Content uploaded by Michael E. Dorcas
Author content
All content in this area was uploaded by Michael E. Dorcas on Oct 17, 2014
Content may be subject to copyright.
SHORTER COMMUNICATIONS SHORTER COMMUNICATIONS
cessfully,
one 3 d earlier than
would be
expected
and
the
others
hatched at
the
same time as
embryos
that
had
not
been
induced
to
pip prematurely.
Acknowledgments.-I
thank
Australia Zoo
and
its
Staff
for
collecting
the mound
gas
samples
and for
supplying
the
crocodile
eggs.
This
project
was
ap-
proved by
the
University
of
Queensland
Animal
Eth-
ics Committee.
LITERATURE
CITED
ACKERMAN,
R.
A.
1977. The
respiratory
gas
exchange
of sea turtle
nests
(Chelonia,
Caretta).
Respir. Phy-
siol. 31:19-38.
ALDERTON,
D.
1991.
Crocodiles and
Alligators
of the
World.
Blandford
Publishing,
New York.
BLACK,
C.
P.,
AND
G.
K.
SNYDER.
1980.
Oxygen
trans-
port
in the
avian
egg
at
high
altitude.
Amer.
Zool.
20:461-468.
BOOTH,
D.
T. 1998.
Nest
temperature
and
respiratory
gases during
natural
incubation
in
the
broad-
shelled river
turtle Chelodina
expansa
(Testudinata:
Chelidae).
Aust.
J.
Zool. 46:183-191.
DEEMING,
D.
C.,
AND M.
W.
J.
FERGUSON.
1990. Re-
duction in
eggshell
conductance to
respiratory gas-
es has
no effect
on
sex
determination
in
Alligator
mississippiensis.
Copeia
1991:240-243.
GRIGG,
G.
C.,
R. M.
G.
WELLS,
AND
L. A. BEARD.
1993.
Allosteric control
of
oxygen
binding
by
haemoglo-
bin
during
embryonic
development
in the
croco-
dile
Crocodylus porosus:
the
role
of red cell
organic
phosphates
and
carbon dioxide.
J.
Exp.
Biol. 175:
15-32.
HARRISON,
K.
E.,
T.
B.
BENTLY,
P.
L.
LUTZ,
AND D.
S.
MARSZALEK.
1978. Water
and
gas
diffusion
in
the
American
crocodile
egg.
Amer.
Zool. 18:637.
KAM,
Y-C. 1993.
Physiological
effects of
hypoxia
on
metabolism and
growth
of turtle
embryos.
Respir.
Physiol.
92:127-138.
PACKARD,
G.
C.,
T.
L.
TAIGEN,
M.
J.
PACKARD,
AND
R.
D.
SHUMAN. 1979.
Water-vapor
conductance of
tes-
tudinian and
crocodilian
eggs
(Class
reptilia).
Res-
pir. Physiol.
38:1-10.
SEYMOUR,
R.
S.
1985.
Physiology
of
megapode
eggs
and mounds. Acta XVIII
Congress
International
Ornithology,
Moscow Vol.
2.,
pp.
854-863.
,
AND R. A.
ACKERMAN.
1980.
Adaptations
to
underground
nesting
in
birds
and
reptiles.
Amer.
Zool.
20:437-447.
WARBURTON,
S.
J.,
D.
HASTINGS,
AND T.
WANG.
1995.
Responses
to chronic
hypoxia
in
embryonic
alli-
gators.
J.
Exp.
Zool. 273:44-50.
WEBB,
G.
J.
W. 1977. The natural
history
of
Crocodylus
porosus:
habitat and
nesting.
In
H.
Messel and
S.T.
Butler
(eds.),
Australian Animals and
Their Envi-
ronment,
pp.
237-284.
Shakespeare
Head
Press,
Sydney.
WHITEHEAD, P.,
AND
R.
S. SEYMOUR.
1990. Patterns
of
metabolic rate in
embryonic
crocodilians
Crocody-
lus
johnstoni
and
Crocodylus
porosus.
Physiol.
Zool.
63:334-352.
WITHERS,
P.
C.
1977. Measurement
of
VO2,
Vco2
and
evaporative
water
loss with a
flow-through
mask.
J.
Appl.
Physiol.
42:120-123.
cessfully,
one 3 d earlier than
would be
expected
and
the
others
hatched at
the
same time as
embryos
that
had
not
been
induced
to
pip prematurely.
Acknowledgments.-I
thank
Australia Zoo
and
its
Staff
for
collecting
the mound
gas
samples
and for
supplying
the
crocodile
eggs.
This
project
was
ap-
proved by
the
University
of
Queensland
Animal
Eth-
ics Committee.
LITERATURE
CITED
ACKERMAN,
R.
A.
1977. The
respiratory
gas
exchange
of sea turtle
nests
(Chelonia,
Caretta).
Respir. Phy-
siol. 31:19-38.
ALDERTON,
D.
1991.
Crocodiles and
Alligators
of the
World.
Blandford
Publishing,
New York.
BLACK,
C.
P.,
AND
G.
K.
SNYDER.
1980.
Oxygen
trans-
port
in the
avian
egg
at
high
altitude.
Amer.
Zool.
20:461-468.
BOOTH,
D.
T. 1998.
Nest
temperature
and
respiratory
gases during
natural
incubation
in
the
broad-
shelled river
turtle Chelodina
expansa
(Testudinata:
Chelidae).
Aust.
J.
Zool. 46:183-191.
DEEMING,
D.
C.,
AND M.
W.
J.
FERGUSON.
1990. Re-
duction in
eggshell
conductance to
respiratory gas-
es has
no effect
on
sex
determination
in
Alligator
mississippiensis.
Copeia
1991:240-243.
GRIGG,
G.
C.,
R. M.
G.
WELLS,
AND
L. A. BEARD.
1993.
Allosteric control
of
oxygen
binding
by
haemoglo-
bin
during
embryonic
development
in the
croco-
dile
Crocodylus porosus:
the
role
of red cell
organic
phosphates
and
carbon dioxide.
J.
Exp.
Biol. 175:
15-32.
HARRISON,
K.
E.,
T.
B.
BENTLY,
P.
L.
LUTZ,
AND D.
S.
MARSZALEK.
1978. Water
and
gas
diffusion
in
the
American
crocodile
egg.
Amer.
Zool. 18:637.
KAM,
Y-C. 1993.
Physiological
effects of
hypoxia
on
metabolism and
growth
of turtle
embryos.
Respir.
Physiol.
92:127-138.
PACKARD,
G.
C.,
T.
L.
TAIGEN,
M.
J.
PACKARD,
AND
R.
D.
SHUMAN. 1979.
Water-vapor
conductance of
tes-
tudinian and
crocodilian
eggs
(Class
reptilia).
Res-
pir. Physiol.
38:1-10.
SEYMOUR,
R.
S.
1985.
Physiology
of
megapode
eggs
and mounds. Acta XVIII
Congress
International
Ornithology,
Moscow Vol.
2.,
pp.
854-863.
,
AND R. A.
ACKERMAN.
1980.
Adaptations
to
underground
nesting
in
birds
and
reptiles.
Amer.
Zool.
20:437-447.
WARBURTON,
S.
J.,
D.
HASTINGS,
AND T.
WANG.
1995.
Responses
to chronic
hypoxia
in
embryonic
alli-
gators.
J.
Exp.
Zool. 273:44-50.
WEBB,
G.
J.
W. 1977. The natural
history
of
Crocodylus
porosus:
habitat and
nesting.
In
H.
Messel and
S.T.
Butler
(eds.),
Australian Animals and
Their Envi-
ronment,
pp.
237-284.
Shakespeare
Head
Press,
Sydney.
WHITEHEAD, P.,
AND
R.
S. SEYMOUR.
1990. Patterns
of
metabolic rate in
embryonic
crocodilians
Crocody-
lus
johnstoni
and
Crocodylus
porosus.
Physiol.
Zool.
63:334-352.
WITHERS,
P.
C.
1977. Measurement
of
VO2,
Vco2
and
evaporative
water
loss with a
flow-through
mask.
J.
Appl.
Physiol.
42:120-123.
Accepted:
19
April
2000.
Accepted:
19
April
2000.
Journal
of
Herpetology,
Vol.
34,
No.
3,
pp.
481485,
2000
Copyright
2000
Society
for the
Study
of
Amphibians
and
Reptiles
Regional
Body
Temperature
Variation
in
Corn
Snakes Measured
Using
Temperature-sensitive
Passive
Integrated Transponders
ANDREW
W. ROARK'2
AND
MICHAEL
E.
DORCAS1'3 'De-
partment
of
Biology,
PO.
Box
1719,
Davidson
College,
Da-
vidson,
North
Carolina
28036,
USA: E-mail:
midorcas@
davidson.edu
Body
temperature
affects
nearly
every
aspect
of the
biology
of
ectotherms
(Huey,
1982;
Lillywhite,
1987;
Peterson
et
al.,
1993).
However,
many
ectotherms do
not
maintain
a
uniform
temperature
among
their dif-
ferent
body regions
(Webb
and
Heatwole,
1971;
Webb
et
al., 1972;
Pough
and
McFarland,
1976;
Dorcas and
Peterson,
1997).
In the
past,
most
researchers have
measured the
body
temperatures
(T,)
of ectotherms at
only
one
location,
either
cloacal or core
Tb.
Because
Tb
differences
among body
regions
are
common
in
many
reptiles
and
other
ectotherms
(Heinrich,
1974;
Block
and
Carey,
1985),
studies
of
ectotherm
thermal
biology
should
consider
both the
degree
of
regional
variation
in
preferred
Tb
and the
precision
with
which
regional
temperatures
are
maintained.
Studies of
head-body
temperature
differences
have
demonstrated that
most
reptiles
maintain
head tem-
peratures
more
precisely
than
body
temperatures
(Heath,
1964;
Dill, 1972;
Dorcas and
Peterson,
1997).
Precise
temperature regulation
in the
head/neck
re-
gion
of
most
ectotherms is
important
because tem-
perature
has
major
effects on
the
functioning
of
the
central
nervous
system,
especially
the
cerebrum
(Klei-
ber,
1961).
Precise
temperature
regulation
in other
parts
of
the
body may
not be
as critical
for
optimal
functioning.
Snakes are ideal
animals in
which to
examine re-
gional
differences
in
Tb.
Because
of
their
elongate
form,
snakes
can
exhibit considerable
regional
tem-
perature
differences
(Peterson
et
al.,
1993).
Addition-
ally, many
snake
species
are
particularly
suited to lab-
oratory
studies because
they
are
easily
cared
for
and
tolerate
invasive
procedures
required
to
monitor their
Tb
(Seigel,
1993).
Here,
we
examined the
extent to which
temperature
variation
occurs
in
different
body regions
of corn
snakes
(Elaphe
guttata),
how
precisely
the
temperature
of each
body region
is
regulated,
and
the effects
of
digestion
on
regional
Tb
variation. Our
secondary
ob-
jective
was
to test the
effectiveness
of
temperature
sen-
sitive,
passive integrated
transponders
(PIT
tags)
for
use
in
thermal
preference
studies of
snakes.
Animals.-We
examined
regional
Tb
variation
in
corn
snakes,
Elaphe
guttata.
We
used 15
snakes
(seven
males,
eight
females),
each
weighing
between
23 and
2Present
Address:
Laboratory
of
Developmental
Neurobiology,
National Institute
of Child
Health and
Human
Development,
National Institutes of
Health,
Bethesda,
Maryland
20892,
USA
3
Corresponding
Author.
Journal
of
Herpetology,
Vol.
34,
No.
3,
pp.
481485,
2000
Copyright
2000
Society
for the
Study
of
Amphibians
and
Reptiles
Regional
Body
Temperature
Variation
in
Corn
Snakes Measured
Using
Temperature-sensitive
Passive
Integrated Transponders
ANDREW
W. ROARK'2
AND
MICHAEL
E.
DORCAS1'3 'De-
partment
of
Biology,
PO.
Box
1719,
Davidson
College,
Da-
vidson,
North
Carolina
28036,
USA: E-mail:
midorcas@
davidson.edu
Body
temperature
affects
nearly
every
aspect
of the
biology
of
ectotherms
(Huey,
1982;
Lillywhite,
1987;
Peterson
et
al.,
1993).
However,
many
ectotherms do
not
maintain
a
uniform
temperature
among
their dif-
ferent
body regions
(Webb
and
Heatwole,
1971;
Webb
et
al., 1972;
Pough
and
McFarland,
1976;
Dorcas and
Peterson,
1997).
In the
past,
most
researchers have
measured the
body
temperatures
(T,)
of ectotherms at
only
one
location,
either
cloacal or core
Tb.
Because
Tb
differences
among body
regions
are
common
in
many
reptiles
and
other
ectotherms
(Heinrich,
1974;
Block
and
Carey,
1985),
studies
of
ectotherm
thermal
biology
should
consider
both the
degree
of
regional
variation
in
preferred
Tb
and the
precision
with
which
regional
temperatures
are
maintained.
Studies of
head-body
temperature
differences
have
demonstrated that
most
reptiles
maintain
head tem-
peratures
more
precisely
than
body
temperatures
(Heath,
1964;
Dill, 1972;
Dorcas and
Peterson,
1997).
Precise
temperature regulation
in the
head/neck
re-
gion
of
most
ectotherms is
important
because tem-
perature
has
major
effects on
the
functioning
of
the
central
nervous
system,
especially
the
cerebrum
(Klei-
ber,
1961).
Precise
temperature
regulation
in other
parts
of
the
body may
not be
as critical
for
optimal
functioning.
Snakes are ideal
animals in
which to
examine re-
gional
differences
in
Tb.
Because
of
their
elongate
form,
snakes
can
exhibit considerable
regional
tem-
perature
differences
(Peterson
et
al.,
1993).
Addition-
ally, many
snake
species
are
particularly
suited to lab-
oratory
studies because
they
are
easily
cared
for
and
tolerate
invasive
procedures
required
to
monitor their
Tb
(Seigel,
1993).
Here,
we
examined the
extent to which
temperature
variation
occurs
in
different
body regions
of corn
snakes
(Elaphe
guttata),
how
precisely
the
temperature
of each
body region
is
regulated,
and
the effects
of
digestion
on
regional
Tb
variation. Our
secondary
ob-
jective
was
to test the
effectiveness
of
temperature
sen-
sitive,
passive integrated
transponders
(PIT
tags)
for
use
in
thermal
preference
studies of
snakes.
Animals.-We
examined
regional
Tb
variation
in
corn
snakes,
Elaphe
guttata.
We
used 15
snakes
(seven
males,
eight
females),
each
weighing
between
23 and
2Present
Address:
Laboratory
of
Developmental
Neurobiology,
National Institute
of Child
Health and
Human
Development,
National Institutes of
Health,
Bethesda,
Maryland
20892,
USA
3
Corresponding
Author.
481 481
SHORTER
COMMUNICATIONS
70
g
and
having
a
SVL between 39.0 cm
and
59.5 cm.
Adult
SVLs are
generally
75-100
cm
(Conant
and Col-
lins,
1991).
Corn snakes were chosen
for
this
study
because
they
are
easily
cared for
in
captivity
and
large
numbers of
similarly
sized
snakes
are
readily
avail-
able. These snakes were
the
offspring
of several wild-
captured
adults from
Hampton
County,
South Caro-
lina.
Experimental Design.-Each
snake
was
maintained
in a
separate
37.8
L
aquarium
containing
a
layer
of
aspen bedding approximately
1.3 cm
thick,
two
wooden blocks
(approximately
2.5
cm
x
2.5
cm x 25
cm),
and
a
piece
of
black,
corrugated
cardboard
with
the same dimensions
as the inside of the
aquarium
minus
a
hole
(10
cm
x
10
cm)
in
one
corer
for
a
water bowl.
The two
blocks
were
placed
at
each
end
of each
aquaria
to
support
the
piece
of black
card-
board
slightly
above
the
substrate,
thus
providing
cover
for
the
snakes
over
the entire
length
of
the
aquaria.
All
aquaria
were stored
on two
racks,
ap-
proximately
45.7 cm above
a lab bench to allow
access
to the
bottoms of the
cages
for
taking temperature
readings
of
snakes.
Masking tape
was
wrapped
around
each
aquarium
below the cardboard
to
keep
the
area below
the cardboard
dark. Water was
provid-
ed ad
libitum and snakes were
fed
laboratory
mice
approximating
25% of
their
body
mass
every
three
weeks.
Because
we
needed access to the bottoms
of the
cag-
es for
taking
temperature
measurements of
the snakes
with the
PIT
reader,
we used a heat source
from
above
to
generate
constant
(24
h/day) thigmothermal
gra-
dients
within the
cages
(Sievert
and
Hutchison,
1988).
To
generate
the thermal
gradients,
we
placed
heat
lamps
with
aluminum reflectors
containing
100-W
in-
candescent
bulbs on
top
of one end of each
aquarium
(i.e.,
it remained dark
underneath
the cardboard
where
the snakes
stayed,
but the
temperature
was
higher
at one
end of the
cage). Temperatures
ranged
from 25?C at the cool
end of each
aquarium
to 35?C
at the warm end.
Laboratory
Thermal
Preference.-Each
snake was
im-
planted
with three
temperature-sensitive
PIT
tags
(Implantable Programmable Temperature
Transpon-
ders,
Biomedic
Data
Systems,
Seaford,
DE).
Tags
(14
mm
long
and 2.2 mm
in
diameter)
were
injected
into
the
body
cavity
of
each
snake
approximately
midway
between
the
snout
and vent and
just
anterior to the
cloaca.
A third
tag
was
surgically implanted
in
the
neck
approximately
2.5 cm behind
the snake's head.
To
implant
the neck
tag,
a 1
mm incision was
made
in the
skin
between
the first dorsal scale row and the
ventrals,
and a
single
suture
was used to close
the
incision
after the
tag
was inserted. Each
tag
was cali-
brated in a water
bath before
implantation.
No anes-
thesia
was
necessary
for
implantation
of the
PIT
tags
and the
snake's
behavior was not
noticeably
affected
by
the
procedure.
Consequently,
we felt confident
that
beginning temperature
measurements
within two
days
of
tag implantation
yielded
accurate results.
Temperature
measurements
were taken
daily
through
the bottom of the
aquaria
so
that the snakes
would
not be disturbed.
All
measurements
were taken
between 1030
and 1230
h
each
day
for
nine weeks.
Data
Analysis.-To
test for
temperature
differences
among
different
body regions,
we
used
a
two-way,
mixed-model
analysis
of
variance
(ANOVA)
with re-
gion
and snake
as
the
independent
variables.
Alpha
was set
at
0.05.
Once
this
comparison
was
made,
paired-sample
t-tests
were run
post-hoc
on the differ-
ences
between individual
regional
temperatures
to
de-
termine if the mean difference between
regional
tem-
peratures
differed
significantly
from zero. If
so,
then
it could be said
that there was
a
significant
difference
between the two
regions.
The
sign
of
the mean
dif-
ference between
the
two
regions
was indicative
of the
region
maintained at
a
higher temperature.
Because of
multiple comparisons,
we reduced our
alpha
for these
tests to 0.017
using
a Bonferroni correction.
We used
a
Z-test to test
for
differences
in thermo-
regulatory precision
in snake
body regions.
Z-scores
were calculated for
each
regional temperature
and
then
compared using
a
two-way,
mixed
model
AN-
OVA with snake
and
region
as the
independent
vari-
ables.
Alpha
was set
at
0.05.
Regional temperatures
two
days prior
to
feeding
were
compared
to
regional
temperatures
two
days
af-
ter
feeding
to
determine
the
effects
of
digestion
on
regional
Tb
variation
(Dorcas
et
al.,
1997).
For the mid-
body
and
posterior regions,
we used
two-way,
mixed-
model ANOVAs
with
feeding
status
(digesting
or
not)
and snake
as
the
independent
variables.
A
one-way
ANOVA,
with
feeding
status
as the
independent
var-
iable,
was used
for
testing
the
effects
of
digestion
on
temperature
regulation
in the
anterior
region
because
of a
number of
missing
data
points (explained
in Re-
sults).
Alpha
was set
at 0.05.
The
temperature-sensitive
PIT
tags
enabled us to
measure
accurately
(with
0.1?C
resolution)
regional
body temperatures
without
disturbing
the snakes.
However,
over the course of
the
study, many
of the
PIT
tags
implanted
in the neck
region
of
the
snakes
moved
posteriorly through
the
body
and most
of
these were
expelled
in the
feces.
We found that 66%
moved the
anterior
tag
to the
midbody
region
or
be-
yond
and
53%
of the snakes
actually
expelled
their
anterior
tag
at least once.
In
some
cases,
tags
moved
within one
day
of
implantation.
Other snakes'
tags
re-
mained
stationary
for
up
to six weeks before
moving.
PIT
tags
were
cleaned
and
immediately re-implanted
following expulsion
and
data were not
used
from
tags
that had moved.
Tags
were
expelled
more
than
once
by
20% of the snakes. In one
snake,
the
PIT
tag
from
the
posterior region
was
expelled
but no
tags implant-
ed
in the
midbody region
were
expelled
during
the
study.
The mean
regional
Tb's
varied
significantly among
individual snakes
(ANOVA,
df
=
14,
F
=
25.97,
P
<
0.001)
and
also
among
body regions
within
individ-
uals
(ANOVA,
df
=
2,
F
=
10.91,
P
=
0.0011;
Fig.
1).
Anterior
temperatures
were
maintained
at
higher
lev-
els than
both
midbody
temperatures (paired-sample
t-test,
df
=
14,
t
=
7.87,
P
<
0.0001;
Table
1)
and
posterior
temperatures
(paired-sample
t-test,
df
=
14,
t
=
8.41,
P <
0.0001;
Table
1).
Midbody
temperatures
did
not differ
significantly
from
posterior
tempera-
tures,
but our
analysis strongly suggests
a
possible
temperature
difference
(paired-sample
t-test,
df
=
14,
t
=
1.97,
P
=
0.0488;
Table
1).
While we found
that
the
precision
with which
body temperature
was
reg-
ulated differed
significantly among
individuals
(Z-
test,
df
=
14,
Z
=
5.01,
P
=
0.0002),
we
did not find
482
SHORTER
COMMUNICATIONS
8
10
-
30-
?
M Anterior
co
8
-
M
Midbody
29
,
6
29
-
:~
0s-~ o~MPosterior
0
28
-
E
2
-
E 27
-
z
0 - -.. I
I
I I
I
------T
I
I
-
zo
*
Nondigesting
E
Digesting
25 26
27 28 29
30
Temperature
(C)
FIG. 1.
Preferred
regional
body temperature
dis-
tribution
in
corn snakes
(Elaphe
guttata).
Mean
anterior,
midbody,
and
posterior temperatures
over the entire
study period
were
calculated
for each snake and
those
means
are
presented
here.
See Table 1 for
sample
siz-
es.
that
thermoregulatory
precision
differed
significantly
among body
regions
(Z-test,
df
=
2,
Z
=
1.21,
P
=
0.30).
The mean
temperatures
for all three
body
re-
gions
were
significantly higher
during digestion
(an-
terior,
single-factor
ANOVA,
df
=
76,
F
=
7.19,
P
=
0.009;
midbody,
two-factor
ANOVA,
df
=
13,
F
=
6.15,
P
=
0.016;
posterior,
two-factor
ANOVA,
df
=
13,
F
=
4.47,
P
=
0.038;
Fig.
2).
As far as we
are
aware,
this
represents
the first
pub-
lished
study
in
which
temperature-sensitive
PIT
tags
have been used
to examine the
thermal
preference
of
snakes.
Overall,
we were
pleased
with
this
technique
and
believe that it allowed
us to
collect data effective-
ly.
Other
techniques
used
to measure the
Tb's
of
rep-
tiles
in
the
laboratory
include
quick-reading
cloacal
thermometers
(Avery,
1982;
Dorcas
et
al.,
1997),
in-
gested
or
surgically implanted
temperature-sensitive
radiotransmitters
(Lillywhite,
1980;
Slip
and
Shine,
1988),
thermocouple
or
thermistor
tethers
(Heath,
Head
Midbody
Tail
FIG. 2.
Preferred
regional
body temperatures
of
snakes
before
and
during digestion
in corn
snakes
(Elaphe
guttata).
Note that mean
digesting tempera-
tures are
significantly greater
than mean
nondigesting
temperatures
for all
body
regions.
Bars
represent
tone
standard
error.
1964;
Tu and
Hutchison,
1994,
1995),
and
hypodermic
probes
(Webb
et
al.,
1972).
Studies
using
radiotelem-
etry
often are
expensive,
require
rather
elaborate
sur-
gical procedures,
and are
limited to
relatively
large
reptiles
that
can
tolerate the
transmitters. Studies
us-
ing
quick-reading
cloacal
thermometers, tethers,
or
probes
require
considerable
disturbance of the
ani-
mals
which
can affect the
results of the
study
(Peter-
son et
al.,
1993).
Temperature
sensitive PIT
tags,
such
as
the
ones we
used
in
this
study, provide
a
relatively
low
cost
(approximately
$11
US
per tag,
$1800
US for
the
reader)
approach
to
measuring
the
Tb's
of both
large
and
relatively
small
reptiles
in the
laboratory.
Additional
advantages
of
temperature-sensitive
PIT
tags
over
traditional
techniques
include the
ability
to
sample
study
animals at
frequent
intervals with min-
imal
disturbance,
the
simple procedure
for
implanting
the
tag,
and the
ability
to
implant tags
in
different
body regions.
Because PIT
tags
are
frequently
used
in
mark-re-
capture
studies of
many
species
of
reptiles
(Camper
TABLE 1.
Preferred
anterior,
midbody,
and
posterior
Tb's
of corn
snakes
(Elaphe
guttata).
Anterior
tempera-
tures were
found to be
significantly
greater
than
midbody.
Values
are
means
?1
SD.
Sample
sizes
are in
parentheses.
Snake
#
Anterior
Tb
Midbody
Tb Posterior
Tb
1
26.7
+
2.29
(23)
26.0
?
2.24
(43)
27.0
+
2.14
(43)
2
28.1
+
1.37
(38)
27.4
+
1.47
(43)
27.3
+
1.66
(45)
3
29.1
+
1.61
(35)
28.1
+
1.78
(45)
27.4
+
3.57
(44)
4 27.4
+
2.03
(32)
27.2
+
2.06
(41)
27.3
+
2.08
(42)
5 29.7
+
1.19
(40)
30.1
+
1.48
(44)
28.8
?
1.77
(44)
6 28.7
+
1.81
(40)
29.0
+
1.85
(43)
29.4
+
1.63
(35)
7
29.3
+
1.39
(27)
29.3
+
1.52
(42)
29.3
+
4.15
(43)
8 28.3
+
1.76
(16)
27.3
+
2.20
(23)
27.5
+
2.04
(22)
9
29.2
+
1.52
(17)
28.5
+
2.00
(18)
28.7
+
1.97
(18)
10
28.6
+
1.78
(39)
27.9
+
1.95
(41)
27.4
+
1.86
(44)
11
29.2
+
1.57
(32)
28.0
+
2.20
(43)
27.4
?
2.43
(44)
12
28.7
+
1.96
(36)
28.1
-
2.53
(42)
27.7
+
2.68
(44)
13
26.5
+
1.16
(26)
26.1
+
1.43
(33)
25.8
+
1.26
(32)
14
27.2
+
1.92
(27)
26.7
+
1.91
(38)
27.1
+
2.00
(41)
15
28.6
+
1.99
(26)
28.6
+
1.91
(31)
28.5
+
1.81
(42)
Mean
Tb
28.3
27.9
27.8
483
Au
SHORTER
COMMUNICATIONS
and
Dixon,
1988;
Keck,
1994;
McDonald and
Dutton,
1996;
Buhlmann and
Tuberville,
1998)
an
important
finding
of our
study
was
the
frequent expulsion
of PIT
tags by
the snakes.
Studies
of PIT
tag
retention in ro-
dents
(Harper
and
Batzli,
1996;
Schooley
et
al.,
1993)
and
fish
(Clugston,
1996)
showed 90-95% retention of
tags.
Several studies have tested for
apparent
detri-
mental effects
of PIT
tags
on
reptiles (Camper
and
Dixon, 1988; Keck, 1994;
Jemison
et
al.,
1995)
but
few
have
commented
on
PIT
tag
loss
in
reptiles
(Germano
and
Williams,
1993;
Jemison
et
al.,
1995).
Both
studies
(Germano
and
Williams,
1993;
Jemison
et
al.,
1995)
recommend
implanting
tags
into
the abdominal cav-
ity,
instead of
subcutaneously,
to reduce
the
possibility
of
tag
loss
through
the
injection
site. Because
all
of
the
tags expelled
by
snakes
in
our
study
were lost
through
the
digestive
tract,
questions
regarding
intra-perito-
neal
implantation
should
be of concern as well. We
recommend
that PIT
tag
retention should not
be as-
sumed
in
any study
and
a
secondary marking
tech-
nique
be used
as a
backup (e.g.,
scale
clipping).
The
ability
of
our
snakes to
expel
PIT
tags through
their
digestive
tracts has
major
implications
for
the
results
of
current
and
past
mark-recapture
studies and thus
warrants further
study.
Our documentation
of
a
small,
but
significant, pre-
ferred
temperature
difference
between the anterior
re-
gion
and
the
rest of
the
body
is consistent
with
past
research
and
supports
the
generalization
that
ecto-
therms
often
maintain
higher
temperatures
in their
anterior
region
(Heath,
1964;
DeWitt,
1967;
Webb
and
Heatwole,
1971;
Hammerson, 1977;
Block and
Carey,
1985;
Gregory,
1990;
Dorcas
and
Peterson,
1997).
Whereas the
mean
temperature
of
the
midbody
region
was not
significantly higher
than
that
of
the
posterior
region,
our
P-value
(0.049)
was
low
enough
to warrant
future
investigation.
While
the
advantages
of
main-
taining
a
higher
head
temperature
have
rarely
been
investigated,
we
suspect
that the
phenomenon
is
re-
lated
to
proper
functioning
of the central
nervous
sys-
tem
(Dorcas
and
Peterson,
1997).
Several
studies
have demonstrated
increased
ther-
moregulatory
precision
(i.e.,
reduced
variance)
in the
head
region
of
reptiles
and other animals
(Heath,
1964;
Webb and
Heatwole,
1971;
Taylor,
1972;
Ham-
merson,
1977;
Dorcas and
Peterson,
1997).
Thus,
we
were
surprised
that
we
found
no
differences in ther-
moregulatory
precision
among
the different
body
re-
gions.
We
hypothesize
that
although
our results ac-
curately
depict
the
precision
of
Tb
regulation,
these
results
cannot be
applied
to
free-ranging
ectotherms
because
temporal
variation
in the thermal environ-
ment
was
nonexistent.
Consequently,
our
snakes could
more
easily
maintain constant
body temperatures
in
all
regions
of their bodies
than could
free-ranging
snakes.
Future
laboratory
studies of
thermoregulatory
precision
in
reptiles
should
incorporate
variation in
the
spatial
and
temporal
distribution
of
available tem-
peratures.
For
example,
thermal
gradients
with a mo-
saic
of
temperatures
that
change
several times a
day
would
mimic
more
closely
situations
faced
by
free-
ranging
animals.
Our documentation
of increased
body
temperature
during
digestion
coincides
with numerous other stud-
ies
(Regal,
1966; Kollar,
1988;
Slip
and
Shine,
1988;
Gibson
et
al., 1989;
Lutterschmidt
and
Reinert, 1990;
Peterson et
al., 1993;
Dorcas
et
al.,
1997).
Postprandial
increases
in
temperature
facilitate faster
digestion
in
corn
snakes
(Greenwald
and
Kanter,
1979)
and
several
other snake
species (Skoczylas,
1970;
Stevenson et
al.,
1985;
Dorcas
et
al.,
1997).
While we
expected
a
mid-
body temperature
increase as was shown
by
Regal
(1966),
anterior and
posterior temperatures
also
in-
creased
during
digestion.
We
suggest
that the ob-
served increase in anterior
and
posterior
temperatures
was
an indirect effect of
increasing
the
midbody
tem-
perature
and does not
necessarily
serve
a
digestive
function.
Future snake research
using
passive integrated
transponders
should
focus
in
several areas.
First,
the
mechanism
by
which PIT
tags
are lost
through
the
digestive
tract should
be
investigated
and the fre-
quency
of
PIT
tag
loss
in
studies
of
free-ranging
snakes
should
be
determined.
Second,
systems
that
automatically
monitor the
Tb's
of
animals
implanted
with PIT
tags
can be
developed
(Peterson
and
Dorcas,
1992)
and should
be used to
expand
our
understand-
ing
of
daily
and seasonal variation
in
thermal
prefer-
ence,
and
the
effects of
factors such as
feeding
and
ecdysis.
Acknowledgments.-K.
Bemd,
E.
Dorcas,
K.
Dorcas,
S.
Lindsay,
R.
Roark,
and
J.
Roberts
provided
useful
comments
on the
manuscript.
We
thank P
Peroni for
help
with
statistical
analysis,
A. Becton for her
assis-
tance
with animal
maintenance,
and
W.
Kalinowski
and
S. Bennett
of the
South
Carolina
Department
of
Natural Resources
for
providing
the snakes used
in
this
study.
We also
thank C.
Peterson for numerous
discussions
resulting
in
many
of the ideas
presented
in
this
paper.
This
project
was conducted under
Ani-
mal Use Protocol
#3-98-02
granted
by
the
Davidson
College
Animal
Care
and
Use
Committee. Financial
support
was
provided
by
the
Department
of
Biology,
Davidson
College,
Davidson NC.
LITERATURE
CITED
AVERY,
R.
A.
1982. Field studies
of
body
temperatures
and
thermoregulation.
In
C. Gans and
F H.
Pough
(eds.),
Biology
of the
Reptilia,
Vol.
12,
pp.
93-166.
Academic
Press,
New
York.
BLOCK,
B.
A.,
AND
F
G.
CAREY. 1985.
Warm brain and
eye temperatures
in
sharks.
J.
Comp. Physiol.
B.
156:229-236.
BUHLMANN,
K.
A.,
AND
T.
D.
TUBERVILLE.
1998. Use of
passive
integrated
transponder
(PIT)
tags
for
marking
small freshwater
turtles. Chel. Conserv.
Biol.
3:102-104.
CAMPER,
J.
D.,
AND
J.
R. DIXON. 1988. Evaluation of a
microchip
marking system
for
amphibians
and
reptiles.
Texas
Parks and
Wildlife
Dept.
Res. Publ.
7100-159:1-22.
CLUGSTON,
J.
P. 1996.
Retention of T-bar anchor
tags
and
passive
integrated transponder
tags by gulf
sturgeons.
N. Amer.
J.
Fish.
Manage.
16:682-685.
CONANT, R.,
AND
J.
T. COLLINS.
1991. A Field Guide
to
Reptiles
and
Amphibians:
Eastern
and Central
North
America.
Houghton
Mifflin
Co., Boston,
Massachusetts.
DEWITT,
C. B. 1967. Precision
of
thermoregulation
and
its
relation to environmental
factors in the desert
iguana,
Dipsosaurus
dorsalis.
Physiol.
Zool. 40:49-
66.
484
SHORTER COMMUNICATIONS
DILL,
C.
D.
1972.
Reptilian
core
temperatures:
varia-
tion within
individuals.
Copeia
1972:577-579.
DORCAS,
M.
E.,
AND
C. R. PETERSON.
1997.
Head-body
temperature
difference
in
free-ranging
rubber
boas.
J.
Herpetol.
31:87-93.
,
AND
M.
E.
T.
FLINT. 1997.
The thermal
biology
of
digestion
in rubber boas
(Charina
bottae):
physiology,
behavior,
and
environmental
con-
straints.
Physiol.
Zool.
70:292-300.
GERMANO,
D.
J.,
AND
D. F.
WILLIAMS. 1993.
Field
eval-
uation
of
using
Passive
Integrated
Transponders
(PIT)
tags
to
permanently
mark lizards.
Herpetol.
Rev. 24:54-56.
GIBSON,
A.
R.,
D. A.
SMUCNY,
AND
J.
KOLLAR.
1989.
The effects
of
feeding
and
ecdysis
on
temperature
selection
by young
garter
snakes
in
a
simple
ther-
mal mosaic.
Can.
J.
Zool.
67:19-23.
GREENWALD,
O.
E.,
AND
M. E. KANTER.
1979.
The ef-
fects of
temperature
and
behavioral
thermoregu-
lation
on
digestive
efficiency
and
rate
in corn
snakes
(Elaphe
guttata
guttata).
Physiol.
Zool. 52:
398-408.
GREGORY,
P. T. 1990.
Temperature
differences
between
head
and
body
in
garter
snakes
(Thamnophis)
at
a
den in central
British
Columbia.
J.
Herpetol.
24:
241-245.
HAMMERSON,
G.
A.
1977.
Head-body
temperature
dif-
ferences
monitored
by telemetry
in
the snake
Mas-
ticophis flagellum
piceus.
Comp.
Biochem.
Physiol.
57:399-402.
HARPER,
S.
J.,
AND G.
0.
BATZLI.
1996.
Monitoring
use
of
runways by
voles
with
passive
integrated
tran-
sponders.
J.
Mammal.
77:364-369.
HEATH,
J.
E. 1964.
Head-body temperature
differences
in
horned
lizards.
Physiol.
Zool.
37:273-279.
HEINRICH,
B. 1974.
Thermoregulation
in
endothermic
insects.
Science
185:747-756.
HUEY,
R.
B. 1982.
Temperature,
physiology,
and
the
ecology
of
reptiles.
In
C. Gans
and E
H.
Pough
(eds.),
Biology
of
the
Reptilia,
Vol.
12,
pp.
25-91.
Academic
Press,
New
York.
JEMISON,
S.
C.,
L. A.
BISHOP,
P. G.
MAY,
AND
T.
M.
FARRELL.
1995.
The
impact
of
PIT-tags
on
growth
and movement
of
the
rattlesnake,
Sistrurus
miliar-
ius.
J.
Herpetol.
29:129-132.
KECK,
M. B. 1994.
Test
for
detrimental
effects
of
pit
tags
in neonatal
snakes.
Copeia
1994:226-228.
KLEIBER,
M.
1961.
The
Fire of
Life:
An
Introduction to
Animal
Energetics.
John
Wiley
&
Sons
Inc.,
New
York.
KOLLAR,
J.
1988.
Influences
on
temperature
selection
in
young
common
garter
snakes
(Thamnophis
sir-
talis).
Unpubl.
M.S.
Thesis,
Cleveland
State
Univ.,
Cleveland,
Ohio.
LILLYWHITE,
H.
B. 1980.
Behavioral
thermoregulation
in
Australian
Elapid
snakes.
Copeia
1980:452-458.
.1987.
Temperature,
energetics,
and
physiolog-
ical
ecology.
In R.
A.
Seigel,
J.
T.
Collins,
and
S.
S.
Novak
(eds.),
Snakes:
Ecology
and
Evolutionary
Biology,
pp.
422-477.
MacMillian
Press,
New
York.
LUTTERSCHMIDT,
W.
I.,
AND
H.
K. REINERT.
1990.
The
effect
of
ingested
transmitters
upon
the
tempera-
ture
preference
of the northern
water
snake,
Nero-
dia s.
sipedon.
Herpetologica
46:39-42.
MCDONALD,
D.
L.,
AND P. H. DUTTON. 1996.
Use
of
PIT
tags
and
photoidentification
to revise
emigra-
tion estimates of
leatherback sea turtles
(Dermoche-
lys
coriacea)
nesting
in St.
Croix,
U.S.
Virgin
Is-
lands,
1979-1995.
Chel.
Conserv.
Biol. 2:148-152.
PETERSON,
C.
R.,
AND M.
E.
DORCAS. 1992.
The use
of
automated
data
acquisition
techniques
in monitor-
ing
amphibian
and
reptile
populations.
In D. R.
McCullough
and R.
H.
Barrett
(eds.),
Wildlife 2001:
Populations,
pp.
369-378.
Elsevier
Applied
Science,
London.
,A.
R. GIBSON,
AND M.
E.
DORCAS.
1993. Snake
thermal
ecology:
the
causes and
consequences
of
body temperature
variation.
In
R.
A.
Seigel
and
J.
T.
Collins
(eds.),
Snakes:
Ecology
and
Behavior,
pp.
241-314.
McGraw
Hill,
New
York.
POUGH,
F
H.,
AND W.
N. MCFARLAND. 1976.
A
phys-
ical
basis
for
head-body temperature
differences
in
reptiles. Comp.
Biochem.
Physiol.
53:301-303.
REGAL,
P.
J.
1966.
Thermophilic response
following
feeding
in
certain
reptiles.
Copeia
3:588-590.
SCHOOLEY,
R.
L.,
B. VAN
HORNE,
AND K. P. BURNHAM.
1993.
Passive
integrated
transponders
for
marking
free-ranging
Townsend's
ground squirrels.
J.
Mam-
mal.
74:480-484.
SEIGEL,
R. A. 1993.
Future
research on
snakes,
or how
to combat "lizard
envy."
In
R.
A.
Seigel,
J.
T. Col-
lins,
and
S.
S.
Novak
(eds.),
Snakes:
Ecology
and
Evolutionary Biology,
pp.
395-401.
MacMillian
Press,
New
York.
SIEVERT,
L.
M.,
AND
V.
H.
HUTCHISON.
1988.
Light
ver-
sus heat:
thermoregulatory
behavior in
a
nocturnal
lizard
(Gekko
gecko).
Herpetologica
44:266-273.
SKOCZYLAS,
R. 1970.
Influence
of
temperature
on
gas-
tric
digestion
in
the
grass
snake
Natrix
natrix
L.
Comp.
Biochem.
Physiol.
33:793-804.
SLIP,
D.
J.,
AND R. SHINE.
1988.
Reptilian
endothermy:
a field
study
of
thermoregulation
by
brooding
di-
amond
pythons.
J.
Zool.
(London)
216:367-378.
STEVENSON,
R.
D.,
C. R.
PETERSON,
AND
J.
S.
TSUJI.
1985. The
thermal
dependence
of
locomotion,
tongue
flicking,
digestion
and
oxygen
consump-
tion
in the
wandering
garter
snake.
Physiol.
Zool.
58:46-57.
TAYLOR,
C. R. 1972.
The desert
gazelle:
a
paradox
re-
solved.
In G.
M. 0.
Maloiy
(ed.),
Comparative
Physiology
of Desert
Animals
Symposium,
Zoo-
logical
Society
of
London,
No.
31,
pp.
215-227.
Ac-
ademic
Press,
London.
Tu,
M.
C.,
AND
V.
H.
HUTCHISON.
1994.
Influence of
pregnancy
on
thermoregulation
of
water
snakes
(Nerodia
rhombifera).
J.
Therm.
Biol. 19:255-259.
,
AND
.
1995.
Interaction
of
photoperiod,
temperature,
season,
and diet
cycles
on
the ther-
moregulation
of
water
snakes
(Nerodia
rhombifera).
Copeia
1995:289-293.
WEBB,
G.
J.,
AND H.
HEATWOLE.
1971.
Patterns
of heat
distribution within
the
bodies
of some
Australian
pythons.
Copeia
1971:209-220.
,
C.
R.
JOHNSON,
AND
B. T. FIRTH.
1972.
Head-
body
temperature
differences
in lizards.
Physiol.
Zool.
45:130-142.
Accepted:
23
April
2000.
485
