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Natural ultraviolet-B exposure of the Texas horned lizard (Phrynosoma cornutum) at a North Texas wildlife refuge.

Active basking in the sun by many lizards is a critical mechanism for thermoregulation (Cowles and Bogert, 1944; Huey, 1982). Some lizard species quickly attain preferred body temperatures higher than ambient by basking early in the day. They might maintain this preferred temperature throughout their activity during the rest of the day either within narrow limits or with less precision. Other lizard species are thermal conformers, and bask little or not at all. When active, they maintain a variable body temperature that conforms to the range of their environment (Huey, 1982). Along this spectrum of thermoregulatory behavior, the Texas horned lizard (Phrynosoma cornutum: Phrynosomatidae) is a thermoregulator that maintains its body temperature within a zone ranging from approximately 35-39[degrees]C (Heath, 1965; Prieto and Whitford, 1971). Thermoregulation and adaptation to environmental temperature changes are primary factors responsible for daily and seasonal cycles of activity and basking in this and other horned lizard species (Burrow et al., 2001; Sherbrooke, 2003).

The sun is not only a source of heat but also ultraviolet (UV) radiation. Exposure to UV radiation from sunlight can have both negative and positive effects on the health and well-being of terrestrial vertebrates. The most detrimental effects of excess UV radiation are tissue and DNA damage that can lead to sterilization and cancer (Hays et al., 1995; Blaustein et al., 1998; Miller et al., 2002; Chang and Zheng, 2003). Inappropriately high exposure doses of short-wave UV radiation causes skin and eye damage and reduced reproductive success in captive reptiles (Ferguson et al., 2002; Gardiner et al., 2009).

The most studied positive effect of ultraviolet-B (UVB; 290-315 nm) is bone health via endogenous vitamin [D.sub.3] production. In many vertebrates, the exposure of skin to UVB causes photolysis of provitamin [D.sub.3] (7-dehydrocholesterol) to previtamin [D.sub.3] followed by thermal isomerization to vitamin [D.sub.3], which then enters the circulatory system. Subsequent hydroxylation in the liver and kidneys produces the biologically active form of vitamin [D.sub.3], 1,25-dihydroxyvitamin [D.sub.3], a hormone critical to calcium and phosphorus metabolism (Holick, 1996, 1999, 2007). Vitamin [D.sub.3] can also enter the circulatory system by ingestion of food containing vitamin [D.sub.3]. Deficiency of vitamin [D.sub.3] in reptiles leads to nutritional metabolic bone disease, reproductive failure, and death (Ferguson et al., 1996; Mader, 2006).

Given the costs and benefits of UV exposure, vertebrates should adaptively regulate their exposure to optimal levels. A protective adaptation for many lizards that bask extensively is a dark subdermal or peritoneal lining that absorbs UV radiation and protects deeper tissues from UV damage (Porter, 1967). A positive adaptation would be the ability to detect UV and voluntarily regulate exposure when there is a need for vitamin [D.sub.3] or, alternatively, when potential UV damage is sensed. One lizard species, the panther chameleon (Furcifer pardalis), can do the former (Ferguson et al., 2003; Karsten et al., 2009). The Cuban brown anole (Anolis sagrei) also appears to possess this ability (Ferguson et al., 2013). To our knowledge the ability for behavioral avoidance of high, potentially detrimental, UV exposure has not yet been rigorously documented in reptiles but has been in frogs and fish (Han et al., 2007; Holtby and Bothwell, 2008).

Researchers have only recently studied UV light exposure of reptiles in nature (Carman et al., 2000; Ferguson et al., 2005; Ferguson et al., 2010). Monitoring of UV index (UVI, a unitless scale of UVB irradiance) of 15 lizard and snake species in the field during their daily and seasonal peak activity has revealed a range of average voluntary UVB exposures. Ferguson et al. (2010) have divided these exposures into four categories or UVB zones. UVB zone 1 includes crepuscular or shade-dwelling species with a median daytime UVI of 0.35; zone 2 includes daytime partial sun or occasional basking species, with a median UVI of 0.9; zone 3 includes full or partial sun basking species, with a median UVI of 1.8; zone 4 includes midday basking species, with a median UVI of 3.1. Lizards inhabiting a higher UVB zone have skins less photosensitive to UVB regarding vitamin D synthesis than those inhabiting a lower UVB zone (Ferguson et al., 2005). This might also reflect a lower sensitivity to UVB damage.

The Texas horned lizard occurs in the arid and semiarid low- and middle-elevation habitats from southeastern Arizona south through northern Mexico and north to central Kansas (Sherbrooke, 2003; Stebbins, 2003; Hodges, 2009). However, populations are declining across its range and the species is listed as threatened in Texas. It is insectivorous, mostly myrmecophagous, subsisting to a great extent on harvester ants (Pogonomyrmex).

The objective of the study was to obtain preliminary baseline information on daily patterns of voluntary UVB exposure and UVB dose of the Texas horned lizard in the context of its thermal environment during sunny warm days at a North Central Texas locality where the species is abundant and protected. Based on its high thermal tolerance (Heath, 1965; Prieto and Whitford, 1971) and the open nature of its desert and grassland habitat, we hypothesized that it is a UVB zone 4 (highest exposure category) species.

MATERIALS AND METHODS--We conducted observational studies on the Texas horned lizard at Matador Wildlife Management Area (Matador WMA, Cottle Co., Texas; 34[degrees]7'N, 100[degrees]19.8'W; elevation 570 m) during May and June from 2008-2012. The management area includes 11,406 ha of rolling plains habitat, including managed grassland and savannah. The terrain consists of bluffs and bottom land of the Middle Pease River. A network of unpaved roads is maintained and allows access to the habitat, which is managed from an ecosystem standpoint to sustain native wildlife populations. Texas horned lizards are common throughout the refuge and lizards use the roads for morning and evening activity.

We utilized two survey methods: spot-check surveys to measure UVB irradiance at the locations of individual lizards encountered in the field, and focal-retrace observations to measure UVB dose of single individuals observed over periods of time. Spot-check surveys included driving a vehicle on Matador WMA roads through the refuge at slow speeds ([less than or equal to] 8 km/h) from approximately 0800-1300 h or from 1600-2100 h on days judged to be sufficiently warm for Texas horned lizard activity (air temperature [[T.sub.a]] > 20[degrees]C and little cloud cover). We usually terminated morning surveys after 1300 h when we had seen no lizards from 1200-1300 h. If we spotted a lizard during this time, we continued searching for one additional hour. Each survey covered approximately 33 km of unpaved Matador WMA roads with no portion of any of the roads resurveyed during the same survey. For the UVB study reported here, we conducted 23 spot-check surveys (12 morning, 11 afternoon-early evening) from 2008-2012. As recommended by Hurlbert (1984) for studies designed to answer questions such as "How does UVB exposure intensity and temperature vary throughout the day?", our replicate sample units (numbers) for each observational category (hour of the day) were single readings taken at the precise location of an individual lizard or means of readings of multiple Texas horned lizards found for an hour of a particular survey. As a hypothetical example, one particular morning survey might include three sightings during the 0900 h, two sightings during the 1000 h, and one during the 1100 h. This would provide one datum (mean) for the 0900 h, one (mean) for the 1000 h, and one (single value) for the 1100 h. Another survey on another day might include four sightings for the 1100 h but none for either the 0900 h or the 1000 h. This would provide only one datum for the 1100 h. We did not include data from three individual sightings that represented the only data for that particular hour for all surveys in subsequent analyses. We also used these sample units to analyze variation among the categories and relationships among variables.

During six of the morning spot-check surveys conducted in 2011 and 2012, we took two readings for each individual, one initial and one after a period of 5-20 min of observation. We chose the number of minutes between the first and second readings for each individual using a table of random numbers between 5 and 20. The goal was to analyze the effect of delayed processing of lizards discovered on the road on UVB exposure intensity and to correct "road bias" (see Discussion).

In order to avoid interfering with additional ongoing research at Matador WMA, we did not mark Texas horned lizards during our study. Although we do not know the exact number of lizards recaptured during the UVB study, lizards at most of the 71 sighting locations were likely to be different individuals. During the same years an independent mark-and-recapture study was conducted by author DCR surveying the same roads by vehicle. All Texas horned lizards encountered by him and his associates were permanently marked by toe-clipping or pit-tagging. During 63 surveys of the mark-and-recapture study only 31 of 154 horned lizards encountered were recaptured individuals (20.13%). Thus, the probability of recapturing a given lizard at the refuge during the years of the two studies was about 0.2. Therefore, we considered that any bias of error variance due to measuring a few individuals twice (pseudoreplication; Hurlbert, 1984) would be small. Accordingly, the sample unit for the analysis of initial vs. delayed readings of individuals using a paired t-test was each individual lizard encountered during the six surveys of Matador WMA conducted in 2011 and 2012.

When the goal was to take only a single reading for each Texas horned lizard encountered, we stopped the vehicle upon detection of the lizard and noted the initial location of the lizard. We captured the lizard immediately by hand or by noose, and measured body temperature ([T.sub.b]) using a quick-reading cloacal thermometer (Miller and Weber, Inc., Ridgewood, New York). We recorded snout-vent length (SVL) in millimeters and body mass in grams with a plastic ruler and Pesola spring scale (Forestry Suppliers Inc. Jackson, Mississippi), respectively. We determined sex for adults by presence or absence of hemi-penal bulges at the base of the tail. We released each lizard in less than 5 min at the location where it was first seen. After release, we measured UVB irradiance, [T.sub.a], and substrate temperature ([T.sub.s]) at the location (see description of techniques below).

When we were to monitor a lizard twice to test for the effect of delayed processing, the lizard was watched by one investigator while the UVB and environmental temperatures were measured by a second investigator. The second investigator took readings at a location close to the lizard and with similar sun exposure but sufficiently far away to avoid causing the lizard to change location (approximately 3 m). After the predetermined delay, we captured and processed the lizard at the second location as described above.

We employed the focal-retrace method on single individuals followed for most of a day. The goal of a focal-retrace session was to estimate the UVB dose (irradiance x time) of an individual Texas horned lizard for each hour of the day throughout most of an entire day. The focal involved locating a single lizard on a day designated as the "focal day." We located a lizard as close to 0900 h as possible and followed it, if possible, until after 1800 h. To enable close future monitoring of UVB exposure, we recorded details of location and time every few minutes ([approximately equal to] 10 min), and also recorded whenever the lizard moved, or whenever its sun exposure changed. After the lizard left a location, we marked that location by inserting a numbered survey flag into the substrate at the site. We took care to neither disturb the lizard nor cause it to relocate when marking its previous locations. Texas horned lizards at the refuge have a relatively short approach distance before showing a predatory flight reaction to a human, e.g., alertness, orientation away from the observer, and flight behavior. We generally remained >3 m from the lizard and moved slowly during observations. Throughout the observation period we recorded general notes on behavior, such as feeding and social interaction, and on environmental changes, such as temporary cloud cover or changes in air movement. We followed three adult Texas horned lizards during most of their activity. We followed each on a separate focal day, one male and one female in 2010 and one male in 2012. At the end of the focal day we captured, weighed, and measured each lizard. We took its body temperature and released it at the site of capture within 5 min.

We could not directly monitor continuous UVB irradiance of a lizard at the lizard's location on a focal day without disturbing the lizard and altering its activity or habitat use pattern. Therefore, we assessed UVB irradiance in the field for each of the three lizards as follows: On the day following the focal day, designated "retrace day," we monitored UVB irradiance, [T.sub.s], and [T.sub.a] at lizard locations marked on the previous day at the same local time as they were occupied on the focal day. For each lizard, we also monitored a single control site, located where it would receive full sun exposure throughout the day, at the beginning of each hour on the retrace day as well as on the focal day to assess the climatic similarity of the focal and retrace days. For all three lizards, values for UVB irradiance at the control sites were similar on the 2 days (mean UVI difference < 1; Table 1), so no adjustments of the estimates for the focal-day UVI were considered necessary. However, temperature values on the retrace day at the control site for the female in 2010 were warmer (>3[degrees]C), so for each hour the estimate for the mean temperature for that hour of her focal day was the retrace-day value of the lizard site reduced by the mean difference in air temperature at the control site for that hour of the 2 days. For the male monitored in 2012 the UVB irradiance was also similar for both the focal and retrace days (UVI difference < 1; Table 1), so no adjustment was needed. However, the temperatures were considerably cooler (<6[degrees]C) on the retrace day, so air temperature estimates for his locations on the focal day were adjusted in similar fashion, increasing the values for lizard locations obtained on the retrace day by the hourly mean difference between the temperatures of control site for the 2 days.

We measured UVB irradiance at lizard locations and control sites using two handheld broad-band UVB meters, the Solarmeter 6.2 (displays [micro]W/[cm.sup.2]) and Solarmeter 6.5 (displays UVI) (Solartech, Inc. Harrison Township, Michigan). These are sensitive to irradiance within the UV range (280-400 nm) and respond most strongly to wavelengths in the UVB range below 320 nm. We took readings by placing the base of the unit on the substrate and orienting the flat sensor disk on the top of the unit ([approximately equals to] 10.8 cm from the base) toward the sun or to the adjacent open sky. If the line to the sun was obscured by features of the habitat at the lizard location on the retrace day, we did not relocate the meter but adjusted the orientation of the meter to generate the maximum reading at each site that the lizard might have experienced. When measuring, we avoided casting a shadow from our bodies upon the meter.

We obtained [T.sub.s] using a digital infrared thermometer (Raytek PM-300, Santa Cruz, California). We held the unit within 5 cm of the substrate and activated it with the laser perpendicular to the substrate. We obtained other temperatures ([T.sub.a] and [T.sub.b]) using a cloacal thermometer. We obtained [T.sub.b] by inserting the bulb of the thermometer into the cloaca of the lizard. We obtained [T.sub.a] by placing the bulb of the thermometer approximately 5 cm above the substrate location. If the location was sun-exposed, we shaded the bulb from direct sunlight with a shadow provided by obstructing direct sunlight approximately 10 cm above the thermometer.

At control sites on focal days and retrace days, we estimated percentage of cloud cover each hour using a spherical crown densitometer (Model A, Forestry Suppliers Inc. Jackson, Mississippi).

We analyzed data on UVI and temperatures from spot-checks as survey means or individual values as described above. To generate UVB dose (irradiance x time) from focal or retrace data, we averaged the UVB readings of the Solarmeter 6.2 from two successive observations of an individual obtained on retrace day and multiplied the average by the elapsed time interval in seconds between the readings. Then we summed the interval dose calculations over a longer observation period to obtain dose value ([micro]J/[cm.sup.2]). To facilitate the presentation, we converted values to J/ [cm.sup.2] ([micro]J/[cm.sup.2] / 1,000,000). We totaled hourly doses over 3-h time periods and for the full observation period. When violations of assumptions of parametric analyses occurred, we analyzed data with appropriate nonparametric tests. We reported values as means [+ or -] 1 SE or SD as indicated. All data were analyzed and processed using Microsoft Excel 2007 or 2013, and SigmaPlot 11.0 (Jandel Corp.).

RESULTS--Daily Patterns of the Thermal Environment, Body Temperature, and Exposure to UVB during Road Activity--On warm sunny days Texas horned lizards surveyed during the 5 years were exposed to UVB irradiance throughout the day when active between 0900-1900 h (Fig. 1a). When lizards were on roads, [T.sub.b] exceeded [T.sub.a] (Fig. 1b). In the morning (0900-1300 h), both [T.sub.b] and [T.sub.s] were significantly > [T.sub.a] ([T.sub.b] = 37.1 [+ or -] 0.59 SE, n = 23; [T.sub.s] = 35.6 [+ or -] 1.13 SE, n = 25; [T.sub.a] = 30.6 [+ or -] 0.52 SE, n = 25; Kruskal-Wallace ANOVA of ranks, H = 27.6, P < 0.001; Dunn's method, P < 0.05). In the late afternoon and early evening (1700-2100 h), [T.sub.b] was significantly > [T.sub.a] ([T.sub.b] = 34.4 [+ or -] 0.80 SE, n =19; [T.sub.a] = 30.3 [+ or -] 0.77 SE, n = 19; ANOVA of values [F.sub.2,47] = 5.3; P = 0.001, P < 0.05, Holm-Sidak t-test) During this period, [T.sub.s] was only slightly > [T.sub.a] ([T.sub.s] = 31.8 [+ or -] 1.01 SE, n = 19) and not significantly different (P > 0.05, Holm-Sidak t-test). We used the nonparametric ANOVA of ranks test and Dunn's method for analysis of morning values due to a violation of the equality of variance assumption of the parametric ANOVA of values.

UVI exposure was significantly higher for Texas horned lizards when first encountered in the morning activity period (5.07 [+ or -] 0.45 SE) than it was for those first encountered in the late-afternoon and early-evening activity period (0.66 [+ or -] 0.46 SE; Mann-Whitney rank sum test t = 215.8, n = 19 [late afternoon and early evening], 25 [morning], P < 0.001). There were significant correlations of UVI exposure with time of day, positive in the morning (y = -16.1 + 2.1x; [R.sup.2] = 0.80, P <0.001, n = 25) and negative in the late afternoon and early evening (y = 5.3 [+ or -] 0.27x; [R.sup.2] = 0.53, P < 0.001, n = 18). There was also a significantly positive correlation between UVI and [T.sub.b] in the morning (y = -14.3 + 0.5x; [R.sup.2] = 0.36; P = 0.002, n = 19) as lizards were exposed to both solar infrared and UVB irradiation while on roads (Fig. 1).

For those individuals monitored twice during road surveys in the mornings of 2011 and 2012, an initial reading of UVI followed by a short delay and a second reading resulted in a significantly lower average UVI exposure of the second reading due to shade-seeking by some lizards. Readings were reduced from a mean UVI of 5.6 to 4.2 (paired t = 2.33; df = 14; P = 0.035).

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Pattern of Daily UVI exposure and UVB Dose for Focal Individuals in 2010--Road surveys and analysis of spot-check data provided little insight into the activity and UVB exposure of Texas horned lizards during most of the afternoon hours, because they were not visible from the road. However, focal-retrace data of individuals revealed patterns of variation throughout the day. These patterns differed among the individuals (Figs. 2 and 3). A male (Figs. 2a and 3a) observed during most of a warm ([T.sub.a] = 34.6[degrees]C), sunny day on 16 June 2010 moved into vegetation at the edge of the road after 1200 h and travelled approximately 140 m during a 5-h period along the road to the east, shuttling between shaded and partially shaded locations on the ground. During this period, he was never more than 1 m from the edge of the road but unlikely to be visible to people in passing vehicles. His UVI exposure was relatively low during the afternoon. At 1700 h he returned to exposed locations on the road and received a higher level of UVI exposure throughout the remainder of the observation period. His [T.sub.b], taken after the period of observation at 1839 h, was 39[degrees]C. A female (Fig. 2b, 3a) observed on a cooler ([T.sub.a] = 31.2[degrees]C) sunny day on 27 May 2010 went deeper into the vegetation adjacent to the road (1-2 m) at about 1000 h and remained off of the road surface until about 1800 h. Her eastward movement along the road was for a much shorter distance (about 30 m, 19 location changes) than that of the male (140 m, 28 location changes). The female experienced a higher afternoon UVI exposure than the male by climbing into herbaceous vegetation and shuttling vertically between fully and partially sunexposed locations. She returned to the open road, where she likely would be visible to people in passing vehicles, at 1800 h. Her [T.sub.b], taken after her period of observation at 1850 h, was 36[degrees]C. Both lizards occupied the same general area along the same road in the morning of their respective focal days but the male travelled much farther to the east than the female.

[FIGURE 3 OMITTED]

The male and female Texas horned lizards in 2010 had different patterns of UVB exposure yet received similar daily UVB doses (Figs. 2 and 3). Thus, on the warmer sunny day in June the male received most of his daily dose in the morning and late afternoon (Fig. 3a). He shunned full sun exposure in the afternoon until 1700 h. By contrast, on the cooler sunny day in May, the female received most of her daily dose in the morning and early afternoon (Fig. 3a). She exposed herself to full sun in the morning and during the warmest time of day in early afternoon. During this time she displayed thermoregulatory cooling behavior by opening her mouth on four occasions for periods of up to 2 min. The male never displayed this behavior during his focal observation period on the warmer day.

The duration of full sun exposures were generally short throughout the day (<5 min) for both the male and female and were interspersed with relocation to and from shaded locations (Fig. 2). Only the male spent an extended period in full sun (1 h) between 1730 and 1830 h.

Effect of the Thermal Extremes and Cloud Cover on UVB Dose--Observation on a day with more extreme weather conditions in 2012 revealed a different pattern of UVB exposure of a Texas horned lizard male. That day (4 June 2012) was unusually hot ([T.sub.a] = 37.4[degrees]C, peak afternoon [T.sub.a] = 40[degrees]C at the lizard site; >42[degrees]C at the control site; Table 1, Fig. 3b) and partly overcast (54% cloud cover; Table 1, Fig. 3b). He avoided all light exposure after 1400 h by burying into the sandy substrate in the shade and remained until late afternoon. His daily dose of UVB was less than one-third that of the male and female observed on the sunny days in 2010, and who remained active aboveground all day.

Size and Sex of Monitored Texas Horned Lizards--When conducting spot-check surveys, we sighted 71 lizards (19 males, 26 females, 19 unsexed juveniles, 7 where age and sex was undetermined). Of those, we captured, measured, and weighed 58 lizards. Adult males had an SVL of 83.1 [+ or -] 7.2 SD mm and a mass of 32.9 [+ or -] 7.2 SD g, n = 15. Adult females had an SVL of 87.5 [+ or -] 8.3 SD mm and a mass of 43.0 [+ or -] 13.5 SD g, n = 26. Juveniles had an SVL of 52.5 [+ or -] 4.1 SD mm and a mass of 7.3 [+ or -] 2.3 SD g, n = 17. Sizes for the male observed during the focal-retrace study in 2010 were an SVL of 81 mm and mass of 30 g. Those for the female observed in 2010 were an SVL of 90 mm and a mass of 52 g. Those for the male observed in 2012 were an SVL of 74 mm and a mass of 24 g.

DISCUSSION--Texas horned lizards studied at Matador WMA in North Central Texas in 2011 and 2012, when initially encountered on the road in the morning, were found to be exposing themselves to UVB with a mean UVI exposure of 5.6. When the same lizards were followed for a short period and some individuals chose to seek shade, the mean dropped to 4.2. During road surveys by automobile, it is less likely for investigators to see Texas horned lizards when lizards are in shade than when in fully exposed locations on the road. This leads to a "road bias" when comparing the UVB exposure of Texas horned lizards surveyed from a moving vehicle to that of other lizard species surveyed by walking through the habitat. When walking and searching, investigators are more likely to see lizards in partial- and full-shade than when they are searching from a moving vehicle, even at slow speeds. Thus, following and repeating the collection of data can correct the road bias and facilitate comparison. Both the "uncorrected" (UVI [approximately equal to] 5) and "corrected" (UVI [approximately equal to] 4) exposure estimates for Texas horned lizards exceed the UVI median exposure of 3.1 for zone-4 lizards reported to date (Ferguson et al., 2010) and support its designation as a UVI zone-4 species. The mean UVI value of 4.2 is similar to that of 4.34 measured for Sceloporus graciosus gracilis in northern California measured throughout the day (Ferguson et al., 2014).

The UVB dose measured for two individual Texas horned lizards followed throughout most of their daily activity period on sunny days ([approximately equal to] 3 J/[cm.sup.2]) exceeds that for any other squamate reptile measured to date. It surpassed even that of S. g. gracilis in northern California, which was [approximately equal to] 2J/[cm.sup.2] for the two individuals monitored by Ferguson et al. (2014). Higher latitude, higher altitude, a shorter activity period, and more haze due to wildfires near the study areas of northern California than at those of North Texas might have reduced the availability of solar UVB and the opportunity for exposure for S. g. gracilis in northern California. More research is needed to determine if the daily UVB doses for the two species are species-specific.

Although we monitored only three individuals for most of the day using the focal-retrace method, researchers can test hypotheses of the causes of variation in the daily pattern of UVB exposure of Texas horned lizards in North Texas with future focal-retrace research. We hypothesize that activity and UV exposure patterns vary with the degree of overcast and extreme thermal conditions. On warmer sunny days shade-seeking increases in late morning and midday UVI exposure is reduced. Thus, the male that was monitored in 2010 was observed on a warmer day than the female and restricted his afternoon sun exposure more than did the female. However, on a hot day when air temperature approached and exceeded upper levels of the optimal thermal range for Texas horned lizards, a male Texas horned lizard ceased aboveground activity, which interrupted his UVB exposure, and reduced his overall dose for the day. As hot days become more frequent after June, Texas horned lizards often escape heat by burrowing into the substrate for much of the afternoon (Fair and Henke, 1998, 1999; Burrow et al., 2001; Sherbrooke, 2003). When thermal conditions ([T.sub.a] and [T.sub.s]) exceed the optimum thermal range of the species, aboveground activity and UVB exposure is likely to be constrained.

The effect of high environmental temperatures on solar exposure may be relevant to conservation of the Texas horned lizard. Throughout much of the distribution of this species, overall temperature increase caused by global warming is likely to alter the availability of suitable thermal microclimates for many lizard species (Angilletta, 2009; Sinervo et al., 2010; Huey et al., 2010). Climate change models that attempt to predict impacts on lizard species (e.g., Buckley, 2008; Williams et al., 2012) should incorporate not only reductions of nutritional energy intake as a parameter but also nutritional quality. The opportunity to endogenously produce vitamin D by exposure to UVB is a component of nutritional quality that could be compromised by increased thermal constraint of aboveground activity.

As shown in previous research, Texas horned lizards rely on open, often bare, ground in the morning and late afternoon for basking (Whiting et al., 1993; Fair and Henke, 1998; Burrow et al., 2001). Accordingly, unpaved roads at Matador WMA are used by lizards as basking sites in the morning until body temperatures, and possibly UVI tolerance, approach the upper limits of the lizard's optimal range. Because Texas horned lizards have a thermal tolerance zone of several degrees Centigrade (Heath, 1965; Sherbrooke, 2003), they appear to allow their [T.sub.b] to gradually increase within this zone as they periodically expose themselves to increasing solar intensity until late morning. At that time they begin to seek shade and might remain on the ground but some, such as the female that we observed in 2010, may continue to seek solar exposure by climbing vertically into vegetation, a behavior also reported previously for this species (Whitford and Bryant, 1979; Sherbrooke, 2003). The significant positive correlation between body temperature and UVI in the morning from spot-check data is consistent with this interpretation of individual behavior. The stimulus to return to roads in late afternoon might be to bask for thermoregulation as the availability of other heat sources wane. However, significant enhancement of daily UVB dose is possible during the early part of their late-afternoon and evening activity period until 1900 h.

Knowledge of the daily patterns of thermal exposure and the UVB zone of reptiles including the Texas horned lizard provides useful information for captive maintenance programs for conservation, education, and research. With this knowledge, captive-animal managers can establish appropriate thermal and UVB gradients and establish natural daily and seasonal patterns for their animals. Because Texas horned lizards shuttle in and out of sunlight in nature, a UVI light gradient ranging from 0-8 should be available to the lizards for up to 9 h per day during spring and summer in captivity. Thermal gradients that allow them to maintain body temperatures ranging from 34-40[degrees]C should also be provided for up to 12 h per day in spring and summer. While experimental documentation is needed to verify whether or not Texas horned lizards are able to regulate their UVB dose behaviorally, studies support the hypothesis that other basking lizard species are capable of adjusting their UVB exposure depending on their internal vitamin D status (Ferguson et al., 2003; Karsten et al., 2009; Ferguson et al., 2013).

We thank M. Vaughan, S. Fredlake, S. Hammack, J. Crowley, J. Chavez, J. Le Van, and S. Bucklin for assistance in the field. K. Karsten made helpful suggestions during the formulation of research procedures. M. Nakamoto provided assistance with the Spanish translation of the abstract. Research was authorized by a permit from Texas Parks and Wildlife to GWF, SPR 0690-146, and permission from Matador WMA. We especially thank the staff of Matador WMA for help and guidance during the field work. Research was approved by Texas Christian University Institutional Animal Care and Use Committee protocol 11/04. Partial funding of the project was by grants from the Faculty Emeritus Research Fund from Texas Christian University to GWF.

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Submitted 8 October 2014.

Acceptance recommended by Associate Editor, Felipe de Jesus Rodnguez Romero, 7 April 2015.

Gary W. Ferguson, * William H. Gehrmann, Andrew M. Brinker, Glenn C. Kroh, and Donald C. Ruthven III

Department of Biology, Box 209030, Texas Christian University, Fort Worth, TX 76129 (GWF, WHG, AMB, GCK) Texas Parks and Wildlife Department, 3036 FM 3256, Paducah, TX 79248 (DCR)

* Correspondent: g.ferguson@tcu.edu
TABLE 1--Cloud cover, ultraviolet index (UVI), and temperature data
for the control sites monitored on both focal days (Day 1) and retrace
days (Day 2) for three Phrynosoma cornutum followed for most of a
focal day at the Matador Wildlife Management Area, Texas. Because
value estimates for the lizard locations on the focal day were
obtained on the retrace day, the control sites provided information on
the climatic similarity between the 2 days for each lizard. A mean UVI
difference between the control values on the 2 days of >1 and a mean
temperature difference >2[degrees]C were arbitrarily considered
grounds for adjusting the estimates for the lizard locations obtained
on the retrace day and applied to the focal day. Abbreviations in the
table are as follows: indiv. (individual), diff. (Day 1 minus Day 2),
[T.sub.s] (substrate temperature), [T.sub.a] (air temperature).

                                            % Clouds     UVI
h       Indiv.                  Date         Day 1      Day 1

0900    Female 2010        27 and 28 May      0.0       1.9
1000    Female 2010        27 and 28 May      0.0       5.0
1100    Female 2010        27 and 28 May      5.0       7.7
1200    Female 2010        27 and 28 May     10.0       9.4
1300    Female 2010        27 and 28 May     10.0       9.5
1400    Female 2010        27 and 28 May     10.0       9.7
1500    Female 2010        27 and 28 May     10.0       8.9
1600    Female 2010        27 and 28 May     10.0       7.2
1700    Female 2010        27 and 28 May      5.0       4.1
1800    Female 2010        27 and 28 May      5.0       1.5
--      Mean female 2010                      6.0       6.4
0900    Male 2010          16 and 17 June     0.0       1.7
1000    Male 2010          16 and 17 June     0.0       4.2
1100    Male 2010          16 and 17 June     5.0       7.5
1200    Male 2010          16 and 17 June    15.0       9.1
1300    Male 2010          16 and 17 June    36.0       8.5
1400    Male 2010          16 and 17 June    40.0       5.3
1500    Male 2010          16 and 17 June     0.0      10.3
1600    Male 2010          16 and 17 June     0.0       7.4
1700    Male 2010          16 and 17 June     0.0       5.0
1800    Male 2010          16 and 17 June     0.0       2.5
--      Mean male 2010                        9.6       6.2
0900    Male 2012           4 and 5 June    100.0       1.8
1000    Male 2012           4 and 5 June     80.00      3.1
1100    Male 2012           4 and 5 June    100.0       4.5
1200    Male 2012           4 and 5 June     90.0       6.5
1300    Male 2012           4 and 5 June     50.0       7.8
1400    Male 2012           4 and 5 June      0.0       9.2
1500    Male 2012           4 and 5 June      0.0       8.6
1600    Male 2012           4 and 5 June     10.0       6.3
1700    Male 2012           4 and 5 June     96.0       1.2
1800    Male 2012           4 and 5 June     10.0       0.5
--      Mean male 2012                      53.6       5.0

          UVI        UVI      [T.sub.s]   [T.sub.s]   [T.sub.s]
h        Day 2      Diff.       Day 1       Day 2       Diff.

0900     2.1       -0.2         30.2        34.0      -3.8
1000     4.9        0.1         37.5        40.0      -2.5
1100     7.3        0.4         40.2        44.6      -4.4
1200     9.3        0.1         45.6        49.0      -3.4
1300     9.6       -0.1         44.6        48.8      -4.2
1400     7.5        2.2         47.8        48.8      -1.0
1500     6.8        2.1         48.8        48.6       0.2
1600     6.4        0.8         39.2        46.0      -6.8
1700     3.5        0.6         37.2        43.6      -6.4
1800     1.4        0.1         34.2        40.6      -6.4
--       5.9        0.6         40.5        44.4      -3.9
0900     1.5        0.2         29.2        29.2       0
1000     4.5       -0.3         30.4        35.4      -5.0
1100     7.7       -0.2         38.4        37.4       1.0
1200    10.1       -1.0         41.8        45.0      -3.2
1300    10.7       -2.2         42.8        45.2      -2.4
1400    10.4       -5.1         43.4        47.4      -4.0
1500     7.3        3.0         45.0        41.6       3.4
1600     7.8       -0.4         44.8        42.0       2.8
1700     4.5        0.5         42.2        45.8      -3.6
1800     2.6       -0.1         40.2        42.8      -2.6
--       6.7        0.6         39.8        41.2      -1.4
0900     0.5        1.3         40.0        23.8      16.2
1000     5.2       -2.1         45.0        34.0      11.0
1100     3.2        1.3         44.6        31.2      13.4
1200     8.3       -1.8         51.6        38.2      13.4
1300    10.4       -2.6         52.8        38.8      14.0
1400     7.2        2.0         55.4        39.2      16.2
1500     8.3        0.3         59.0        43.6      15.4
1600     6.1        0.2         57.8        43.2      14.6
1700     3.7       -2.5         43.6        41.2       2.4
1800     1.0       -0.5         37.4        37.4       0
--       5.4        0.4         48.8        37.1      11.7

        [T.sub.a]   [T.sub.a]   [T.sub.a]
h         Day 1       Day 2       Diff.

0900      23.7        26.3      -2.6
1000      27.6        34.2      -6.6
1100      28.0        33.6      -5.6
1200      30.7        37.0      -6.3
1300      33.1        39.2      -6.1
1400      34.0        34.2      -0.2
1500      35.8        34.8       1.0
1600      33.9        37.8      -3.9
1700      31.7        37.2      -5.5
1800      32.4        35.6      -3.2
--        31.1        35.0      -3.9
0900      27.3        26.6       0.7
1000      30.3        30.1       0.2
1100      31.8        30.7       1.1
1200      34.5        32.8       1.7
1300      34.0        35.0      -1.0
1400      34.8        35.1      -0.3
1500      35.5        35.2       0.3
1600      34.8        37.2      -2.4
1700      35.1        36.9      -1.8
1800      34.0        35.5      -1.5
--        33.2        33.5      -0.3
0900      32.2        22.8       9.4
1000      39.5        28.0      11.5
1100      36.5        28.2       8.3
1200      38.0        31.8       6.2
1300      39.5        34.5       5.0
1400      41.0        35.0       6.0
1500      42.5        36.2       6.3
1600      41.0        35.0       6.0
1700      38.0        35.5       2.5
1800      35.0        34.0       1.0
--        38.3        32.1       6.2
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Author:Ferguson, Gary W.; Gehrmann, William H.; Brinker, Andrew M.; Kroh, Glenn C.; Ruthven, Donald C., III
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1U7TX
Date:Jun 1, 2015
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