Herpetological Conservation and Biology 9(2):309−321. Submitted: 14 November 2014; Accepted: 2 July 2014; Published: 12 October 2014.
PHYSIOLOGICAL ECOLOGY OF THE GROUND SKINK, SCINCELLA LATERALIS IN SOUTH CAROLINA: THERMAL BIOLOGY, METABOLISM, WATER LOSS, AND SEASONAL PATTERNS
SCOTT L. PARKER
Department of Biology, Coastal Carolina University, P.O. Box 261954, Conway, South Carolina 29528-6054 USA, e-mail: [email protected]
Abstract.— Reptiles with small body size and high surface-to-volume ratios face challenges in thermoregulation and water balance because they rapidly exchange heat and lose moisture via evaporation to the environment. The purpose of this study is to determine the thermoregulatory mode of the skink Scincella lateralis in the field, as well as how temperature and season influence metabolism and water balance in this species. I measured field body temperatures (Tbf) and environmental temperatures during May to December 2012. I measured selected substrate temperatures in laboratory thermal gradients. For both summer and winter acclimatized skinks, I measured oxygen consumption at 24, 28, 32 and 36 °C. In the laboratory, I measured rates of heating and cooling in dry or humid air to determine the influence of evaporative cooling on heat exchange. I measured evaporative water loss at 28, 32 and 36 °C. In the field, skinks thermoregulated more effectively during autumn/winter (de - db = 9.0) than spring/summer (de - db =2.1), yet maintained similar average body temperatures between seasons (Tb autumn/winter: 28.0 °C vs. Tb spring/summer: 29.2 °C). Metabolic rates of summer and winter acclimatized skinks measured in the laboratory were temperature insensitive between 28–33 °C (Q10 ≈ 1), corresponding to the skink’s preferred temperature range. Metabolic rates were approximately twice as high during summer than winter indicating no seasonal acclimatory increase in metabolic rate. Heating and cooling rates in dry versus humid air indicated that skinks heated more slowly than they cooled in dry air, whereas heating and cooling rates were similar in humid air. Results of the study suggests that distribution and activity of skinks may depend on availability of microenvironments with suitable temperature and moisture conditions, which permit skinks to maintain body temperature and water balance within preferred ranges.
Key Words.— Evaporation; heating rate; lizards; oxygen consumption; thermal acclimation; thermoregulation
Quirt et al. 2006). Water balance is also intimately INTRODUCTION linked to the thermal environment because evaporative water loss increases with temperature (Mautz 1980, Understanding how environmental factors influence reviewed in Lillywhite 2006). As a consequence, spatial distribution and seasonal activity patterns of temperature can influence activity and habitat use organisms is one of the fundamental goals of ecological through its effect on water balance (Dawson et al. 1966; studies. Even in geographically widespread species, Neilson 2002; Kearney and Porter 2004). distribution across the landscape is often patchy, with One of the fundamental ways the thermal environment local abundance determined by microhabitat impacts physiology of ectotherms is through its effect on characteristics of the landscape matrix (Brown 1984). metabolism (Andrews and Pough 1985; Angilletta Temperature and moisture are two primary abiotic 2001). Metabolic rate in reptiles is generally an factors that influence the spatial distribution and activity exponential function of ambient temperature (Murrish patterns of small ectothermic vertebrates such as lizards and Vance 1968; Alesksiuk 1971). Departure from (Adolph 1990; Neilson 2002; Parker and Andrews 2007; thermal dependence of metabolic processes, however, Basundhara et al. 2010). Metabolic rate in ectotherms is occurs in several species of reptiles and is indicated by a also temperature-dependent, therefore activity is decreasing Q10 (i.e. decreased sensitivity of metabolism constrained both by thermal quality and temporal to temperature change) with increasing temperature near availability of temperatures that enhance essential the preferred body temperature (e.g. Aleksiuk 1971; processes such as foraging, digestion, and reproduction Dutton and Fitzpatrick 1975; Bennett and Dawson 1976; (Grant and Dunham 1988; Adolph 1990). Behavioral Cartland and Grimmond 1994; Wu et al. 2009). Q10 is thermoregulation effectively increases daily activity time the temperature coefficient describing the increase in by allowing individuals to exploit thermally favorable reaction rate of chemical process over 10 °C (Bĕlehrádek microenvironments and thereby maintain body 1930). Additionally, metabolic rate reflects acclimatory temperatures (Tb) within optimal ranges for enhanced adjustments in physiological processes associated with physiological function (e.g. Adolph and Porter 1993; seasonal changes in temperature (John-Alder 1984;
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Beyer and Spotila 1994). Although there is considerable (Hudson and Bertram 1966; pers. observ.). Daily variation among species, winter-active lizard species maximum temperatures in July average 33 °C, with often exhibit higher metabolic rates over a given temperatures not uncommonly exceeding 36 °C temperature range during winter compared to summer (National Oceanic and Atmospheric Administration (Dutton and Fitzpatrick 1975; Tsuji 1988). This pattern 2013. National Climatic Data Center. Monthly presumably reflects a compensatory acclimatory climatological summary for Conway, South Carolina. response to maintain function of physiological processes Available at http://www.ncdc.noaa.gov/cdo-web/ at cooler seasonal temperatures. In light of these [Accessed 1 July 2013]). In contrast, daily maximum observations, measuring metabolic responses to temperatures in January average 14 °C. Based on its temperature is important for studies in physiological relatively small size and high surface to volume ratio, S. ecology because it provides information on fundamental lateralis should have limited capacity to resist changes to physiological processes such as energy allocation, in temperature and moisture compared to larger species growth, and reproduction, which ultimately affect of lizards (Dawson et al. 1966; Fraser and Grigg 1984; individual fitness (Secor and Nagy 1994; Litzgus and Stevenson 1985). Surprisingly, very few comprehensive Hopkins 2003; Zaiden 2003). studies have examined the thermoregulatory mode of S. The Ground Skink (Scincella lateralis; Fig. 1) is a lateralis in the field nor determined how environmental small (0.6–1.5 g) diurnal scincid lizard with a temperature influences thermoregulation, metabolism, geographic distribution across the United States and water balance in this common species of lizard. To corresponding closely to that of the humid subtropical meet these aims, I tested three hypotheses: (1) S. climate zone defined by the Köppen climate lateralis selects thermal environments randomly within classification system (reviewed in Ackerman 1941). its habitat (i.e., is a thermoconformer); (2) metabolic rate Scincella lateralis differs from the majority of North is elevated during winter to compensate for lower American lizard species in that it is generally considered ambient temperatures during the winter season; and (3) a forest-dweller (Lewis 1951; Conant and Collins 1998) S. lateralis heat more slowly than they cool due to high with a relatively low preferred Tb of approximately 29 surface to volume ratio and corresponding elevated °C (Hudson and Bertram 1966). Lizard species evaporative water loss. inhabiting forested environments are generally predicted to be thermconformers, and accordingly, exert relatively MATERIALS AND METHODS little active thermoregulatory behavior due to the high cost of thermoregulation in environments where sunlight Collection and animal maintenance.—I collected patches are limited (Huey and Slatkin 1976). Smith adult Scincella lateralis (n = 64) in Conway, Horry (1997) concluded that thermal biology of S. lateralis is County, South Carolina, USA (33°47'8.72"N, consistent with that of a thermoconformer, because Tb of 79°2'0.04"W) from May, 2012 to December, 2012. The skinks in the field is closely correlated with ground research area consisted of an approximately 2 ha area of temperature. In contrast, body temperatures of captive S. mixed pine and hardwood forest including large areas of lateralis measured in laboratory thermal gradients dry open clearings covered by patchy short perennial suggests that S. lateralis actively thermoregulates, grasses and small shrubs (< 1.5 m; Fig. 1). Immediately avoiding ambient temperatures between 15–25 °C while after capture I measured surface body temperatures (see actively selecting ambient temperatures between 25–36 methods below). From these captured individuals, I °C (Hudson and Bertram 1966). In absence of obtained measurements of selected substrate comparative data on selected body temperatures relative temperature, metabolic rate, water loss and heating and to available environmental temperatures, however, the cooling rates (described below). thermoregulatory mode of S. lateralis remains undefined I transported lizards captured in the field soon after for skinks in the field. If S. lateralis is a capture to Coastal Carolina University and housed them thermoconformer, individuals should exhibit little in plastic terraria (290 × 220 × 220 mm, three to four directed temperature selection and instead occupy individuals per container). Terraria were provided with thermal environments at random within their habitat a substrate of shredded coconut fibers (Zoo Med Eco- (Huey et al. 1977; Adolph 1990). Alternatively, if S. Earth, Zoo Med, San Luis Obispo, California, USA) for lateralis engages in behavioral thermoregulation, lizards to bury in and a layer of clean dry oak leaves as a individuals should select thermal environments non- matrix for both cover as well as for basking. I fed randomly to maintain Tb within their preferred range. lizards small banded crickets (Gryllodes sigillatus) every The latter alternative, of course, assumes that other day and provided them with water by misting competitors or predators do not restrict the range of daily. To ensure lizards remained acclimated to seasonal thermoregulatory options available. environmental conditions, I maintained terraria outdoors In coastal South Carolina, S. lateralis is active year under a covered open air shelter. The outdoor housing round over a wide range of seasonal temperatures arrangement allowed lizards to be acclimated to ambient
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Pennsylvania, USA). The IR thermometer was calibrated against a National Institute of Standards and Technology (NIST)-certified thermometer. I used the measurement of surface body temperature with the IR thermometer to estimate core body temperature because measurements can be obtained more quickly with less handling than required for cloacal temperatures. Calibration trials indicated that surface body temperatures did not differ significantly from cloacal temperatures (t = 0.14, df = 8, P = 0.89); surface body temperatures were within ± 0.5 °C of cloacal temperatures measured using a thermocouple thermometer calibrated using a National Institute of Standards and Technology (NIST)-certified thermometer. Accordingly, surface body temperature is hereafter referred to as field body temperature (Tbf). After initial capture, lizards were quickly grasped by the hind leg, suspended in the air within 5 cm of the surface of the ground so that I could measure Tbf. I judged that the measurement of Tbf in this manner reduced convective heat loss by wind, while also reducing potential conductive exchange that could result by maintaining skinks in contact with the ground. I obtained field body temperatures by holding the IR thermometer approximately 10 cm above the dorsal body surface of the skink. Given an IR beam field of view ratio of 50:1, the area of temperature being measured at 10 cm above the body surface is approximately 1 mm in diameter. There was no significant difference in Tbf among male (28.6 ± 0.680 °C, n = 23), gravid female (30.4 ± 0.90 °C, n = 17), and FIGURE 1. (A) Adult Scincella lateralis from Conway, Horry non-gravid female (28.8 ± 0.67 °C, n = 24) skinks (F2,60 County, South Carolina, USA. (B) Representative image of S. = 1.50, P = 0.223), thus sexes were pooled in all lateralis habitat in research area. analyses of Tbf. I conducted surveys for skinks seasonal temperature and photoperiod. During spring throughout August, however, I did not find any adult S. and summer, lizards received morning sun (0700–1000) lateralis in this month. Consequently, I did not record but were otherwise shaded for the majority of the day. field body temperatures of skinks during this time. During fall and winter, lizards received direct sunlight in I obtained all body temperature measurements from their enclosures for approximately 5 h (0800–1300) per 0900–2000 in spring/summer and 0900–1800 in day. These periods of sun are likely reasonable autumn/winter. I measured field body temperatures 3–5 approximations of the seasonal amounts of direct days per week throughout the sampling period and sunlight that skinks would experience in their searches were conducted with equal frequency during environment. During late spring and summer, for morning (0900–1159), afternoon (1200–1459), late example, high environmental temperature largely limits afternoon (1500–1759), and evening (1800–2000). The activity of skinks to morning and evening hours (see only exception was that surveys for measurement of Tbf results section). Conversely, in winter, skinks have ended at 1800 during autumn/winter due to the shortened greater access to sunlight on the surface of the ground photoperiod and resultant cessation of skink activity. due to loss of leaves from deciduous trees. Although the interval over which I measured temperatures was unequal between seasons (9 h Thermoregulation: field and selected substrate fall/winter versus 11 h spring/summer), this approach temperatures.—I measured surface body temperatures better captured daily thermoregulatory patterns of skinks of adult male and female S. lateralis (n = 64) in the field than would have been possible by restricting seasonal within 1 min of capture (nearest 0.01 °C) using a measurements to the same time frame (0900–1800) handheld infrared (IR) thermometer (VWR, model during both summer and winter. To test whether number 36934-182, VWR International, Radnor, unequal sampling interval biased comparisons of monthly Tbfs, I analyzed mean monthly Tbf using a
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single-factor ANOVA, but with spring/summer Tbf data 0.67 °C, n = 24) skinks (F2,53 = 0.80, P=0.922), thus I from 1800–2000 removed from the analysis. Exclusion pooled sexes in all analyses of Tsel. I used the central of the 1800–2000 Tbf data did not change results of the 50% of selected substrate temperatures to calculate the initial analysis of Tbf as function of month (F6,55 = 1.20, set point temperature range (Tset). P = 0.34); in either case, Tbf did not vary significantly among months (see Results section) regardless of Thermoregulation: environmental temperatures.—I whether I made statistical contrasts using the unequal or measured environmental temperatures (Te) at the study equal time frames for temperature measurement. I site during the skink daily activity period (nearest 0.1 estimated skink activity based on the frequency of °C) from 0900–2000 May-September (August omitted) temperature measurements obtained during the daily and 0900–1800 October-December 2012 using activity period. Thermochron temperature data loggers (Model #, Maxim Integrated, San Jose, California). I sealed data loggers I measured selected substrate temperatures (Tsel, n = inside waterproof metal jackets (painted with brown 57) of adult male and female S. lateralis July-November “sandable” primer) and partially buried so that the (nearest 0.01 °C) in laboratory thermal gradients using a surface of the jacket of data loggers were flush with the thermocouple thermometer (Model 800024C, Sper surface of the ground. Scincella lateralis are almost Scientific, Scottsdale, Arizona, USA). I covered the exclusively ground dwelling lizards (Conant and Collins bottoms of the gradients with 5–10 mm of shredded 1998), therefore, substrate temperatures are likely coconut husk and housed the gradients in a room representative of temperatures that skinks encounter in maintained at a constant temperature of 23 °C. I their environment. Reflective/absorbance values have suspended heat lamps at graded heights along each not been determined for S. lateralis, consequently, the runway to produce a linear temperature gradient ranging brown sandable primer used to paint waterproof jackets from 24 to 45 °C. The gradients were surrounded with for data loggers may not match the actual foam insulation to minimize temperature fluctuations in reflectance/absorbance characteristics of this species. the gradient. I fasted lizards for 48 h before placing However, given the small size of S. lateralis and the them in the gradients to ensure that they were post- relatively long period of time over which daily absorptive (Robert and Thompson 2000). At 1600 on environmental temperature data were obtained (8 the day after fasting, I removed lizards from group months), I judged that the contribution of reflectance to enclosures and placed them into runways (one lizard per overall thermal profiles would be relatively minor (Shine runway) and allowed them to equilibrate overnight (Daut and Kearney 2001). The results of my study comparing and Andrews 1993). I turned on heat lamps at 0800 and data logger temperatures to models/carcass support this I measured selected substrate temperature of each lizard conclusion (see below). I placed two to three data approximately every 2 h beginning at 0900 until 2000. I loggers randomly within each of the following habitat turned off heat lamps after the final measurement was categories: forest clearing (no canopy cover), open forest made at 2000. I measured selected substrate (20–50% canopy cover), dense forest (> 60% canopy temperatures by placing the thermocouple probe on the cover). I determined habitat categories by sampling surface of the substrate at the midpoint of the lizard’s canopy cover at three locations within each habitat using body. Because of their small size, I deemed direct a spherical densiometer. measurement of cloacal temperatures impractical Environmental temperatures are herein considered because repeated measurements of Tsel would have likely operative temperatures (Bakken et al. 1985; Bakken and resulted in excessive stress to individuals. Substrate Angilletta 2014) based on the assumption that data temperatures at mid-body are a common and reliable loggers provide comparable estimates of operative method to estimate Tsel in small lizard species with high temperature that skinks experience in the field (Vitt and surface to volume ratios (Andrews 1994; Wu et al. Sartorious 1999; Robert et al. 2006; Vickers et al. 2011). 2009). To verify this assumption, I placed a S. lateralis To verify this assumption, I recorded environmental carcass (0.851 g) at five locations spanning the length of temperatures using ibutton data loggers sealed inside the thermal gradient and allowed it to equilibrate for 20 metal jackets (n = 2, described above), and thermocouple min at each location followed by measurement of thermometers inserted inside a copper S. lateralis model substrate and cloacal temperatures using the Sper and a S. lateralis carcass. The model consisted of a 20 × Scientific thermocouple probe. Substrate and cloacal 5 mm section of copper tubing painted with brown temperatures did not differ significantly (t = 0.14, df = 8, sandable primer and sealed on each end with aquarium P = 0.89). On average, the two sets of measurements cement. I inserted a copper constantan thermocouple differed by less than ± 0.2 °C. Preliminary analysis thermometer approximately 10 mm inside the center of indicated that there was no significant difference in Tsel the model. Care was taken to ensure that the among male (28.5 ± 0.32 °C, n = 23), gravid female thermocouple was not in contact with the sides of the (28.3 ± 0.69 °C n = 9), and non-gravid female (28.6 ± model. I measured carcass temperatures by inserting a
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Temperatures among ibutton data recorded and analyzed data using Sable System Software -1 loggers, model, and carcass did not differ significantly and I calculated mean V̇ O2 (ml O2 h ) from a minimum (F2,14 = 0.215, P = 0.81), and on average, sets of of 5 min of steady state oxygen consumption (Hare et al. temperature measurements among the three categories 2006). differed by less than 1 °C. The approach used to calculate Te admittedly does not provide a high Comparisons of rates of heating, cooling, and water resolution representation of the range of thermal loss.—I determined total evaporative water loss (ml H2O heterogeneity within habitats. The measurements g-1 h-1) at 28, 32, 36 °C in August 2012 by measuring the nonetheless quantify general thermal characteristics of change in lizard mass over time at each temperature. I the major habitats used by skinks during the year. fasted lizards (n = 17, 0.4–1.2 g) for 48 h, weighed them to the nearest 0.001 g, and placed them in mesh bags (50 Indices of thermoregulation and thermal quality of mm × 90mm) in a controlled constant temperature environment.—I measured the accuracy of incubator at 35% relative humidity for 4 h. If lizards thermoregulation (db) and thermal quality of habitat (de) urinated or defecated after initial weighing or while in following Hertz et al. (1993). Accuracy of mesh bags, I did not include the individuals in analyses. thermoregulation (db) was assessed as the mean of the Lizards were not otherwise restrained during the absolute value of deviations of Tbf from the mean set measurement period, and I collected all data between point temperature (Tset). I assessed the thermal quality 1200–1700. After the allotted time, I removed lizards (de) of the three habitats within the study area as the and re-weighed them. I calculated total evaporative mean of the absolute value of deviations of Te from Tset. water loss as the difference in initial lizard mass from If db < de, then lizards are selecting thermal final mass. I randomly assigned lizards to one of the microhabitats non-randomly. I assessed the three temperature treatments and I only used each effectiveness of thermoregulation as de - db following individual once in each temperature trial. Blouin-Demers and Weatherhead (2001). A value of de - I measured heating and cooling rates of male and db < 0 indicates that animals avoid thermally favorable female S. lateralis (n = 14, 0.7–1.5 g) in dry air (35% habitats. A value of de - db = 0 indicates perfect relative humidity) and under humid (90–98% relative thermoconformity, whereas de - db > 1 indicates humidity) conditions. I determined rates of heating and thermoregulation. To facilitate comparisons of cooling using a step change in temperature (15–33 °C) effectiveness of thermoregulation between seasons, I under each condition. To prevent lizards from escaping, grouped data from May-September as the spring/summer I placed skinks in open-ended aluminum chambers (100 season and October-December as the autumn/winter × 25 mm) with a small amount of cotton inserted into season. each end. To determine rates of heating and cooling under humid conditions, I sealed skinks contained within Effect of temperature and season on standard the aluminum cylinder inside a plastic aquarium (290 × metabolic rate.—I measured standard metabolic rates of 220 × 220 mm) to which I added a small volume of adult male and non-gravid female S. lateralis in July (n = water to elevate the relative humidity to 90–98%. I 21) 2012 and January (n = 21) 2013 as rates of oxygen monitored relative humidity using a SPER Scientific consumption (V̇ O2) at four discrete temperatures (24, 28, Mini Environmental Quality meter (model no. 850070; 32, 36 °C) using an Oxzilla II oxygen analyzer (Sable Sper Scientific, Scottsdale, Arizona, USA). I determined Systems, Las Vegas, Nevada, USA) and flow-through heating and cooling rates of skinks in dry air in similar respirometry. I acclimated lizards to seasonal fashion except that I placed skinks within an aluminum temperature conditions (described above) prior to cylinder and then sealed inside a dry plastic aquarium measurement of V̇ O2. I fasted lizards for 48 h prior to with a ventilated top to prevent moisture condensation. measurement of V̇ O2 to ensure a post-absorptive state Humidity in dry chambers ranged from 28–36%. Skinks (Robert and Thompson 2000; Iglesias et al. 2003). I were first equilibrated to a body temperature of 15 °C in allocated four to five lizards to each temperature a Percival programmable environmental chamber treatment, and I only used lizards once in each (Percival Scientific, Perry, Iowa, USA). I measured temperature treatment. All measurements were rates of heating and cooling under each moisture conducted during the evening between 2100–0100. I condition by transferring skinks equilibrated to 15 °C
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and individual skink as the repeated measure. I analyzed metabolic rate using a two-way ANCOVA with temperature and season as factors and body mass as the covariate. I analyzed evaporative water loss using a one- way ANCOVA with temperature as a factor and initial body mass as a covariate. Preliminary analysis indicated that males and females did not differ in Tsel, therefore data from both sexes were combined in all subsequent analyses. I analyzed rates of heating and cooling in dry versus humid air using a paired t-test. Before using ANCOVA, I tested the assumption of homogeneity of slopes and I tested the assumption of normality for ANOVAs and ANCOVAs using the Proc Univariate procedure in SAS (all P values > 0.05). For all ANCOVAs, I made post hoc pair-wise comparisons using a least significant difference test on least squared means. For all ANOVAs, I used a Tukey’s honestly significant difference test as the post hoc pair-wise comparison. I considered indices of thermoregulation, data on microhabitat temperatures, and assessment of skink activity (based on time of capture) as descriptions and were not compared statistically. I reported data as the mean ± SEM unless otherwise reported, and probability values ≤ 0.05 were considered significant.
FIGURE 2. Field and selected substrate temperatures of Scincella RESULTS lateralis in South Carolina. (A) Field body temperatures (Tbf) measured May 2012-December 2012. (B) Selected substrate temperatures (Tsel) measured in laboratory thermal gradients during Thermoregulation: field and selected substrate July-November, 2012. Dashed vertical lines are central 50% of body temperatures.—Overall field body temperatures (Tbf) of temperatures (Tset). S. laterialis ranged from 20.4–40.5 °C and selected immediately to a separate environmental chamber set at substrate temperatures in thermal gradients (Tsel) ranged 33 °C. Using a copper constantan thermocouple probe from 22.5–35.3 °C (Fig. 2a, b). Central 50% of Tbf inserted approximately 5 mm into the cloaca, I measured ranged from 26.8– 30.4 °C (mean 29.1 ± 0.42), whereas body temperature continuously during heating and thermogradient Tset was 27.1–29.7 (mean: 28.8 ± 0.22 cooling. I recorded body temperatures (nearest 0.01 °C ) °C). Central 50% of Tbf was greater during using a Sper Scientific temperature data logger (model November/December (26–31 °C) than in June/July no. 800024C) calibrated against a National Institute of (27.5–31 °C). Mean Tbf did not vary significantly over Standards and Technology (NIST)- certified the eight-month study period (Table 1). Overall Tbf did not vary significantly over the daily thermometer. Rates of heating (Ƭh) and cooling (Ƭc) were expressed as thermal time constants according to activity period (0900–2000, F3,60 = 0.14, P = 0.931, Fig. the methodology used by Smith (1976). 3), however, Tsel in thermal gradients was significantly higher in late afternoon (29.2 °C) compared to the Statistical analyses.—I conducted statistical analyses morning (27.6 °C), or evening (28.1 °C; F3,16 =5.19, P = using SAS statistical software package (SAS Institute, 0.002, Fig. 3). Skinks were active throughout the day Cary, North Carolina, USA). I analyze the effect of during springtime as evidenced by the distribution of Tbfs month on T using one-way analysis of variance recorded as a function of time of day, but activity was bf limited primarily during the morning and late afternoon (ANOVA) and the effect of time of day on Tsel using repeated measures ANOVA with time of day as a factor or early evening during summer. During autumn and
TABLE 1. Mean (mean ± SE) and sample size (n) of field body temperatures (Tbf) of Scincella lateralis in South Carolina, measured during May-December (August omitted), 2012, and results of One way ANOVA testing differences among months.
May June July Sept Oct Nov Dec Result
29.9 ± 0.8 (8) 29.9 ± 0.7 (20) 29.5 ± 0.3 (5) 28.3 ± 1.1 (5) 29.3 ± 1.3 (11) 27.3 ± 1.4 (9) 27.3 ± 2.1 (6) F6,57 = 0.96, P = 0.46
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FIGURE 3. Mean field (open circles) and selected substrate FIGURE 4. Field body temperatures of Scincella lateralis in South temperature (filled circles) of adult Scincella lateralis in South Carolina as a function of time of day and season. Filled diamonds: Carolina as a function of time of day. M: morning, A: afternoon, LA: spring; open circles: summer; filled rectangles: autumn; asterisk: late afternoon, E: evening. Error bars are ± one standard error. winter. ○ = Tb Field, ● = TSEL, * = outlier. Asterisks indicate significant difference in body temperature among time of day (P < 0.05). winter skink Tbfs were recorded primarily during the in forest clearing and open forests were similar, although morning and early afternoon suggesting skinks were open forests had the widest range in temperature of the preferentially active during this time (Fig. 4). three habitat classes (Fig. 5b). Winter temperatures in dense forest were generally cooler and least variable of Thermoregulation: seasonal changes.—Deviation of the habitat classes. Moreover, during winter there was Tbf from Tset was lower during spring /summer (db = no overlap between central 50% of any of the three 0.93) compared to autumn/winter (db = 2.4, Table 2). habitat classes and lizard Tset. Likewise, deviation of Te from Tset was also lower in spring/summer (de = 3) compared to autumn/winter (de = Effect of temperature and season on standard 11.4). In contrast, thermoregulatory effectiveness was metabolic rate.—Temperature had a significant effect on approximately four times higher during autumn/ winter rate of oxygen consumption in S. lateralis (F3,33 = 9.34, (de - db = 9) compared to spring/summer (de - db = 2.1). P < 0.001) with metabolic rate at 24 °C significantly These values indicate that while skinks thermoregulated lower than at 28, 32, and 36 °C (Fig. 6). during both seasons, they deviated less from Correspondingly, metabolic rate during both summer thermoconformity during spring/summer whereas they and winter was most temperature sensitive between 24– deviated greatly from thermoconformity (i.e., greater 28 °C (Q10 = 5.8) and relatively temperature insensitive effectiveness) during autumn/winter. between 28–33 °C (Q10 = 1.1). Overall Q10 was 2.4 over During spring and summer, forest clearings were the entire temperature range. Season had a significant warmer and had a wider temperature range compared to effect on metabolic rate (F1,33 = 6.0, P = 0.022) with open forest and dense forest habitats (Fig. 5a). summer metabolic rates approximately twice as high at Temperatures in closed forest were coolest and least 28 and 36 °C during spring/summer than those in the variable of the three habitat classes. Although all three autumn/winter (Fig. 6). habitats showed some overlap with the preferred range of lizard Tbf, temperatures in open forest had the greatest Comparisons of rates of heating, cooling, and water overlap with lizard preferred Tbf (central 50% open loss.—Statistical contrast of the ratio of thermal time forest: 26.5–32 °C vs. lizard Tset: 27.5–31 °C). In constants for heating and cooling (Ƭh/Ƭc) indicates that S. contrast, during winter, the central 50% of temperatures
TABLE 2. Mean seasonal field body temperature (Tbf), seasonal environmental temperatures (Te), accuracy of thermoregulation (db), thermal quality of habitat (de), and thermoregulatory effectiveness (de - db) for Scincella lateralis in South Carolina. Values are means ± SE and sample sizes (n) for seasonal field body temperature. Te and de data are grand means from hourly substrate temperature measurements collected during the daily activity period from May-September (0900–2000) and October-December (0900–1800), 2012.
Season Tbf Te db de de - db
Spring/Summer 29.6 ± 0.42 (38) 30.0 ± 1.8 0.93 ± 0.32 3.0 ± 0.93 2.07
Autumn/Winter 27.8 ± 0.84 (26) 15 ± 0.84 2.4 ± 0.38 11.4 ± 0.50 9.0
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FIGURE 6. Mean oxygen consumption of adult Scincella lateralis at 24, 28, 32, and 36 °C measured in summer (filled circles) and winter (open circles). Error bars are ± one standard error. Asterisks indicate temperatures at which rate of oxygen consumption differs between summer and winter (P < 0.05). ● = MR Summer, ○ = MR Winter.
FIGURE 5. Set point temperature (Tset, shaded vertical bar) and range (dashed vertical lines) of field body temperatures for Scincella lateralis in South Carolina and operative environmental temperatures (horizontal bars) during summer (A) and Winter (B). Horizontal bars are central 50% of operative environmental temperatures in clearing (open bar), open forest (light shaded) and dense forest (dark shaded) environments. Solid horizontal lines are the range in operative temperature recorded in each environment.
lateralis takes longer to heat than to cool in dry, FIGURE 7. Mean total water loss of Scincella lateralis at 28, 32, compared to humid air (t = 3.13, df = 6, P = 0.023; Table and 36 °C and 35% relative humidity. Error bars are ± one standard error. Different letters above symbols indicate significant 3). In dry air, thermal time constants for heating were difference in evaporative water loss among temperature treatments approximately 1.4 times longer than that of cooling. In (P < 0.05). contrast, thermal time constants for heating and cooling were approximately equal when lizards were maintained at 90–98% relative humidity. Carolina maintains Tbs between approximately 26 and 31 Temperature had a significant effect on total water °C throughout the year. These values are similar to loss (F2,14 = 24.4, P < 0.001, Fig. 7). Total water loss those reported in populations of S. lateralis in Texas was higher at 36 than at 32 and 28 °C (Tukey’s HSD, P (25–30 °C; Hudson and Bertram 1966) and Oklahoma < 0.05) but did not differ between the 28 °C vs. 32 °C (23–34 °C; Smith 1997). The Tb of S. lateralis is thus treatments. Water loss was approximately three times several degrees lower than that of the majority of North higher in the 36 °C compared to the 28 °C treatment. American skink species, which typically maintain relatively warm average Tbs of approximately 31–33 °C DISCUSSION (Fitch 1954; Brattstrom 1965; Pentecost 1974). The relatively low preferred Tb of S. lateralis may be one Thermal biology.—Scincella lateralis in South reason for the marked variation in daily activity patterns
TABLE 3. Mean ± SE and sample size (n) of thermal time constants (minutes) for heating (Ƭh), and cooling (Ƭc) of Scincella lateralis in dry (relative humidity 24–35%) and humid air (relative humidity 90–98%). Temperature step 15–33 °C. Both values of τh/ τc were significantly different (P < 0.05) between means (paired t-tests). Dry air Humid air Lizard mass τh τc τh/ τc Lizard mass (g) τh τc τh/ τc (g) 0.911 ± 0.085 5.61 ± 0.75 4.04 ± 0.37 1.38 ± 0.12 0.944 ± 0.112 3.58 ± 0.274 3.92 ± 0.367 0.93 ± 0.065 (7) (7) (7) (7) (7) (7) (7) (7)
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Herpetological Conservation and Biology across seasons. During spring, for example, skinks are allowing body temperature to fluctuate passively with observed throughout most of the day. As air environmental temperature (i.e., thermoconformity). temperatures increase in June, overall activity of S. Indeed, this pattern appears to be true for several forest- lateralis is primarily limited to morning and evening dwelling species (Alcala and Brown 1966; Rummery et hours suggesting that high temperatures during late al. 1995; Huey et al. 2009). In contrast, results of this spring and summer may preclude activity on the surface study indicate that S. lateralis is an effective of the ground during the afternoon (Smith 1997). thermoregulator. First, S. lateralis selects a relatively Relatively cool micro-habitats in densely forested narrow range of body temperatures between habitats, however, may allow skinks to remain active for approximately 26–31 °C both in the field and in longer periods in summer. During autumn and winter, laboratory thermal gradients. Second, skinks are able to skinks are active on sunny days primarily in the morning maintain these preferred temperatures in the face of daily and early afternoon. Small size and relatively low and seasonal variation in thermal environment. Finally, preferred Tb are characteristics often associated with indices measuring precision of thermoregulation of S. lizard species with year round activity patterns (Huey lateralis in relation to quality of the thermal environment and Pianka 1977). The small size and relatively low Tb indicate that skinks select temperatures non-randomly of S. lateralis is therefore likely advantageous with respect to that available in the environment. particularly under cool conditions by allowing rapid heat The quality of thermal environment in the study area exchange with the environment (Fraser and Grigg 1984). varied greatly between summer and winter, yet skinks During winter, for example, rapid heating allows skinks were able to thermoregulate effectively during both to warm quickly and remain active even on relatively seasons. Thermoregulatory effectiveness (db - de) ranged cool days. Small body size, high surface to volume ratio from approximately 2.1 in summer to 9.0 in winter and relatively cool preferred Tb are thus likely traits indicating that skinks invested more in thermoregulation which permit individuals of S. lateralis to remain active during winter than in summer. For S. lateralis, the during winter in South Carolina. physiological disadvantage of less effective Despite maintaining relatively consistent Tbs while thermoregulation is likely to be relatively low in spring active, there was a trend of increasing Tbf beginning in and summer since there are a variety of microhabitats the morning and peaking in late afternoon. Similarly, in available to skinks where Te corresponds closely to Tset the thermal gradient, skinks selected significantly higher (de = 3).. For example, the central 50% of temperatures temperatures during late afternoon (29.2 °C) compared in the three habitat classes (forest clearing, open forest, to morning (27.6 °C) and evening (28.2 °C) paralleling and dense forest) had considerable overlap with Tset. the trend observed in the field. These observations During late spring and summer, skinks largely ceased suggest that skinks in the field tend toward actively activity during the afternoon (pers. observ.), and thus selecting higher Tbs in late afternoon as opposed to avoided times when high air temperatures greatly passively letting Tb vary with the environment. exceeded Tset. Conversely, during late autumn and Selection of higher Tb in late afternoon could represent a winter, the thermal environment was far more circadian-mediated shift in thermoregulatory behavior challenging (de = 11.4), however, skinks nevertheless which reflects a period of increasing activity late in the thermoregulated much more effectively than in afternoon when environmental temperatures rise or fall spring/summer. During autumn/winter, there was no within their preferred range (Ellis et al. 2006). Slight overlap in central 50% of environmental temperatures in variation in Tb during the daily activity period is not the three habitats and skink Tset. Despite this constraint, uncommon among thermoregulating reptiles (Clark and however, skinks were able to maintain Tbs within the Kroll 1974; Huey and Pianka 1977). In Australian preferred range (26–31 °C) and attain approximately the Sleepy Lizards (Tiliqua rugosa), for example, Tb peaks same maximum Tb in both winter and summer. During late in the afternoon despite overall thermoregulatory winter, the cost of thermoconformity would likely be behaviors that maintain Tb between 33–35 °C (Firth and substantial since non-thermoregulating skinks would Belan 1998). have low Tb and correspondingly poor physiological performance (Blouin-Demers and Nadeau 2005; Herczeg Evaluation of thermoregulatory behavior.—The et al. 2006). The results of the present study are hypothesis that S. lateralis is a thermoconformer in the consistent with previous work on Black Rat Snakes field was not supported. Costs of thermoregulation for (Pantherophis obsoleta) where individuals from a cool small reptiles are predicted to be higher in forested high latitude, and presumably high-cost thermal environments because of the limited availability of environment, have comparable thermoregulatory sunlight patches compared to open locations (Huey and effectiveness (de - db ≈ 3.1; Blouin-Demers and Slatkin 1976; Hertz et al. 1993). Accordingly, forest- Weatherhead 2001) to spring/summer-active S. lateralis dwelling lizards could mitigate increased cost of (de - db ≈ 2.1). thermoregulation in shady forested environments by
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Lizards employ a combination of behavioral strategies metabolic rates at 24, 28, 33, 36 °C were approximately and physiological mechanisms to thermoregulate ( Huey double that of lizards measured in winter. The lower and Pianka 1977). Unlike relatively large lizards (i.e. > overall metabolic rates in winter likely reflect reduced 5 g) with greater thermal inertia, shuttling between sun energetic demands associated with absence of and shade as a primary means of thermoregulation may reproduction, and reduced overall activity time (Beyer be problematic for S. lateralis because Tb is likely to and Spotila 1994). Seasonal hormone profiles have not fluctuate widely between these two environments. been measured for S. lateralis, however, it is also likely Similarly, it seems unlikely that S. lateralis could use that seasonal changes in hormone concentrations such as physiological mechanisms to modify heat exchange such thyroxine or corticosterone may contribute to the as alteration of cutaneous circulation to either reduce or increased metabolic rate during spring and summer and enhance heat loss (Fraser and Grigg 1984). In light of reduced metabolic rate during winter (John-Alder 1984, these constraints, S. lateralis appears to thermoregulate 1990). primarily by using different microhabitats (e.g. forest clearings, open forest, dense forest) and by regulating Heating, cooling, and water loss.—The hypothesis time of activity on a daily and seasonal basis. that heating rate is reduced by evaporative cooling was Differential use of various elements of structural supported. When maintained in dry air, individuals of S. - microhabitat habitat is one strategy used by lizards to lateralis heat more slowly (mean Τh = 5.6 ± 0.75 °C min 1 -1 maintain Tbs within preferred ranges (Grant and Dunham ) than they cool (mean Ƭc = 4.04 ± 0.37 °C min ). This 1988; Adolph 1990). The phrynosomatid lizard effect was eliminated when skinks were maintained Sceloporus occidentalis, for example, selects more under conditions of high relative humidity (98% RH: Ƭh -1 arboreal perches during summer in hot desert = 3.58 ± 0.12 °C min vs. 98% RH: Ƭc = 3.92 ± 0.37 °C environments where thermal microenvironments are min-1). These observations indicate that evaporative cooler than those close to the surface of the ground cooling is likely responsible for the slower rate of (Adolph 1990). Because S. lateralis is almost entirely heating in dry compared to humid air. Similarly, at a terrestrial and rarely climbs (Conant and Collins 1998), relative humidity of 47%, the Australian skink, it is likely that skinks can also thermoregulate by using Lampropholis delicata (approx 0.9 g) also heated more -1 different structural elements of the ground substrate (e.g. slowly (Ƭh = 4.23 °C min ) than they cooled (Ƭc = 3.24 leaves, grasses, debris) within their environment. The °C min-1; Fraser and Grigg 1984). In contrast, thermal extent to which S. lateralis uses subsurface heating constants are approximately twice as high for a environments is not known, but these environments typical medium sized skink Eulamprus tympanum (12.8 could be an important thermal resource, particularly g, Ƭh = 11.0; Fraser and Grigg 1984). While the reduced during summer when ground temperatures may preclude heating rate observed in small lizards as a result of activity on the surface for at least part of the day. evaporative cooling is likely attributable to their high surface to volume ratio rather than to direct Influence of temperature and season on metabolic physiological control, evaporative cooling may rate.—The observed increase in V̇ O2 as a function of Tb nonetheless help buffer lizards from rapid over heating and overall Q10 of approximately 2 is typical of many when active on the surface of the ground. A reduced diurnal lizard species (Bennett 1982; Pough and heating rate would be advantageous for small lizards like Andrews 1985). The rate of oxygen consumption in S. S. lateralis, which are likely to encounter hot sunny open lateralis, however, does not vary significantly from 28 to environments when foraging or traversing across habitat 36 °C, suggesting that metabolic rate is independent of patches. temperature over the range of temperatures commonly Evaporative water loss is typically high in small achieved in the field. Moreover, during both summer lizards (Heatwole and Veron 1977) suggesting that and winter, metabolic rate was temperature insensitive access to moist microenvironments may be important for between 28–33 °C with Q10 values of approximately one small lizard species including S. lateralis. At 36 °C, -1 -1 recorded over this temperature range. This range in water loss was approximately 13 mg H2O g h temperature also corresponds closely to the central 50% corresponding to loss of approximately 28% of body of temperatures skinks adopted in the field and mass per day. Direct comparisons of rates of laboratory. The marked increase in V̇ O2 (and hence Q10 evaporative water loss with other lizard species is values) at 24 and at 36 °C (though non-significant) may difficult due to variation in methodology used by indicate threshold temperatures at which temperature- different researchers. Nonetheless, evaporative water dependent shifts in metabolic physiology occur. The loss of S. lateralis (mean mass: 0.79 g) measured at 28 hypothesis that S. lateralis exhibits a compensatory °C and 35% relative humidity in this study are increase in winter metabolic rate compared to that of comparable to that of the gecko Sphaerodactylus summer, as predicted for some winter-active lizard cinereus (mean mass 0.6 g) measured at 30 °C and 0% species (Tsuji 1988) was rejected. Overall, summer relative humidity. Individuals of S. lateralis lost
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-1 -1 approximately 3.5 mg H2O g h corresponding to National Wildlife Refuge. Work was conducted under 13.5% of body mass day -1 compared to a loss of 16.8 % Coastal Carolina Animal Ethics Approval 2012.09. body mass day-1 in S. cinereus (Dunson and Branham 1981). Collectively, these observations suggest that LITERATURE CITED environmental moisture as well as temperature may constrain distribution and activity pattern of S. lateralis. Ackerman, E.A. 1941. The Köppen classification of climates in North America. Geographical Review Implications for distributional patterns and 31:105–111. thermoregulation.—Physiological requirements of S. Adolph, S.C. 1990. Influence of behavioral lateralis likely influence its habitat use and distributional thermoregulation on microhabitat use by two pattern across the landscape. A patchy matrix of open Sceloporus lizards. Ecology 71:315–327. and shaded environments allows skinks to maintain body Adolph, S.C., and W.P. Porter. 1993. Temperature, temperature and water balance within preferred ranges activity, and lizard life histories. The American despite relatively wide variation in seasonal temperature Naturalist 142:273–295. and presumably, moisture conditions. In addition, food Alcala, A.C., and W.C. Brown. 1966. Thermal relations availability as well as competition and predation (e.g., of two tropical lizards on Negros Island, Philippine Huey and Slatkin 1976) likely interact with temperature Islands. Copeia 1966:593–594. and moisture to influence habitat selection (Huey 1982). Aleksiuk, M. 1971. Temperature-dependent shifts in the The results of the study also underscore the metabolism of a cool temperate reptile, Thamnophis importance of considering potential costs of sirtalis parietalis. Comparative Biochemistry and thermoconformity versus advantages of Physiology 39A:495–503. thermoregulation particularly for small species Andrews, R.M. 1994. Activity and thermal biology of inhabiting environments that undergo relatively extreme the Sand-swimming Skink Neoseps reynoldsi: diel and temperature fluctuations. For S. lateralis, seasonal patterns. Copeia 1994:91–99. thermoconformity would risk individuals experiencing Andrews, R.M., and F.H. Pough. 1985. Metabolism of dangerously high Tb in summer whereas passively squamate reptiles: allometric and ecological maintaining low Tb in winter would limit functions such relationships. Physiological Zoology 58:214–231. as locomotor performance, assimilation, as well as Angilletta, M.J. 2001. Variation in metabolic rate severely constrain activity time (Blouin-Demers and between populations of a geographically widespread Nadeau 2005; Vickers et al. 2011). In contrast, lizard. Physiological and Biochemical Zoology 74:11– thermoconformity would appear to be most 21. advantageous for species inhabiting tropical forests Bakken, G.S., W.R. Santee, and D.J. Erskine. 1985. where temperatures under the canopy are relatively mild Operative and standard operative temperature: tools and invariant year round (Inger 1959; Alcala and Brown for thermal energetics studies. Integrative and 1966). In these environments, thermoregulatory Comparative Biology 25:933–943. opportunities are limited and temperature extremes are Bakken, G.S., and M.J. Angilletta, Jr. 2014. How to rare. Accordingly, under these conditions, costs of avoid errors when quantifying thermal environments. thermoconformity are likely to be relatively low. The Functional Ecology 28:98–107 thermoregulatory behavior observed in S. lateralis Basundhara, C., S. Bhupathy, and B.K. Acharya. 2010. support the model that precision of temperature Distribution pattern of reptiles along an eastern regulation is a malleable trait that varies according to Himalayan elevation gradient, India. Acta Oecologica seasonal changes in costs and benefits in the 36:16–22. environment. 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SCOTT L. PARKER (right, with a Malaclemmys terrapin) is an Assistant Professor of Biology at Coastal Carolina University, Conway, South Carolina, USA. He began working in lizard physiological ecology during the mid 1990s while an undergraduate at the University of California Santa Barbara. He completed a Master’s degree at California State University, San Bernardino where he studied thermal and reproductive biology of Sceloporus lizards in desert and montane environments. In 2006, he completed his Ph.D. at Virginia Polytechnic Institute and State University on physiological and ecological constraints on the evolution of viviparity in sceloporine lizards. After completing his Ph.D., he began a post-doctoral fellowship at the University of Sydney studying the role of angiogenesis in the evolution of viviparity of Australian skinks. He accepted an academic position in the Department of Biology at Coastal Carolina University in 2010 where he continues to work on physiological ecology and reproductive physiology of reptiles. (Photographed by Beckett Hills).
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