Author's Accepted Manuscript
Colouration affects heating and cooling in three colour morphs of the Australian bluetongue lizard, Tiliqua scincoides Michael R.S. Geen, Gregory R. Johnston
www.elsevier.com/locate/jtherbio
PII: DOI: Reference:
S0306-4565(14)00064-3 http://dx.doi.org/10.1016/j.jtherbio.2014.04.004 TB1515
To appear in:
Journal of Thermal Biology
Received date: 5 September 2013 Revised date: 24 April 2014 Accepted date: 24 April 2014 Cite this article as: Michael R.S. Geen, Gregory R. Johnston, Colouration affects heating and cooling in three colour morphs of the Australian bluetongue lizard, Tiliqua scincoides, Journal of Thermal Biology, http://dx.doi.org/10.1016/j. jtherbio.2014.04.004 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ColourationaffectsheatingandcoolinginthreecolourmorphsoftheAustralianbluetonguelizard, Tiliquascincoides. MichaelR.S.Geena&GregoryR.Johnstona,b
a
SchoolofBiologicalSciences,FlindersUniversity,BedfordPark5042,Australia
b
VertebratesSection,SouthAustralianMuseum,NorthTerrace,Adelaide5000,Australia
Correspondingauthor:
DrGregJohnston,
HonoraryResearchAssociate
VertebratesSection,SouthAustralianMuseum,
NorthTerrace,Adelaide5000,Australia
P:+61883703021
1
E:[email protected](GRJ)
E:[email protected](MRSG)
ABSTRACT
Thecolourmediatedthermoregulationhypothesispredictsthatdarkbodycolour(lowreflectance) allowsorganismstogainheatmoreefficientlythandoespalecolouration(highreflectance).This predictionisintuitiveandwidelyassumedtobetrue,buthaspoorempiricalsupport.Weusedrare, captivebred,mutantmelanistic,albinoandwildtypeAustralianbluetonguelizards,Tiliquascincoides tomeasuretheeffectsofskinreflectanceontheheatingandcoolingrates.Wemeasuredheating underanartificialradiantheatsourceandcoolingratesinanicecooledboxusinglivelizardsinaroom withstillair.Theeffectofskinreflectanceonheattransferwasclear,despitethesubstantialinfluence ofbodysize.MelanisticT.scincoidesshowedlowreflectanceandgainedheatfasterthanhighly reflectivealbinos.Melanisticlizardsalsolostheatfasterthanalbinos.Wildtypelizardswere intermediateinreflectance,gainedheatatratesindistinguishablefrommelanisticlizards,andlost heatatratesindistinguishablefromalbinolizards.Thisstudysystemallowedustocontrolforvariables thatwereconfoundedinotherstudiesandmayexplaintheinconsistentsupportforthecolour
2
mediatedthermoregulationhypothesis.Ourresultsprovideclearevidencethatskinreflectance influencestherateofheatingandcoolinginectotherms.
Keywords: albinism - melanism - reflectance - reptiles - colour-mediated thermoregulation – thermal melanism - Tiliqua
1. Introduction
The colour of animals affects many aspects of their biology. It may play a role in concealment, communication, homeostasis, or some combination of these (Caro, 2005; Cott, 1940). Theoretically, colour can be an important influence on an organism’s thermal energy balance due to dermal absorptance of solar radiation (Bartlett and Gates, 1967). The colour-mediated thermoregulation hypothesis predicts that dark-coloured organisms should heat faster than equivalent light-coloured organisms. Concomitantly, absorptance of radiant energy should be slower in light-coloured organisms because they have greater reflectance. This prediction is intuitive and widely assumed to be true. However, the extent to which colour actually mediates thermoregulation in living organisms remains unclear, given that many other factors also influence thermal energy balance (Gates, 1980). Furthermore the colour-mediated
3
thermoregulation hypothesis has poor empirical support in the literature (see Umbers et al., 2013 for a review of the literature on invertebrates & Table 1 for a summary of the relevant literature in ectothermic vertebrates). In ectotherms, body temperature has profound effects on physiological and behavioural performance (Huey and Kingsolver, 1989; Peterson et al., 1993). Consequently, they use a variety of means to regulate their temperature (Huey, 1982). In endotherms, coat or feather colour can modify the physiological costs of maintaining constant body temperature (Heppner, 1970; Hetem et al., 2009). For both endotherms and ectotherms the occurrence of melanistic populations at low latitudes, or in montane, peninsular or coastal habitats, fits with the notion that low dermal reflectance provides a thermal advantage in environments exposed to low ambient temperatures (Clusella-Trullas et al., 2007; Majerus, 1998). Umbers et al. (2013) have ably reviewed the empirical tests of the colour-mediated thermoregulation hypothesis in invertebrates. We extend their review to include papers on ectothermic vertebrates (Table 1). Investigations using inanimate operative temperature models or dead animals have demonstrated that, in the absence of physiological and behavioural regulation, reflectance can have an effect on core temperature (Clusella-Trullas et al., 2009; Shine and Kearney, 2001; Wasserthal, 1975). However, studies of live ectotherms have produced variable results (Table 1). For example, colour had no detectable influence on heat budget in 17 of 31 studies of invertebrates (Umbers et al., 2013). Similarly among ectothermic vertebrates, some studies have found a relationship between colour and heating rate (Forsman, 1995; Gibson and Falls, 1979a; Tanaka, 2005; Vences et al., 2002), whereas others have not (Bittner et al., 2002; Clusella-Trullas et al., 2009; Crisp et al., 1979; Pearson, 1977; see Table 1). Past studies of colour-mediated thermoregulation are confounded by considerable variation
4
in methodology such as the means of quantifying colouration and temperature, the use of natural colour variants versus painted animals or temperature models, and the type of colour variation being investigated (e.g. differently coloured species, intraspecific colour morphs, or colour change within individuals; see Umbers et al. 2013 and Table 1). Most studies of colourmediated thermoregulation have described colour qualitatively, rather than quantitatively (Umbers et al., 2013 & Table 1). Additionally, the rate of cooling may be as important as the rate of heating for organisms in thermally challenging environments, yet few studies have measured the influence of colour on both heating and cooling in the context of the colourmediated thermoregulation (cf. Pearson, 1977; Rice and Bradshaw, 1980). The variable influence of reflectance on heat transfer reported in the literature may be due to other biological factors that overwhelm the influence of skin reflectance, or on the circumstances under which heating/cooling was measured. Simultaneous temperature dependant changes in blood flow and visible reflectance confound the influence of skin reflectance on rates of heating and cooling (Bartholemew and Tucker, 1963; Cowles, 1958; Rice and Bradshaw, 1980). Dermal reflectance is most likely to influence heating and cooling rates under still conditions with a radiant heat source, such as the sun. In order to test the influence of colour on the thermal biology of ectotherms one would ideally measure skin reflectance and heating/cooling rates in a radiant environment using a single species which exhibits extreme (black-white) variation in colour and shows no physiological colour change. The Australian bluetongue lizard (Tiliqua scincoides) fulfils these criteria. We took advantage of an existing captive breeding program of rare albino and melanistic mutant colour forms of bluetongue lizard the to test the predictions of the colourmediated thermoregulation hypothesis. If this hypothesis is true we would expect (1)
5
individuals with low reflectance to heat-up more quickly than individuals with high reflectance. Conversely we would expect (2) individuals with low reflectance with cool-down more quickly than individuals with high reflectance.
2.Materialsandmethods
2.1.Studyspecies
T.scincoidesarelarge(
Colouration affects heating and cooling in three colour morphs of the Australian bluetongue lizard, Tiliqua scincoides Michael R.S. Geen, Gregory R. Johnston
www.elsevier.com/locate/jtherbio
PII: DOI: Reference:
S0306-4565(14)00064-3 http://dx.doi.org/10.1016/j.jtherbio.2014.04.004 TB1515
To appear in:
Journal of Thermal Biology
Received date: 5 September 2013 Revised date: 24 April 2014 Accepted date: 24 April 2014 Cite this article as: Michael R.S. Geen, Gregory R. Johnston, Colouration affects heating and cooling in three colour morphs of the Australian bluetongue lizard, Tiliqua scincoides, Journal of Thermal Biology, http://dx.doi.org/10.1016/j. jtherbio.2014.04.004 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ColourationaffectsheatingandcoolinginthreecolourmorphsoftheAustralianbluetonguelizard, Tiliquascincoides. MichaelR.S.Geena&GregoryR.Johnstona,b
a
SchoolofBiologicalSciences,FlindersUniversity,BedfordPark5042,Australia
b
VertebratesSection,SouthAustralianMuseum,NorthTerrace,Adelaide5000,Australia
Correspondingauthor:
DrGregJohnston,
HonoraryResearchAssociate
VertebratesSection,SouthAustralianMuseum,
NorthTerrace,Adelaide5000,Australia
P:+61883703021
1
E:[email protected](GRJ)
E:[email protected](MRSG)
ABSTRACT
Thecolourmediatedthermoregulationhypothesispredictsthatdarkbodycolour(lowreflectance) allowsorganismstogainheatmoreefficientlythandoespalecolouration(highreflectance).This predictionisintuitiveandwidelyassumedtobetrue,buthaspoorempiricalsupport.Weusedrare, captivebred,mutantmelanistic,albinoandwildtypeAustralianbluetonguelizards,Tiliquascincoides tomeasuretheeffectsofskinreflectanceontheheatingandcoolingrates.Wemeasuredheating underanartificialradiantheatsourceandcoolingratesinanicecooledboxusinglivelizardsinaroom withstillair.Theeffectofskinreflectanceonheattransferwasclear,despitethesubstantialinfluence ofbodysize.MelanisticT.scincoidesshowedlowreflectanceandgainedheatfasterthanhighly reflectivealbinos.Melanisticlizardsalsolostheatfasterthanalbinos.Wildtypelizardswere intermediateinreflectance,gainedheatatratesindistinguishablefrommelanisticlizards,andlost heatatratesindistinguishablefromalbinolizards.Thisstudysystemallowedustocontrolforvariables thatwereconfoundedinotherstudiesandmayexplaintheinconsistentsupportforthecolour
2
mediatedthermoregulationhypothesis.Ourresultsprovideclearevidencethatskinreflectance influencestherateofheatingandcoolinginectotherms.
Keywords: albinism - melanism - reflectance - reptiles - colour-mediated thermoregulation – thermal melanism - Tiliqua
1. Introduction
The colour of animals affects many aspects of their biology. It may play a role in concealment, communication, homeostasis, or some combination of these (Caro, 2005; Cott, 1940). Theoretically, colour can be an important influence on an organism’s thermal energy balance due to dermal absorptance of solar radiation (Bartlett and Gates, 1967). The colour-mediated thermoregulation hypothesis predicts that dark-coloured organisms should heat faster than equivalent light-coloured organisms. Concomitantly, absorptance of radiant energy should be slower in light-coloured organisms because they have greater reflectance. This prediction is intuitive and widely assumed to be true. However, the extent to which colour actually mediates thermoregulation in living organisms remains unclear, given that many other factors also influence thermal energy balance (Gates, 1980). Furthermore the colour-mediated
3
thermoregulation hypothesis has poor empirical support in the literature (see Umbers et al., 2013 for a review of the literature on invertebrates & Table 1 for a summary of the relevant literature in ectothermic vertebrates). In ectotherms, body temperature has profound effects on physiological and behavioural performance (Huey and Kingsolver, 1989; Peterson et al., 1993). Consequently, they use a variety of means to regulate their temperature (Huey, 1982). In endotherms, coat or feather colour can modify the physiological costs of maintaining constant body temperature (Heppner, 1970; Hetem et al., 2009). For both endotherms and ectotherms the occurrence of melanistic populations at low latitudes, or in montane, peninsular or coastal habitats, fits with the notion that low dermal reflectance provides a thermal advantage in environments exposed to low ambient temperatures (Clusella-Trullas et al., 2007; Majerus, 1998). Umbers et al. (2013) have ably reviewed the empirical tests of the colour-mediated thermoregulation hypothesis in invertebrates. We extend their review to include papers on ectothermic vertebrates (Table 1). Investigations using inanimate operative temperature models or dead animals have demonstrated that, in the absence of physiological and behavioural regulation, reflectance can have an effect on core temperature (Clusella-Trullas et al., 2009; Shine and Kearney, 2001; Wasserthal, 1975). However, studies of live ectotherms have produced variable results (Table 1). For example, colour had no detectable influence on heat budget in 17 of 31 studies of invertebrates (Umbers et al., 2013). Similarly among ectothermic vertebrates, some studies have found a relationship between colour and heating rate (Forsman, 1995; Gibson and Falls, 1979a; Tanaka, 2005; Vences et al., 2002), whereas others have not (Bittner et al., 2002; Clusella-Trullas et al., 2009; Crisp et al., 1979; Pearson, 1977; see Table 1). Past studies of colour-mediated thermoregulation are confounded by considerable variation
4
in methodology such as the means of quantifying colouration and temperature, the use of natural colour variants versus painted animals or temperature models, and the type of colour variation being investigated (e.g. differently coloured species, intraspecific colour morphs, or colour change within individuals; see Umbers et al. 2013 and Table 1). Most studies of colourmediated thermoregulation have described colour qualitatively, rather than quantitatively (Umbers et al., 2013 & Table 1). Additionally, the rate of cooling may be as important as the rate of heating for organisms in thermally challenging environments, yet few studies have measured the influence of colour on both heating and cooling in the context of the colourmediated thermoregulation (cf. Pearson, 1977; Rice and Bradshaw, 1980). The variable influence of reflectance on heat transfer reported in the literature may be due to other biological factors that overwhelm the influence of skin reflectance, or on the circumstances under which heating/cooling was measured. Simultaneous temperature dependant changes in blood flow and visible reflectance confound the influence of skin reflectance on rates of heating and cooling (Bartholemew and Tucker, 1963; Cowles, 1958; Rice and Bradshaw, 1980). Dermal reflectance is most likely to influence heating and cooling rates under still conditions with a radiant heat source, such as the sun. In order to test the influence of colour on the thermal biology of ectotherms one would ideally measure skin reflectance and heating/cooling rates in a radiant environment using a single species which exhibits extreme (black-white) variation in colour and shows no physiological colour change. The Australian bluetongue lizard (Tiliqua scincoides) fulfils these criteria. We took advantage of an existing captive breeding program of rare albino and melanistic mutant colour forms of bluetongue lizard the to test the predictions of the colourmediated thermoregulation hypothesis. If this hypothesis is true we would expect (1)
5
individuals with low reflectance to heat-up more quickly than individuals with high reflectance. Conversely we would expect (2) individuals with low reflectance with cool-down more quickly than individuals with high reflectance.
2.Materialsandmethods
2.1.Studyspecies
T.scincoidesarelarge(
