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ARTICLE IN PRESS

Journal of Thermal Biology 33 (2008) 57–61 www.elsevier.com/locate/jtherbio

Lizards in the slow lane: Thermal biology of chameleons

Robin M. AndrewsÃ

Department of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA

Received 15 August 2007; accepted 26 October 2007

Abstract

1. Field body temperatures (Tb’s) of Chamaeleo chamaeleon in southwestern Spain averaged 28 1C in October and 30 1C in June. Slopes of regressions of Tb on Ta (ambient temperature at perch height) indicated that individuals were able to maintain a preferred body temperature of about 30 1C in June but not in October. 2. Review of data from the literature indicated that chameleons in general have ﬁeld body temperatures and selected body temperatures (means 30 and 31 1C, respectively) that are low relative to those of most other diurnal lizards. r 2007 Elsevier Ltd. All rights reserved.

Keywords: Chamaeleo chamaeleon; Chamaeleonidae; Field body temperature; Selected body temperature; Thermal biology; Thermoregulation

1. Introduction characterized by prey capture by ballistic tongue projection, zygodactylus grasping feet, prehensile tails, slow Body temperatures of lizards measured during normal deliberate movements, and reliance on crypsis for predator activity in the field (Tb) exhibit a strong phylogenetic signal avoidance (Wainwright and Bennett, 1992; Cuadrado at the generic level, and even at higher taxonomic levels et al., 2001; Butler, 2005). An a priori expectation from (Avery, 1982; van Berkum, 1988; Huey et al., 1989; their homogeneous ‘slow-lane’ lifestyle and energy-con- Andrews, 1998). These patterns emerge despite variation servative behavior is that the family would be characterized in Tb that results from the constraints and opportunities by relatively low Tb’s. provided by particular habitats, weather patterns, inter- This study had two major objectives. The first was to add specific interactions, etc. (Huey and Slatkin, 1976; Downes to the very limited set of information available on the and Shine, 1998; Rock et al., 2002). Nonetheless, phylo- thermal biology of chameleons. In accord, I measured Tb’s genetic patterns can be sharpened with a metric that of Chamaeleo chamaeleon in Spain. C. chamaeleon is widely disentangles body temperature from environmental influ- distributed in northern Africa with isolated populations in ences. Tsel, the body temperature selected by lizards on Spain and Portugal and on a number of Mediterranean laboratory thermal gradients, provides information on islands (Pleguezuelos et al., 1999). In Spain, the species is actual thermal ‘preference’ (Huey et al., 1989; Andrews, restricted to small patches of native Mediterranean scrub 1998; Hertz et al., 1993). along the southwestern coast (Mellado et al., 2001). The The above characterization of the thermal biology of second objective was to summarize available information lizards is based largely on data from a subset of lizard on the thermal biology of the Chamaeleonidae and to diversity, re Anolis, Sceloporus, macroteiids, skinks, and compare this information with that of other diurnal lizards. geckos. Are these characterizations applicable to other lizard groups? Chameleons comprise a relatively large 2. Materials and methods (about 130 species) group of highly specialized arboreal predators (Necas, 1999; Pough et al., 2004). The family is I made observations on the thermal biology of C. chamaeleon in and around the Jardin Botańico at Rota ÃTel.: +1 540 231 5728; fax: +1 540 231 9307. and at the Centro Recuperacioń Especies Amenazadas E-mail address: [email protected] facility at El Puerto de Santa Marıá, Ca´diz Province,

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Spain, during 25–27 October 2005 and on 14 June 2006. thermoregulation were the greatest. Coastal locations were Measurements of Tb were made between 1000 and 1400 h. arbitrarily assigned an elevation of 20 m if elevation was The weather was sunny with scattered clouds (2 days in not given in the paper. Tsel’s were from studies on October and in June) or hazy (1 day in October). In individuals in laboratory thermal gradients or in outdoor general, October is relatively cool and June is relatively cages provided with areas of full sun and heavy shade. warm; mean maximum temperatures at El Puerto de Santa Ambient temperature gradients in both situations provided Marıá for these months for 2001–2006 were 24.7 and chameleons the potential to achieve Tb’s well above and 29.3 1C, respectively. Individuals ranged in size from 50 to below actual selected body temperatures. 123 mm snout–vent length (4–37 g), although most indivi- Parametric analyses were conducted using SAS software duals were adults (SVLs 485 mm). (SAS Institute, 1996). Probability values of less than 0.05 Body temperatures of chameleons were measured within were considered significant. The assumption of homoge- a few seconds of capture. In June, Tb’s (n ¼ 16) were neity of slopes for ANCOVAs was satisfied by testing for measured with an Omega thermocouple thermometer significance of the interaction of the covariate with (Model HH21) inserted 1–2 cm into the cloaca. In October, treatment variables. temperatures of 22 individuals were measured using an infrared (IR) thermometer (Raytek Raynger ST60). Read- ings were taken at the center of the trunk region on the 3. Results and discussion right and left flanks (Hare et al., 2007). Cloacal temperatures of seven of these individuals were also measured using 3.1. Observations on C. chamaeleon a Schultheis quick-reading thermometer immediately after recording IR temperatures. To determine the association Chameleons were typically perched in the sun or in between cloacal temperature and IR temperature, Tb partial shade at 30–50 cm (range 0–200 cm) above the (cloacal) was used as the dependent variable and the lower, ground. Retama monosperma was the most commonly used higher, and mean of the two IR temperatures were used as perch site; this was the most common shrub on the study independent variables in regression analyses. The higher of areas, although chameleons were occasionally found on the two IR temperatures provided the best predictor of Tb other shrubby vegetation. Thermoregulatory behavior of 2 (Tb ¼ 0.44+0.96 IR, F1,5 ¼ 40.0, P ¼ 0.0015, R ¼ 0.89). chameleons consisted of movements between the exposed Equations for all three IR temperatures predicted Tb’s branches on the sides and tops of shrubs and their accurately at the high end of the observed Tb range. At an relatively shaded centers. Thirty-five of the 38 chameleons IR value of 31 1C, for example, the models predicted Tb’s observed were females. of 30.5–31.5 1C. At the low end of the observed Tb range, Overall, Tb’s of chameleons averaged 28.8 1C(n ¼ 38, however, the model using the higher of the two IR range 24.0–32.3 1C). Tb was related to Ta (Fig. 1)as 2 temperatures performed far better than the other models. Tb ¼ 13.0+0.62Ta (F1,36 ¼ 30.5, Po0.0001, R ¼ 0.46). At an IR value of 25 1C, for example, the former model The slope (b ¼ 0.62) differed from 1.0 (t ¼ 3.3, po0.01, predicted a Tb of 25.4 1C and the mean IR and the lower of Sokal and Rohlf, 1981). the two IR temperature models underestimated Tb by Seasonal differences were pronounced. Tb’s were lower 1.1 and 2.9 1C, respectively. The higher of the IR values during October than during June (F1,36 ¼ 9.7, P ¼ 0.004, was accordingly used as a surrogate for Tb for the 15 one-factor ANOVA) in accord with lower Ta’s. Respective individuals for whom Tb was not measured directly. Shaded air temperatures (Ta) at 1 cm above the perch site were measured with the Omega thermocouple thermometer. The Omega and Schultheis thermometers were calibrated against a NIST-certified thermometer in the laboratory. Data on long-term (2001–2006) ambient temperatures were obtained for the Estacioń Meteorolo´gi- ca de Puerto de Santa Marıá posted on the web site of the Instituto Andaluz de Investigacioń y Formacioń Agraria y Pesquera. Additional observations on the thermal biology of chameleons were found from web-based and standard literature searches. The data were screened for quality and consistency (e.g. presentation of original data, adequate sample size, data presented for adults, or at least, relatively large individuals in a population, observations of T made Fig. 1. Body temperature (Tb) as a function of ambient temperature (Ta) b for Chamaeleon chamaeleon (n ¼ 38). Data collected in October are during the normal daytime activity period). When ob- indicated by solid circles and data collected in June by open circles. The servations of Tb’s were reported for different seasons, dashed line represents isothermy and the solid line is the overall regression

I used data for the season when the opportunities for between Tb and Ta. Author's personal copy

ARTICLE IN PRESS R.M. Andrews / Journal of Thermal Biology 33 (2008) 57–61 59 mean Tb’s for October and June were 28.0 1C (range 3.2. Selected and field body temperatures of chameleons 24.5–32.3 1C) and 29.8 1C (range 27.6–31.6 1C) and respective mean Ta’s were 24.5 and 26.5 1C. During October when I found information on Tsel or Tb or both for 17 Ta was relatively low, Tb was positively correlated with Ta populations and 12 species of chameleons (Table 1). With (r ¼ 0.66, P ¼ 0.001, n ¼ 22). In contrast, during June the exception of Furcifer pardalis from Madagascar, all when Ta was relatively high, Tb was independent of Ta species were African. The overall mean Tsel was 30.9 1C (r ¼ 0.33, P ¼ 0.22, n ¼ 16). Nonetheless, after accounting with a range of 25.0–33.4 1C. Mean Tb was 29.7 1C with a for Ta, Tb’s in October and June did not differ (F1,35 ¼ 1.7, range of 22.2–32.5 1C. While mean Tsel and Tb were similar, P ¼ 0.19, one-factor ANCOVA with Ta as the covariate). the range of Tsel’s was less than the range of Tb’s. Tsel and Individual C. chamaeleon were active thermoregulators. Tb were not correlated (r ¼ 0.04, P ¼ 0.91, n ¼ 10). Tb was Overall, the slope of the regression between Tb and Ta was not related to latitude (r ¼ 0.19, P ¼ 0.54, n ¼ 13) but was less than 1; Tb’s were relatively high when Ta was the negatively correlated with elevation (r ¼0.58, P ¼ 0.04, lowest and relatively low when Ta was the highest. n ¼ 13). Inspection of the data (Fig. 2) indicated that Moreover, the lower, higher, and mean of the two IR individuals were able to maintain Tb’s of about 31 1Cupto temperatures were very similar to observed Tb’s when Tb’s about 2000 m; at higher elevations Tb’s declined below were relatively high (31 1C), but only the higher of the IR preferred levels. temperatures was similar to Tb when Tb was low (25 1C). These observations suggest that at low ambient temperatures chameleons were oriented perpendicular to the sun such that the shaded flank would have a lower IR than the insolated flank, but that when ambient temperature was high, chameleons were not directly exposed to the sun and as a consequence their IR and (cloacal) Tb’s were similar. The ‘preferred’ Tb of C. chamaeleon was about 30 1C, the mean Tb observed in June. This conclusion is based on the observations that: (1) maximum observed Tb’s were the same in October and June, that is, 32 1C, (2) Tb was not correlated with Ta in June; the independence of Tb relative to Ta indicates active thermoregulation, and (3) Tb’s observed in June were exhibited during the time of year with the greatest potential for raising Tb’s to preferred levels; long-term maximum ambient temperatures for June, 1 July, and August averaged 29.3, 30.5, and 30.0 C, Fig. 2. Field body temperatures (Tb) of chameleons as a function of respectively. elevation. Data are from Table 1.

Table 1 Mean ﬁeld and selected body temperatures (1C) of chameleons

Species Selected Tsel’s Field Tb’s Elevation (m) Latitude Source

BRpu 25.0 28.1 140 341S Burrage (1973) CHaf 31.0 – 20 371N Dimaki et al. (2000) CHbi 31.1 28.9 2000 21S Bennett (2004) CHca 32.9 – 40 171N Zari (1993) CHca 30.4 – – – Andrews, unpublished CHch – 29.8 20 371N This study CHch 31.6 – 20 381N Dimaki et al. (2000) CHdi – 31.2 1830 261S Stebbins (1961) CHdi 32.8 32.0 800 21S Bennett (2004) CHel 33.4 32.5 1800 01N Bennett (2004) CHho – 26.0 43000 11S Hebrard et al. (1982) CHho 30.2 31.3 1700 21S Bennett (2004) CHja 32.1 30.4 1700 21S Bennett (2004) CHna 29.3 32.0 1000 231S Burrage (1973) (inland) CHna 29.3 30.9 100 231S Burrage (1973) (coastal) CHsc 32.6 22.2 3300 01S Bennett (2004) FUpa 31.0 31.3 20 151S Ferguson et al. (2004)

BRpu: Bradypodion pumilum; CHaf: Chamaeleo africanus; CHbi: Chamaeleo bitaeniatus; CHca: Chamaeleo calyptratus; CHch: Chamaeleo chamaeleon; CHdi: Chamaeleo dilepis; CHel: Chamaeleo ellioti; CHho: Chamaeleo hohnelii; CHja: Chamaeleo jacksonii; CHna: Chamaeleo namaquensis; CHsc: Chamaeleo schubotzi; FUpa: Furcifer pardalis. Author's personal copy

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Chameleons exhibit relatively low Tb’s for diurnal dion pumilum are active at a wide range of Tb’s as a result of lizards. For example, Tb’s of species from low to moderate diel and seasonal changes in weather (Burrage, 1973). elevations (o1700 m) averaged 31 1C with a range of only While members of the family Chamaeleonidae may share 28.1–32.0 1C(Table 1). In contrast, diurnal lizard species of most, if not all, features of a slow-lane lifestyle, informa- open-habitats at low to moderate elevations exhibit mean tion on their thermal biology is limited to the genera Tb’s of 34–40 1C(Huey et al., 1989; Andrews, 1998; Belliure Chamaeleo, Furcifer, and Bradypodion. Because their et al., 1996). This difference does not reflect habitat per se geographic ranges include the diversity of habitats occu- because chameleons also exhibt low Tb’s relative to pied by the entire family, it is unlikely that the thermal sympatric diurnal lizards (Psammodromus: Belliure et al., biology of these genera reflects thermal specialization based 1996; Mabuya: Hebrard et al., 1982). Despite relatively low on habitat. Nonetheless, generalizations provided here Tb’s, however, chameleons are not thermoconformers or should only tentatively be extended to the family as a thermally passive (Bennett, 2004). The similarity of Tb and whole. Tsel indicates that chameleons actively maintain body 1 temperatures about 30 C when ambient conditions permit. Acknowledgments At very high elevations, chameleons and other lizards are seldom able to achieve ‘preferred’ temperatures because of I would like to thank the Morris Animal Foundation for low ambient temperature and pervasive cloud cover financial support for fieldwork, Carmen Dıáz-Paniagua (Hebrard et al., 1982; Andrews, 1998; Bennett, 2004). and Adolfo Marco for logistic support, and Juan Go´mez, 1 Nonetheless, a Tsel of about 30 C is typical. For example, Juan Patinõ, and Liliana Quinõnes for their assistance in when Chamaeleo schubotzi individuals were transplanted the field. from 3300 to 1700 m, Tb’s increased from 22 1C(Bennett, 2004) to over 30 1C(Angilletta et al., 2006). Relatively low body temperatures thus appear to be part References of a suite of coadapted characters of chameleons. Abu-Ghalyun, Y., Greenwald, L., Hetherington, T.E., Gaunt, A.S., 1988. Chameleons rely on camouflage for predator avoidance The physiological basis of slow locomotion in chameleons. J. Exp. (Cuadrado et al., 2001). They are ‘cruising’ predators that Zool. 245, 225–231. move slowly, but relatively frequently (Butler, 2005). Andrews, R.M., 1998. Geographic variation in field body temperature of Locomotion speed is limited by the physiology, biochem- Sceloporus lizards. J. Therm. Biol. 23, 329–334. istry, and morphology of muscles (Guppy and Davison, Andrews, R.M., Pough, F.H., 1985. Metabolism of squamate reptiles: allometric and ecological relationships. Physiol. Zool. 58, 214–231. 1982; Abu-Ghalyun et al., 1988). Prey capture occurs at a Angilletta Jr., M.J., Bennett, A.F., Gunderley, H., Navas, C.A., distance by tongue projection once cautious movement has Seebacher, F., Wilson, R.S., 2006. Coadaptation: a unifying principle brought the chameleon within striking distance. Chame- in evolutionary thermal biology. Physiol. Biochem. Zool. 79, 282–294. leons feed frequently and most prey items, including Avery, R.A., 1982. Field studies of body temperatures and thermoregula- spiders, heteroptera, and flying insects such as diptera tion. In: Gans, C., Pough, F.H. (Eds.), Biology of the Reptilia, Physiology C, vol. 12. Academic Press, New York, pp. 93–166. and hymenoptera, are small (Pleguezuelos et al., 1999; Belliure, J., Carrascal, L.M., Diaz, J.A., 1996. Covariation of thermal Hofer et al., 2003). Chameleons, however, do not share the biology and foraging mode in two Mediterrranean lacertid lizards. reduced standard metabolism that characterizes reclusive Ecology 77, 1163–1173. predators such as gekkonids and xantusiids (Andrews and Bennett, A.F., 2004. Thermoregulation in African chameleons. In: Morris, Pough, 1985). Standard (fasting, during normal period of S., Vosloo, A. (Eds.), Animals and Environments. Proceedings of the Third International Conference of Comparative Physiology and inactivity) metabolic rates of Chamaeleo calyptratus are Biochemistry, International Congress Series, vol. 1275. Elsevier, similar to those of other day-active lizards (data in Zari Amsterdam, pp. 234–241. (1993) were compared with predictive equations of Burrage, B.R., 1973. Comparative ecology and behaviour of Chamaeleo Andrews and Pough, 1985). Nonetheless, field metabolic pumilus pumilus (Gmelin) and C. namaquensis A. Smith (Sauria: rates of chameleons are likely to be lower than those of Chamaeleonidae). Ann. S. Afr. Mus. 61, 1–158. Butler, M.A., 2005. Foraging mode of the chameleon, Bradypodion other day-active lizards because of the combination of slow pumilum: a challenge to the sit-and-wait versus active forager locomotion and relatively low Tb’s. Tb’s are often paradigm? Biol. J. Linn. Soc. 84, 797–808. substantially lower than Tsel because individuals are active Cuadrado, M., Martıńez, J., Lo´pez, P., 2001. Camouflage and escape at times of day and seasons when they are unable to decisions in the common chameleon Chamaeleo chamaeleon. Biol. J. thermoregulate carefully. A Chamaeleo hohnelii, for exam- Linn. Soc. 72, 547–554. Dimaki, M., Valakos, E.D., Legakis, A., 2000. Variation in body ple, projected its tongue and captured a prey item when its temperature of the African chameleon Chamaeleo africanus Laurenti, Tb was 7 1C(Hebrard et al., 1982) and Chamaeleo jacksonii 1768 and the common chameleon Chamaeleo chamaeleon (Linnaeus, individuals fed and moved about at Tb’s of 10 1C(Bennett, 1758). Belg. J. Zool. 130 (Suppl.), 89–93. 2004). C. chamaeleon individuals are active year round Downes, S., Shine, R., 1998. Heat, safety or solitude? Anim. Behav. 55, despite low winter temperatures (Mellado et al., 2001); the 1387–1396. Ferguson, G.W., Murphy, J.B., Ramanamanjato, J.-B., Raselimanana, lowest temperatures at my study sites are in January and A.P., 2004. The Panther Chameleon: Color Variation, Natural February, with mean monthly minimum and maximum History, Conservation, and Captive Management. Krieger Publishing ambient temperatures of 5 and 16 1C. Similarly, Bradypo- Co., Malabar, FL. Author's personal copy

ARTICLE IN PRESS R.M. Andrews / Journal of Thermal Biology 33 (2008) 57–61 61

Hare, J.R., Whitworth, E., Cree, A., 2007. Correct orientation of a hand- Necas, P., 1999. Chameleons: Nature’s Hidden Jewels. Edition Chimaira, held infrared thermometer is important for accurate measurement of Frankfurt am Main, 348pp. body temperatures in small lizards and tuatara. Herpetol. Rev. 38, Pleguezuelos, J.M., Poveda, J.C., Monterrubio, R., Ontiveros, D., 1999. 311–315. Feeding habits of the common chameleon, Chamaeleo chamaeleon Hebrard, J.J., Reilly, S.M., Guppy, M., 1982. Thermal ecology of (Linnaeus, 1758) in the southeastern Iberian Peninsula. Isr. J. Zool. 45, Chamaeleo hohnelli and Mabuya varia in the Aberdare Mountains; 267–276. constraints on heterothermy in an alpine habitat. J. East Afr. Nat. Pough, F.H., Andrews, R.M., Crump, M.L., Cadle, J.E., Savitzky, Hist. Soc. 176, 1–8. A.H., Wells, K.D., 2004. Herpetology. Prentice-Hall, New York, Hertz, P.E., Huey, R.B., Stevenson, R.D., 1993. Evaluating temperature 726pp. regulation by field-active ectotherms: the fallacy of the inappropriate Rock, J., Cree, A., Andrews, R.M., 2002. The effect of reproductive question. Am. Nat. 142, 796–818. condition on thermoregulation in a viviparous gecko from a cool Hofer, U., Baur, H., Bersier, L., 2003. Ecology of three sympatric species climate. J. Therm. Biol. 27, 17–27. of the genus Chamaeleo in a tropical upland forest in Cameroon. SAS Institute, 1996. SAS Version 8.2. SAS Institute, Cary, NC. J. Herpetol. 37, 203–207. Sokal, R.R., Rohlf, F.J., 1981. Biometry: The Principles and Practice of Huey, R.B., Slatkin, M., 1976. Cost and benefits of lizard thermoregula- Statistics in Biological Research. W.H. Freeman, New York, 859pp. tion. Q. Rev. Biol. 51, 363–384. Stebbins, R.C., 1961. Body temperature studies in South African lizards. Huey, R.B., Niewiarowski, P.H., Kaufmann, J., Heron, J.C., 1989. Koedoe 4, 54–67. Thermal biology of nocturnal ectotherms: is sprint performance of van Berkum, F.H., 1988. Latitudinal patterns of the thermal sensitivity of geckos maximal at low body temperatures? Physiol. Zool. 62, 488–504. sprint speed in lizards. Am. Nat. 132, 327–343. Guppy, M., Davison, W., 1982. The hare and the tortoise: metabolic Wainwright, P.C., Bennett, A.F., 1992. The mechanism of tongue strategies in cardiac and skeletal muscules of the skink and the projection in chameleons. I. Electromyographic tests of functional chameleon. J. Exp. Zool. 220, 289–295. hypotheses. J. Exp. Biol. 168, 1–21. Mellado, J., Gimeńez, L., Go´mez, J.J., Sanjuań, M., 2001. El camaleońen Zari, T.A., 1993. Effects of body mass and temperature on standard Andalucıá. Distribucioń actual y amenazas para su supervivencia. metabolic rate of the desert chameleon Chamaeleo calyptratus. J. Arid Fundacioń Alcalde Zoilo Ruiz-Mateos, Coleccioń Rabeta Ruta, no. 6. Environ. 24, 75–80.