Comparison of Body Temperatures across Physiological States in Syntopic Snake Species (Thamnophis sirtalis and Nerodia sipedon) from Pennsylvania

Abstract

Physiological states in snakes, such as digestion, gestation, and ecdysis, have been associated with different body temperatures (BT), yet few studies have examined these associations in a comparative context for wild-caught animals. We collected body and environmental temperatures for 2 natricine snake species—Thamnophis sirtalis (Common Gartersnake) and Nerodia sipedon (Common Watersnake)—from 4 artificial wetlands at the Letterkenny Army Depot, Franklin County, PA. We measured thermal data and associated microclimates from snakes captured under tin cover boards during monthly searches from Spring to Fall of 2012 (April–October). From 47 Common Gartersnakes and 20 Common Watersnakes, we found that most individuals of both species had a BT between 20 and 30 °C, which is consistent with data from other populations. Inter- and intraspecific comparisons of snake BTs in different physiological states revealed that Common Gartersnakes operated at higher temperatures than Common Watersnakes. Common Watersnakes thermoregulated within a generally narrower range of temperatures than Common Gartersnakes. The wide-ranging thermal ecology of the Common Gartersnake may facilitate its flexibility to occupy many habitats across an extensive geographic distribution and perhaps predispose it to greater adaptability in a changing thermal environment. We summarize our data on snake BTs and their associations with relevant environmental temperatures, discuss snake BT ranges across distinct physiological groups, and compare our results to those of other snake populations. Our findings provide a baseline to understand the degree to which operating snake temperatures, and consequently physiological processes, will change because of future warming in the Northeast.

Full text

Northeastern Naturalist Vol. 26, No. 4
D.F. Hughes, P.R. Delis, and W.E. Meshaka Jr
2019
749
NORTHEASTERN NATURALIST
2019 26(4):749–760
Comparison of Body Temperatures Across Physiological
States in Syntopic Snake Species (Thamnophis sirtalis and
Nerodia sipedon) from Pennsylvania
Daniel F. Hughes1,2, Pablo R. Delis2, and Walter E. Meshaka Jr.3
Abstract - Physiological states in snakes, such as digestion, gestation, and ecdysis, have
been associated with different body temperatures (BT), yet few studies have examined
these associations in a comparative context for wild-caught animals. We collected body and
environmental temperatures for 2 natricine snake species—Thamnophis sirtalis (Common
Gartersnake) and Nerodia sipedon (Common Watersnake)—from 4 articial wetlands at the
Letterkenny Army Depot, Franklin County, PA. We measured thermal data and associated
microclimates from snakes captured under tin cover boards during monthly searches from
Spring to Fall of 2012 (April–October). From 47 Common Gartersnakes and 20 Common
Watersnakes, we found that most individuals of both species had a BT between 20 and
30 °C, which is consistent with data from other populations. Inter- and intraspecic com-
parisons of snake BTs in different physiological states revealed that Common Gartersnakes
operated at higher temperatures than Common Watersnakes. Common Watersnakes thermo-
regulated within a generally narrower range of temperatures than Common Gartersnakes.
The wide-ranging thermal ecology of the Common Gartersnake may facilitate its exibility
to occupy many habitats across an extensive geographic distribution and perhaps predispose
it to greater adaptability in a changing thermal environment. We summarize our data on
snake BTs and their associations with relevant environmental temperatures, discuss snake
BT ranges across distinct physiological groups, and compare our results to those of other
snake populations. Our ndings provide a baseline to understand the degree to which oper-
ating snake temperatures, and consequently physiological processes, will change because
of future warming in the Northeast.
Introduction
Differences in temperature affect all aspects of life for snakes, especially their
behavior, physiology, and reproduction (Hertz et al. 1993). When environmental
temperatures (ET) are extreme, snakes can control their body temperature (BT)
through behavior and thereby avoid unfavorable temperatures or potentially dam-
aging thermal conditions (Lillywhite 2001). Snakes actively maintain their BT
within suitable physiological limits, and the span of measured BTs achievable by
snakes in the eld under various climatic conditions is known as operating body
temperature (OBT). As per Ernst et al. (2014), OBT is strictly a eld measurement
of BTs and is not equivalent to preferred body temperature, which is determined
1Department of Animal Sciences and Department of Agriculture and Biological Engineer-
ing, University of Illinois at Urbana-Champaign, 1304 West Pennsylvania Avenue, Urbana,
IL 61801. 2Department of Biology, Shippensburg University, 1871 Old Main Drive, Ship-
pensburg, PA 17257. 3Section of Zoology and Botany, State Museum of Pennsylvania, 300
North Street, Harrisburg, PA 17120. *Corresponding author - dfhughes@illinois.edu.
Manuscript Editor: Todd Rimkus
Downloaded From: https://bioone.org/journals/Northeastern-Naturalist on 04 Nov 2019
Terms of Use: https://bioone.org/terms-of-useAccess provided by University of Illinois at Urbana-Champaign

Northeastern Naturalist
750
D.F. Hughes, P.R. Delis, and W.E. Meshaka Jr
2019 Vol. 26, No. 4
experimentally by exposing snakes to a thermal gradient in the laboratory (e.g.,
Kitchell 1969). Field-based thermal data on the occurrences of BTs that snakes
achieve under different climatic conditions can help to elucidate the relationship
between ET and snake ecology at a site, assess how snake species respond to geo-
graphic temperature gradients, and predict how future changes in ET may affect
snake BTs.
Reports with thermal information for North American snake species are com-
mon (Brattstrom 1965, Ernst and Ernst 2003, Peterson 1987). However, far fewer
studies explore thermal data across different life stages, sexes, and physiological
conditions within and between species at a single study site, with some notable
exceptions (Carpenter 1956, Elick et al. 1980, Ernst et al. 2014, Fitch 1956). We
set out to document the variation in OBT of 2 snake species while under tin cover
at articial wetlands in the northeastern United States. Our goals were threefold:
to understand (1) whether syntopic snake species, with known ecological differ-
ences, exhibit similar variation in BT across sexes, size classes, and microhabitats;
(2) whether differences in physiological state had any inuence on measured BTs
intra- and interspecically; and (3) how our thermal data t within the thermal biol-
ogy of populations in other regions of the United States.
Materials and Methods
In March of 2012, we deployed 54 corrugated tin sheets (dimensions: 2 m x 1 m)
at 4 articial wetlands in Zone I—an active test area—of Letterkenny Army Depot
(LEAD), a military base in Chambersburg, Franklin County, south-central Pennsyl-
vania. We varied the distance of cover boards from the edge of the water—either
offshore (2 m away) or upland (10 m away)—to determine the extent that selected
microhabitats affected snake BTs. We applied this board arrangement in an alternat-
ing manner at each wetland, which resulted in 26 boards placed offshore and 28 in
upland areas. We checked cover boards for snakes each month from April to Octo-
ber of 2012. We also conducted 2 opportunistic surveys—checking under boards,
inspecting natural hiding places, and capturing active snakes—in September and
October for a total of 9 site visits. More details regarding the study site in Zone I
of LEAD are described in Hughes et al. (2018), including information on the focal
ponds, deployment of cover boards, snake species composition, and seasonal activ-
ity of the snake assemblage. See Delis et al. (2010) and Meshaka and Delis (2014)
for descriptions of the herpetofaunal community and long-term trends in the snake
populations of Zone II, the natural buffer area for Zone I.
We measured various temperatures associated with captured snakes and their
immediate environment. We recorded the internal BT of snakes directly after cap-
ture with a Fluke 51II Thermometer to the nearest 0.1 °C, where the temperature
bulb was inserted 1–2 cm into the cloaca until the values stabilized on the screen,
at which time the data were recorded. To minimize any potential heat transfer,
an effort was made to handle the snakes as little as possible prior to recording
cloacal measurements. We measured snake BTs for neonates orally to minimize
potential damage. We measured soil-surface temperature (SST) and board-surface
Downloaded From: https://bioone.org/journals/Northeastern-Naturalist on 04 Nov 2019
Terms of Use: https://bioone.org/terms-of-useAccess provided by University of Illinois at Urbana-Champaign

Northeastern Naturalist Vol. 26, No. 4
D.F. Hughes, P.R. Delis, and W.E. Meshaka Jr
2019
751
temperature (BST) to the nearest 0.1 °C with a Pro Exotics PE-2 Infrared Ther-
mometer held ~0.3 m from the ground or board, respectively. We measured SST
from under cover boards at the approximate spot where the snake was found. We
downloaded air temperatures (AT) for 2012 from the National Oceanic and Atmo-
spheric Administration (NOAA) website for Chambersburg, PA, which is ~10 km
from LEAD (https://www.ncdc.noaa.gov/).
We collected morphometric and life-history data for each captured snake,
including body size as snout–vent length (SVL) measured to the nearest 0.1 cm
with a tape measure, sex determined by the presence of hemipenes in males, and
reproductive stage of females assessed by ventral palpation. We visually inspected
snakes for the presence of an external injury (either fresh or healing), checked
whether their eyes were cloudy indicating ecdysis, and gently palpated stomachs to
determine if a food item was recently eaten. We set the minimum body size (SVL)
at sexual maturity in Thamnophis sirtalis L. (Common Gartersnake) at 27 cm for
males and 36 cm for females and in Nerodia sipedon L. (Common Watersnake) at
32 cm for males and 51 cm for females (Hulse et al. 2001). For both species, as-
signment of young-of-the-year (YoY) was based on the average SVL of neonates
in Pennsylvania (20 cm; Hulse et al. 2001).
We used Excel 2016 (Microsoft Inc., Redmond, WA) and program R version
3.4.4 (R Core Team 2018) to calculate descriptive statistics and conduct statisti-
cal analyses, including tests for normal distribution, regression analyses, 2-sample
t-tests, and ANOVAs. All statistical analyses were characterized as signicant at
P < 0.05. We did not make adjustments for multiple comparisons because the data
derive from observations on nature (Rothman 1990).
Results
OBT
Most of the 47 Common Gartersnakes (77%) had BTs of 20–30 °C and nearly
45% were within a narrower span of 22–27 °C (Table 1). Most of the 20 Common
Watersnakes (85%) also had BTs of 20–30 °C and 60% were within a narrower span
of 22–27 °C (Table 2).
Digestion
Common Gartersnakes with a food bulge had a higher mean BT than those that
lacked a recent meal (t = -1.69, df = 45, P = 0.049; Fig. 1). The mean BT of Com-
mon Watersnakes with a food bulge was not different from those lacking a recent
meal (t = 0.57, df = 18, P = 0.29). Mean BT associated with a recent meal was
higher in Common Gartersnakes than Common Watersnakes undergoing the same
physiological challenge (t = -2.24, df = 15, P = 0.04).
Ecdysis
Common Gartersnakes with cloudy eyes—a sign ecdysis will occur soon—did
not have a different mean BT than those not in a visible stage of shedding (t = -1.11,
df = 45, P = 0.14; Fig. 1). The mean BT of Common Watersnakes with cloudy eyes
did not differ from those that lacked this obvious sign of ecdysis (t = -1.32, df = 18,
Downloaded From: https://bioone.org/journals/Northeastern-Naturalist on 04 Nov 2019
Terms of Use: https://bioone.org/terms-of-useAccess provided by University of Illinois at Urbana-Champaign

Northeastern Naturalist
752
D.F. Hughes, P.R. Delis, and W.E. Meshaka Jr
2019 Vol. 26, No. 4
Table 1. Cloacal body temperatures and environmental temperatures of Thamnophis sirtalis (Common Gartersnake) at Letterkenny Army Depot, Franklin
County, PA. BT = body temperature; BST = board-surface temperature; SST = soil-surface temperature. All temperatures in degrees celsius. Mean value
is followed by ± 1 standard deviation, min–max in parentheses, and sample size.
BT BST SST
Mean ± SE Min–max n Mean ± SE Min–max n Mean ± SE Min–max n
All 27.55 ± 3.67 19.7–36.6 47 25.85 ± 4.62 14.6–34.2 35 21.08 ± 4.44 14.3–30.6 35
Males 26.6 - 1 22.7 - 1 21.8 - 1
Females 26.92 ± 3.59 19.7–33.9 33 26.18 ± 3.95 16.1–33.4 22 21.34 ± 3.85 14.8–28.1 22
Juveniles 28.81 ± 3.31 26.1–36.6 9 23.21 ± 5.10 14.6–29.4 8 17.93 ± 4.24 14.3–26.1 8
Neonates 30.10 ± 4.61 24.6–35.6 4 30.10 ± 5.11 23.0–34.2 4 25.78 ± 4.57 19.8–30.6 4
Gravid females 25.96 ± 3.65 20.0–32.6 10 23.79 ± 1.55 21.6–26.6 7 18.83 ± 5.20 15.6–20.8 7
Non-gravid females 27.34 ± 3.57 19.7–33.9 23 27.30 ± 4.26 16.1–33.4 15 22.51 ± 4.00 14.8–28.1 15
In shed (cloudy eyes) 28.38 ± 4.06 22.5–36.6 16 26.77 ± 5.02 14.6–33.4 11 22.43 ± 4.47 14.8–27.6 11
Not shedding 27.10 ± 3.44 19.7–35.6 31 25.43 ± 4.47 16.1–34.2 24 20.46 ± 4.38 14.3–30.6 24
Food bulge present 29.25 ± 3.56 23.5–35.6 10 28.04 ± 5.02 21.6–34.2 9 22.79 ± 6.07 15.3–30.6 9
No food bulge 27.10 ± 3.61 19.7–36.6 37 25.09 ± 4.32 14.6–33.4 26 20.48 ± 3.69 14.3–27.6 26
Injured 27.30 ± 3.95 20.0–33.9 16 27.06 ± 4.06 22.6–33.4 11 22.18 ± 4.23 14.8–27.6 11
Uninjured 27.68 ± 3.58 19.7–36.6 31 25.30 ± 4.83 14.6–34.2 24 20.57 ± 4.53 14.3–30.6 24
Under cover <2 m to water 27.37 ± 3.66 22.5–35.6 20 25.61 ± 5.16 16.1–33.4 16 20.64 ± 4.99 14.8–28.1 16
Under cover >10 m to water 27.67 ± 4.04 19.7–36.6 20 25.92 ± 4.33 14.6–34.2 18 21.17 ± 3.95 14.3–30.6 18
Captured while moving 27.35 ± 3.07 23.9–32.6 6 - - - - - -
>36 cm in SVL 26.91 ± 3.54 19.7–33.9 34 26.03 ± 3.92 16.1–33.4 23 21.36 ± 3.76 14.8–28.1 23
<36 cm in SVL 29.21 ± 3.61 24.6–36.6 13 25.51 ± 5.91 14.6–34.2 12 20.54 ± 5.66 14.3–30.6 12
Captured before 1200 hr 27.36 ± 3.62 20.0–36.6 26 26.19 ± 3.98 16.1–34.2 23 21.98 ± 3.81 15.6–30.6 23
Captured after 1200 hr 27.78 ± 3.8 19.7–35.6 21 25.20 ± 5.79 14.6–33.4 12 19.34 ± 5.19 14.3–27.6 12
Spring (April–May) 27.43 ± 1.23 26.1–29.0 6 19.98 ± 3.04 14.6–21.6 5 15.10 ± 0.44 14.3–15.3 5
Summer (June–August) 28.42 ± 4.23 20.0–36.6 26 26.99 ± 4.30 16.1–34.2 23 22.31 ± 4.18 15.6–30.6 23
Autumn (September–October) 26.09 ± 2.83 19.7–30.3 15 26.30 ± 3.59 22.7–31.1 7 21.29 ± 3.42 14.8–25.1 7
Downloaded From: https://bioone.org/journals/Northeastern-Naturalist on 04 Nov 2019
Terms of Use: https://bioone.org/terms-of-useAccess provided by University of Illinois at Urbana-Champaign

Northeastern Naturalist Vol. 26, No. 4
D.F. Hughes, P.R. Delis, and W.E. Meshaka Jr
2019
753
Table 2. Cloacal body temperatures and environmental temperatures of Nerodia sipedon (Common Watersnake) at Letterkenny Army Depot, Franklin
County, PA. BT = body temperature; BST = board-surface temperature; SST = soil-surface temperature. All temperatures in degrees Celsius. Mean value
is followed by ± 1 standard deviation, range in parentheses, and sample size.
BT BST SST
Mean ± SE Min–max n Mean ± SE Min–max n Mean ± SE Min–max n
All 26.36 ± 3.57 20.2–34.6 20 26.28 ± 4.33 20.1–33.9 16 20.13 ± 4.05 12.8–26.1 16
Males 24.70 ± 2.15 22.5–26.8 3 24.40 - 1 20.00 - 1
Females 26.38 ± 4.22 20.2–34.6 9 26.09 ± 3.88 20.1–31.5 8 20.44 ± 4.33 12.8–26.1 8
Juveniles 27.06 ± 3.62 22.5–31.4 7 27.60 ± 5.32 21.8–33.9 6 20.30 ± 4.58 14.3–25.5 6
Neonates 26.3 - 1 21.80 - 1 17.00 - 1
Gravid females 26.80 ± 2.26 25.2–28.4 2 27.40 ± 3.54 24.9–29.9 2 20.35 ± 1.77 19.1–21.6 2
Non-gravid females 26.26 ± 4.77 20.2–34.6 7 25.65 ± 4.20 20.1–31.5 6 20.47 ± 5.06 12.8–26.1 6
In shed (cloudy eyes) 27.50 ± 3.68 22.6–34.6 9 27.88 ± 4.74 21.8–33.9 8 20.98 ± 4.37 14.3–26.1 8
Not shedding 25.40 ± 3.35 20.2–31.4 11 24.69 ± 3.45 20.1–29.9 8 19.29 ± 3.79 12.8–25.8 8
Food bulge present 25.73 ± 2.92 21.6–30.3 7 25.20 ± 4.99 21.8–33.9 5 19.70 ± 3.38 17.1–25.5 5
No food bulge 26.70 ± 3.94 20.2–34.6 13 26.77 ± 4.12 20.1–33.9 11 20.33 ± 4.46 12.8–26.1 11
Injured 28.26 ± 4.6 22.6–34.6 5 28.80 ± 4.32 23.8–33.9 5 21.32 ± 4.86 14.3–26.1 5
Uninjured 25.73 ± 3.09 20.2–31.4 15 25.14 ± 4.00 20.1–33.9 11 19.59 ± 3.76 12.8–25.8 11
Under cover <2 m to water 26.31 ± 3.77 20.2–34.6 18 26.59 ± 4.56 20.1–33.9 14 20.29 ± 4.32 12.8–26.1 14
Under cover >10 m to water 26.8 - 1 24.40 - 1 20 .00 - 1
Captured while moving - - - - - - - - -
>51 cm in SVL 24.24 ± 3.31 20.2–28.4 5 24.23 ± 4.27 20.1–29.9 4 17.85 ± 3.7 12.8–21.6 4
<51 cm in SVL 27.07 ± 3.46 22.5–34.6 15 26.97 ± 4.31 21.8–33.9 12 20.89 ± 4.02 14.3–26.1 12
Captured before 1200 hr 27.94 ± 2.44 25.2–31.4 8 27.51 ± 4.47 22.0–33.9 8 20.95 ± 3.04 17.9–25.5 8
Captured after 1200 hr 25.31 ± 3.89 20.2–34.6 12 25.05 ± 4.09 20.1–31.5 8 19.31 ± 4.94 12.8–26.1 8
Spring (April–May) 26.15 ± 0.21 26.0–26.3 2 21.80 ± 0.00 21.8–21.8 2 17.00 ± 0.00 17.0–17.0 2
Summer (June–August) 28.06 ± 2.95 25.2–34.6 10 26.52 ± 2.98 22.0–31.5 10 20.98 ± 2.89 17.9–26.1 10
Autumn (September–October) 24.29 ± 3.78 20.2–30.3 8 27.93 ± 7.06 20.1–33.9 4 19.53 ± 6.93 12.8–25.5 4
Downloaded From: https://bioone.org/journals/Northeastern-Naturalist on 04 Nov 2019
Terms of Use: https://bioone.org/terms-of-useAccess provided by University of Illinois at Urbana-Champaign

Northeastern Naturalist
754
D.F. Hughes, P.R. Delis, and W.E. Meshaka Jr
2019 Vol. 26, No. 4
P = 0.1). Mean BT associated with ecdysis was similar between the 2 species (t =
-0.55, df = 18, P = 0.59).
Recovering from injury
Common Gartersnakes with an obvious external injury did not have a different
mean BT than those lacking signs of a fresh wound (t = -0.32, df = 28. P = 0.75;
Fig. 1). Injured Common Watersnakes had a higher, but not significantly different,
mean BT than those lacking a visible injury (t = -1.15, df = 5, P = 0.3). Common
Gartersnakes and Common Watersnakes with injuries had similar mean BTs (t =
-0.42, df = 6, P = 0.69).
Gestation
Gravid female Common Gartersnakes had a lower, but not signicantly differ-
ent, mean BT than non-gravid adult females (t = -1.02, df = 31, P = 0.32; Fig. 1).
Only 2 Common Watersnakes were gravid and thus we could not compare BTs.
Ontogeny
We did not detect a linear association between body size of Common Garter-
snakes and their BT (R2 = 0.04, F1,45 = 1.89, P = 0.18). Large Common Gartersnakes
(SVL > 36 cm) had a lower mean BT than those with an SVL < 36 cm (t = 1.98,
df = 45, P = 0.03; Fig. 1). We also did not detect a linear relationship between body
size of Common Watersnakes and their BT (R2 = 0.15, F1,18 = 3.1, P = 0.095). Large
Common Watersnakes (SVL > 51 cm) had lower, but not signicantly different,
mean BT to those with an SVL < 51 cm (t = 1.59, df = 18, P = 0.06). Large Common
Gartersnakes (SVL > 36 cm) and large Common Watersnakes (SVL > 51 cm) had
similar mean BTs (t = 1.67, df = 5, P = 0.16). Small Common Gartersnakes (SVL <
Figure 1. Average body temperatures of Thamnophis sirtalis (Common Gartersnake) and
Nerodia sipedon (Common Watersnake) across physiological states from Letterkenny Army
Depot, Franklin County, PA. Error bars represent ± 1 standard error. Sample sizes are below
each column.
Downloaded From: https://bioone.org/journals/Northeastern-Naturalist on 04 Nov 2019
Terms of Use: https://bioone.org/terms-of-useAccess provided by University of Illinois at Urbana-Champaign

Northeastern Naturalist Vol. 26, No. 4
D.F. Hughes, P.R. Delis, and W.E. Meshaka Jr
2019
755
36 cm) and small Common Watersnakes (SVL < 51 cm) also had similar mean BTs
(t = 1.6, df = 26, P = 0.12).
Time of day
Common Gartersnakes captured in the morning (before noon) had a similar
mean BT to those captured in the afternoon (t = -0.39, df = 45, P = 0.7; Fig. 1).
Common Watersnakes captured in the morning also had a similar mean BT to those
captured in the afternoon (t = 1.85, df = 18, P = 0.08). Common Gartersnakes and
Common Watersnakes captured in the morning had a similar mean BT (t = 0.52,
df = 17, P = 0.61), as did individuals between these species captured in the after-
noon (t = -1.78, df = 31, P = 0.08).
Seasonal variation
The mean BTs in both snake species generally followed seasonal changes in
environmental temperatures through the sampling months. Common Gartersnakes,
however, did not exhibit any signicant differences in mean BT across the major
seasons (F2,44 = 2.01, P = 0.15). Likewise, Common Watersnakes did not exhibit
signicant seasonal differences in mean BT (F2,17 = 3.02, P = 0.08).
Distance to water
The mean and range of BTs of Common Gartersnakes found under offshore
boards were nearly identical to those of conspecics found under upland boards
(t = 0.24, df = 38, P = 0.81), suggesting that board distance to water did not inu-
ence BTs. A single male Common Watersnake was captured under an upland board
and all others were captured under offshore boards, and so we could not compare
BTs based on distance to water for that species.
Environmental temperatures
Cloacal BT in the Common Gartersnake was associated with AT (R2 = 0.27,
F1,45 = 16.56, P = 0.0002), BST (R2 = 0.49, F1,33 = 31.81, P < 0.001), and SST (R2 =
0.46, F1,33 = 28.67, P < 0.001). In Common Watersnakes, cloacal BT was strongly
associated with AT (R2 = 0.73, F1,18 = 48.23, P < 0.001), BST (R2 = 0.63, F1,14 =
23.39, P < 0.0002), and SST (R2 = 0.72, F1,14 = 35.64, P < 0.001). For both spe-
cies, mean OBTs were higher than mean BSTs and SSTs measured across nearly
all categories (F2,166 = 37.7, P < 0.001), indicating that snakes consistently thermo-
regulated at temperatures that were higher than their immediate environment.
Discussion
Do wild snakes select a different BT range when experiencing a physiological
challenge? Fitch (1956) suggested that to maximize physiological processes, such
as digestion, gestation, and ecdysis, snakes will make optimal use of their thermal
environment. Kitchell (1969) found that when presented with a thermal gradient
in the laboratory, Common Gartersnakes and Common Watersnakes selected BTs
that were different when they were experiencing a physiological challenge, such as
choosing a slightly higher BT during digestion (Common Gartersnakes: 24–33.8
Downloaded From: https://bioone.org/journals/Northeastern-Naturalist on 04 Nov 2019
Terms of Use: https://bioone.org/terms-of-useAccess provided by University of Illinois at Urbana-Champaign

Northeastern Naturalist
756
D.F. Hughes, P.R. Delis, and W.E. Meshaka Jr
2019 Vol. 26, No. 4
°C [mean = 30.6 °C], Common Watersnakes: 22.2–31.6 °C [mean = 28.8 °C]) and
signicantly lower BTs during ecdysis (Common Gartersnakes: 15.8–26 °C [mean
= 18.6 °C], Common Watersnakes: 17.2–20.4 °C [mean = 18.7 °C]). We found that
the span of BTs for Common Gartersnakes and Common Watersnakes with obvious
food bulges and those with cloudy eyes were different from those of snakes not
experiencing these physiological processes. However, these differences were only
statistically signicant in Common Gartersnakes post-feeding. In general, Com-
mon Gartersnakes had generally higher operative temperatures across physiological
states than Common Watersnakes. In a prior study, Brown and Weatherhead (2000)
found that Common Watersnakes did not exhibit a major thermophilic response to
controlled feeding in the laboratory (change of +1 °C) or to supplemental feeding
in the eld (change of +1.1 °C). Our data suggest that gravid Common Gartersnakes
thermoregulated within a narrower range of BTs than non-gravid females. Indeed,
Charland (1995) found that gravid Common Gartersnakes had a higher mean BT
(30.5 °C) and a narrower range of BTs than non-gravid females (mean = 29.6
°C) throughout gestation in the laboratory. In a radio-telemetry study, Brown and
Weatherhead (2000) revealed that gravid Common Watersnakes thermoregulated
more precisely and at warmer temperatures than non-gravid females, but only
during July and August. Similarly, across 7 species of Garter Snakes measured in
the wild, Rosen (1991) found that the BTs in gravid females were higher and less
variable (mean 30.12 °C, ± 1.91 SD, n = 54) than non-gravid females (mean 29.14
°C, ± 2.63 SD, n = 47). Conversely, Gibson and Falls (1979) found that gravid Com-
mon Gartersnakes had a similar mean BT to non-gravid females, measured from
free-ranging animals via the cloaca.
Differences in the measured extent of thermal responses by snakes to physi-
ological challenges seem to be inuenced by several methodological factors among
studies, including if snake BTs were measured in the eld or laboratory, whether
snakes were captured under articial cover or free-ranging, or if temperature
measurements were derived from radio-telemetry or point-measurements via the
cloaca. Despite an apparent lack of consensus in the literature, it seems that snakes
do select a different BTs in response to physiological challenges. However, the
magnitude of that response is contingent upon methodological differences across
studies and local circumstances, such as the stage at which the physiological state
had reached when measured and environmental microclimates. Even with these ca-
veats, measuring the 2 species in the same place at the same time provides a direct
comparison of OBTs.
We found no differences between the thermal characteristics of upland boards
and offshore boards selected by the Common Gartersnake, which were encountered
in similar numbers with similar BTs in both board locations. Varying the board
distance from the shore, however, revealed a stark, but unsurprising, contrast in the
number of Common Watersnake captures, such that greater than 90% were captured
under offshore boards. Our ndings are consistent with Scribner and Weatherhead
(1995), who found that Common Watersnakes were almost exclusively encountered
along the shoreline, whereas Common Gartersnakes were found in a wider variety
of microhabitats including many that were not contiguous to water.
Downloaded From: https://bioone.org/journals/Northeastern-Naturalist on 04 Nov 2019
Terms of Use: https://bioone.org/terms-of-useAccess provided by University of Illinois at Urbana-Champaign

Northeastern Naturalist Vol. 26, No. 4
D.F. Hughes, P.R. Delis, and W.E. Meshaka Jr
2019
757
The proclivity of the Common Watersnake to seek offshore microhabitats more
frequently than syntopic Common Gartersnakes is most likely associated with 3
main factors: diet, behavior, and temperature. First, Common Watersnakes have a
highly piscivorous diet (Ernst and Ernst 2003), thus shoreline microhabitats provide
an ideal vantage point for hunting sh. Second, when Common Watersnakes are
startled, they use an aquatic escape route more often than Common Gartersnakes,
which rely more on crypsis as an antipredator behavior (Scribner and Weatherhead
1995, Weatherhead and Robertson 1992). Lastly, despite the fact that we did not de-
tect a pronounced thermal difference between board locations (due to a low sample
size), temperature does in fact inuence microhabitat selection in the Common
Watersnake, such that open offshore sites provide a more optimal thermal landscape
compared to upland sites (Robertson and Weatherhead 1992). In fact, microhabitat
selection is more important for controlling BT than other behavioral adjustments in
snakes, such as postural choices (Stevenson 1985b).
Thermal data from many North American snake species indicate that they are
generally active at temperatures between 20 °C and 30 °C (Ernst and Ernst 2003).
Our findings for the Common Gartersnake showed that nearly 77% of individu-
als fell within a BT of 20–30 °C. The span of BTs we measured for the Common
Gartersnake were strikingly similar to a population in Michigan, of which 70%
of those snakes had BTs of 20–30 °C (Carpenter 1956). Nevertheless, there is
extensive variation in reported BT ranges for Common Gartersnakes through-
out the species’ geographic range. In Schoolcraft County, MI, BTs of Common
Gartersnakes were 24–31.8 °C (mean = 27.3 °C); in Livingston County, MI, the
min–max was 20.4–34.4 °C (mean = 28.3 °C) with a min–max of 22.6–34.4 °C
(mean = 28.9 °C) for females and 20.4–33 °C (mean = 27.2 °C) for males; and
in Liberty County, GA, BTs were 26.9–34.3 °C (mean = 30.5 °C) (Rosen 1991).
In Washtenaw County, MI, BTs of Common Gartersnakes were 9–35 °C (mean =
25.6 °C) with a min–max of 12.4–35 °C (mean = 27.3 °C) for females and 9–33
°C (mean = 24.1 °C) for males (Carpenter 1956). In Bedford County, PA, BTs
of 30.0–30.4 °C (mean = 30.2 °C) were recorded from 4 Common Gartersnakes
(Rosen 1991). In Erie County, PA, Common Gartersnake BTs were 0.2–30.8 °C
(mean = 15.6 °C) (Gray 2014). In Fairfax County, VA, Ernst et al. (2014) reported
BT min–max of 13.2–32.5 °C (mean = 23.5 °C) overall and 14–32 °C (mean =
21.2 °C) for snakes captured under cover.
We agree with Gibson and Falls (1979) that comparisons to available data on the
BTs for the Common Gartersnake (and for most snake species) are difcult because
many studies do not report or account for the large number of parameters that inu-
ence BT at the time when the measurements were taken, such as the snake’s activity,
body size and sex of the snake, number of snakes measured, time of year and day
when the snake was captured, and weather conditions at the time of capture. We note
that our reported BTs (19.7–36.6 °C, mean = 27.6 °C) were determined from 47 Com-
mon Gartersnakes captured under tin cover that were measured diurnally on mostly
sunny days during April to October of 2012 in Pennsylvania. In thermal-gradient
experiments, Common Gartersnakes selected a temperatures of 16–35 °C (Kitchell
Downloaded From: https://bioone.org/journals/Northeastern-Naturalist on 04 Nov 2019
Terms of Use: https://bioone.org/terms-of-useAccess provided by University of Illinois at Urbana-Champaign

Northeastern Naturalist
758
D.F. Hughes, P.R. Delis, and W.E. Meshaka Jr
2019 Vol. 26, No. 4
1969, Lueth 1941); the critical thermal maximum for the species is 38–41 °C and
the minimum is 2.7–3.6 °C (Brattstrom 1965). Smaller Common Gartersnakes had
a higher mean BT than larger snakes, which agrees with the ndings of Carpenter
(1956). Larger snakes have greater thermal inertia than smaller snakes (Stevenson
1985a), and thus warm much slower than smaller ones (Bittner et al. 2002).
The Common Watersnakes we measured exhibited a more conservative range
of body temperatures compared to Common Gartersnakes, with 85% having BTs
between 20 °C and 30 °C and 60% within 22–27 °C. There is variation in the
reported min–max body temperature measured for Common Watersnake popula-
tions throughout its range. In Fairfax County, VA, Ernst et al. (2014) found that
52% of Common Watersnakes had BTs within 23–26 °C, and 69% of males were
within 23–26 °C and 87% of females were within 20–31 °C. Ernst et al. (2014)
also reported an overall BT min–max for Common Watersnakes of 14.4–30 °C
(mean = 23.9 °C), yet none of those snakes were captured under cover. In Osage
County, KS, Clarke (1958) found that nearly 86% of active Common Watersnakes
were found at an AT of 21.1–37.2 °C. In Douglas County, KS, Fitch (1956) found
body temperatures of 16–29.5 °C from 4 individuals. At the northern limit of their
range in Ontario, Canada, Brown and Weatherhead (2000) found BTs of 7.9–27.9
°C during the active season from May to August. Kitchell (1969) found that when
provided with a thermal gradient in the lab, Common Watersnakes normally chose
a BT within 20.8–34.7 °C. Lueth (1941) found that the maximum tolerable ATs for
Common Watersnakes in a thermal laboratory gradient were 36.5–43 °C and that
they can survive (up to 56 days) at 1.5 °C, but will not survive at -2 °C.
Anthropogenically accelerated climate change manifests heterogeneously
across global ecosystems, but most habitats in the northeastern United States
are projected to become warmer and wetter (IPCC 2018, NASA 2019). As tem-
peratures increase, reptiles will undoubtedly experience immediate impacts,
especially at the biochemical and physiological levels. Given the tight relation-
ship between snakes and temperature (Stevenson et al. 1985), the first stages of
warming are likely to produce positive results for American snakes by expanding
suitable habitats and increasing species richness in some areas (Currie 2001).
However, beneficial aspects of projected warming should be interpreted with cau-
tion because reptiles often perform sub-optimally at the high end of their thermal
tolerance (Clusellas-Trullas et al. 2011). Although it seems unlikely that the up-
per thermal limit will be reached, the possibility of environmental temperatures
exceeding the thermal optimum for most Northeastern snake species is high.
The wider range of BTs consistently achieved by the Common Gartersnake sug-
gest that it will exhibit greater adaptability than the Common Watersnake to the
thermal challenges posed by global climate change. We speculate that the contem-
porary physiology of snakes will change if warming predictions are realized over
the next century, and consequently, studying the thermal biology of wild snake
species today provides a baseline to detect future shifts and the possible tempera-
ture-induced responses of snakes.
Downloaded From: https://bioone.org/journals/Northeastern-Naturalist on 04 Nov 2019
Terms of Use: https://bioone.org/terms-of-useAccess provided by University of Illinois at Urbana-Champaign

Northeastern Naturalist Vol. 26, No. 4
D.F. Hughes, P.R. Delis, and W.E. Meshaka Jr
2019
759
Acknowledgments
We dedicate this work to Carl H. Ernst and Henry S. Fitch, pioneers in the thermal biology
of wild snakes. We are indebted to Craig Kindlin, Sam Pelesky, and Matt Miller of the Natural
Resources Ofce at Letterkenny Army Depot (LEAD) for their assistance on this project and
many others at this facility. We also thank the base commander of LEAD, Colonel Provancha.
Our project was funded by Shippensburg University. Research was conducted with approval
of Shippensburg University’s Institutional Animal Care and Use Committee.
Literature Cited
Bittner, T.D., R.B. King, and J.M. Kern. 2002. Effects of body size and melanism on the
thermal biology of Garter Snakes (Thamnophis sirtalis). Copeia 2002:477–482.
Brattstrom, B.H. 1965. Body temperatures of reptiles. American Midland Naturalist
73:376–422.
Brown, G.P., and P.J. Weatherhead. 2000. Thermal ecology and sexual size dimorphism in
Northern Water Snakes, Nerodia sipedon. Ecological Monographs 70:311–330.
Carpenter, C.C. 1956. Body temperatures of three species of Thamnophis. Ecology
37:732–735.
Charland, M.B. 1995. Thermal consequences of reptilian viviparity: Thermoregulation in
gravid and nongravid Garter Snakes (Thamnophis). Journal of Herpetology 29:383–390.
Clarke, R.F. 1958. Ecological study of reptiles and amphibians in Osage County, Kansas.
Emporia State Research Studies 7:1–52.
Clusella-Trullas, S., T.M. Blackburn, and S.L. Chown. 2011. Climatic predictors of temper-
ature performance curve parameters in ectotherms imply complex responses to climate
change. The American Naturalist 177:738–751.
Currie, D.J. 2001. Projected effects of climate change on patterns of vertebrate and tree
species richness in the conterminous United States. Ecosystems 4:216–225.
Delis, P.R., C. Kindlin, and R.L. Stewart. 2010. The herpetofauna of Letterkenny Army
Depot, south-central Pennsylvania: A starting point to the long-term monitoring and
management of amphibians and reptiles. Journal of Kansas Herpetology 34:11–16.
Elick, G.E., J.A. Sealander, and R.J. Beumer. 1980. Temperature preferenda, body tempera-
ture tolerances, and habitat selection of small colubrid snakes. Transactions Missouri
Academy of Sciences 13:21–31.
Ernst, C.H., and E.M. Ernst. 2003. Snakes of the United States and Canada. Smithsonian
Institution Press, Washington, DC. 668 pp.
Ernst, C.H., T.R. Creque, J.M. Orr, T.D. Hartsell, and A.F. Laemmerzahl. 2014. Operating
body temperatures in a snake community of Northern Virginia. Northeastern Naturalist
21:247–258.
Fitch, H.S. 1956. Temperature responses in free-living amphibians and reptiles of northeast-
ern Kansas. University of Kansas Publications, Museum of Natural History 8:417–476.
Gibson, A.R., and B.B. Falls. 1979. Thermal biology of the Common Garter Snake Tham-
nophis sirtalis (L.). I. Temporal variation, environmental effects, and sex differences.
Oecologia 43:79–97.
Gray, B.S. 2014. Seasonal activity and temperature relationships of the Eastern Garter-
snake, Thamnophis sirtalis sirtalis (Linnaeus, 1758), from an urban population in Erie
County, Pennsylvania. Bulletin of the Maryland Herpetological Society 50:22–33.
Hertz, P.E., R.B. Huey, and R.D. Stevenson. 1993. Evaluating temperature regulation by
eld-active ectotherms: The fallacy of the inappropriate question. American Natural-
ist 142:796–818.
Downloaded From: https://bioone.org/journals/Northeastern-Naturalist on 04 Nov 2019
Terms of Use: https://bioone.org/terms-of-useAccess provided by University of Illinois at Urbana-Champaign

Northeastern Naturalist
760
D.F. Hughes, P.R. Delis, and W.E. Meshaka Jr
2019 Vol. 26, No. 4
Hughes, D.F., P.R. Delis, and W.E. Meshaka Jr. 2018. Studies of a snake assemblage from
articial ponds at an active-military site in Pennsylvania. Herpetology Notes 11:35–48.
Hulse, A.C., C.J. McCoy, and E.J. Censky. 2001. Amphibians and Reptiles of Pennsylvania
and the Northeast. Cornell University Press, Ithaca, NY. 419 pp.
Intergovernmental Panel on Climate Change (IPCC). 2018. Summary for policymakers. Pp.
1–32, In V. Masson-Delmotte, P. Zhai, H.-O. Pörtner, D. Roberts, J. Skea, P.R. Shukla,
A. Pirani, Moufouma-Okia, C. Péan, R. Pidcock, S. Connors, J.B.R. Matthews, Y. Chen,
X. Zhou, M.I. Gomis, E. Lonnoy, Maycock, M. Tignor, and T. Watereld (Eds.). Global
Warming of 1.5 °C: An IPCC Special Report. World Meteorological Organization, Ge-
neva, Switzerland. 630 pp.
Kitchell, J.F. 1969. Thermophilic and thermophobic responses of snakes in a thermal gradi-
ent. Copeia 1969:189–191.
Lillywhite, H.B. 2001. Temperature, energetics, and physiological ecology. Pp. 422–477,
In R.A. Seigel, J.T. Collins, and S.S. Novak (Eds.). Snakes, Ecology, and Evolutionary
Biology. Blackburn Press, Caldwell, NJ. 529 pp.
Lueth, F.X. 1941. Effects of temperature on snakes. Copeia 1941:125–132.
Meshaka, W.E., Jr., and P.R. Delis. 2014. Snake assemblage structures and seasonal activity
patterns on a military base in south-central Pennsylvania: Land management implica-
tions for snake conservation. Journal of North American Herpetology 1:7–20.
National Aeronautics and Space Agency (NASA), 2019. 2018 was fourth warmest year in
continued warming trend, according to NASA, NOAA. Available at: https://climate.
nasa.gov/news/2841/2018-fourth-warmest-year-in-continued-warming-trend-accord-
ing-to-nasa-noaa/. Accessed: 22 February 2019.
Peterson, C.R. 1987. Daily variation in the body temperatures of free-ranging garter snakes.
Ecology 68:160–169.
R Core Team. 2018. R version 3.4.4: A language and environment for statistical computing.
R Foundation for Statistical Computing, Vienna, Austria. Available online at https://
www.R-project.org.
Robertson, I.C., and P.J. Weatherhead. 1992. The role of temperature in microhabitat
selection by Northern Water Snakes (Nerodia sipedon). Canadian Journal of Zoology
70:417–422.
Rosen, P.C. 1991. Comparative eld study of thermal preferenda in Garter Snakes (Tham-
nophis). Journal of Herpetology 25:301–312.
Rothman, K.J. 1990. No adjustments are needed for multiple comparisons. Epidemiology
1:43–46.
Scribner, S.J., and P.J. Weatherhead. 1995. Locomotion and antipredator behaviour in three
species of semi-aquatic snakes. Canadian Journal of Zoology 73:321–329.
Stevenson, R.D. 1985a. Body size and limits to the daily range of body temperature in ter-
restrial ectotherms. The American Naturalist 125:102–117.
Stevenson, R.D. 1985b. The relative importance of behavioral and physiological adjust-
ments controlling body temperature in terrestrial ectotherms. The American Naturalist
126:362–386.
Stevenson, R.D., C.R. Peterson, and J.S. Tsuji. 1985. The thermal dependence of loco-
motion, tongue icking, digestion, and oxygen consumption in the Wandering Garter
Snake. Physiological Zoology 58:46–57.
Weatherhead, P.J., and I.C. Robertson. 1992. Thermal constraints on swimming perfor-
mance and escape response of Northern Water Snakes (Nerodia sipedon). Canadian
Journal of Zoology 70:94–98.
Downloaded From: https://bioone.org/journals/Northeastern-Naturalist on 04 Nov 2019
Terms of Use: https://bioone.org/terms-of-useAccess provided by University of Illinois at Urbana-Champaign