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NOTE / NOTE
Minimal overwintering temperatures of red-sided
garter snakes (Thamnophis sirtalis parietalis): a
possible cue for emergence?
Deborah I. Lutterschmidt, Michael P. LeMaster, and Robert T. Mason
Abstract: Red-sided garter snakes (Thamnophis sirtalis parietalis (Say in James, 1823)) in Manitoba, Canada, undergo
8 months of continuous winter dormancy prior to spring emergence. As in other ectothermic species, increases in ground
temperature may be the cue for emergence from winter dormancy in these populations. To test this hypothesis, we meas-
ured body temperatures during winter dormancy by surgically implanting small temperature loggers into 32 female red-
sided garter snakes before they entered their native hibernaculum. The following spring, we recaptured seven of the snakes
implanted with temperature loggers. Body temperature declined gradually from mid-September (14.7 ± 0.24 8C, mean ±
SE) to early April (1.1 ± 0.16 8C, mean ± SE) during winter dormancy, reaching minimal values approximately 1 month
prior to spring emergence. Body temperatures of emerging snakes ranged from 0.5 8C during early spring to 6.3 8C during
late spring (3.4 ± 0.84 8C, mean ± SE). These results do not support the hypothesis that an increase in ground temperature
(and hence body temperature) is necessary for emergence from winter dormancy. We suggest that critically low tempera-
tures (i.e., 0.5–1 8C) are a Zeitgeber entraining an endogenous circannual cycle that regulates snake emergence. These re-
sults offer new insight into the mechanisms regulating seasonal emergence from winter dormancy.
Re
´sume
´:Les couleuvres raye
´es a
`flancs rouges (Thamnophis sirtalis parietalis (Say in James, 1823)) du Manitoba, Can-
ada, comple
`tent 8 mois continus de dormance d’hiver avant leur e
´mergence au printemps. Comme c’est le cas chez
d’autres espe
`ces ectothermes, l’accroissement de la tempe
´rature du sol est peut-e
ˆtre le signal pour l’e
´mergence de la dorm-
ance hivernale chez ces populations. Afin de ve
´rifier cette hypothe
`se, nous avons mesure
´la tempe
´rature corporelle de 32
couleuvres raye
´es a
`flancs rouges femelles durant la dormance d’hiver en leur inse
´rant par chirurgie de petits enregistreurs
de tempe
´rature avant qu’elles n’entrent dans leurs hibernacles d’origine. Le printemps suivant, nous avons re
´cupe
´re
´sept
des couleuvres porteuses d’enregistreurs de tempe
´rature. La tempe
´rature corporelle de
´cline graduellement de la mi-septembre
(14,7 ± 0,24 8C, moyenne ± erreur type) au de
´but d’avril (1,1 ± 0,16 8C, moyenne ± erreur type) durant la dormance
d’hiver, atteignant un minimum environ un mois avant l’e
´mergence printanie
`re. La tempe
´rature corporelle des couleu-
vres a
`l’e
´mergence varie de 0,5 8Caude
´but du printemps a
`6,3 8Ca
`la fin du printemps (3,4 ± 0,84 8C, moyenne ±
erreur type). Ces re
´sultats n’appuient pas l’hypothe
`se qui veut qu’un accroissement de la tempe
´rature du sol (et par
conse
´quent de la tempe
´rature corporelle) soit ne
´cessaire pour l’e
´mergence de la dormance d’hiver. Nous croyons que
les tempe
´ratures basses critiques (c.-a
`-d., 0,5–1 8C) agissent comme Zeitgeber pour e
´tablir un cycle circannuel qui re
`-
gle l’e
´mergence des couleuvres. Ces re
´sultats ouvrent de nouvelles perspectives sur les me
´canismes re
´gulateurs de
l’e
´mergence saisonnie
`re de la dormance d’hiver.
[Traduit par la Re
´daction]
Introduction
Most vertebrates exhibit some seasonality in many behav-
ioral and physiological processes. One of the most reliable
environmental cues thought to function in regulating season-
ality in vertebrates is photoperiod. Unlike other environmen-
tal signals (e.g., temperature and humidity) that can vary
quite dramatically both within seasons and among years,
changes in photoperiod length accurately and reliably reflect
changing environmental seasons. Many ectotherms inhabit-
ing north-temperate climates, however, undergo periods of
prolonged winter dormancy prior to spring breeding. Animals
that occupy underground hibernacula during winter dor-
mancy are not exposed, or receive little exposure, to chang-
ing photoperiodic conditions (e.g., Whittier et al. 1987;
Grobman 1990). Thus, photoperiod is likely not a critical
Received 10 November 2005. Accepted 2 March 2006. Published on the NRC Research Press Web site at http://cjz.nrc.ca on 6 June
2006.
D.I. Lutterschmidt1and R.T. Mason. Department of Zoology, Oregon State University, Corvallis, OR 97331, USA.
M.P. LeMaster. Department of Biology, Western Oregon University, Monmouth, OR 97361, USA.
1Corresponding author (e-mail: luttersd@science.oregonstate.edu).
771
Can. J. Zool. 84: 771–777 (2006) doi:10.1139/Z06-043 #2006 NRC Canada
factor in synchronizing spring emergence from overwinter-
ing locations. For example, photoperiod prior to and during
winter dormancy has no influence on the initiation and
timing of reproductive behavior of red-sided garter snakes
(Thamnophis sirtalis parietalis (Say in James, 1823)) upon
spring emergence (Nelson et al. 1987; Whittier et al.
1987). Rather, temperature appears to be the most impor-
tant environmental cue for synchronizing reproduction in
reptiles (Licht 1972, 1984; Duvall et al. 1982; Whittier et
al. 1987).
In some ectothermic species, increases in ambient and
ground temperatures during spring are thought to play a
role in initiating emergence from winter dormancy and sub-
sequent reproductive behavior (e.g., Hawley and Aleksiuk
1975, 1976; Jacob and Painter 1980; Crews and Garstka
1982; Licht 1984; Whittier et al. 1987; Macartney et al.
1989; Crawford 1991). For example, emergence from winter
dormancy in the box turtles Terrapene carolina (L., 1758)
and Terrapene ornata (Agassiz, 1857) occurs after subsur-
face ground temperatures increase for several consecutive
days (Grobman 1990). Emergence of northern Pacific rattle-
snakes (Crotalus oreganus oreganus (Holbrook, 1840)) also
occurs as hibernaculum temperatures increase (Macartney et
al. 1989). Etheridge et al. (1983) demonstrated experimentally
that increasing ambient temperatures stimulate emergence
of the six-lined racerunner (Cnemidophorus sexlineatus (L.,
1766)) from winter dormancy. However, some ectothermic
species (especially those inhabiting extreme northern lati-
tudes) can occupy underground dens at depths where
ground temperatures do not change significantly prior to
spring emergence (e.g., Macartney et al. 1989), suggesting
that increases in ground temperatures may not be the only
thermal cue used by reptiles.
To better understand the environmental cues regulating
spring emergence and reproduction in reptiles, we measured
body temperatures of red-sided garter snakes during winter
dormancy under natural field conditions. Red-sided garter
snakes are the most northerly living reptile in North Amer-
ica and are found in extremely large numbers throughout
south-central Manitoba, Canada. These northern-latitude
populations of snakes undergo a period of continuous winter
dormancy for approximately 8 months each year. Following
spring emergence, an attenuated mating season lasting ap-
proximately 4–5 weeks is initiated (e.g., Crews and Garstka
1982). In this well-studied dissociated breeder, mating be-
havior is triggered by increases in environmental tempera-
tures following winter dormancy (Ross and Crews 1978;
Garstka et al. 1982; Bona-Gallo and Licht 1983; Krohmer
and Crews 1987; Whittier et al. 1987).
Given the unique life history traits of these snake popula-
tions, temperature is likely the most important proximate en-
vironmental cue governing the initiation of emergence from
winter dormancy. Previous studies investigating the role of
temperature in regulating spring emergence in red-sided gar-
ter snakes were conducted in the laboratory (e.g., Bona-
Gallo and Licht 1983; Krohmer and Crews 1987; Whittier
et al. 1987). Furthermore, these studies focused on the role
of temperature in initiating reproductive behavior, as it is a
more conspicuous end point to measure. There are limited
data regarding overwintering temperatures of ectotherms
under natural field conditions, especially in northern lati-
tudes. In addition, few field studies have focused on the
thermal cues regulating spring emergence. We examined the
efficacy of temperature as an important cue for synchroniz-
ing spring emergence under natural field conditions. Specif-
ically, we sought to determine if hibernaculum temperatures
(and hence snake body temperatures) increase significantly
prior to emergence from winter dormancy. Because the ini-
tiation of spring emergence of red-sided garter snakes is in-
dependent of changes in photoperiodic conditions (Nelson et
al.1987; Whittier et al.1987), this model system provides an
excellent opportunity to examine the role of temperature as
the primary environmental cue synchronizing emergence
from prolonged winter dormancy.
Materials and methods
Experiments were conducted in the field with free-ranging
red-sided garter snakes in the Interlake region of Manitoba,
Canada (50830’N, 97830’W). All experimental protocols
were approved by the Oregon State University Animal Care
and Use Committee (protocol No. 2661) and were in accord-
ance with the Guide for the Care and Use of Laboratory An-
imals (National Institutes of Health 1985). This research was
approved by the Manitoba Wildlife Animal Care Committee
(protocol No. 2002-06) and was performed under the author-
ity of Manitoba Wildlife scientific permit No. WSP 03009.
Similar to Grayson and Dorcas (2004) and Angilletta and
Krochmal (2003), we measured body temperatures of red-
sided garter snakes during winter dormancy by surgically
implanting snakes with small temperature loggers (Thermo-
chron iButton; Dallas Semiconductor, Dallas, Texas). Data
loggers were programmed to sample temperature once every
3 h using the 32-Bit iButton-TMEX Runtime Environment
software (Dallas Semiconductor, Dallas, Texas). This sam-
pling rate was used to ensure continuous recordings of body
temperatures throughout the 8-month dormancy period (i.e.,
for approximately 256 days). The sampling times of all data
loggers were synchronized so that body temperatures of in-
dividual snakes were recorded at the same time of day.
Thirty-two female red-sided garter snakes having a snout–
vent length ‡62 cm (71.2 ± 0.78 cm, mean ± SE) were col-
lected in the fall (9–15 September 2003) after snakes returned
to the den site to overwinter. Female snakes were used in
this study because of their much larger body size. Snakes
were anesthetized with sodium brevital (0.003 mL of 0.5%
(m/v) brevital/g body mass) and a temperature logger was
surgically implanted into the peritoneal cavity. Data log-
gers (17.4 mm diameter 5.7 mm height, 3.1 g) were
2.2% of the mean body mass of snakes (range = 2.8% of
the smallest snake to 1.4% of the largest snake) and pro-
duced a slight, noticeable bulge in the midbody area con-
taining the temperature logger. To aid in recapture of
female snakes during the spring when they are emerging
among thousands of garter snakes, we individually scale-
clipped each snake with a unique number and a silver se-
quin was secured to the parietal scales with glue. Snakes
were allowed to recover from surgery for 1–5 days before
being released at the site of capture, where they were al-
lowed to hibernate under natural conditions.
The following spring, we recaptured seven of the snakes
implanted with temperature loggers. We attribute this recap-
772 Can. J. Zool. Vol. 84, 2006
#2006 NRC Canada
ture rate to the difficulty of locating snakes among the ex-
tremely large numbers of snakes (~35 000; Shine et al.
2006) at this den site. Mortality may have contributed to re-
ducing the number of females recaptured, but mortality rates
of red-sided garter snakes during winter dormancy in the
field are unknown. All females were captured immediately
following emergence from the hibernaculum and the specific
time and date of capture were recorded for each snake. The
temperature loggers were surgically removed and the fe-
males were released at the site of capture following recov-
ery; data were downloaded for analysis. Only body
temperature data for snakes prior to complete emergence
were used in the analyses of winter dormancy temperatures.
Ground temperatures were measured during the period of
winter dormancy at six different soil depths (0, 0.3, 0.6, 0.9,
1.2, and 1.5 m) using Thermochron iButton temperature log-
gers. Data loggers were programmed to sample temperature
once every 3 h and synchronized with the data loggers re-
cording body temperatures of female snakes. To protect the
data loggers from groundwater during the observation pe-
riod, we sealed each iButton in a small balloon (not inflated)
before placement in the ground. Owing to the rocky terrain
at the den site and because the den site is located on public
property, ground temperatures were measured at the field
station approximately 20 km north of the den (50837’N,
97832’W). To aid in the retrieval of temperature loggers in
the spring, we first dug a hole 1.5 m deep by inserting a
metal cylinder into the ground. Temperature loggers were then
placed into the ground at 0.3 m intervals. To mimic the rocky
terrain at the den site, we used gravel to fill the spaces be-
tween data loggers and placed rocks over the site. Mean high
and low ambient temperatures during September 2003
through May 2004 were obtained for a nearby area (Lundar,
Manitoba; 50843’N, 97851’W) from Environment Canada.
All data are reported as means ± SE, unless otherwise in-
dicated.
Results
Body temperatures of female red-sided garter snakes de-
clined gradually from mid-September (14.7 ± 0.24 8C) to
early April (1.1 ± 0.16 8C) during the 8-month dormancy
period (Fig. 1). Body temperatures did not reach minimal
values until April, approximately 1 month prior to the begin-
ning of spring emergence. Mean body temperature of snakes
1 week prior to emergence was 2.6 ± 0.39 8C. Mean body
temperature of snakes 1 day prior to emergence was 3.4 ±
0.84 8C. Because female garter snakes emerge over the en-
tire 4-week mating season, mean body temperature 1 day
prior to emergence ranged from 0.5 8C when snakes
emerged during early spring to 6.3 8C when snakes emerged
during late spring. Prehibernation body mass of snakes was
significantly higher than posthibernation body mass (P<
0.001 from a paired ttest; data not shown). The mean percent
body mass loss of female snakes during winter dormancy
was 10.4% ± 1.6%.
Mean high ambient temperatures were below 0 8C from
late October through late March (Fig. 2). Although the
underground hibernaculum protected snakes from ambient
temperatures, snakes could only escape freezing tempera-
tures at a depth of 1.2 m or greater (Fig. 3). Groundwater
was observed at soil depths of 1.2 and 1.5 m during retrieval
of the ground temperature dataloggers. During the period of
spring emergence (i.e., from 29 April to 22 May, weeks 34–
37 of winter dormancy), ground temperatures at depths of
1.2 and 1.5 m increased by only 3.0 and 2.5 8C, respectively
(Fig. 3).
Time (weeks in winter dormancy)
0 4 8 12 16 20 24 28 32 36 40
Body Temperature (ºC)
-2
0
2
4
6
8
10
12
14
16
18
20
22
Oct. Dec. Feb. Apr.
3
63
2
Fig. 1. Body temperatures of female red-sided garter snakes (Thamnophis sirtalis parietalis) during winter dormancy in dens under natural
field conditions in Manitoba, Canada. Unless otherwise noted by sample sizes above the SE bars, each data point is a weekly mean ± 1 SE
of 7 snakes.
Lutterschmidt et al. 773
#2006 NRC Canada
Discussion
Our results indicate that red-sided garter snakes near the
northern limit of this species’ range in Manitoba, Canada,
have a mean minimum body temperature of 1.1 ± 0.16 8C
during winter dormancy. This body temperature is much
lower than that estimated previously for these populations of
snakes during hibernation (i.e., 3–6 8C; Whittier et al. 1987).
The range of body temperatures that we observed during
winter dormancy is similar to that reported by Macartney
et al. (1989), who measured body temperatures of red-
sided garter snakes in a communal den in northern Alberta,
Canada. However, owing to the failure of the radioteleme-
try equipment, body temperatures of only one red-sided
garter snake could be monitored (Macartney et al. 1989).
The mean body temperature of this snake during hibernation
was 3.9 ± 0.34 8C (mean ± SE; n= 16 observations during
hibernation); body temperature ranged from 1.8 to 6.5 8C
(Macartney et al. 1989).
Body temperatures of snakes remained above 0 8C
throughout winter dormancy and were similar to ground
temperatures observed at a depth of 1.5 m from November
through late April (weeks 12–33; Fig. 4). These results
support previous findings that garter snakes cannot endure
prolonged freezing stress (reviewed in Storey and Storey
1992) and instead seek thermally buffered hibernaculum
sites. It is evident that ambient temperatures directly influ-
ence hibernaculum temperatures during the dormancy period,
especially at shallower hibernaculum depths (Figs. 2, 3).
Ground temperature measurements indicate that snakes
must have moved to a depth of at least 1.2 m below the den
surface to escape freezing temperatures (Fig. 3). At depths
of 1.2 and 1.5 m, ground temperatures decreased gradually
but were fairly stable during the period of winter dor-
mancy; ground temperatures at these soil depths increased
no more than 3 8C during the period of spring emergence
(weeks 34–37; Fig. 3).
An increase in hibernaculum temperatures could poten-
tially be a cue for emergence, but the underlying mechanism
must be sensitive to very small changes in temperature (i.e.,
2.5–3.0 8C) over a period of <1 month. Similar patterns of
spring emergence have been observed in the box turtles T.
carolina and T. ornata (Grobman 1990). Spring emergence
(and subsequent reproductive behavior) of red-sided garter
snakes may be controlled by an endogenous circannual
rhythm that is entrained by the slight increase in ground
temperatures observed during this study (e.g., Licht 1972;
Gregory 1982).
In contrast, some snakes were observed to emerge from
the hibernaculum without a significant increase in body tem-
perature. These results therefore do not support the hypothe-
sis that an increase in ground temperature (and therefore
body temperature) is a necessary cue for emergence from
winter dormancy. For example, during early to mid-May,
two snakes emerged at a body temperature of only 0.5 8C.
These observations are similar to those reported by Macart-
ney et al. (1989), who also observed cloacal temperatures as
low as 0.5 8C in emerging garter snakes. In late May, how-
ever, body temperatures of emerging snakes were as high as
6.3 8C. This higher body temperature at emergence is likely
attributable to the higher ground temperatures experienced at
the hibernaculum surface as snakes emerged later in the sea-
son (Fig. 3). During the period of spring emergence (May,
weeks 34–37), ground temperatures at depths of 1.2 and
1.5 m did not increase above 4 8C. Thus, snakes (i.e., ecto-
therms) with body temperatures higher than 4 8C prior to
Time (weeks)
0 4 8 1216202428323640
-40
-20
0
20
High temperature
Low temperature
Ambient Temperature (ºC)
Oct. Dec. Feb. Apr.
Fig. 2. Mean high and low ambient temperatures from September 2003 to May 2004 (i.e., during the dormancy period of red-sided garter
snakes). Data were obtained for a nearby area from Environment Canada. Each data point is a weekly mean ± 1 SE.
774 Can. J. Zool. Vol. 84, 2006
#2006 NRC Canada
complete emergence must have been occupying shallower
locations within the hibernaculum, and therefore were likely
already in the process of emergence. (Although ground tem-
peratures were recorded at a site approximately 20 km north
of the den, we presume that ground temperatures do not dif-
fer greatly between these sites.) We currently have no way
of estimating the time required for a snake to make its jour-
ney from the location of winter dormancy within the hiber-
naculum to the surface of the den. We hypothesize that the
time required for complete emergence is highly variable
among snakes and depends upon the position of each snake
within the hibernaculum, as entrances into the den and the
den itself are composed of narrow, rocky tunnels. Indeed,
early versus late emergence from hibernacula has been
correlated with snake depth in other studies (e.g., Carpenter
1953). Thus, increases in body temperature prior to emer-
Time (weeks)
0 4 8 12 16 20 24 28 32 36 40
Ground Temperature (ºC)
-8
-4
0
4
8
12
1.5 m
1.2 m
0.9 m
0.6 m
0.3 m
0m
Oct. Dec. Feb. Apr.
Fig. 3. Ground temperatures during the dormancy period of red-sided garter snakes at six different soil depths (0, 0.3, 0.6, 0.9, 1.2, and
1.5 m). Temperatures were measured at a site near the snake hibernaculum. Each data point is a weekly mean ± 1 SE.
Time (weeks in winter dormancy)
0 4 8 1216202428323640
Temperature (ºC)
-2
0
2
4
6
8
10
12
14
16
18
20
22
Ground temperature at a depth of 1.2 m
Ground temperature at a depth of 1.5 m
Body temperature of female snakes
3
63
2
Oct. Dec. Feb. Apr.
Fig. 4. Body temperatures of red-sided garter snakes during winter dormancy shown with ground temperatures at depths of 1.2 and 1.5 m.
Unless otherwise noted by sample sizes above the SE bars, each data point for body temperature is a weekly mean ± 1 SE of 7 snakes;
ground temperatures are a weekly mean ± 1 SE.
Lutterschmidt et al. 775
#2006 NRC Canada
gence (especially increases above ground temperatures at
depths of 1.2 and 1.5 m) most likely reflect the vertical
migration of snakes to the surface of the hibernaculum.
We speculate that critically low temperatures (i.e., 0.5–
18C) may play a role in initiating snake emergence. For ex-
ample, mean snake body temperatures were similar to those
temperatures observed at a depth of 1.5 m from November
through late April (from weeks 12–33; Fig. 4). However,
the mean body temperature of snakes increased more rapidly
than ground temperatures at this depth (Fig. 4), suggesting
that snakes were vertically migrating to the surface of the
hibernaculum during weeks 34–37 of winter dormancy.
However, it again must be noted that ground temperatures
were recorded at a site away from the hibernaculum. These
observations suggest that when snakes reach a critical mini-
mum temperature, they may be stimulated to change their
vertical position in the den. Such critically low temperatures
(and (or) the duration of exposure to low temperatures) may
act as a Zeitgeber entraining an endogenous circannual cycle
that governs spring emergence from winter dormancy.
There is precedence for vertical migration within hiberna-
cula during winter dormancy in other ectothermic species.
Sexton and Marion (1981) demonstrated that emergence of
prairie rattlesnakes (Crotalus viridis (Rafinesque, 1818))
from winter hibernacula is regulated by a reversing thermal
gradient within natural dens. In northern latitudes, where
ambient temperatures can be below freezing during much of
the winter, hibernating ectotherms select the warmest por-
tion of the naturally occurring thermal gradient in the hiber-
naculum (Sexton and Marion 1981). Thus, in the early
stages of winter dormancy, the cooling of the hibernaculum
surface stimulates animals to migrate farther into the den.
Vertical migration to the surface of the den occurs during
the spring, when surface temperatures warm more quickly
then the lower portions of the hibernaculum (e.g., Sexton
and Marion 1981; Etheridge et al. 1983; Grobman 1990).
It is unlikely that the vertical migration of red-sided garter
snakes within the den results from active behavioral thermo-
regulation, as snakes can emerge from winter dormancy at
body temperatures of only 0.5 8C (Macartney et al. 1989;
this study). Rather, vertical migration within and emergence
from hibernacula may be regulated by a circannual cycle
that is influenced by low temperatures. Because of the ex-
treme environmental constraints on survival and reproduc-
tion in these northern populations of garter snakes, it is
likely that a very sensitive mechanism regulating spring
emergence has evolved in these populations.
Further research is necessary to determine the temperature
threshold as well as the role of other environmental cues
(e.g., humidity) in initiating vertical migration within and
emergence from hibernacula. Studies of the spatial and tem-
poral distribution of snakes in hibernacula, perhaps via arti-
ficial dens, would be particularly informative about the role
of minimal overwintering temperatures in spring emergence.
We are currently investigating how temperature cues interact
with circadian and circannual hormone cycles to regulate
spring emergence and reproductive behavior. Because male
and female red-sided garter snakes demonstrate differential
timing of emergence from winter dormancy, future studies
examining possible sex differences in the mechanisms regu-
lating spring emergence are needed. Such studies would pro-
vide much insight into the circannual rhythms and
environmental cues regulating seasonality in ectothermic
vertebrates.
Acknowledgments
We thank the Manitoba Department of Conservation and
Dave Roberts for technical assistance; Al and Gerry Johnson
for support and encouragement; Stevan J. Arnold, Arianne J.
Cease, Suzanne R. Estes, Amanda Lane, Ruth Nesbitt, Rick
Shine, Jonno K. Webb, and Michael Westphal for their as-
sistance in recapturing snakes during spring emergence;
William I. Lutterschmidt, Eric D. Roth, and Rick Shine for
their helpful advice regarding the logistics of this study; and
William I. Lutterschmidt and two anonymous reviewers for
their critical review of the manuscript. This work was sup-
ported in part by a P.O.E. Scholar Award to D.I.L.
References
Angilletta, M.J., and Krochmal, A.R. 2003. The thermochron: a
truly miniature and inexpensive termpature-logger. Herpetol.
Rev. 34: 31–32.
Bona-Gallo, A., and Licht, P. 1983. Effect of temperature on sexual
receptivity and ovarian recrudescence in the garter snake, Tham-
nophis sirtalis parietalis. Herpetologica, 39: 173–182.
Carpenter, C.C. 1953. A study of hibernacula and hibernating asso-
ciations of snakes and amphibians in Michigan. Ecology, 34: 74–
80.
Crawford, K.M. 1991. The winter environment of painted turtles,
Chrysemys picta: temperature, dissolved oxygen, and potential
cues for emergence. Can. J. Zool. 69: 2493–2498.
Crews, D., and Garstka, W.R. 1982. The ecological physiology of
reproduction in the garter snake. Sci. Am. 247: 158–168.
Duvall, D., Guillete, L.J., Jr., and Jones, R.E. 1982. Environmental
control of reptilian reproductive cycles. In Biology of the repti-
lian. Vol. 13. Edited by C. Gans and F.H. Pough. Academic
Press, London. pp. 201–231.
Etheridge, K., Wit, L.C., and Sellers, J.C. 1983. Hibernation in the
lizard Cnemidophorus sexlineatus (Lacertilia: Teiidae). Copeia,
1983: 206–214.
Garstka, W.R., Camazine, B., and Crews, D. 1982. Interactions of
behavior and physiology during the annual reproductive cycle of
the red-sided garter snake, Thamnophis sirtalis parietalis. Her-
petologica, 38: 104–123.
Grayson, K.L., and Dorcas, M.E. 2004. Seasonal temperature varia-
tion in the painted turtle (Chrysemys picta). Herpetologica, 60:
325–336.
Gregory, P.T. 1982. Reptilian hibernation. In Biology of the repti-
lian. Vol. 13. Edited by C. Gans and F.H. Pough. Academic
Press, London. pp. 53–154.
Grobman, A.B. 1990. The effect of soil temperatures on emergence
from hibernation of Terrapene carolina and T. ornata. Am.
Midl. Nat. 124: 366–371.
Hawley, A.W.L., and Aleksiuk, M. 1975. Thermal regulation of
spring mating behavior in the red-sided garter snake (Thamno-
phis sirtalis parietalis). Can. J. Zool. 53: 768–776.
Hawley, A.W.L., and Aleksiuk, M. 1976. The influence of photo-
period and temperature on seasonal testicular recrudescence in
the red-sided garter snake (Thamnophis sirtalis parietalis).
Comp. Biochem. Physiol. A, 53: 215–221. doi:10.1016/S0300-
9629(76)80058-8. PMID: 2423.
Jacob, S.J., and Painter, C.W. 1980. Overwinter thermal ecology of
Crotalus viridis in the north-central plains of New Mexico. Co-
peia, 1980: 799–805.
776 Can. J. Zool. Vol. 84, 2006
#2006 NRC Canada
Krohmer, R.W., and Crews, D. 1987. Temperature activation of
courtship behavior in the male red-sided garter snake (Thamno-
phis sirtalis parietalis): Role of the anterior hypothalamus-pre-
optic area. Behav. Neurosci. 101: 228–236. doi:10.1037/0735-
7044.101.2.228. PMID: 3580125.
Licht, P. 1972. Environmental physiology of reptilian breeding cy-
cles: Role of temperature. Gen. Comp. Endocrinol. 3(Suppl.):
477–488. doi:10.1016/0016-6480(72)90178-5.
Licht, P. 1984. Seasonal cycles in reptilian reproductive physiol-
ogy. In Marshall’s physiology of reproduction. Edited by E.
Lamming. Churchill Livingstone, Edinburgh, UK. pp. 206–282.
Macartney, J.M., Larsen, K.W., and Gregory, P.T. 1989. Body tem-
peratures and movements of hibernating snakes (Crotalus and
Thamnophis) and thermal gradients of natural hibernacula. Can.
J. Zool. 67: 108–114.
National Institutes of Health. 1985. Guide for care and use of la-
boratory animals. National Institutes of Health, Bethesda, Md.
NIH Publ. No. 85-23.
Nelson, R.J., Mason, R.T., Krohmer, R.W., and Crews, D. 1987.
Pinealectomy blocks vernal courtship behavior in red-sided gar-
ter snakes. Physiol. Behav. 39: 231–233. doi:10.1016/0031-
9384(87)90014-X. PMID: 3575458.
Ross, P., Jr., and Crews, D. 1978. Stimuli influencing mating beha-
vior in the garter snake, Thamnophis radix. Behav. Ecol. Socio-
biol. 4: 133–142. doi:10.1007/BF00354976.
Sexton, O.W., and Marion, K.R. 1981. Experimental analysis of
movements by prairie rattlesnakes, Crotalus viridis, during hiber-
nation. Oecologia (Berl.), 51: 37–41. doi:10.1007/BF00344649.
Shine, R., Langkilde, T., Wall, M., and Mason, R.T. 2006. Tem-
poral dynamics of emergence and dispersal of garter snakes
from a communal den in Manitoba. Wildl. Res. 33: 103–111.
Storey, K.B., and Storey, J.M. 1992. Natural freeze tolerance in ec-
tothermic vertebrates. Annu. Rev. Physiol. 54: 619–637. doi:10.
1146/annurev.ph.54.030192.003155. PMID: 1562185.
Whittier, J.M., Mason, R.T., Crews, D., and Licht, P. 1987. Role of
light and temperature in the regulation of reproduction in the
red-sided garter snake, Thamnophis sirtalis parietalis. Can. J.
Zool. 65: 2090–2096.
Lutterschmidt et al. 777
#2006 NRC Canada
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