Zoo Biology 29 : 317–334 (2010)

RESEARCH ARTICLE

Voluntary Exposure of Some
Western-Hemisphere Snake andLizard Species to Ultraviolet-B
Radiation in the Field: How Much
Ultraviolet-B Should a Lizard or
Snake Receive in Captivity?
Gary W. Ferguson,1 Andrew M. Brinker,1 William H. Gehrmann,1Stacey E. Bucklin,1 Frances M. Baines,2 and Steve J. Mackin3
1

Department of Biology, Texas Christian University, Fort Worth, Texas
Greenfield, School Lane, Govilon, Abergavenny, Monmouthshire, Wales, United Kingdom
3
Solartech Inc., Harrison Township, Michigan
2Studies of voluntary exposure to ultraviolet-B (UVB) radiation from the sun inthe ﬁeld were conducted in the southern US and Jamaica for 15 species of lizards
and snakes occupying various habitats. Species were sorted into four zones of
UVB exposure ranging from a median UV index of 0.35 for zone 1 to 3.1 for zone
4. Guidelines for UVB exposure in captivity of these and species occupying
similar light environments are presented. Data for most species were collectedduring mid-day during the spring breeding season, which appeared to be the timeof maximum exposure. For two species of Sceloporus studied more intensively
there was signiﬁcant variation of exposure among times of the day and amongseasons. So, all-day studies over the entire active season are necessary to fully
understand the pattern of natural exposure for a particular diurnal species.
Environmental and body temperature and thermoregulation as well as UVB/
vitamin D photoregulation inﬂuences exposure to UVB. Regressions allowing theinter-conversion of readings among some meters with different detector
sensitivities are presented. Readings of natural sunlight predict the same
photobiosynthetic potential for vitamin D as the same reading from artiﬁcial
Correspondence to: Gary W. Ferguson, Department of Biology, Texas Christian University, Box 298930,
Fort Worth, Texas 76129. E-mail: g.ferguson@tcu.edu

Received 7 November 2008; Accepted 13 April 2009
DOI 10.1002/zoo.20255
Published online 29 May 2009 in Wiley InterScience (www.interscience.wiley.com).

r 2009 Wiley-Liss, Inc.

318 Ferguson et al.
sources whose wavelength distribution within the UVB band of the source iscomparable to that of sunlight. Research approaches to further increase ourunderstanding of vitamin D and UVB use and requirements for squamate reptiles
in captivity are outlined. Zoo Biol 29:317–334, 2010. r 2009 Wiley-Liss, Inc.

Keywords: ultraviolet; ﬁeld exposure; captive requirements; UV-index

INTRODUCTION
Basking reptiles are exposed to ultraviolet-B (UVB) radiation (290–320 nm) innature and many species have morphological adaptations to protect themselves fromUVB damage to vital organs including darkly pigmented UVB-absorptive layers inthe skin and peritoneal linings of the coelom and viscera [Porter, 1967]. Exposure toexcess UVB can cause eye and skin damage, skin cancer and poor reproduction in
reptiles and amphibians [Hays et al., 1995; Blaustein et al., 1998; Ferguson et al.,
2002; Gehrmann, 2006; Baines, 2007].
In contrast to tissue and DNA damage, exposure of many vertebrate species,
including reptiles, to UVB radiation results in positive consequences, including theendogenous production of vitamin D3 [MacLaughlin et al., 1982; Chen et al., 1993;
Holick et al., 1995; Tian et al., 1996; Laing and Fraser, 1999; Carman et al., 2000;
Laing et al., 2001; Aucone et al., 2003; Ferguson et al., 2003, 2005, Acierno et al.,2006, 2008].Vitamin D3 is the precursor of a vital hormone (1,25 dihydroxy-vitamin
D3 or calcitriol) that regulates calcium–phosphorus balance and immune responses[Holick, 1999; Brames, 2007].
Vitamin D3 can also be obtained from dietary sources [Holick, 1989a; Allenet al., 1999].Vitamin D deﬁciency in vertebrates, including reptiles, results in poor
health and reproduction [Narbaitz and Tsang, 1989; Ferguson et al., 1996; Packard
and Clark, 1996]. However, excess dietary vitamin D can result in toxic effects anddeath [Ferguson et al., 1996 Wallach, 1996]. On the contrary, high doses of UVB,
given a light source with similar spectral power distribution (SPD) to sunlight, do
not cause excess vitamin D3 and the associated toxic effects, because biologicallyinert photoproducts are produced in the skin with higher UVB exposures [Webbet al., 1989; Holick, 2004]. Optimum levels of UVB or Vitamin D are largely
unknown for most species [but see Ferguson et al., 2002].
In addition to the beneﬁcial role of UV in vitamin D production, there is also
evidence that lizards can see UV light [Loew et al., 2002; Bowmaker et al., 2005],
adjust their exposure to UV for vitamin D photoregulation [Ferguson et al., 2003;
Karsten et al., 2009], as well as use reﬂected UV light from the skin of a social
partner for communication [Fleishman et al., 1993; Whiting et al., 2006].
Armed with this knowledge, the availability of artiﬁcial UVB-producing lamps
and the availability of inexpensive UVB meters, the question remains: What is the
optimum UVB exposure to which a captive reptile should be subjected?
To help answer the question we need to know the natural irradiance levels of
UVB to which an animal voluntarily exposes itself in the wild. In this report we
provide information on the natural exposure for 15 species of lizards and snakes
gathered from the wild. We provide tentative estimates of the UVB zones occupiedby species as reference guidelines for levels to provide for animals in captivity. We
also discuss and review procedures pioneered to more fully understand the UVB andZoo Biology

UVB Exposure of Squamates in the Field 319

vitamin D requirements of lizard and snake species and how knowledge gained fromeach of these can be applied to determine the proper UVB environment and dietary
vitamin D intake for captive species.
METHODS
From 2002 to 2008 studies were conducted along the north coast of Jamaica
and at several locations in the southern and western U.S. to measure the UVB
exposure of lizards and snakes encountered in the ﬁeld. The general procedure
involved searching habitat, encountering a specimen, and recording the UVB
irradiance with a broadband UVB meter and time of day at the location where theanimal was ﬁrst seen. Air and substrate temperatures were also recorded. Sun
exposure of each specimen encountered was subjectively judged as ‘‘sun,’’ ‘‘partial,’’or ‘‘shade’’ and in most cases measured with a visible-spectrum (400–700 nm)
General Electric type 214 light meter (Cleveland, OH). Maximum possible UVB
exposure within the cruising distance of the animal was also noted. Orientation of
the detector surface of the meters was perpendicular to the substrate and the animal’s
body and/or pointed into the sun. Where both orientations were employed, thehigher reading was analyzed for this report.
Three types of broadband UVB meters were employed in successive studies
during the study period including Gigahertz Optik UVB meter (Gigahertz-Optik,
Inc., Newburyport, MA), Solarmeter 6.2, and Solarmeter 6.4 (Solartech, Inc.,
Harrison Township, MI). Recent studies have shown the readings from different
meters to result in different output when exposed to the same levels of sunlight[Gehrmann et al., 2004a,b]. This is partly due to differences in the detector sensitivity
among meters to various wavelengths in the UVB-band of the spectrum. However,
the relationships between meter readings in natural sunlight are robustly predictable
and readings from different meters can be inter-converted (Figs. 1 and 2). The
detectors of the S6.4 meter and another Solartech meter (S6.5) (not used in thisstudy) are identically sensitive only to the shorter wavelengths of UVB that havebeen shown to most closely correlate with conversion of pro-vitamin D3 toprevitamin D3 in vitro [Lindgren et al., 2008]. The Gigahertz Optik and S6.2 meters
have a broader sensitivity within the UVB range. Readings from the S6.4 meter(IU/min) can be directly converted to those of the 6.5 m (UV index [UVI]) by
dividing by 7.14. Using this quantitative relationship, or the regression in Figure 1,
we converted values measured with S6.2 or 6.4 meters to UVI, because of its moregeneral acceptance for measuring UVB irradiance. Some readings obtained onlywith the Gigahertz Optik meter were ﬁrst converted to S6.2 readings using theregression in Figure 2.
We tested the ability of the Solartech 6.4 meter to predict photoproductconversion of provitamin D when exposed to either natural or artiﬁcial UVB lightsources to determine whether ﬁeld values can be compared directly to those ofindoor captive environments from the point-of-view of vitamin D production. In
vitro models [ampules containing an alcohol solution of provitamin D; Lu et al.,
1992; Chen et al., 1993] were exposed either to the sun or to a 20 Watt Reptisun 10.0
ﬂuorescent tube (Zoo Med Inc., San Luis Obispo, CA), which has a UVB SPD
similar to that of the sun and is widely used in herpetoculture. Exposure was for 12,
24, 40, or 56 min. Irradiance of the two sources was matched at an average of 43 IU/
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320 Ferguson et al.

Fig. 1. Regression of simultaneous readings from the Solartech 6.2 m and the Solartech
6.5 m from sun exposure in northern Australia and the Dallas-Fort Worth metroplex in
North-Texas.

Fig. 2. Regression of simultaneous readings from the Gigahertz Optik and Solartech 6.2 m
exposed to sunlight in Monahans Sandhills State Park, Texas.

min measured with a Solartech 6.4 meter. Regressions of percent photoproduct vs.
exposure time were compared between sources.
Studies in Jamaica on the lizards Anolis lineotopus, Anolis grahami, and Anolis
sagrei were conducted at the Hofstra University Marine Lab in Priory, St. Ann’s
Parish in March 2004. Studies in the US were conducted at several locations: (1)from April–September, 2005 at Old Sabine Wildlife Management Area on the snakes
Agkistrodon piscivorous, Elaphe obsoleta, Thamnophis proximus, Nerodia fasciata,
and Nerodia erythrogaster; (2) in May and June, 2005 at Monahans State Park,
Ward Co., Texas on the lizard Uta stansburiana stejnegeri; (3) at Kisatchee National
Forest, Natchitoches Par., Louisiana on the lizards Sceloporus undulatus hyacinthinus and Anolis carolinensis; (4) at Rita Blanca National Grassland, Dallam Co.,

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UVB Exposure of Squamates in the Field 321

Texas on the lizards Holbrookia maculata and Sceloporus undulatus garmani; (5) inMay 2007 on Sceloporus graciosus at various localities in California and Colorado;(6) from April–October 2007 on the lizard Sceloporus olivaceous in Tarrant Co.
Texas; (7) in July 2008 on the lizard Sceloporus graciosus in Lassen National
Volcanic Park, California.
For comparison (Table 1), values from the spring and early summer
corresponding to the active breeding season were used. Data were accumulated
throughout the day and were mostly conﬁned to the period of peak activity and sun
exposure between 0800 and 1500 hr. All data were analyzed using Sigmastat 3.5(Jandel Corporation) or SYSTAT version 10.2 (SYSTAT Software Inc.).
RESULTS
There was considerable variation among taxa and habitats in mean UVB
exposure (Table 1). It was convenient to divide the species into four UVB-zones,
which corresponded roughly to their ecological contexts and which were labeled inaccord with light availability (Table 1) For localities where multiple species occurred,differences clearly reﬂected differences in habitat preference, which included
variations in substrate, temperature, and light throughout the entire spectrum aswell as UVB. The exposure of most species was not monitored throughout their
entire activity season and can vary signiﬁcantly with both season (Fig. 3) and thetime of day [Fig. 4; Ferguson et al., 2005]. Therefore, the comparisons here may or
may not use complete species- or population-typical values, which can only be
determined by all-day, season-long studies. For that reason in our comparison we
did not test for statistical signiﬁcance of our differences among species, althoughstandard deviations of our data are presented.
Day-long or season-long studies of two species of Sceloporus revealed
signiﬁcant variance of exposure among months of the activity season for the Texas
spiny lizard Sceloporus olivaceous (Fig. 3) and among times of the day for thesagebrush lizard Sceloporus graciosus (Fig. 4). The exposure variance among months
was signiﬁcant for the Texas spiny lizards with exposure during July (month 4) andAugust (month 5) being signiﬁcantly lower than exposure in April (month 1), May(month 2), and October (month 7) (Kruskal–Wallace one-way ANOVA on ranks
and Dunn’s multiple comparison method; Po0.05). In this study UVB exposure ofcontrols (exposed sites) was signiﬁcantly higher than that of the lizards(Kruskal–Wallace one way ANOVA on ranks; Po0.05).
The exposure variance among time categories was signiﬁcant for the sagebrushlizards with exposure during 1100–1300 hr being signiﬁcantly higher than exposure
during 1500–1800 hr (Kruskal–Wallace one-way ANOVA on ranks and Dunn’s
multiple comparison method; Po0.05). For the controls exposure during
0900–1100 hr and 1500–1800 hr was signiﬁcantly lower than exposure during the
1100–1300 hr time-period. In this study also exposure of controls was signiﬁcantly
higher than that of the lizards (Kruskal–Wallace one way ANOVA on ranks;
Po0.01). In both studies lizards avoided the maximum exposure available to them
most of the time (Figs. 3 and 4).
The thermal environment strongly inﬂuenced the UVB exposure of the lizards.
For three lizard species (Sceloporus undulatus hyacinthinus, Anolis carolinensis, andHolbrookia maculata, data pooled) UVB exposure was strongly correlated withZoo Biology

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Holbrookia maculata (25)Lesser Earless Lizard
Sceloporus graciosus (10)Sagebrush Lizard

Uta stansburiana stejnegeri (13)Desert Side-blotched Lizard
Sceloporus undulatus hyacinthinus (18)
Eastern Fence Lizard
Anolis sagrei (13)
Cuban brown Anole
Sceloporus olivaceous (30 in May)
Texas Spiny Lizard

Thamnophis proximus (18)Western Ribbon Snake
Anolis grahami (12)Jamaican Blue-pants Anole
Anolis carolinensis (19)Green Anole
Nerodia erythrogaster (10)
Yellow-bellied Water Snake

0.270.18 (0–0.6)

Agkistrodon piscivorus (11)
Cottonmouth Water Moccasin
Elaphe obsoleta (6)Texas Rat Snake
Anolis lineotopus (17)Jamaican Brown Anole
Nerodia fasciata (4)Broad-banded Water Snake

3.173.22 (0.4–9.5)

2.970.98 (1.5–4.5)

2.671.89 (0.1–7.4)

1.871.13 (0.6–4.1)

1.771.62 (0.3–4.9)

1.370.65 (0.4–2.9)

0.970.99 (0.1–2.7)

0.970.68 (0.2–3.0)

0.870.33 (0.3–1.1)

0.870.77 (0.2–1.1)

0.770.42 (0.2–1.1)

0.670.36 (0.2–1.4)

0.470.27 (0–0.8)

Average UVI7SD(range)Species (number of individuals)
Common name

4

–

3

–

2

–

1

UVB ZONE

2.6–3.5 or 4 (3.1)–

1.0–2.6 (1.8)–

0.7–1.0 (0.9)–

0–0.7 (0.35)

UVB Zone range(median)Zone 4 mid day baskers;
thermoregulator–

Zone 3 full-sun or partial sun;thermoregulator–

Zone 2 partial sun or occasional
full-sun basker;
thermoregulator–

Zone 1 crepuscular or shade;thermal conformer

Zone description

TABLE 1. UVB zone reference guidelines determined from average irradiance of randomly encountered individuals in the ﬁeld

322 Ferguson et al.

Uta stansburiana stejnegeri (13)Desert Side-blotched Lizard
Sceloporus undulatus hyacinthinus (18)
Eastern Fence Lizard
Anolis sagrei (13)
Cuban Brown Anole
Sceloporus olivaceous(30 in May)
Texas Spiny Lizard

Thamnophis proximus (18)Western Ribbon Snake
Anolis grahami (12)Jamaican Blue-pants Anole
Anolis carolinensis (19)Green Anole
Nerodia erythrogaster (10)
Yellow-bellied Water Snake

Agkistrodon piscivorus (11)
Cottonmouth Water Moccasin
Elaphe obsoleta (6)Texas Rat Snake
Anolis lineotopus (17)Jamaican Brown Anole
Nerodia fasciata (4)Broad-banded Water Snake

Sceloporus undulatus garmani (3)Northern Prairie Lizard

18713.5 (1–53)

1378.0 (4–29)

12711.6 (2–34)

974.6 (3–21)

777.0 (1–19)

674.8 (1–21)

672.3 (2–8)

575.5 (1–23)

573.0 (1–8)

472.6 (1–10)

371.9 (0–6)

–

3

–

2

–

1

ZONE

Average IU/min7SD(range)271.3 (0–4)–

3.271.51 (2.2–4.9)–

7–18 (13)–

5–7 (6)–

0–5 (2.5)

Zone range (median)––Zone 3 full-sun or partial sun;thermoregulator–

Zone 2 partial sun or occasional
full-sun basker;
thermoregulator–

Zone 1 crepuscular or shade;thermal conformer

Zone description–

UVB Exposure of Squamates in the Field 323

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23710.8 (16–35)

22723.0 (3–68)

2177.0 (10–32)

Average IU/min7SD(range)

–

4

ZONE

–

18–25 or 4 (22)Zone range (median)–Zone 4 mid day baskers;
thermoregulator

Zone description

UVB-irradiance Zone reference guidelines are based on the natural exposure levels of lizards and snakes spot-checked in the ﬁeld during their activity
period in the spring–early summer breeding season. The average number of sightings per species was 14 (range 3–30). Species are grouped into four
light-exposure habitat zones with increasing average exposure levels from 1 to 4. Two reference guidelines are presented: one for UVI and one
for IU/min.

Holbrookia maculata (25)Lesser Earless Lizard
Sceloporus graciosus (10)Sagebrush Lizard
Sceloporus undulatus garmani (3)Northern Prairie Lizard

TABLE 1. Continued

324 Ferguson et al.

UVB Exposure of Squamates in the Field 325

Fig. 3. Mean mid-day exposure of ultraviolet light (UVI) at the locations of randomly
encountered, free-living Texas Spiny lizards Sceloporus olivaceous (gray bars) and nearby sunexposed control sites (hatched bars) in Fort Worth, Texas from April through October 2007.
Observations were from 1000 to1400 hr on 51 different days. Capped bars are one standard
deviation. Numbers in bars are sample sizes. Comparing months, different letters above lizard
bars (a vs. b) indicate signiﬁcant differences of exposure. Exposure differences between lizards
and controls were also signiﬁcant (see text).

Fig. 4. Mean ultraviolet exposure (UVI) of locations of randomly encountered, free-living
Sagebrush lizards Sceloporus graciosus (gray bars) and nearby sun-exposed control sites(hatched bars) in Lassen National Park, California from 0900 to 1800 hr monitored over a
two-day observation period in July 2008. Numbers in bars are sample sizes. Comparing time
periods, different letters above lizard bars (a vs. b) and above control site bars (c vs. d) indicate
signiﬁcant differences of exposure among time periods for lizards and control sites,
respectively. Exposure differences between lizards and control sites were also signiﬁcant (seetext).

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326 Ferguson et al.

cloacal temperature (Fig. 5). For Texas spiny lizards (Sceloporus olivaceous) the
seasonal variation was associated with a noticeable temperature threshold (Fig. 6).
When air temperatures approached or exceeded 321C, the animal sought shade,resulting in a lower exposure to UVB than at cooler temperatures. At high ambient
temperatures the animals have considerably lower exposure than is available if fully
exposed. The ‘‘preferred’’ temperature of this species, which is considered to be an
active thermoregulator, is 32–361C, varying somewhat with the seasons [Blair, 1960].

Fig. 5. UVB exposure as a function of cloacal temperature for three species of lizards(Sceloporus undulatus hyacinthinus, Anolis carolinensis, and Holbrookia maculata, data
pooled). UVB was measured at the site where the lizard was ﬁrst seen. Cloacal temperatures
were recorded within 30 sec of capture and usually within 2-min of initial sighting. Data fromlizards that required Z5 min of pursuit before capture are not included.

Fig. 6. UVB exposure as a function of air temperature (Ta) for Texas spiny lizards(Sceloporus olivaceous). Dashed line emphasizes a temperature threshold effect. At
temperatures above 321C mean and variance of UVI were noticeably reduced. Both UVB
and Ta were taken at the lizard’s location. Data points are individual sightings.

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UVB Exposure of Squamates in the Field 327

Fig. 7. Percent photoproduct in ampules vs. time exposed to sunlight or an artiﬁcial UVB
source (20 Watt ZooMed Reptisun 10.0 ﬂuorescent tube). Each ampule was exposed to thesame average irradiance (43 IU/min) measured with the Solartech 6.4 m. There were no
signiﬁcant differences in slope or intercept of the regressions for the sun vs. the Reptisun tube
(see text).

The UVI at the exposed control sites in the Texas spiny lizard study was lower
than the exposed, sunny, clear, mid-day readings reported for the Dallas/Fort Wortharea for the past several years (maximum 10–11) ( http://www.cpc.ncep.noaa.gov/
products/stratosphere/uv_index/uv_annual.shtml). Also, the seasonal variation was
not as expected (highest in spring vs. mid-summer). This may have been due to thegreater than average cloud-cover for the summer of 2007 and/or that the sites were
not in fully open exposed areas. Also, any effects of nearby trees would be greater in
mid-summer when leaf cover is increased.
Comparison of photoproduct conversion from in vitro models vs. duration of
exposure with irradiance levels controlled revealed no signiﬁcant difference between
the slopes or intercepts of the regressions for the sun and the ZooMed Reptisun 10.0
ﬂuorescent tube (ANOVA Source by exposure time interaction and source effect,
P40.05; Fig. 7). Therefore, the same average irradiance reading from either source
predicted the same potential vitamin D production.

DISCUSSION
To our knowledge this is among the ﬁrst reports quantitatively estimating
natural UVB-exposure of lizards and snakes [see also Carman et al., 2000; Ferguson
et al., 2005]. Based on the natural UVB exposure levels of 15 species of snakes andlizards from the southern and western U.S. and Jamaica, general recommendationsof average and range of levels of exposure (irradiance) are presented for species
occupying certain types of light environments (Table 1). Keepers of these species in
captivity can reasonably expect to subject an animal to these levels with no danger
caused by overexposure (but see Baines [2007] for cautions associated with certain
types of artiﬁcial light sources). If animals are kept in an enclosure large enough to
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328 Ferguson et al.

produce a suitable UVB gradient and which provides a UVB refuge (we recommend
this) so that they can photo-regulate their UVB exposure based on their vitamin
D-condition, the maximum values in the zone range column of Table 1 arerecommended for the closest accessible point to the UVB source. If animals are
kept in small enclosures where a UVB irradiance gradient is difﬁcult to attain andthere is no UVB refuge (we do not recommend this), the median values in the zone
range column of Table 1 are probably more appropriate. Data on UVB dose
(irradiance  time) for free-living natural species require monitoring individuals
throughout their activity cycle and are just now becoming available for a handful of
species [Carman et al., 2000; Ferguson et al., 2005]. For captive species of special
concern, ﬁeld data on dose will provide information on what voluntary exposure
durations might be expected in captivity and provide information on the UVB
requirements of the species. The general application of these guidelines may belimited to Western-Hemisphere-dwelling small lizards and snakes. More ﬁeld dataon turtles, crocodilians, and large-sized squamates from more regions of the world
are needed to update and increase the general value of these guidelines.
At least four cautions need to be emphasized in applying these guidelines tocaptivity. First, because the exact UVB irradiance tolerances and requirements for a given
species other than those in this study are unknown and may vary with age, reproduction,and health of a specimen, it is important to provide a captive animal with a refuge fromany UVB source, i.e., to provide a large UVB gradient accessible by the animal. There isevidence that lizards can use a gradient to self-regulate their exposure (see below).
Second, an animal should be closely watched after a new UVB source isestablished in an enclosure and adjustments made depending on the captive’s behavior.
Studies have shown that some lizards are capable of precisely regulating their exposure
to UVB [Ferguson et al., 2003; Karsten et al., 2009]. Ferguson et al. [2003] showed that
panther chameleons exposed to UVB gradients, that were not linked to thermal
gradients and were generated using artiﬁcial ﬂuorescent lamps in the laboratory, canregulate UVB exposure independently from temperature regulation. Nevertheless,lizards in the ﬁeld readily seek refuge from the sun, which is a strong UVB and heatsource, when their thermal requirements are satisﬁed (Figs. 3, 4, and 6) and thermal
preferences can inﬂuence and constrain UVB exposure and vitamin D/UVB
photoregulation. If the captive animal avoids a UVB source, the UVB may be toostrong, or the temperature at that location may be too hot or too cold, or the visible
light may be inappropriate; the source should be evaluated. It is important to makesure that the ambient cage temperature is not too hot or cool and that unnaturally highlevels of UVB are not accessible to a basking species at the thermal basking site.
Third, when setting up a UVB source it is important to consider not the total
UVB output of the lamp but the actual irradiance at the basking site and the UVB
gradient produced by the lamp, in other words, its UVB ‘‘footprint’’ in the vivarium.
This depends upon the distance of the basking site from the light source, the shape ofthe beam (which is determined by the type of the lamp and any reﬂectors in use), andalso the UV absorption properties of any barrier between the lamp and the reptile,
such as mesh, plastic, or glass. Such barriers may attenuate or even completely blockout the UVB irradiance [Burger et al., 2007].
A fourth caution for applying these guidelines is that, despite the resultspresented here, a reading from these meters from the ﬁeld may or may not be directlycomparable to the same reading from some artiﬁcial light sources regarding vitamin
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UVB Exposure of Squamates in the Field 329

D production potential. MacLaughlin et al. [1982] showed that UVB from some
artiﬁcial sources can result in a substantially higher rate of photoproduct production
than natural sunlight. The SPD of the Zoo Med Reptisun ﬂuorescent tube, as well as
most artiﬁcial light sources manufactured for use in reptile herpetoculture, is broadly
similar to that of the sun in the UVB range. The Solartech 6.4 and 6.5 meters will
predict vitamin D synthesis equally well from either the sun or the artiﬁcial sourcesof this type (Note: some models of the Solartech 6.4 and 6.5 meters manufactured
after August 2008 may be suitable for outdoor use only; ours were manufactured
before this date).
However, some artiﬁcial lamps, including the FS sunlamps intended for use inresearch, produce signiﬁcant amounts of low-wavelength irradiance (short wavelength UVB 280–290 nm and, rarely, UVC), which, although it will enhance vitamin
D production, can also cause serious damage to eyes and skin, and even cause death[Hibma, 2004; Baines, 2007]. Because of the differences in the SPD of these sources
with that of the sun, these sources produce more vitamin D than predicted by
the meters along with deleterious effects due to short wavelength ultraviolet
radiation. We strongly discourage the use of artiﬁcial light sources that havenot been manufactured and tested for speciﬁc use in herpetoculture (see Baines[2007] and Lindgren et al. [2008] for comparison of various artiﬁcial UVB sourcesmanufactured for herpetoculture).
Our knowledge of natural intake of vitamin D3 from the diet is meager and thefew data for insectivorous species suggest that it is low (maximum daily intake of
37 ng or 1.5 IU/g of food based on stomach content analysis of animals collected in
the ﬁeld during a day and the assumption that they ﬁll their stomachs once a day)[Carman et al., 2000; Ferguson et al., 2005]. While some herpetoculturists haveavoided the use of UVB and report successful propagation from the use of dietary
sources alone [see Ferguson et al., 1996], to our knowledge there are no quantitative
studies determining optimal doses of dietary vitamin D3 for any reptile species
maintained without access to UVB. Nor are there any data indicating an ability oflizards or snakes to regulate their dietary vitamin D intake via behavioral selection offood sources rich or poor in vitamin D content. There are data that some lizards canselectively choose dietary alternatives presumably to balance nutrient intake[Auffenberg, 1988; Eason, 1990], so behavioral regulation of dietary vitamin D istheoretically possible, but current knowledge makes it difﬁcult to recommend an
appropriate level of dietary supplementation. We recommend that lizard and snake
keepers rely primarily on UVB exposure for provisioning of vitamin D. Since small
amounts of vitamin D3 have been found in gut contents of diurnal insectivorous
lizards, a combination of suitable UVB lighting and very low levels of vitamin D3
supplementation may be appropriate for most diurnal lizards and snakes.
Once the natural UVB exposure levels are determined for a species, several
other questions must be answered through ﬁeld and laboratory study to more fully
understand the UVB and vitamin D requirements of a species.
(1) How long does an animal expose itself to its preferred levels in nature? This
determines the UVB dosage (irradiance  time) that an animal normally receives andthe UVB requirements of a species. Such data can be obtained during noninvasiveﬁeld studies by monitoring single animals for the duration of an activity cycle. In
recent research, animals have been followed throughout an activity cycle and timespent at speciﬁc locations monitored (focal-day). On a subsequent day of similar
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solar conditions, animal locations were revisited and UVB exposure determined byplacing in vitro models at the previous-day locations and for the same time (retraceday). The models were exposed for 3 hr time periods during which they wererepeatedly relocated to follow the lizard’s previous day pathway. Using a regression
equation relating UVB dose (Y) to percent photoproduct produced from the original
provitamin D content of the models (X), UVB exposure dose of the lizard can be
estimated for that time period [Ferguson et al., 2005]. Instead of retracing the lizard’s
path with ampules, retrace can involve measuring UVB irradiance at short intervals
with a meter. From these data the average irradiance per unit time and dose can becalculated.
Other useful information, which is much more difﬁcult to obtain and requires
invasive and expensive analytical procedures, is as follows.
(2) What is the natural dietary intake levels of vitamin D3? The higher the
dietary intake, the less UVB exposure may be required to maintain vitamin D
condition. Stomach contents of wild, free-living animals need to be obtained andanalyzed by HPLC techniques [Carman et al., 2000; Ferguson et al., 2005]. Small
animals may need to be sacriﬁced to obtain complete stomach contents, althoughstomach-ﬂushing techniques and behavioral observation may be feasible forsome species [Legler and Sullivan, 1979; Watters, 2008]. If the diet is specialized
and well-known, preingested samples can be collected in the ﬁeld and analyzed[Watters, 2008].
(3) What are the circulating calcidiol and vitamin D3 levels of animals in natureand in captivity? Calcidiol (25-hydroxy vitamin D3) is the immediate precursor to
calcitriol and is considered the primary storage form of vitamin D3 [Haddad, 1999;
Laing and Fraser, 1999]. Calcidiol is considered to be the best indicator of thevitamin D status of an animal. Levels in nature provide a benchmark for thesuitability of the UVB environment and dietary vitamin D levels in captivity[Gillespie et al., 2000; Laing et al., 2001; Aucone et al., 2003; Ramer et al., 2005].
Animals need to be bled and the serum analyzed [Chen et al., 1990]. In captivity, lowlevels of calcidiol are indicative of vitamin D deﬁciency. Circulating levels of
calcidiol that are too high can result in toxicity. This is unlikely to occur in wild
reptiles, since excess vitamin D3 is never produced by sunlit skin, and natural reptile
diets contain very little vitamin D3. In captivity over-supplementation with dietary
vitamin D3 is the most likely cause.
(4) What is the degree to which a species can regulate its exposure to UVB
depending on its vitamin D-condition? While one species, the panther chameleon, hasbeen shown to do this with great precision [Jones et al., 1996; Ferguson et al., 2003;
Karsten et al., 2009] and other species may have this ability [Bernard et al., 1991;
Aucone et al., 2003], careful laboratory and ﬁeld research is required to document
this ability in other species. If a species can self-regulate its UVB exposure to
maintain optimal vitamin D3 status, then providing a suitable species-speciﬁc UVB
gradient in the vivarium may be all that is necessary for this to occur. However, thethermal inﬂuence on the expression of UVB/vitamin D photoregulation is ofparticular importance. Further study is essential to evaluate the way in which thelocation of heat and visible light sources in the vivarium affect photoregulatory
behavior. The natural co-existence of heat and UV found under sunlight is notguaranteed under artiﬁcial lighting and thermoregulation may take precedence if thisco-existence is not provided [Dickinson and Fa, 1997].
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UVB Exposure of Squamates in the Field 331(5) How sensitive is the skin to UVB regarding the production of vitamin D3? Skin
sensitivity to UVB with regard to conversion of provitamin D to vitamin D andother photoproducts has been documented in all vertebrates from ﬁsh to primates[Holick, 1989b; Holick et al., 1995]. By exposing patches of skin to artiﬁcial UVB
lights, lizard species have been shown to vary in skin sensitivity inversely to theaverage UVB-irradiance to which the species is exposed in the ﬁeld [Carman et al.,
2000; Ferguson et al., 2005]. Animals from high UVB zones may require high levels
in captivity to avoid vitamin D deﬁciency. Study of more species is warranted to test
the generality of this relationship.
(6) What are the optimum levels of vitamin D condition for proper health andreproduction of the animal? In a study of panther chameleons [Ferguson et al., 2002],
neonate females were raised through maturity and reproduction under different
enforced daily UVB levels. Their reproductive success was measured in terms of thenumber of second-generation hatchlings produced. An optimum dose withmaximum success was determined above or below which reproductive success was
lower. In the absence of these labor-intensive studies, matching the captive levels of
circulating vitamin D and calcidiol to those in wild breeding animals can be an
estimate of optimum levels. This, of course, assumes that ﬁeld levels are always
optimal.

CONCLUSIONS
1. North American and Jamaican squamate reptiles occupied habitats consisting offour zones of voluntary UVB exposure, ranging from a median UV exposureindex of 0.35–3.1.
2. Exposure levels vary signiﬁcantly throughout the day and across seasons, so
future studies should encompass the entire day and all seasons to gain a more
complete understanding of typical exposure for a target species.
3. Environmental and body temperatures inﬂuence exposure to the sun andexposure to UVB. Thermoregulation may constrain exposure to the sun andUVB when environmental temperatures exceed optimal temperature.
4. From these data zoo keepers and herpetoculturists can estimate optimum medianand maximum exposure levels for enclosures of captive species whose naturallight habitat is known or can be surmised. When Solartech 6.4 or 6.5 UVB meters
are used, identical readings from the sun and an artiﬁcial UVB source, whose
SPD is similar to that of the sun in the UVB range, at a given distance indicatethat a similar rate of photobiosynthesis of Vitamin D3 may be expected from thesunlight and from that lamp at that particular distance.
5. Because animals may be able to regulate their exposure to UVB, we recommendthat keepers maintain animals with a UVB gradient from the maximum levels
ascertained in this study to a zero UVB-refuge and watch their animals todetermine how they use the gradient. If they expose themselves continuously, themaximum level might be adjusted upward gradually by moving the source closer
or using a stronger UVB source, but care should be taken to not set maximum
levels unnaturally high. If the animals avoid the UVB source or continuously use
the refuge, the maximum available level of UVB should be lowered or the source

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332 Ferguson et al.

turned off temporarily to see whether the animal starts leaving the refuge in
response to lower UVB. Visible light levels and temperatures near the source
should also be evaluated.
6. Optimal dietary vitamin D3 levels are unknown for any lizard or snake species. If
supplemental dietary vitamin D3 is offered when adequate UVB lighting is used,levels of vitamin D should not exceed those currently reported from the intestinal
contents of wild diurnal insectivorous lizards (about 1–2 IU/g of food/day).
7. Several experimental approaches to better understand UVB and vitamin D
requirements of lizards and snakes are suggested when time, space, money, animalcare regulations, and manpower permit.
ACKNOWLEDGMENTS
We thank ofﬁcials and personnel associated with the following establishmentsfor permission to conduct ﬁeld activities on property under their supervision:
The Hofstra University Marine Station, Texas Parks and Wildlife, Old Sabine
Wildlife Management Area, Monahans State Park, Kisatchee National Forest,
Rita Blanca National Grassland, Lassen Volcanic National Park. We thankGlenn Kroh and John Pinder for help and logistic support in the ﬁeld at Lassen
Volcanic National Park and other locations in the Western United States.
Numerous other people helped to collect data, including Adam Kingeter, Kaydee
Doss, Jeff LeVan, Brian Rogers, and Cameron Pool. We thank Neil Ford for his
help in arranging access to the Old Sabine Wildlife Management Area and John
Horner for his help in arranging access to the Kisatchee National Forest. We thankthe Fort Worth Zoo for the use of light sources for parts of the study. Partial funding
for the research was from a grant from the Eppley Foundation to GWF. Allprocedures were approved by the Institutional Animal Care and Use Commitee at
TCU.
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