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Body surface temperature and length in relation to the thermal biology of lizards

Body surface temperature and length in relation to the thermal biology of lizards Volume 1 † Number 2 † June 2008 10.1093/biohorizons/hzn014 ......................................................................................................................................................................................................................................... Research article Body surface temperature and length in relation to the thermal biology of lizards Daniel Garrick* Canterbury Christ Church University, Canterbury, UK. * Corresponding author: Flat 4, 89 Henver Road, Newquay, Cornwall TR7 3DJ, UK. Email: daniel_garrick@hotmail.co.uk Supervisor: Georges Dussart, Canterbury Christ Church University, Canterbury, UK. ........................................................................................................................................................................................................................................ This study investigated body surface temperature (T ) in 22 lizards of 18 species. The difference between T and ambient temperature bs bs (T ) was correlated with size. The greater T 2 T differentials, which were recorded in larger lizards, may occur as a result of heat transfer a bs a from the core to surface in prevention of overheating. The structure of the integument may contribute to heat dissipation. Heliothermy and thigmothermy as forms of thermoregulation were also incorporated into the data set. Heliothermic lizards showed a positive cor- relation between length and T 2 T . Thigmothermic lizards, however, exhibited a negative correlation. Differences in size and rate of bs a conductive heat transfer are put forward as possible reasons for the negative correlation. Key words: thigmothermy, heliothermy, lizard, length. ........................................................................................................................................................................................................................................ Lizards, like most reptiles, are ectothermic. Ectothermy is the Heliothermy is a well-documented area in lizard reliance on external heat sources to increase body tempera- biology. A principal reason for this bias is that diurnal 1, 2 ture. Thus lizards gain heat, principally, from their basking lizard species are often the dominant vertebrates in environment. To achieve optimum body temperature hot arid environments and data on these animals are rela- lizards perform different thermoregulatory behaviours. tively easy to obtain. In contrast, Belliure and Carrascal Thermoregulation is a well-documented area of reptile suggest thigmothermy is a less well-studied aspect of 3– 5 biology. animal thermal relations. The use of thermoregulation to achieve and maintain In general, thigmothermy is practised by species that have optimum body temperature has contributed to the great limited access to solar radiation. Most studies of lizard 12, 13 diversity of lizards and even allowed colonization of temper- thigmothermy have considered diurnal species. Among ate regions. For example, through simple body posturing, diurnal lizards, thigmothermy is normally practised by some species within the South American genus Liolaemus species in forest environments where incoming solar radi- can attain body temperatures 308C above the ambient temp- ation is impeded by the tree canopy. Morgan suggests erature. Such a high differential, though uncommon, that in such environments, thermally discrete microclimates emphasizes the diversity of thermal relations among lizards. are important. In contrast thigmothermic behaviour is rela- Heliothermy and thigmothermy are further means of tively more important for nocturnal lizards, which do not ectothermal thermoregulation. Heliothermy is heat gain receive any solar radiation input. by short wavelength solar radiation. Thigmothermy involves Previous studies of thermal interactions between lizard and heat conduction to the reptile body by direct contact with a environment have predominantly used the internal body temp- warm substratum. In practise, heliothermy and thig- erature (T ) (i.e. cloacal) and ambient temperature (T ) differ- b a 12, 15 – 17 15 16 mothermy enable lizards to compensate for the thermal con- ential. Auffenberg and Stevenson related body ditions of the habitat. Heliothermy and thigmothermy in temperature to size. These authors concluded that larger size lizards are therefore related to habitats and life-history conferred a greater T 2 T differential due to thermal b a strategies. inertia. Thermal inertia is based upon the physical properties ......................................................................................................................................................................................................................................... 2008 The Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 136 Bioscience Horizons † Volume 1 † Number 2 † June 2008 Research article ......................................................................................................................................................................................................................................... Table 2. Key to list of collections used in study of heat dissipation whereby larger objects retain heat for longer than smaller objects due to reduced surface-to-volume Collection Abbreviation scaling. Such a phenomenon has been demonstrated in extant ................................................................................................................ crocodilian species and has been proposed for elevated temp- Private collection P 2, 18, 19 eratures in large dinosaur species. Terrazoo Rheinberg T In contrast with previous work, this paper investigates Zoo Duisburg ZD radiant heat transmission using body surface temperature Zoom Erlebniswelt ZE (T ). Cowles suggested that the dermal surface of reptiles bs could act as a heat collector and dispenser. Therefore the question arises as to whether the previous identified relation- ships between core and ambient temperatures are similar to the differentials between T and T ? The following experi- bs a ment aims to investigate the correlation between length and T 2 T differential. A further aim is to gain a greater under- b a standing of heliothermy and thigmothermy in a range of lizard species. Materials and methods Prior to the main experiment, a preliminary study was Figure 1. The four anatomical sites used for data collection in experiment. carried out. Data were collected from three individual lizards of three species of differing size. The preliminary 13:00 – 16:00 hours. All measurements were taken indoors study was used to determine first, how readings would be within enclosures. recorded and secondly, the general protocol for the main Temperature was measured using a DT-8812 infrared experiment. The study also determined whereabouts on the non-contact thermometer. The thermometer is laser body it was possible to collect temperatures accurately pointed and provides measurement collection at a distance without the need for physical contact. to spot ratio of 8:1. The resolution is 2208C to 2008Cin Data collected in the study were obtained from captive 0.18C intervals, with a display accuracy of +2.0%. lizards maintained indoors under artificial conditions. Temperature readings were recorded in degree Celsius (8C). Environments of captive lizards are mostly constant since Measurements were taken within 200 mm of study animal. heat sources and photoperiods are regulated. For the investi- Each measurement recorded the T at a predetermined ana- bs gation undertaken here, this is an advantage since it allows a tomical site. The four sites chosen for data collection were fair comparison of inter-specific effects. mid-body lateral (MBL), lower fore leg (LF), lower hind leg (LH) and mid-caudal (T) (Figure 1). To get a temperature Body surface temperature (T ) 2 ambient temperature bs reading the thermometer laser was aimed at a point 20 mm (T ) differential above the chosen anatomical site (as specified by manufac- Data were obtained from four private and zoological insti- turers). Five consecutive readings were taken at each site. tutions in the UK and Germany (Table 1). Overall data for T was also measured by five consecutive readings. For the the main experiment were collected from 22 individual purpose of the experiment T was, as defined by Pough lizards representing 18 species in 6 families (Table 2). and Gans, the mean air temperature outside the boundary Data acquisition took place in September 2006 between layer in the immediate vicinity of the lizard (i.e. within 300 mm radius of study animal). There was a 20-s delay Table 1. Abbreviations used in text between each reading. Between sites and T readings there was a delay of 3 min. This delay allowed the infrared Symbol Definition ................................................................................................................ sensor to equilibrate. Most of the study animals (90%) LF Lower fore leg body site were exposed within enclosure when readings were taken. LH Lower hind leg body site However, readings from two individuals were taken while sheltered (see Table 3). There was no physical contact with MBL Mid-body lateral body site the study animal during data collection. T Mid-caudal site T Ambient temperature Heliothermy and thigmothermy T Body temperature The protocols described above were used for the measure- T Body surface temperature bs ment of heliothermic and thigmothermic species. Species ......................................................................................................................................................................................................................................... 137 Research article Bioscience Horizons † Volume 1 † Number 2 † June 2008 ......................................................................................................................................................................................................................................... Table 3. Individuals measured in study with T 2 T differentials and heliothermic/thigmothermic categorization. Note both sheltered and bs a non-sheltered individuals are included in this table. Heliothermic thigmothermic classification is prior to output of discriminant analysis (see Materials and Methods).Abbrieviations for collection are given in Table 2 Common name Scientific name Family Length (mm) MBL T 2 T Heliothermic/ Collection bs a Differential thigmothermic ........................................................................................................................................................................................................................................ Frilled Dragon Chlamydosaurus kingii Agamidae 550 2.6 H ZD Frilled Dragon Chlamydosaurus kingii Agamidae 600 3 H T Collared Lizard Crotaphytus collaris Iguanidae 200 1.2 H P Spiny-tail Iguana Ctenosaura similis Iguanidae 750 4.2 H P Rhinoceros Iguana Cyclura cornuta Iguanidae 1500 5.1 H T Leopard Gecko Eublepharis macularis Gekkonidae 220 0.4 T P Canary Island Lizard Gallotia stehlini Lacertidae 450 2.3 H P Canary Island Lizard G. stehlini (shelter) Lacertidae 400 1.3 H P Tokay Gecko Gekko gecko Gekkonidae 250 0.1 T ZE Fat-tailed Gecko Hemitheconyx caudicinctus Gekkonidae 220 0.2 T P Green Iguana Iguana iguana Iguanidae 750 3.7 H ZE Green Iguana I. iguana Iguanidae 1800 2.5 H ZD Eyed Lizard Lacerta lepida Lacertidae 100 0.7 H P Star Agama Laudakia stellio brachydactylus Agamidae 200 1.4 H P Frog-eyed Gecko Teratoscincus scincus Gekkonidae 150 0.6 T P Blue-tongued Skink Tiliqua gigas Scincidae 400 2.7 H ZD Blue-tongued Skink T. gigas (shelter) Scincidae 350 0.8 H ZD Shingleback Skink Trachydosaurus rugosus Scincidae 350 2.5 H T Moroccan Uromastyx Uromastyx acanthinurus Agamidae 300 2.6 H ZE Saharan Uromastyx Uromastyx geyri Agamidae 400 2.3 H P Ridge-tailed Monitor Varanus acanthurus Varanidae 550 3.2 H T Gould’s Monitor Varanus gouldii Varanidae 1800 4.3 H T were categorized as heliothermic or thigmothermic in Results accordance to whether a species was diurnal (heliotherm) or nocturnal (thigmotherm). No further thermoregulatory Overall data collection: site body surface temperature categories were accounted for. (T ) versus ambient temperature (T ) bs a First, the temperature relations of the four anatomical sites on the reptile body were compared with each other for the Statistical methods 22 lizards (Figure 2). Figure 2 shows close correlations Statistical analyses were performed in accordance to the pro- between T and T for all four sites. All anatomical sites bs a tocols described in Zar. The correlation method used have similar gradients. Coefficients (r ) for the sites range throughout the experiment was non-parametric Spearman’s from 0.946 to 0.974. Such results suggest a positive corre- Rank. Multiple regression analysis ( performed through lation between T and T at each of the sites. bs a Microsoft Excel) was used in conjunction with Spearman’s Overall, LH exhibited the lowest temperature (Figure 1). Rank correlation. One-way ANOVA (as provided by Proportionately, 27% LH readings were lower than T .In MINITAB) was used to analyse site T 2 T differential bs a contrast, 22% of T and 9% of LF readings were lower versus length. Data input for the one-way ANOVA was pre- than T . MBL showed no readings lower than T (0%). a a ceded by an F test to check homogeneity of variance. The max Therefore, attention was focused on MBL as it more F test is used to screen samples for normal distribution of max closely represents the animal’s internal temperature. data. Discriminant analysis was provided by MINITAB. This method is used to separate sampling units into their true Inter-family comparison groupings. Data input involves pre-classification of sampling units. In the case of my study pre-classification comprised The 18 different species measured represent 6 different two units: heliothermic or thigmothermic. Each individual’s families (Figure 3, Table 2). Data for each anatomical site unit was plotted with T 2 T differential. for each individual were averaged and categorized by family. bs a ......................................................................................................................................................................................................................................... 138 Bioscience Horizons † Volume 1 † Number 2 † June 2008 Research article ......................................................................................................................................................................................................................................... Figure 2. Mean site temperature for 22 individual lizards against the mean Figure 4. T 2 T differentials, from 22 individual lizards, against length 2 bs a ambient temperature. r values are given as LF: 0.974, LH: 0.966, MBL: (log ). 0.946, T: 0.946 (see Table 1 for key to abbreviations). Figure 3. Comparison of mean T (for all four anatomical sites) between Figure 5. Comparison of the 18 heliothermic and 4 thigmothermic species bs the six lizard families used in study. Standard deviation is given as 4.57. measured in study showing T 2 T differential against length (log ). bs a 10 Figure 3 shows that the Gekkonidae exhibited the lowest mean Heliothermy and thigmothermy T (25.58C), whereas the Agamidae exhibited the highest bs Eighteen heliothermic lizards and four thigmothermic lizards mean T (36.98C). bs were studied in accordance to the prior classification described in Materials and Methods (see Table 2 for individ- Body surface temperature (T ) 2 ambient temperature bs uals; Figure 5). Figure 5 shows a positive correlation between (T ) differential versus length a T 2 T differential and length for the heliothermic species bs a data (r ¼ 0.623). In contrast, the thigmothermic species One-way ANOVA analysis showed MBL to be the anatom- data set shows a negative slope (r ¼ 20.830). ical site with the greatest T 2 T differential (Figure 4). bs a To assess level of confidence in determining heliothermy Other anatomical sites displayed more variable readings and thigmothermy in the study species, a discriminant analy- and T 2 T differential between all four sites fluctuated bs a sis was performed using T 2 T differential from MBL considerably. One-way ANOVA showed significant differ- bs a readings. Discriminant analysis showed a confidence level ence (P, 0.001). The MBL data were used to give T 2 T bs a of 77% correct classifications. Five misclassifications resulted differential as the independent variable, to be compared in species pre-classified as heliothermic being classified as with log length. Figure 4 indicates a positive correlation thigmothermic. The sheltered individuals (Tiliqua gigas, between T 2 T differential and log length (r ¼ 0.666). bs a 10 Gallotia stehlini) measured in the study were both incorrectly Multiple regression analysis of the data set gave F as 39.9, classified. The further misclassifications were Lacerta lepida, thus indicating a strong signal-to-noise ratio (regression Crotaphytus collaris and Laudakia stellio brachydactylus. MS/residual MS). The given P-value from the regression No thigmothermic species were misclassified. analysis was ,0.001. ......................................................................................................................................................................................................................................... 139 Research article Bioscience Horizons † Volume 1 † Number 2 † June 2008 ......................................................................................................................................................................................................................................... differentials in V. komodoensis to physiology. The large Discussion differentials recorded in V. gouldii and C. cornuta could Overall, the data set suggests that anatomical T is associ- bs therefore indicate the existence of some form of physiological ated with T (Figure 2), which is congruent with the estab- heat production in these species. With thermal inertia, lished concept that lizards are ectothermic. greater differentials in larger species might reflect transfer of internally generated heat from body core to surface. Body surface temperature (T ) 2 ambient temperature bs Heat dissipation through the integument may help prevent (T ) differential versus length larger species from overheating. Central to the study was the comparison of T 2 T differ- If T 2 T differential is generally correlated with size it bs a b a ential ( from MBL reading) with length. The relationship could counteract short-term changes in T . Small species between length and T 2 T differential might be explained need to actively bask for a fraction of the time required for bs a 22 28 by the role of integument. Licht and Bennett compared a large species . Therefore small lizards are able to resume scaleless snake and a normal snake and suggested that activity within much shorter time frames than larger reptile integument was not a significant heat insulator. species. To counteract an inevitable greater rate of cooling, Scales are undoubtedly important to radiative and conduc- smaller lizards perform short-term intermittent patterns of tive heat exchange. However, if convective heat is lost thermoregulation and activity throughout the day. through an integument it could suggest endogenous heat pro- Bergmann’s rule states that animals at higher latitudes are duction. Such heat production has been demonstrated for generally larger than those in the tropics. In contrast, some reptile species. For example, digestion is known to Ashton and Feldman observe the opposite for snakes and induce both a faster metabolic rate and increased body temp- lizards. Smaller size and therefore greater rate of heat gain 23, 24 erature in some species. Brattstrom (cited in would be of greater benefit at higher latitudes due to Auffenberg ) notes that the integument of the varanid increased seasonal variation in temperatures. Thus there Varanus varius was only poorly effective at retarding heat may be a larger versus smaller trade-off in lizards. loss and Stevenson includes thermal conductance One of the two largest lizards (1800 mm) in my study, between core and surface layer in a mathematical model of Iguana iguana, displayed a T 2 T differential of 2.58C. bs a thermal balance in ectotherms. In accordance with the other data collected here, a lizard Readings from the MBL anatomical site exhibited a mean of this size should have a bigger T 2 T differential. To bs a T 2 T differential of 2.168C, which represented a thermal put the result into context, a smaller (750 mm) sub-adult bs a difference of 36.8%, 64.9% and 83.2% greater than the individual of I. iguana demonstrated a T 2 T differential bs a other three sites. One-way ANOVA of site T 2 T differen- of 3.7ºC. The reason for the disparity may lie in the con- bs a tials showed significant variation (P , 0.001) between all ditions in which the large individual was housed. The large four sites. The MBL site is located on the trunk of the I. iguana was housed in a large, open display as part of a lizard. The proximity of MBL to body organs and thus multi-species exhibit in a zoo. No heat sources were provided potential endogenous heat sources may be the and T fluctuated with T in the building. Avery states that a a reason for the greater T 2 T differentials recorded at this iguanids, in general, are active at high constant temperatures. bs a anatomical site. Wild adult I. iguana bask prominently and thus raise their Bartholomew suggested that thermal conductance is so T . Therefore without access to any direct radiative or con- great in lizards that endogenous heat is lost at a rate that is ductive heat source in the zoo, the study individual would proportional to its production. In small lizards, endogenous not be able to raise its T . In addition, the surrounding T b a heat production is insignificant due to the rapid dynamics of of the large I. iguana was one of the lowest (23.5ºC) in the heat gain and loss as a result of greater surface-to-volume data set. Thus it is possible that at certain temperatures T bs ratios. However, in large lizards endogenous heat can be sig- conforms more to T . If such a phenomenon does occur, a 15, 25, 26 nificant. In this present study, Varanus gouldii was smaller T and T differential would result in reduced heat bs a one of the largest species and it exhibited a T 2 T differ- loss from core. Reduced heat loss at a lower T supports bs a a ential of 4.3ºC. The greatest T 2 T differential, of 5.18C, the suggestion that integument dissipates heat in large bs a was recorded from the iguanid Cyclura cornuta. Although lizards when under periods of high T . the latter species is shorter than V. gouldii, it is of greater Heliothermy and thigmothermy bulk and thus may suggest mass to be a factor in heat exchange. Mass was not taken into account in this study, An objective of the study was to compare heliothermy and but could be a consideration for future lines of investigation. thigmothermy in lizards. The results showed that T 2 T bs a Greater T 2 T differential in large ectotherm species is differential in heliothermic species was positively correlated b a 18, 27 often attributed to thermal inertia. The Komodo with length. Thigmothermic species, on the other hand Monitor (Varanus komodoensis) is the world’s largest seemed to show a negative correlation, though there were extant lizard species. Auffenberg accredits T 2 T relatively few data. b a ......................................................................................................................................................................................................................................... 140 Bioscience Horizons † Volume 1 † Number 2 † June 2008 Research article ......................................................................................................................................................................................................................................... Bennett correlated maximal locomotor capacity in present study suggest that low temperature is more important lizards with T . Bennett concluded that species performed than shelter, which would then be considered coincidental at their peak at higher T (higher than that would be experi- with low T . Shelters are often less influenced by short-term a a enced in the wild for some). Bennett’s results suggest environmental temperature fluctuations and thus can provide heliothermy could enhance lizard performance. Rummery stable microclimates. Therefore, it is probable that shelters et al. view heliothermy as a high cost method of raising are used to maintain selected body temperature through body temperature. For example, diurnal species which intermittent use. often bask prominently in open areas to maximize radiative Adolph notes that some terrestrial sheltered microhabi- heat gain are exposed to increased risk of predation. Large tats are warmer than exposed arboreal perches. In relation heliothermic species are at less risk of predation. Also, to the present study the statement is not true, as recorded because of their large size, their higher T means that rela- T was much greater outside of the shelter (2.4 – 3.9ºC). b a tively less time is spent basking. Most lizard species, However, such a situation would be expected under captive however, are of small to moderate size and therefore conditions where oscillations in T are almost non-existent. heliothermy is risky. Natural habitats, however, offer a more varied spatial distri- Nocturnal lizards face different constraints since they bution of differing thermal microclimates. Therefore wild cannot thermoregulate in the classical sense. Some nocturnal lizards are presented with greater opportunities to exert species use protected basking where the protection is control, which would lead them to establish their optimum afforded by a crevice or thick vegetation that does not body temperature. impede solar radiation. Protected basking therefore, is In the discussion of heliothermy and thigmothermy, it used by some lizard species that remain inactive during the should be remembered that neither are definitive means of day but become active at night using the heat gained while thermoregulation. Pough et al. states that heliothermy at rest. Equally, some species use camouflage to enable dis- and thigmothermy are ends of a spectrum in thermoregula- creet basking. For the purpose of these analyses, nocturnal tion. Within heliothermy, further categorizations include lizards were categorized as thigmothermic. All the thig- whether a species performs shuttling or posturing thermore- mothermic lizards in this study were geckos. Geckos gulatory behaviours. Such behaviours were not accounted for control T actively through selection of substrata and pas- the present study. sively through activity times (according to location or In summary, the results suggest that radiant heat trans- season). Inter-family comparison shows that the mission from the integument is greater in larger individuals. Gekkonidae exhibit the lowest mean overall T of all Exactly why this occurs is unknown and thus requires further bs six families in the study. Also, all geckos recorded low investigation. T 2 T differentials and were of relatively small size One possibility is that the integument of larger lizards bs a (,250 mm). The negative correlation between T 2 T shields them more efficiently than smaller bodied species bs a differential and length seen in the study could suggest that from radiative heat gain, thus preventing the overheating of geckos might get a metabolic benefit from smaller size. bodies that already possess greater T –T differentials, b a Thermal conductance is greater during heating than in because of thermal inertia. Therefore, the results obtained cooling. However, larger lizards require a longer period could simply be attributed to heat reflecting from the integu- of contact with the substratum to reach their optimum ment rather than transfer from the core. However, this body temperature. Therefore smaller size enables optimum hypothesis does not encompass the younger stages of body temperature to be reached in a shorter time frame. growth when maximizing radiative heat gain would be The same principle applies to heliothermic species and radia- imperative. tive heat gain. This study could be improved by examining more individ- The discriminant analysis showed five misclassifications. uals and species. A starting point for further study could use Sheltered individuals of T. gigas and G. stehlini were among measurements of species larger than those in this study. As the incorrectly classified taxa. In contrast, non-sheltered mentioned earlier, mass could also be measured to compli- individuals of these species were classified correctly as ment length in order to give a better picture of individuals’ heliothermic. Both sheltered and non-sheltered individuals of volume. the same species were within the same enclosures. However, A second line of investigation could be to compare dorsal temperature measurements from one of each species were T and ventral T . Tercafs notes differences in radiative bs bs taken from individuals hiding in an enclosure refuge. transmission between dorsal and ventral integuments. Such Sheltered individuals of T. gigas and G. stehlini showed a comparison could improve our knowledge of the role of markedly low T 2 T differentials compared with non- conduction in lizard thermal relations. Also substratum bs a sheltered individuals. Regal stated that lizards seek low temperature could be included in a future study and integu- temperatures when not active. Data obtained from the ments of a selection of species could be examined. ......................................................................................................................................................................................................................................... 141 Research article Bioscience Horizons † Volume 1 † Number 2 † June 2008 ......................................................................................................................................................................................................................................... 10. Avery RA (1982) Field studies of body temperatures and thermoregulation. Most of the species studied here (82%) were heliotherms. In C Gans, eds, Biology of the Reptilia. New York: Academic Press, pp. 93–166. The limited number of thigmothermic species for this group 11. Kearney M, Predavec M (2000) Do nocturnal ectotherms thermoregulate? A means that no strong conclusions can be drawn regarding the study of the temperate gecko Christinus marmoratus. Ecology 81: relationship between length and T –T differential. bs a 2984–2996. However, the results raise issues for future study. For 12. Huey RB, Webster TP (1975) Thermal biology of a solitary lizard: Anolis mar- example, does T –T differential decrease further with bs a moratus of Guadeloupe. Ecology 56: 445–452. greater length in thigmothermic lizards? Also how does the 13. Rummery C, Shine R, Houston DL et al. (1995) Thermal biology of thermal performance of diurnal thigmothermic species, the Australian forest dragon, Hypsilurus spinipes (Agamidae). Copeia: 818–827. such as those present in deep forest habitats, compare with 14. Morgan KR (1988) Body temperature, energy metabolism, and stamina in nocturnal species? The dearth of information on lizard thig- two Neotropical forest lizards (Ameiva, Teiidae). J Herpetol 22: 236–241. mothermy is an incentive to continue the line of 15. Auffenberg W (1981) The Behavioural Ecology of the Komodo Monitor. investigation. Gainesville: University Presses of Florida. 16. Stevenson RD (1985) Body size and limits to the daily range of body temp- erature in terrestrial ectotherms. Am Nat 125: 102–117. Funding 17. Mautz WJ (1994) Thermal biology and microhabitats of Xantusiid lizards. In This project was self funded, although Canterbury Christ PR Brown, JW Wright, eds. Herpetology of the North American Deserts. Church University did provide some funding for equipment. Excelsior: Southwestern Herpetologists Society, pp. 227–238. 18. Reid REH (1997) Dinosaurian physiology: The case for “intermediate” dino- saurs”. In JO Farlow, MK Brett-Surman, eds, The Complete Dinosaur. Acknowledgements Bloomington: Indiana University Press, pp. 449–473. 19. Gillooly JF, Allen AP, Charnov EL (2006) Dinosaur fossils predict body temp- The author would like to thank the invaluable assistance of eratures. PLoS Biol 4: 0001–0003. Stefan Terlinden who provided opportunity to collect data in 20. Cowles RB (1958) Possible origin of dermal temperature regulation. Evolution Germany. Equal gratitude is bestowed to staff at Zoo 12: 347–357. Duisburg, Zoom Erlebniswelt at Gelsenkirchen and 21. Zar JH (1996) Biostatistical Analysis. New Jersey: Prentice Hall. Terrazoo Rheinberg who permitted use of their lizards in 22. Licht P, Bennet AF (1972) A scaleless snake: tests of the role of reptilian the study. In addition the author thanks Chris Davies for scales in water loss and heat transfer. Copeia: 702–707. allowing his private collection to be used for data collection. 23. Marcellini DL, Peters A (1982) Preliminary observations on endogenous heat Finally, I would like to thank Professor Georges Dussart for production after feeding in Python molurus. J Herpetol 16: 92–95. his helpful guidance throughout the project. 24. Tattersall GJ, Milsom WK, Abe AS et al. (2004) The thermogenesis of diges- tion in rattlesnakes. J Exp Biol 207: 579–585. 25. Bartholomew GA (1982) Physiological control of body temperature. In References C Gans, eds. Biology of the Reptilia. New York: Academic Press, pp.167–211. 26. Pough FH, Andrews RM, Cadle JE et al. (2004) Herpetology, 3rd eds. New 1. Nelson DO, Heath JE, Prosser CL (1984) Evolution of temperature regulatory Jersey: Pearson Education, Inc. mechanisms. Am Zool 24: 791–807. 27. Bakker RT (1986) The Dinosaur Heresies. New York: William Morrow and 2. Pough FH, Janis CM, Heiser JB (2005) Vertebrate Life, 7th edn. New Jersey: Company, Inc. Pearson Education, Inc. 28. Dı´az JA (1994) Field thermoregulatory behaviour in the western Canarian 3. Gans C, Pough FH (1982) Physiological ecology: its debt to reptilian studies, lizard Gallotia galloti. J Herpetol 28: 325–333. its value to students of reptiles. In C Gans, eds, Biology of the Reptilia. New York: Academic Press, pp. 1–13. 29. Wilmer P, Stone G, Johnston I (2005) Environmental Physiology of Animals. Oxford: Blackwell. 4. Adolph SC (1990) Influence of behavioural thermoregulation on microhabi- tat use by two Sceloporus lizards. Ecology 71: 315–327. 30. Ashton KG, Feldman CR (2003) Bergmann’s rule in nonavian reptiles: turtles follow it, lizards and snakes reverse it. Evolution 57: 1151–1163. 5. King D, Green B, Herrera E (1994) Thermoregulation in a large Teiid lizard, Tupinambis teguixin, in Venezuela. Copeia 3: 806–808. 31. Bennett AF (1987) Evolution of the control of body temperature: is warmer better? In P Dejours, L Bolis, CR Taylor, et al., eds. Comparative Physiology: Life 6. Schmidt-Nielsen K (1997) Animal Physiology, 5th edn. Cambridge: in Water and on Land. Padova: Fidia Research Series, IX-Liviana Press. pp. Cambridge University Press. 421–431. 7. Pough FH, Gans C (1982) The vocabulary of reptilian thermoregulation. In 32. Avery RA (1979) Lizards: A Study in Thermoregulation. London: Edward C Gans, eds, Biology of the Reptilia. New York: Academic Press, pp. 17–23. Arnold. 8. Belliure J, Carrascal LM (2002) Influence of heat transmission mode on 33. Regal PJ (1967) Voluntary hypothermia in reptiles. Science New Series 155: heating rates and on the selection of patches for heating in a 1551–1553. Mediterranean lizard. Physiol Biochem Zool 75: 369–376. 34. Tercafs RR (1963) Transmission of ultra-violet, visible and infra-red radiation 9. Belliure J, Carrascal LM, Dı´az JA (1996) Covariation of thermal biology and through the keratinous layer of reptile skin (Serpentes and Sauria). Ecology foraging mode in two Mediterranean Lacertid lizards. Ecology 77: 44: 214–218. 1163–1173. ........................................................................................................................................................................................................................................ Submitted on 30 September 2007; accepted on 28 January 2008; advance access publication 17 April 2008 ......................................................................................................................................................................................................................................... http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Bioscience Horizons Oxford University Press

Body surface temperature and length in relation to the thermal biology of lizards

Bioscience Horizons , Volume 1 (2) – Jun 17, 2008

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Abstract

Volume 1 † Number 2 † June 2008 10.1093/biohorizons/hzn014 ......................................................................................................................................................................................................................................... Research article Body surface temperature and length in relation to the thermal biology of lizards Daniel Garrick* Canterbury Christ Church University, Canterbury, UK. * Corresponding author: Flat 4, 89 Henver Road, Newquay, Cornwall TR7 3DJ, UK. Email: daniel_garrick@hotmail.co.uk Supervisor: Georges Dussart, Canterbury Christ Church University, Canterbury, UK. ........................................................................................................................................................................................................................................ This study investigated body surface temperature (T ) in 22 lizards of 18 species. The difference between T and ambient temperature bs bs (T ) was correlated with size. The greater T 2 T differentials, which were recorded in larger lizards, may occur as a result of heat transfer a bs a from the core to surface in prevention of overheating. The structure of the integument may contribute to heat dissipation. Heliothermy and thigmothermy as forms of thermoregulation were also incorporated into the data set. Heliothermic lizards showed a positive cor- relation between length and T 2 T . Thigmothermic lizards, however, exhibited a negative correlation. Differences in size and rate of bs a conductive heat transfer are put forward as possible reasons for the negative correlation. Key words: thigmothermy, heliothermy, lizard, length. ........................................................................................................................................................................................................................................ Lizards, like most reptiles, are ectothermic. Ectothermy is the Heliothermy is a well-documented area in lizard reliance on external heat sources to increase body tempera- biology. A principal reason for this bias is that diurnal 1, 2 ture. Thus lizards gain heat, principally, from their basking lizard species are often the dominant vertebrates in environment. To achieve optimum body temperature hot arid environments and data on these animals are rela- lizards perform different thermoregulatory behaviours. tively easy to obtain. In contrast, Belliure and Carrascal Thermoregulation is a well-documented area of reptile suggest thigmothermy is a less well-studied aspect of 3– 5 biology. animal thermal relations. The use of thermoregulation to achieve and maintain In general, thigmothermy is practised by species that have optimum body temperature has contributed to the great limited access to solar radiation. Most studies of lizard 12, 13 diversity of lizards and even allowed colonization of temper- thigmothermy have considered diurnal species. Among ate regions. For example, through simple body posturing, diurnal lizards, thigmothermy is normally practised by some species within the South American genus Liolaemus species in forest environments where incoming solar radi- can attain body temperatures 308C above the ambient temp- ation is impeded by the tree canopy. Morgan suggests erature. Such a high differential, though uncommon, that in such environments, thermally discrete microclimates emphasizes the diversity of thermal relations among lizards. are important. In contrast thigmothermic behaviour is rela- Heliothermy and thigmothermy are further means of tively more important for nocturnal lizards, which do not ectothermal thermoregulation. Heliothermy is heat gain receive any solar radiation input. by short wavelength solar radiation. Thigmothermy involves Previous studies of thermal interactions between lizard and heat conduction to the reptile body by direct contact with a environment have predominantly used the internal body temp- warm substratum. In practise, heliothermy and thig- erature (T ) (i.e. cloacal) and ambient temperature (T ) differ- b a 12, 15 – 17 15 16 mothermy enable lizards to compensate for the thermal con- ential. Auffenberg and Stevenson related body ditions of the habitat. Heliothermy and thigmothermy in temperature to size. These authors concluded that larger size lizards are therefore related to habitats and life-history conferred a greater T 2 T differential due to thermal b a strategies. inertia. Thermal inertia is based upon the physical properties ......................................................................................................................................................................................................................................... 2008 The Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 136 Bioscience Horizons † Volume 1 † Number 2 † June 2008 Research article ......................................................................................................................................................................................................................................... Table 2. Key to list of collections used in study of heat dissipation whereby larger objects retain heat for longer than smaller objects due to reduced surface-to-volume Collection Abbreviation scaling. Such a phenomenon has been demonstrated in extant ................................................................................................................ crocodilian species and has been proposed for elevated temp- Private collection P 2, 18, 19 eratures in large dinosaur species. Terrazoo Rheinberg T In contrast with previous work, this paper investigates Zoo Duisburg ZD radiant heat transmission using body surface temperature Zoom Erlebniswelt ZE (T ). Cowles suggested that the dermal surface of reptiles bs could act as a heat collector and dispenser. Therefore the question arises as to whether the previous identified relation- ships between core and ambient temperatures are similar to the differentials between T and T ? The following experi- bs a ment aims to investigate the correlation between length and T 2 T differential. A further aim is to gain a greater under- b a standing of heliothermy and thigmothermy in a range of lizard species. Materials and methods Prior to the main experiment, a preliminary study was Figure 1. The four anatomical sites used for data collection in experiment. carried out. Data were collected from three individual lizards of three species of differing size. The preliminary 13:00 – 16:00 hours. All measurements were taken indoors study was used to determine first, how readings would be within enclosures. recorded and secondly, the general protocol for the main Temperature was measured using a DT-8812 infrared experiment. The study also determined whereabouts on the non-contact thermometer. The thermometer is laser body it was possible to collect temperatures accurately pointed and provides measurement collection at a distance without the need for physical contact. to spot ratio of 8:1. The resolution is 2208C to 2008Cin Data collected in the study were obtained from captive 0.18C intervals, with a display accuracy of +2.0%. lizards maintained indoors under artificial conditions. Temperature readings were recorded in degree Celsius (8C). Environments of captive lizards are mostly constant since Measurements were taken within 200 mm of study animal. heat sources and photoperiods are regulated. For the investi- Each measurement recorded the T at a predetermined ana- bs gation undertaken here, this is an advantage since it allows a tomical site. The four sites chosen for data collection were fair comparison of inter-specific effects. mid-body lateral (MBL), lower fore leg (LF), lower hind leg (LH) and mid-caudal (T) (Figure 1). To get a temperature Body surface temperature (T ) 2 ambient temperature bs reading the thermometer laser was aimed at a point 20 mm (T ) differential above the chosen anatomical site (as specified by manufac- Data were obtained from four private and zoological insti- turers). Five consecutive readings were taken at each site. tutions in the UK and Germany (Table 1). Overall data for T was also measured by five consecutive readings. For the the main experiment were collected from 22 individual purpose of the experiment T was, as defined by Pough lizards representing 18 species in 6 families (Table 2). and Gans, the mean air temperature outside the boundary Data acquisition took place in September 2006 between layer in the immediate vicinity of the lizard (i.e. within 300 mm radius of study animal). There was a 20-s delay Table 1. Abbreviations used in text between each reading. Between sites and T readings there was a delay of 3 min. This delay allowed the infrared Symbol Definition ................................................................................................................ sensor to equilibrate. Most of the study animals (90%) LF Lower fore leg body site were exposed within enclosure when readings were taken. LH Lower hind leg body site However, readings from two individuals were taken while sheltered (see Table 3). There was no physical contact with MBL Mid-body lateral body site the study animal during data collection. T Mid-caudal site T Ambient temperature Heliothermy and thigmothermy T Body temperature The protocols described above were used for the measure- T Body surface temperature bs ment of heliothermic and thigmothermic species. Species ......................................................................................................................................................................................................................................... 137 Research article Bioscience Horizons † Volume 1 † Number 2 † June 2008 ......................................................................................................................................................................................................................................... Table 3. Individuals measured in study with T 2 T differentials and heliothermic/thigmothermic categorization. Note both sheltered and bs a non-sheltered individuals are included in this table. Heliothermic thigmothermic classification is prior to output of discriminant analysis (see Materials and Methods).Abbrieviations for collection are given in Table 2 Common name Scientific name Family Length (mm) MBL T 2 T Heliothermic/ Collection bs a Differential thigmothermic ........................................................................................................................................................................................................................................ Frilled Dragon Chlamydosaurus kingii Agamidae 550 2.6 H ZD Frilled Dragon Chlamydosaurus kingii Agamidae 600 3 H T Collared Lizard Crotaphytus collaris Iguanidae 200 1.2 H P Spiny-tail Iguana Ctenosaura similis Iguanidae 750 4.2 H P Rhinoceros Iguana Cyclura cornuta Iguanidae 1500 5.1 H T Leopard Gecko Eublepharis macularis Gekkonidae 220 0.4 T P Canary Island Lizard Gallotia stehlini Lacertidae 450 2.3 H P Canary Island Lizard G. stehlini (shelter) Lacertidae 400 1.3 H P Tokay Gecko Gekko gecko Gekkonidae 250 0.1 T ZE Fat-tailed Gecko Hemitheconyx caudicinctus Gekkonidae 220 0.2 T P Green Iguana Iguana iguana Iguanidae 750 3.7 H ZE Green Iguana I. iguana Iguanidae 1800 2.5 H ZD Eyed Lizard Lacerta lepida Lacertidae 100 0.7 H P Star Agama Laudakia stellio brachydactylus Agamidae 200 1.4 H P Frog-eyed Gecko Teratoscincus scincus Gekkonidae 150 0.6 T P Blue-tongued Skink Tiliqua gigas Scincidae 400 2.7 H ZD Blue-tongued Skink T. gigas (shelter) Scincidae 350 0.8 H ZD Shingleback Skink Trachydosaurus rugosus Scincidae 350 2.5 H T Moroccan Uromastyx Uromastyx acanthinurus Agamidae 300 2.6 H ZE Saharan Uromastyx Uromastyx geyri Agamidae 400 2.3 H P Ridge-tailed Monitor Varanus acanthurus Varanidae 550 3.2 H T Gould’s Monitor Varanus gouldii Varanidae 1800 4.3 H T were categorized as heliothermic or thigmothermic in Results accordance to whether a species was diurnal (heliotherm) or nocturnal (thigmotherm). No further thermoregulatory Overall data collection: site body surface temperature categories were accounted for. (T ) versus ambient temperature (T ) bs a First, the temperature relations of the four anatomical sites on the reptile body were compared with each other for the Statistical methods 22 lizards (Figure 2). Figure 2 shows close correlations Statistical analyses were performed in accordance to the pro- between T and T for all four sites. All anatomical sites bs a tocols described in Zar. The correlation method used have similar gradients. Coefficients (r ) for the sites range throughout the experiment was non-parametric Spearman’s from 0.946 to 0.974. Such results suggest a positive corre- Rank. Multiple regression analysis ( performed through lation between T and T at each of the sites. bs a Microsoft Excel) was used in conjunction with Spearman’s Overall, LH exhibited the lowest temperature (Figure 1). Rank correlation. One-way ANOVA (as provided by Proportionately, 27% LH readings were lower than T .In MINITAB) was used to analyse site T 2 T differential bs a contrast, 22% of T and 9% of LF readings were lower versus length. Data input for the one-way ANOVA was pre- than T . MBL showed no readings lower than T (0%). a a ceded by an F test to check homogeneity of variance. The max Therefore, attention was focused on MBL as it more F test is used to screen samples for normal distribution of max closely represents the animal’s internal temperature. data. Discriminant analysis was provided by MINITAB. This method is used to separate sampling units into their true Inter-family comparison groupings. Data input involves pre-classification of sampling units. In the case of my study pre-classification comprised The 18 different species measured represent 6 different two units: heliothermic or thigmothermic. Each individual’s families (Figure 3, Table 2). Data for each anatomical site unit was plotted with T 2 T differential. for each individual were averaged and categorized by family. bs a ......................................................................................................................................................................................................................................... 138 Bioscience Horizons † Volume 1 † Number 2 † June 2008 Research article ......................................................................................................................................................................................................................................... Figure 2. Mean site temperature for 22 individual lizards against the mean Figure 4. T 2 T differentials, from 22 individual lizards, against length 2 bs a ambient temperature. r values are given as LF: 0.974, LH: 0.966, MBL: (log ). 0.946, T: 0.946 (see Table 1 for key to abbreviations). Figure 3. Comparison of mean T (for all four anatomical sites) between Figure 5. Comparison of the 18 heliothermic and 4 thigmothermic species bs the six lizard families used in study. Standard deviation is given as 4.57. measured in study showing T 2 T differential against length (log ). bs a 10 Figure 3 shows that the Gekkonidae exhibited the lowest mean Heliothermy and thigmothermy T (25.58C), whereas the Agamidae exhibited the highest bs Eighteen heliothermic lizards and four thigmothermic lizards mean T (36.98C). bs were studied in accordance to the prior classification described in Materials and Methods (see Table 2 for individ- Body surface temperature (T ) 2 ambient temperature bs uals; Figure 5). Figure 5 shows a positive correlation between (T ) differential versus length a T 2 T differential and length for the heliothermic species bs a data (r ¼ 0.623). In contrast, the thigmothermic species One-way ANOVA analysis showed MBL to be the anatom- data set shows a negative slope (r ¼ 20.830). ical site with the greatest T 2 T differential (Figure 4). bs a To assess level of confidence in determining heliothermy Other anatomical sites displayed more variable readings and thigmothermy in the study species, a discriminant analy- and T 2 T differential between all four sites fluctuated bs a sis was performed using T 2 T differential from MBL considerably. One-way ANOVA showed significant differ- bs a readings. Discriminant analysis showed a confidence level ence (P, 0.001). The MBL data were used to give T 2 T bs a of 77% correct classifications. Five misclassifications resulted differential as the independent variable, to be compared in species pre-classified as heliothermic being classified as with log length. Figure 4 indicates a positive correlation thigmothermic. The sheltered individuals (Tiliqua gigas, between T 2 T differential and log length (r ¼ 0.666). bs a 10 Gallotia stehlini) measured in the study were both incorrectly Multiple regression analysis of the data set gave F as 39.9, classified. The further misclassifications were Lacerta lepida, thus indicating a strong signal-to-noise ratio (regression Crotaphytus collaris and Laudakia stellio brachydactylus. MS/residual MS). The given P-value from the regression No thigmothermic species were misclassified. analysis was ,0.001. ......................................................................................................................................................................................................................................... 139 Research article Bioscience Horizons † Volume 1 † Number 2 † June 2008 ......................................................................................................................................................................................................................................... differentials in V. komodoensis to physiology. The large Discussion differentials recorded in V. gouldii and C. cornuta could Overall, the data set suggests that anatomical T is associ- bs therefore indicate the existence of some form of physiological ated with T (Figure 2), which is congruent with the estab- heat production in these species. With thermal inertia, lished concept that lizards are ectothermic. greater differentials in larger species might reflect transfer of internally generated heat from body core to surface. Body surface temperature (T ) 2 ambient temperature bs Heat dissipation through the integument may help prevent (T ) differential versus length larger species from overheating. Central to the study was the comparison of T 2 T differ- If T 2 T differential is generally correlated with size it bs a b a ential ( from MBL reading) with length. The relationship could counteract short-term changes in T . Small species between length and T 2 T differential might be explained need to actively bask for a fraction of the time required for bs a 22 28 by the role of integument. Licht and Bennett compared a large species . Therefore small lizards are able to resume scaleless snake and a normal snake and suggested that activity within much shorter time frames than larger reptile integument was not a significant heat insulator. species. To counteract an inevitable greater rate of cooling, Scales are undoubtedly important to radiative and conduc- smaller lizards perform short-term intermittent patterns of tive heat exchange. However, if convective heat is lost thermoregulation and activity throughout the day. through an integument it could suggest endogenous heat pro- Bergmann’s rule states that animals at higher latitudes are duction. Such heat production has been demonstrated for generally larger than those in the tropics. In contrast, some reptile species. For example, digestion is known to Ashton and Feldman observe the opposite for snakes and induce both a faster metabolic rate and increased body temp- lizards. Smaller size and therefore greater rate of heat gain 23, 24 erature in some species. Brattstrom (cited in would be of greater benefit at higher latitudes due to Auffenberg ) notes that the integument of the varanid increased seasonal variation in temperatures. Thus there Varanus varius was only poorly effective at retarding heat may be a larger versus smaller trade-off in lizards. loss and Stevenson includes thermal conductance One of the two largest lizards (1800 mm) in my study, between core and surface layer in a mathematical model of Iguana iguana, displayed a T 2 T differential of 2.58C. bs a thermal balance in ectotherms. In accordance with the other data collected here, a lizard Readings from the MBL anatomical site exhibited a mean of this size should have a bigger T 2 T differential. To bs a T 2 T differential of 2.168C, which represented a thermal put the result into context, a smaller (750 mm) sub-adult bs a difference of 36.8%, 64.9% and 83.2% greater than the individual of I. iguana demonstrated a T 2 T differential bs a other three sites. One-way ANOVA of site T 2 T differen- of 3.7ºC. The reason for the disparity may lie in the con- bs a tials showed significant variation (P , 0.001) between all ditions in which the large individual was housed. The large four sites. The MBL site is located on the trunk of the I. iguana was housed in a large, open display as part of a lizard. The proximity of MBL to body organs and thus multi-species exhibit in a zoo. No heat sources were provided potential endogenous heat sources may be the and T fluctuated with T in the building. Avery states that a a reason for the greater T 2 T differentials recorded at this iguanids, in general, are active at high constant temperatures. bs a anatomical site. Wild adult I. iguana bask prominently and thus raise their Bartholomew suggested that thermal conductance is so T . Therefore without access to any direct radiative or con- great in lizards that endogenous heat is lost at a rate that is ductive heat source in the zoo, the study individual would proportional to its production. In small lizards, endogenous not be able to raise its T . In addition, the surrounding T b a heat production is insignificant due to the rapid dynamics of of the large I. iguana was one of the lowest (23.5ºC) in the heat gain and loss as a result of greater surface-to-volume data set. Thus it is possible that at certain temperatures T bs ratios. However, in large lizards endogenous heat can be sig- conforms more to T . If such a phenomenon does occur, a 15, 25, 26 nificant. In this present study, Varanus gouldii was smaller T and T differential would result in reduced heat bs a one of the largest species and it exhibited a T 2 T differ- loss from core. Reduced heat loss at a lower T supports bs a a ential of 4.3ºC. The greatest T 2 T differential, of 5.18C, the suggestion that integument dissipates heat in large bs a was recorded from the iguanid Cyclura cornuta. Although lizards when under periods of high T . the latter species is shorter than V. gouldii, it is of greater Heliothermy and thigmothermy bulk and thus may suggest mass to be a factor in heat exchange. Mass was not taken into account in this study, An objective of the study was to compare heliothermy and but could be a consideration for future lines of investigation. thigmothermy in lizards. The results showed that T 2 T bs a Greater T 2 T differential in large ectotherm species is differential in heliothermic species was positively correlated b a 18, 27 often attributed to thermal inertia. The Komodo with length. Thigmothermic species, on the other hand Monitor (Varanus komodoensis) is the world’s largest seemed to show a negative correlation, though there were extant lizard species. Auffenberg accredits T 2 T relatively few data. b a ......................................................................................................................................................................................................................................... 140 Bioscience Horizons † Volume 1 † Number 2 † June 2008 Research article ......................................................................................................................................................................................................................................... Bennett correlated maximal locomotor capacity in present study suggest that low temperature is more important lizards with T . Bennett concluded that species performed than shelter, which would then be considered coincidental at their peak at higher T (higher than that would be experi- with low T . Shelters are often less influenced by short-term a a enced in the wild for some). Bennett’s results suggest environmental temperature fluctuations and thus can provide heliothermy could enhance lizard performance. Rummery stable microclimates. Therefore, it is probable that shelters et al. view heliothermy as a high cost method of raising are used to maintain selected body temperature through body temperature. For example, diurnal species which intermittent use. often bask prominently in open areas to maximize radiative Adolph notes that some terrestrial sheltered microhabi- heat gain are exposed to increased risk of predation. Large tats are warmer than exposed arboreal perches. In relation heliothermic species are at less risk of predation. Also, to the present study the statement is not true, as recorded because of their large size, their higher T means that rela- T was much greater outside of the shelter (2.4 – 3.9ºC). b a tively less time is spent basking. Most lizard species, However, such a situation would be expected under captive however, are of small to moderate size and therefore conditions where oscillations in T are almost non-existent. heliothermy is risky. Natural habitats, however, offer a more varied spatial distri- Nocturnal lizards face different constraints since they bution of differing thermal microclimates. Therefore wild cannot thermoregulate in the classical sense. Some nocturnal lizards are presented with greater opportunities to exert species use protected basking where the protection is control, which would lead them to establish their optimum afforded by a crevice or thick vegetation that does not body temperature. impede solar radiation. Protected basking therefore, is In the discussion of heliothermy and thigmothermy, it used by some lizard species that remain inactive during the should be remembered that neither are definitive means of day but become active at night using the heat gained while thermoregulation. Pough et al. states that heliothermy at rest. Equally, some species use camouflage to enable dis- and thigmothermy are ends of a spectrum in thermoregula- creet basking. For the purpose of these analyses, nocturnal tion. Within heliothermy, further categorizations include lizards were categorized as thigmothermic. All the thig- whether a species performs shuttling or posturing thermore- mothermic lizards in this study were geckos. Geckos gulatory behaviours. Such behaviours were not accounted for control T actively through selection of substrata and pas- the present study. sively through activity times (according to location or In summary, the results suggest that radiant heat trans- season). Inter-family comparison shows that the mission from the integument is greater in larger individuals. Gekkonidae exhibit the lowest mean overall T of all Exactly why this occurs is unknown and thus requires further bs six families in the study. Also, all geckos recorded low investigation. T 2 T differentials and were of relatively small size One possibility is that the integument of larger lizards bs a (,250 mm). The negative correlation between T 2 T shields them more efficiently than smaller bodied species bs a differential and length seen in the study could suggest that from radiative heat gain, thus preventing the overheating of geckos might get a metabolic benefit from smaller size. bodies that already possess greater T –T differentials, b a Thermal conductance is greater during heating than in because of thermal inertia. Therefore, the results obtained cooling. However, larger lizards require a longer period could simply be attributed to heat reflecting from the integu- of contact with the substratum to reach their optimum ment rather than transfer from the core. However, this body temperature. Therefore smaller size enables optimum hypothesis does not encompass the younger stages of body temperature to be reached in a shorter time frame. growth when maximizing radiative heat gain would be The same principle applies to heliothermic species and radia- imperative. tive heat gain. This study could be improved by examining more individ- The discriminant analysis showed five misclassifications. uals and species. A starting point for further study could use Sheltered individuals of T. gigas and G. stehlini were among measurements of species larger than those in this study. As the incorrectly classified taxa. In contrast, non-sheltered mentioned earlier, mass could also be measured to compli- individuals of these species were classified correctly as ment length in order to give a better picture of individuals’ heliothermic. Both sheltered and non-sheltered individuals of volume. the same species were within the same enclosures. However, A second line of investigation could be to compare dorsal temperature measurements from one of each species were T and ventral T . Tercafs notes differences in radiative bs bs taken from individuals hiding in an enclosure refuge. transmission between dorsal and ventral integuments. Such Sheltered individuals of T. gigas and G. stehlini showed a comparison could improve our knowledge of the role of markedly low T 2 T differentials compared with non- conduction in lizard thermal relations. Also substratum bs a sheltered individuals. Regal stated that lizards seek low temperature could be included in a future study and integu- temperatures when not active. Data obtained from the ments of a selection of species could be examined. ......................................................................................................................................................................................................................................... 141 Research article Bioscience Horizons † Volume 1 † Number 2 † June 2008 ......................................................................................................................................................................................................................................... 10. Avery RA (1982) Field studies of body temperatures and thermoregulation. Most of the species studied here (82%) were heliotherms. In C Gans, eds, Biology of the Reptilia. New York: Academic Press, pp. 93–166. The limited number of thigmothermic species for this group 11. Kearney M, Predavec M (2000) Do nocturnal ectotherms thermoregulate? A means that no strong conclusions can be drawn regarding the study of the temperate gecko Christinus marmoratus. Ecology 81: relationship between length and T –T differential. bs a 2984–2996. However, the results raise issues for future study. For 12. Huey RB, Webster TP (1975) Thermal biology of a solitary lizard: Anolis mar- example, does T –T differential decrease further with bs a moratus of Guadeloupe. Ecology 56: 445–452. greater length in thigmothermic lizards? Also how does the 13. Rummery C, Shine R, Houston DL et al. (1995) Thermal biology of thermal performance of diurnal thigmothermic species, the Australian forest dragon, Hypsilurus spinipes (Agamidae). Copeia: 818–827. such as those present in deep forest habitats, compare with 14. Morgan KR (1988) Body temperature, energy metabolism, and stamina in nocturnal species? The dearth of information on lizard thig- two Neotropical forest lizards (Ameiva, Teiidae). J Herpetol 22: 236–241. mothermy is an incentive to continue the line of 15. Auffenberg W (1981) The Behavioural Ecology of the Komodo Monitor. investigation. Gainesville: University Presses of Florida. 16. Stevenson RD (1985) Body size and limits to the daily range of body temp- erature in terrestrial ectotherms. Am Nat 125: 102–117. Funding 17. Mautz WJ (1994) Thermal biology and microhabitats of Xantusiid lizards. In This project was self funded, although Canterbury Christ PR Brown, JW Wright, eds. Herpetology of the North American Deserts. Church University did provide some funding for equipment. Excelsior: Southwestern Herpetologists Society, pp. 227–238. 18. Reid REH (1997) Dinosaurian physiology: The case for “intermediate” dino- saurs”. In JO Farlow, MK Brett-Surman, eds, The Complete Dinosaur. Acknowledgements Bloomington: Indiana University Press, pp. 449–473. 19. Gillooly JF, Allen AP, Charnov EL (2006) Dinosaur fossils predict body temp- The author would like to thank the invaluable assistance of eratures. PLoS Biol 4: 0001–0003. Stefan Terlinden who provided opportunity to collect data in 20. Cowles RB (1958) Possible origin of dermal temperature regulation. Evolution Germany. Equal gratitude is bestowed to staff at Zoo 12: 347–357. Duisburg, Zoom Erlebniswelt at Gelsenkirchen and 21. Zar JH (1996) Biostatistical Analysis. New Jersey: Prentice Hall. Terrazoo Rheinberg who permitted use of their lizards in 22. Licht P, Bennet AF (1972) A scaleless snake: tests of the role of reptilian the study. In addition the author thanks Chris Davies for scales in water loss and heat transfer. Copeia: 702–707. allowing his private collection to be used for data collection. 23. Marcellini DL, Peters A (1982) Preliminary observations on endogenous heat Finally, I would like to thank Professor Georges Dussart for production after feeding in Python molurus. J Herpetol 16: 92–95. his helpful guidance throughout the project. 24. Tattersall GJ, Milsom WK, Abe AS et al. (2004) The thermogenesis of diges- tion in rattlesnakes. J Exp Biol 207: 579–585. 25. Bartholomew GA (1982) Physiological control of body temperature. In References C Gans, eds. Biology of the Reptilia. New York: Academic Press, pp.167–211. 26. Pough FH, Andrews RM, Cadle JE et al. (2004) Herpetology, 3rd eds. New 1. Nelson DO, Heath JE, Prosser CL (1984) Evolution of temperature regulatory Jersey: Pearson Education, Inc. mechanisms. Am Zool 24: 791–807. 27. Bakker RT (1986) The Dinosaur Heresies. New York: William Morrow and 2. Pough FH, Janis CM, Heiser JB (2005) Vertebrate Life, 7th edn. New Jersey: Company, Inc. Pearson Education, Inc. 28. Dı´az JA (1994) Field thermoregulatory behaviour in the western Canarian 3. Gans C, Pough FH (1982) Physiological ecology: its debt to reptilian studies, lizard Gallotia galloti. J Herpetol 28: 325–333. its value to students of reptiles. In C Gans, eds, Biology of the Reptilia. New York: Academic Press, pp. 1–13. 29. Wilmer P, Stone G, Johnston I (2005) Environmental Physiology of Animals. Oxford: Blackwell. 4. Adolph SC (1990) Influence of behavioural thermoregulation on microhabi- tat use by two Sceloporus lizards. Ecology 71: 315–327. 30. Ashton KG, Feldman CR (2003) Bergmann’s rule in nonavian reptiles: turtles follow it, lizards and snakes reverse it. Evolution 57: 1151–1163. 5. King D, Green B, Herrera E (1994) Thermoregulation in a large Teiid lizard, Tupinambis teguixin, in Venezuela. Copeia 3: 806–808. 31. Bennett AF (1987) Evolution of the control of body temperature: is warmer better? In P Dejours, L Bolis, CR Taylor, et al., eds. Comparative Physiology: Life 6. Schmidt-Nielsen K (1997) Animal Physiology, 5th edn. Cambridge: in Water and on Land. Padova: Fidia Research Series, IX-Liviana Press. pp. Cambridge University Press. 421–431. 7. Pough FH, Gans C (1982) The vocabulary of reptilian thermoregulation. In 32. Avery RA (1979) Lizards: A Study in Thermoregulation. London: Edward C Gans, eds, Biology of the Reptilia. New York: Academic Press, pp. 17–23. Arnold. 8. Belliure J, Carrascal LM (2002) Influence of heat transmission mode on 33. Regal PJ (1967) Voluntary hypothermia in reptiles. Science New Series 155: heating rates and on the selection of patches for heating in a 1551–1553. Mediterranean lizard. Physiol Biochem Zool 75: 369–376. 34. Tercafs RR (1963) Transmission of ultra-violet, visible and infra-red radiation 9. Belliure J, Carrascal LM, Dı´az JA (1996) Covariation of thermal biology and through the keratinous layer of reptile skin (Serpentes and Sauria). Ecology foraging mode in two Mediterranean Lacertid lizards. Ecology 77: 44: 214–218. 1163–1173. ........................................................................................................................................................................................................................................ Submitted on 30 September 2007; accepted on 28 January 2008; advance access publication 17 April 2008 .........................................................................................................................................................................................................................................

Journal

Bioscience HorizonsOxford University Press

Published: Jun 17, 2008

Keywords: Key words thigmothermy heliothermy lizard length

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