROVE AND SAVANNA LARGE THERMOREGULATING DRAGON

60

TEMPERATURE (°C)

55 50 45

SAVANNA (Te)

40 35

TSET

30

DARGE DRAGON FOREST (Te) MANGROVE (Te)

25 20

0600

1800

0600

TIME (HOURS) Fig. 6. Plots representing temperature ( 1C) for (1) operative environmental temperature (Te) obtained from monitoring copper cylinders every 20 min in savanna, forest and mangrove habitats, (2) the body temperature (Tb) obtained from ingested iButton loggers every 20 min and (3) TSET range (shaded horizontal bar; Phillips, 1984) for representative small (A), medium (B) and large (C) free ranging Komodo dragons.

dragons had similar daytime Tb. But, conclusions on mass specific differences cannot be obtained because there was considerable variation of Tb within each group and the body mass of individuals was not reported. In a laboratory study, Walsh et al. (1999) also compared Tb of adult and juvenile dragons, and like Wikramanayake et al. (1999) found these groups to have similar body temperatures (35.5, 35 1C, respectively). However, in the same manner as Wikramanayake et al. (1999) the body mass of these animals was not recorded. Overall, these previous studies allude to a wide range of active Tb between 32.7 and 37.7 1C and each suffers limitation in either the design or data reporting that prevent identifying the presence or absence of size dependent differences in Tb of free ranging Komodo dragons. Our study, on the other hand, identifies the ability of dragons to thermoregulate a preferred Tb and establishes that this is a species-specific trait with an overall mean of about 35 1C shared by all size groups. Small, medium and large dragons heated faster than they cooled. We believe this involves a physiological process because copper cylinder models of all size groups in each of the habitat types heated and cooled at the same rates. Dragons could therefore be exhibiting an adaptive cardiovascular response (i.e. heart rate hysteresis) with enhanced peripheral vasodilation during heating compared to vasoconstriction during cooling as described in other varanid lizards (Grigg et al., 1979; Seebacher and Grigg, 2001; Seebacher and Shine, 2004). Interestingly,

McNab and Auffenberg (1976) calculated cooling constants on four dragons ranging from 7–35 kg and found these values to be well below that predicted by allometric equations of varanids (Bartholomew and Tucker, 1964). However, this may be a result of these animals being tethered overnight in the open sky and therefore do not represent naturally occurring conditions. In contrast, we were able to monitor simultaneously the Tb of dragons from the ingested iButton loggers and the ambient temperature (Ta) that dragons experience by using the Tidbit loggers located on top of the tracking transmitters attached to free ranging animals. As a result, we were able to calculate the cooling constant (a) on unimpaired dragons of varying body mass. As pointed our by Bakken (1976), the cooling constant is best determined using Te of animals in a laboratory setting with a stable end temperature (Bartholomew and Lasiewski, 1965). In spite of this, our calculations using Ta of free ranging dragons resulted in the allometric relationship: a ¼ 1.23 M  0.766 which, unlike the results of McNab and Auffenberg (1976), is very close to the value reported by Bartholomew and Tucker (1964) for varanids. The benefit of enhanced heating would allow dragons of all size groups to reach their preferred Tb rapidly while the benefit of slow cooling would retard the Tb drop during the night prior to rewarming in the morning. Equilibrium between Tb and the environment was never achieved, suggesting that slowing the

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14 12 10

Mean Tb 33.5º ▼

8 6 4 2 0

TSET

16 PERCENT OF OBSERVATIONS (%)

PERCENT OF OBSERVATIONS (%)

16

MEDIUM DRAGONS

SMALL DRAGONS TSET

26 28 30 32 34 36 38 40 42 44 46 48 50 52 54 56

Mean Tb 33.5º ▼

14 12 10 8 6 4 2 0

26 28 30 32 34 36 38 40 42 44 46 48 50 52 54 56

TEMPERATURE (°C)

TEMPERATURE (°C) LARGE DRAGONS

PERCE NT OF OBSERVATIONS (%)

16 14 12

TSET Mean Tb 32.5º ▼

10 8 6 4 2 0

26 28 30 32 34 36 38 40 42 44 46 48 50 52 54 56 TEMPERATURE (°C)

Fig. 7. Plots of % of observations of Tb (taken every 20 min between 0600 and 1900) that were recorded at 0.5 1C categories from small (A; n¼5), medium (B; n¼ 6) and large (C; n¼7) free ranging Komodo dragons with TSET represented by vertical shaded bars (Phillips, 1984) and . symbol depicts the mean daily Tb.

cooling rate during the night did reduce the amplitude of change required to reach the preferred Tb the next day. Indeed, there was a significant size related difference between the daily minimum and maximum Tb with large dragons showing a 5.1 1C change compared to 7.3 1C for small dragons. There are fitness costs and benefits to thermoregulation (Huey, 1982). The longer an animal basks to get to its preferred Tb, the greater the risk (e.g. predation; resource defense issues). But, the longer an animal remains within its preferred Tb range with optimal function, the greater the benefit. Small dragons heated faster than large dragons and there was a linear relationship with a lower cooling constant and high thermal conductivity for larger dragons when expressed on a whole animal basis. However, it appears that this evens itself out over size groups in that the duration of the preferred Tb is the same for combined size groups commencing at around 1300 h and ending at about 1800 h. These times are within the ranges reported by Wikramanayake et al. (1999) and Green et al. (1991). Even though there was no significant difference between size groups in the time for beginning or ending the preferred Tb plateau, there was a trend

for larger dragons to begin and end their preferred Tb later in the day than medium and smaller dragons resulting in a similar duration for the preferred plateau for all size groups. Four features established by Hertz et al. (1993) and emphasized by Bauwens et al. (1996) that are needed for a comprehensive assessment of behavioral thermoregulation by animals in the field are: (1) data on behavioral mechanisms such as shuttling activity that can alter rates of heat exchange and produce Tb’s that differ from a random sample of Te’s, (2) the selected temperature range or TSET that identifies the Tb’s that reptiles attempt to achieve in the absence of environmental constraints on temperature regulation, (3) the distribution of available Te’s which predict the Tb distribution in a population of reptiles that do not regulate Tb, and (4) field active Tb’s of a population that represent the final product of either temperature regulation or thermal conformity (see Bauwens et al., 1996). From our studies, we now understand that the three size groups engage in different thermoregulatory behaviors ranging from sun shuttling and continuous foraging to sedentary microhabitat selection during sit-and-wait predation (Harlow et al., in press). We have previously determined the TSET

FOREST

TSET

16 14

PERCENT OF OBSERVATIONS (%)

PERCENT OF OBSERVATIONS (%)

H.J. Harlow et al. / Journal of Thermal Biology 35 (2010) 338–347

Mean Te 32.0?C ▼

12 10 8 6 4 2 0

16 14

MANGROVE TSET

12 10 8 6 4 2 0

26 28 30 32 34 36 38 40 42 44 46 48 50 52 54 56 TEMPERATURE (°C)

Mean Te 29.4° ▼

345

26 28 30 32 34 36 38 40 42 44 46 48 50 52 54 56 TEMPERATURE (°C)

SAVANNA TSET

PERCENT OF OBSREVATIONS (%)

16 14

Mean Te 42.5°C ▼

12 10 8 6 4 2 0

26 28 30 32 34 36 38 40 42 44 46 48 50 52 54 56 TEMPERATURE (°C)

Fig. 8. Plots of % observations of Te (taken every 20 min from medium sized copper cylinders between 0600 and 1900) recorded at 0.5 1C categories in forest (A), mangrove (B) and savanna (C) habitats. TSET is represented by vertical shaded bars (Phillips, 1984) and . symbol depicts the mean daily Te.

Table 2A Index of the closeness of thermoregulation to TSET (db), index of effectiveness of thermoregulation (E) and index for exploitation of the available time in the TSET range (Ex) by small, medium and large Komodo dragons. Dragon size

d¯b (1C)

E

Ex (%)

Small Medium Large

0.722 0.357 0.747

0.215 0.608 0.719

66 82 64

Table 2B Index of average thermal quality of a habitat (de). Index for exploitation of the available time in the TSET range (Ex) by a medium sized cylinder in the savanna, forest and mangrove habitats and index of effectiveness of thermoregulation (E) by small, medium and large Komodo dragons. Habitat type d¯e (1C) Ex (%) E Small dragons Medium dragons Large dragons Savanna Forest Mangrove

7.71 0.91 2.50

15 45 9

0.906 0.215 0.712

0.954 0.608 0.857

0.903 0.179 0.701

values of Komodo dragon housed in the Jakarta zoo (Phillips, 1984). We used copper cylinder models with low heat capacity, a similar general shape as dragons and painted a color to approximate absorbance qualities of field animals as suggested by Hertz et al. (1993). These models were placed into the 3 representative habitats found on the island. Three to five days of continuous deep core body temperatures were obtained from ingested iButton temperature loggers that provided continuous Tb profiles at 20 min intervals on free ranging dragons. As a result, we have met the criteria recommended by Hertz et al. (1993) and Bauwens et al. (1996) to use these data and evaluate thermoregulatory efficiency as well as habitat use by dragons in our study area. Here we use plots that superimpose the mean frequency of each Tb achieved during hours of activity with the TSET range (Fig. 7A–C) to determine the percent of time animals are within their TSET. This percentage is referred to as the index of thermal exploitation (Ex) and expresses the amount of time available to each size group of dragons to achieve a Tb within the set-point range (Christian and Weaver, 1996). Small and large dragons spend 66% and 64% of their daily activity within the TSET while medium sized dragons spend a considerably greater (82%) amount of time within the TSET range as expressed by a higher

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Ex value. In addition, the index of closeness of thermoregulation (db) indicates lower deviation from TSET by medium sized dragons compared to other size groups (Table 2A and B). In spite of this, they do not have a longer duration of their preferred Tb compared to the other size groups. However, a potential benefit from the higher Ex and db of medium sized dragons would be that they spend less time in peripheral thermal environments and thereby conserve energy by remaining longer in a more thermally homogenous environment. This is supported by medium sized dragons having an index of effectiveness of thermoregulation (E) value indicative of the lowest cost for thermoregulation of all size groups. In other varanid lizards, E can exhibit large seasonal variation reflecting differences in activity and thus access to heterogeneity in microclimate (Christian and Weaver, 1996). If Komodo dragons exhibit differences in daily activity to support ontogenetic differences in foraging ecology (e.g. habitat use) then interactions between body mass and activity might be expected to influence E (Seebacher and Shine, 2004). Also of interest is the lower average mean Tb for larger dragons. While their preferred Tb is not significantly different from that of medium and small dragons, it appears that they spend a greater part of the day with Tb’s below the TSET range but never above it. Our observations support that of Green et al. (1991) that larger dragons may be achieving a lower daily mean Tb. In contrast to this left skewed distribution of Tb by large dragons, the small dragons have a greater body temperature range that is often well above the TSET but they also thermoregulate a similar preferred Tb as the other size groups. Several reasons may explain this difference and may be directly related to ontogenetic differences in foraging ecology interacting with the physical properties of a Komodo dragon’s mass. Overall, dragons spent 7–10 h thermoregulating within their TSET. Interestingly, the duration (1300–1800 h) where dragons of all size groups maintain their preferred Tb (34–35.6 1C: Fig. 2) with high cellular enzyme and organ function (Dawson, 1975), is primarily within their TSET range. This preferred temperature range is also similar to the 34– 36.5 1C recorded for other terrestrial varanid lizards in Australia (at least during summer) and may suggest a relatively conserved physiological thermal optima despite obvious phylogenetic and ecological differences among species (Christian and Weaver, 1996; Seebacher and Grigg, 2001). We calculated the d e (mean deviation between Te and TSET) that represents the thermal quality of the habitat (Hertz et al., 1993). A small d e implies that the optimal microclimate conditions are abundant in the habitat, but if the d e is large, the dragons must thermoregulate carefully to stay within the TSET range. In this regard, the savanna habitat is the most extreme (d e ¼7.7) followed by the mangrove (d e ¼2.2) with the shade forest providing the most abundant optimal microclimate conditions (d e ¼0.91). Fig. 6A–C exemplifies this relationship by showing the large deviation between Tb of dragons from the extremely high mean daily Te (42.5 1C) in the savanna and low mean daily Te (29.4 1C) in the mangrove. Even though there was a general 1–2 h lag in response time, the dragon Tb was closely matched to that of the shade forest (Figs. 6 and 8). Indeed, the forest habitat offers conditions conducive to thermoregulation within the dragon’s set-point range 45% of the day compared to only 9% in the mangrove and 15% in the savanna. While dragons forage between these 3 habitat types, it has been observed that little time is spent in the open savanna other than transient movements through the animals’ foraging range. The mangrove offers temporary refugia, but, it is the forest that presents the most thermally advantageous habitat. Additionally, it is this area that is associated with the greatest diversity of prey abundance with small rodents and lizards for the smaller predators to larger ungulates for the sitand-wait hunters.

5. 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 nonthermoregulating copper models and large dragons cool slower than small dragons, but they retain the same duration of the preferred Tb plateau by exhibiting a lower daily difference between maximum and minimum Tb. Medium sized dragons appear to have a greater efficiency of thermoregulation that could be linked to size specific differences in their foraging ecology. Forest habitat offers the most suitable thermal habitat and provides the greatest number of hours with conditions within the dragon’s thermal activity zone. The five islands that are home for Komodo dragons are experiencing a proliferation of prickly pear cactus (Opuntia sp.) as a non-endemic invader species. A potential concern is that this cactus may impact Komodo dragons by reducing forest habitat edge as an important component of their thermoregulatory and foraging capacity.

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