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Pythons metabolize prey to fuel the response to feeding

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We investigated the energy source fuelling the post-feeding metabolic upregulation (specific dynamic action, SDA) in pythons (Python regius). Our goal was to distinguish between two alternatives: (i) snakes fuel SDA by metabolizing energy depots from their tissues; or (ii) snakes fuel SDA by metabolizing their prey. To characterize the postprandial response of pythons we used transcutaneous ultrasonography to measure organ-size changes and respirometry to record oxygen consumption. To discriminate unequivocally between the two hypotheses, we enriched mice (= prey) with the stable isotope of carbon (13C). For two weeks after feeding we quantified the CO2 exhaled by pythons and determined its isotopic 13C/12C signature. Ultrasonography and respirometry showed typical postprandial responses in pythons. After feeding, the isotope ratio of the exhaled breath changed rapidly to values that characterized enriched mouse tissue, followed by a very slow change towards less enriched values over a period of two weeks after feeding. We conclude that pythons metabolize their prey to fuel SDA. The slowly declining delta13C values indicate that less enriched tissues (bone, cartilage and collagen) from the mouse become available after several days of digestion.
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Received 4 November 2003
Accepted 8 January 2004
Published online 24 March 2004
Pythons metabolize prey to fuel the response to
feeding
J. Matthias Starck
1,2*
, Patrick Moser
2
, Roland A. Werner
3
and Petra Linke
3
1
Department of Biology II, University of Munich (LMU), Luisenstrasse 14–16, D-80333 Munich, Germany
2
Institute of Zoology and Evolutionary Biology, University of Jena, Erbertstrasse 1, D-07743 Jena, Germany
3
Max-Planck-Institute of Biogeochemistry, Winzerlaer Str. 10, D-07745 Jena, Germany
We investigated the energy source fuelling the post-feeding metabolic upregulation (specific dynamic
action, SDA) in pythons (Python regius). Our goal was to distinguish between two alternatives: (i) snakes
fuel SDA by metabolizing energy depots from their tissues; or (ii) snakes fuel SDA by metabolizing their
prey. To characterize the postprandial response of pythons we used transcutaneous ultrasonography to
measure organ-size changes and respirometry to record oxygen consumption. To discriminate unequivo-
cally between the two hypotheses, we enriched mice (= prey) with the stable isotope of carbon (
13
C). For
two weeks after feeding we quantified the CO
2
exhaled by pythons and determined its isotopic
13
C/
12
C
signature. Ultrasonography and respirometry showed typical postprandial responses in pythons. After feed-
ing, the isotope ratio of the exhaled breath changed rapidly to values that characterized enriched mouse
tissue, followed by a very slow change towards less enriched values over a period of two weeks after
feeding. We conclude that pythons metabolize their prey to fuel SDA. The slowly declining δ
13
C values
indicate that less enriched tissues (bone, cartilage and collagen) from the mouse become available after
several days of digestion.
Keywords: stable isotopes; phenotypic flexibility; specific dynamic action; postprandial response
1. INTRODUCTION
The digestion and absorption of the nutrients contained
in a meal impose metabolic costs. This is especially evi-
dent in intermittent feeders, for example, reptiles. Many
lizards and snakes, some turtles and all crocodiles feed
intermittently (Ross 1987; Zug et al. 2001). Snakes, and
in particular the Burmese python, Python molurus, have
become unique model organisms in which to study the
physiological and morphological responses to feeding and
fasting (Secor & Diamond 1998). They tolerate long fast-
ing periods and then swallow a large meal, up to their own
body mass, which they assimilate within a week or two
(Green 1997). During fasting, the digestive system of
these ‘sit-and-wait foragers’ is small, and, presumably the
metabolic costs of running it are relatively low. However,
within 1 or 2 days after feeding, the size of the digestive
system increases, and gastric functions including the
expression of intestinal enzymes and intestinal brush-
border nutrient transporters are upregulated (Secor &
Diamond 1995). This rapid postprandial response is asso-
ciated with an upregulation of the metabolic rate, the spe-
cific dynamic action (SDA; Benedict 1932; Brody 1945;
Kleiber 1975). Increase in the size of the small intestine
is based on an increase in enterocyte size (cellular
hypertrophy) and does not involve the production of new
tissue (Starck & Beese 2001, 2002). The temporal associ-
ation of activation of the gastrointestinal tract, upregu-
lation of metabolic rate and the increase in organ size
stimulated the idea that sit-and-wait foraging snakes must
invest (pay) large amounts of energy mobilized from their
tissue stores (Secor & Diamond 1995) before they can
*
Author for correspondence (starck@uni-muenchen.de).
Proc. R. Soc. Lond. B (2004) 271, 903–908 903 2004 The Royal Society
DOI 10.1098/rspb.2004.2681
absorb (pump) the prey. Secor & Diamond (1995) coined
the term ‘pay before pumping’, an analogy to how some
gasoline stations operate in the USA.
Because the initial investment in pythons appears to be
relatively high, the question arises, what source fuels SDA?
Two possible sources of fuel for SDA can be hypothesized:
(i) in snakes only pre-digestive costs (i.e. initiation of
digestive processes) are paid by intracellular and
plasma fuel, while all other energy requirements dur-
ing postprandial metabolic upregulation are fuelled
from digested prey;
(ii) alternatively, one may assume that fuel is mobilized
from the snake’s energy depots (Secor & Diamond
1995, 1998; Secor & Nagy 2000; Secor 2001, 2003).
Only after restoration of the digestive system could
nutrients be absorbed and the fuel deposits reloaded
(Secor 2001, 2003).
Mobilization and metabolic breakdown of energy
depots built up after a meal would occur later during
maintenance or during the next cycle of postprandial
upregulation.
To characterize the postprandial response of Python
regius and to compare it with that of other snake species,
we used transcutaneous ultrasonography to measure
organ-size changes (small intestine and liver) and respiro-
metry to measure changes in metabolic rate. To determine
the origin of fuel for SDA, we used techniques allowing
us to quantify the ratios of the stable isotopes
13
C and
12
C.
These isotopes are incorporated into the carbon skeletons
of lipids, carbohydrates and proteins of the prey and do
not interfere with digestion and oxidation of the prey. If
the prey possesses a
13
C/
12
C signature distinctly different
from that of the snake, then analysis of the
13
C/
12
C
904 J. M. Starck and others Source of fuel for SDA
signature of the exhaled CO
2
could determine the source
of the catabolized fuel—the meal or the snake. The analy-
sis of ratios of stable isotopes of carbon (
13
C and
12
C) in
exhaled air is a completely non-invasive tool to trace car-
bon or nitrogen through metabolic pathways (Hatch et al.
2002; Karasov & Martinez del
´
o 2004; Martinez del
´
o & Wolf 2004). The
13
C/
12
C signature of exhaled CO
2
is a reliable estimator of the isotopic composition of the
substrates catabolized by an animal (Tieszen & Fagre
1993). We fed
13
C-enriched prey to snakes to determine
whether SDA is fuelled from endogenous energy stores or
from the prey directly. If SDA is fuelled through metabolic
breakdown of the prey, we expect the exhaled CO
2
to be
enriched in
13
C originating from the prey. Of course,
resource mixing is possible between the prey and the
snake’s tissue. However, an isotope profile of the snake’s
exhaled CO
2
that is similar to that of the prey will indicate
that SDA is fuelled more or less exclusively by breakdown
of the prey, while isotope profiles more intermediate
between those of the snake’s adipose tissue and the prey
will indicate different levels of resource mixing. If, by con-
trast, SDA is fuelled through metabolic breakdown of the
snake’s energy depots, for example fatty acids from adi-
pose tissue or protein from muscle and other tissue stores,
we would expect that the
13
C/
12
C signature of the exhaled
CO
2
of the snake would mirror the isotopic composition
of the tissue of the snake. During fasting and digesting,
the source of fuel would be the snake’s tissue, and conse-
quently the
13
C/
12
C signature in exhaled breath is not
expected to change immediately after feeding.
2. MATERIAL AND METHODS
(a) Animals
We purchased 10 juvenile captive-raised pythons, P. regius
(body mass range of 120–209 g, median of 150 g), from a com-
mercial breeder (CITES no.: E0343/02). Animals were housed
in 50 cm × 50 cm × 80 cm cages, with water, heating and shelter.
Cage temperature ranged from 25 to 30 °C, air humidity was
70% and light was 12 L : 12 D. Snakes were fed with live mice
at biweekly intervals. Meal size was ca. 25% of the snake’s body
mass. The net gain in body mass of the snakes was on average
7% after one meal. The snakes were kept in the laboratory for
six months prior to experimentation.
(b) Preparation of food
Gravid mice (CD1 strain) were obtained from the university’s
breeding stock (Department of Biology, University of Jena) and
randomly assigned to one of two groups. In the first group,
females and their offspring were fed standard rodent pellets
(Altromin 1320; crude protein 10%, crude fat 4%, crude fibre
6%, ash 7%, moisture 13.5% and nitrogen-free extract 50.5%).
In the other group, females and their offspring were fed exclus-
ively on corn, supplemented with vitamins and protein (minced
meat) sufficient to satisfy growth requirements. Measurement of
exhaled CO
2
from mice reared on the corn diet showed that
they were clearly enriched in
13
C(δ
13
C of –16.26 ± 2.05‰)
relative to mice fed on standard rodent pellets (δ
13
C of –25.89 ±
0.189‰; difference in δ
13
C of 9.63‰). Five snakes were fed on
the
13
C-enriched mice and three snakes were fed on mice raised
on standard rodent pellets. The remaining two juvenile pythons
were used for tissue samples (described in § 2f ).
Proc. R. Soc. Lond. B (2004)
(c) Ultrasonography
We used a portable Sonosite 180plus ultrasonography system
(Sonosite Inc., Bothel, WA, USA) equipped with a 5–10 MHz
broadband linear array transducer for B-image ultrasonography.
The spatial resolution of the system is less than 0.02 mm. The
snakes were scanned while partly submersed in water, resulting
in a working distance of 1–2 cm, which allows for optimal image
quality. Ultrasound sessions were recorded on digital video, and
still images for morphometry of organ size were later extracted
from videotapes. The livers and the small intestines of six snakes
(three snakes fed enriched mice and three snakes fed pellet-diet
mice) were scanned daily, from 2 days before until 12 days after
feeding. Ultrasound measurements were taken from the same
regions of the liver and small intestine for each snake.
(d) Morphometry and statistics
From video recordings of ultrasound sessions we extracted
still images at 760 × 840 pixel resolution. A minimum of five
images per session were retrieved for both the liver and small
intestine. We used SigmaScan v. 5.0 (Jandel Sci., SPSS Inc.,
Chicago, IL, USA) as the morphometry program. From ultra-
sonographs, we measured the cross-section of the liver and the
thickness of the mucosa of the small intestine. From the liver
cross-sections we took one measurement; from the small-
intestinal mucosa we took multiple measurements. We used
daily means of multiple measurements for statistics. None of the
variables differed from a normal distribution. Values as given
are means ± standard deviation (s.d.) of n individuals. We used
repeated-measures analysis of covariance (repeated-measures
ANCOVA) to analyse the data. Feeding group (enriched mice
versus standard mice) was the inter-subject factor, day after
feeding was the within-subject factor and body mass was the
covariate. If the covariate was not significant, we used a univari-
ate ANOVA with Tukey–honestly significant difference (HSD)
post hoc test to analyse differences among days. SPSS v. 11.0
was used for all statistical analyses.
(e) Respirometry
Rates of oxygen consumption (V
˙
O
2
) were measured in an
open flow system (FOX Field Oxygen Analyser; Sable Systems,
Las Vegas, NV, USA). The oxygen consumptions of eight
snakes (mean body mass = 147 ± 34 g) were measured once per
day starting 3 days before feeding and continuing until 11 days
after feeding. Measurements were made at 30 °C in the dark for
90–120 min. The volume of the metabolic chamber was 500 ml.
The air stream (35 ml min
1
) was bubbled through a solution
of concentrated KOH to scrub off CO
2
and dried (silica gel blue;
Roth GmbH, Germany) before entering the metabolic chamber.
The air stream vented from the metabolic chamber to the O
2
analyser was re-dried before entering the oxygen analyser. We
calculated mass-specific V
˙
O
2
(ml g
–1
h
–1
), corrected for standard
temperature and pressure, by taking the lowest 10 min interval
that did not change by more than 0.01% O
2
concentration.
Metabolic data were analysed with the Data Can software
(Sable Systems Inc.).
(f ) Samples for isotope analysis
At the end of each metabolic trial, three breath samples were
taken directly from the air stream leaving the oxygen analyser.
Breath samples were aspired in evacuated 10 ml glass containers
sealed with airtight septa (Exetainer; Labco Ltd, High
Wycombe, UK). Tissue samples were taken from two snakes
that had rejected food for several weeks. These snakes were
Source of fuel for SDA J. M. Starck and others 905
killed by an overdose of pentobarbital (Nembutal; Hoechst
Roussel Vet, Germany). Three samples each (0.1–0.5 g) of adi-
pose tissue, muscle and liver were taken from each snake and
frozen at –25 °C (other tissues were preserved for future
studies). Later, tissue samples were dried at 55 °C for 24 h and
prepared for isotopic analysis as described in § 2g.
(g) Stable-isotope analysis
We measured the δ
13
C of exhaled CO
2
and tissue samples
from the snakes and performed post-run off-line calculation and
blank correction for assigning the final δ
13
C values on the V-
PDB (Vienna-Pee Dee Belemnite) scale following the ‘IT prin-
ciple’ as described in Werner & Brand (2001). Bulk tissue
samples, laboratory reference materials (including quality-
control standards) and blanks were dried, ground into a fine
powder, loaded into tin cups and combusted quantitatively
using an elemental analyser (NA 1110 equipped with an AS 128
autosampler, both CE Instruments, Rodano, Italy) attached to
a delta C isotope ratio mass spectrometer (Finnigan MAT, Bre-
men, Germany) using a ConFlo III interface (Werner et al.
1999). Breath samples were measured with a gas chromatograph
(GasBench II; Finnigan MAT). A sample vial is analysed by
piercing the septum with a double-wall needle connected to two
fused silica capillaries. The feed capillary delivers pure He; the
exhaust capillary flushes the sample gas in He at a rate of ca.
0.3 ml min
1
over a Nafion dryer and then through an injection
loop from which a GC run (Poraplot Q 25 m × 320 µm i.e. held
at room temperature) is started for separating the CO
2
from
residual breath air. Usually, seven injections were done from one
sample. The resulting CO
2
peaks were evaluated isotopically and
placed on the V-PDB scale using laboratory air standards.
3. RESULTS
(a) Ultrasound morphometry
In fasting snakes, the thickness of the small-intestinal
mucosa was on average 4.5 ± 0.7 mm (n = 6). Within 48 h
after feeding, mucosal thickness doubled to reach
8.7 ± 1.1 mm (n = 6). Four days after feeding the thickness
of the mucosa began to decrease (figure 1). Two weeks
after feeding the thickness of the mucosa had returned to
the size in fasted snakes. Mucosal-size changes were inde-
pendent of whether snakes were fed standard mice or iso-
topically enriched mice (repeated-measures ANCOVA:
F
1,3
= 0.417, p = n.s., body mass was not significant as a
covariate). Differences between days were analysed with
a Tukey–HSD post hoc test. On the first day after feeding
the mucosal thickness was already significantly thicker
than during fasting (Tukey–HSD:
= 0.05; see figure 1).
Mucosal thickness peaked at days 2 and 3 after feeding.
Although slowly declining from day 4 after feeding, the
mucosal thickness was significantly higher than during
fasting until day 10 after feeding.
The cross-sectional diameter of the liver increased from
11 ± 0.1 mm in fasting snakes to 13 ± 0.2 mm at days 3
and 4 after feeding. Food type, i.e. normal versus iso-
topically enriched mice, had no effect on the response. We
pooled data from two days before feeding and two days
after feeding for statistical analysis. Feeding had a highly
significant effect on liver size (univariate ANCOVA:
F
1.1
= 14.33, p 0.001, body mass was not significant as
a covariate). The size increase occurred later than that in
the small intestine and was less clearly marked. Liver size
Proc. R. Soc. Lond. B (2004)
2 0 2 4 6 8 10 12
time from feeding (days)
10
9
8
7
6
5
4
mucosal thickness (mm)
feeding
a
a
a
bc
bc
c
c
b
b
b
b
b
b
ab
ab
Figure 1. Postprandial response of the thickness of the
small-intestinal mucosa as measured by ultrasonography in
Python regius (n = 6 snakes). Multiple measurements of each
individual were averaged by individual and day. Because
there were no differences between snakes fed on standard
mice and snakes fed on isotopically enriched mice, we
pooled all data for the graph. Values are means ± s.d.
Measurements started 3 days before feeding (which took
place on day 0) and continued for 12 days after feeding.
Tukey–HSD test for differences among means: means
labelled with different letters are significantly different
(
= 0.05).
0.25
0.20
0.15
0.10
0.05
oxygen consumption (ml h
1
g
1
)
4 2 024681012
time from feedin
g
(
da
y
s
)
a
a
a
a
a
a
feeding
c
c
c
c
bbb
b
b
Figure 2. Oxygen consumption of Python regius (n = 8) for
3 days before and 11 days after feeding a meal equivalent to
ca. 25% of body mass. Because there were no differences
between snakes fed on standard mice and snakes fed on
isotopically enriched mice, we pooled all data for the graph.
Values are means ± s.d. Tukey–HSD test for differences
among means: means labelled with different letters are
significantly different (
= 0.05).
remained enlarged for a longer period and did not decline
to the original size within the study period of two weeks.
(b) Oxygen consumption
The oxygen consumption of fasting snakes (n = 8) was
0.07 ± 0.03 ml O
2
h
1
g
1
(average of 3 measurements
taken on 3 different days before feeding, i.e. one measure-
ment on day 3, one on day 2 and one on day 1 before
feeding). Two days after swallowing a meal of 25% of their
body mass, the snakes’ oxygen consumption peaked at
906 J. M. Starck and others Source of fuel for SDA
Table 1. The δ
13
C values of tissues and exhaled air.
(Three to five repeats were measured for n individuals.)
source δ
13
C (‰) n
snake adipose tissue, –25.06 ± 1.42 2
control
snake muscle tissue, –23.99 ± 0.11 2
control
snake liver tissue, –23.32 ± 1.63 2
control
mouse fed corn diet –16.26 ± 2.05 5
(exhaled air)
mouse fed standard –26.10 ± 0.19 5
food (exhaled air)
snakes fasting –24.30 ± 0.03 8
snakes fed enriched –15.50 ± 1.32 5
mice (day 1)
snakes fed standard –22.10 ± 0.23 3
mice (day 1)
0.21 ± 0.06 ml O
2
h
1
g
1
, i.e. metabolic rate increased by
a factor of 3.0 (figure 2). Oxygen consumption declined
relatively rapidly and reached fasting values within one to
two weeks after feeding. The stable-isotope composition
of the prey had no effect on oxygen consumption. All
snakes responded in exactly the same manner (repeated-
measures ANCOVA: F
1,3
= 2.67, p = 0.201) and body
mass was not significant as a covariate. When the data
were tested with a univariate ANOVA followed by a
Tukey–HSD test for differences among means, we
detected three subgroupings, i.e. before feeding, peak
values immediately after feeding and a decline of oxygen
consumption until day 9. On day 10 after feeding, oxygen
consumption had returned to fasting level (figure 2).
(c) Stable-isotope ratios
Stable-isotope ratios for muscle, adipose tissue and liver
are given in table 1. The isotope ratio (δ
13
C ‰) for the
exhaled CO
2
of fasting snakes (n = 8) was
24.30 ± 0.03‰. This value is within the 95% confidence
limits of the δ
13
C in the adipose tissue of snakes (of
25.06 ± 1.42‰; table 1). Although we lack statistical
power in this comparison, the
13
C/
12
C signature of the
exhaled CO
2
of fasting snakes is closest to the isotopic
composition of their adipose tissue. The snakes’ exhaled
CO
2
had a lower δ
13
C (by 1.8‰) than the exhaled CO
2
of mice fed on conventional pellets, reflecting the isotopic
fractionation of bulk diet to breath CO
2
in the snake.
Within 24 h after feeding, the
13
C/
12
C signature of exhaled
breath of snakes fed
13
C-enriched mice (n = 5) rose rapidly
to peak ratios of –15.5 ± 1.32‰ at 48 h after feeding.
Thus, the δ
13
C of snakes exceeded the –16.26 ± 2.05‰
measured for the exhaled CO
2
of mice fed on corn diet
(figure 3). From the third day after feeding, the isotope
ratio of the exhaled CO
2
of snakes declined slowly towards
more depleted values. By the end of measurements,
14 days after feeding, the snakes had not reached fasting
δ
13
C values.
In snakes that were fed mice raised on standard pellet
food the δ
13
C of exhaled CO
2
rose slightly from the fasting
value of –24.3 ± 0.03‰ to –22.10 ± 0.23‰ (average of
n = 3 animals over a period of 3 days after feeding; figure
Proc. R. Soc. Lond. B (2004)
3). The enrichment of
13
C in the exhaled breath occurred
within 24 h after feeding. The dynamics of the δ
13
C ratios
in both groups document a switch in fuelling metabolism
from the snakes’ own energy depots to the prey.
Repeated-measures ANCOVA with body mass as the
covariate showed a highly significant effect of isotopic
composition of food on isotopic composition of exhaled
air (F
1,3
= 99.17, p = 0.002); body mass was not significant
as a covariate (F
1,3
= 0.502, p = 0.53). To test for differ-
ences between days we separated the two groups (snakes
fed enriched mice and snakes fed ‘standard’ mice) and
used the Tukey–HSD post hoc test to check for significant
differences among means within each group indepen-
dently. For both feeding groups the test recognized two
subgroups, i.e. before feeding and after feeding (figure 3).
The δ
13
C values before feeding were significantly lower
than those after feeding (ANOVA with Tukey–HSD post
hoc: p 0.05).
4. DISCUSSION
Changes in organ size and oxygen consumption after
feeding were within the range that is known from other
studies of snakes, including different Python species
(Dorcas et al. 1997; Thompson & Withers 1999; Secor &
Diamond 2000; Bedford & Christian 2001; Starck &
Beese 2001, 2002; Overgaard et al. 1999, 2002; Toledo
et al. 2003; Wang et al. 2003; Zaidan & Beaupre 2003).
The postprandial response was moderate (twofold
increase in mucosal thickness and V
˙
O
2
; slight increase in
liver size) because meal size was only ca. 25% of the
pythons’ body mass and maintenance temperatures
ranged between 25 and 30 °C. Under these conditions we
did not expect stronger responses. Histological studies of
P. regius (T. Wang, A. Holmgren and J. M. Starck, unpub-
lished data) revealed exactly the same cytological response
to feeding as previously described in Burmese python and
garter snakes (Starck & Beese 2001, 2002).
Fasting snakes had δ
13
C ratios that were slightly more
negative than those of their prey. This difference was not
unexpected as it reflects the isotopic fractionation of bulk
diet to breath. Similar values have been reported for differ-
ences between total carbon in food items and exhaled CO
2
in other vertebrates (Tieszen & Fagre 1993; Hatch et al.
2002). Twenty-four hours after feeding snakes with iso-
topically enriched mice, the CO
2
of the exhaled air of the
snakes was enriched in
13
C. This shows unambiguously
that the snakes switched the source of fuel. No other
13
C-
source is possible, which shows that the snakes have meta-
bolized the prey to fuel the postprandial metabolism. The
peak in
13
C enrichment of exhaled breath suggests that,
at least for a day or two after feeding, the snakes fuelled
their metabolism predominantly with nutrients assimilated
from their prey. The changes in the δ
13
C profile towards
more negative values (figure 3) a few days later suggests
two interpretations as follows.
(i) It may indicate an increasing contribution of less
enriched prey tissue such as bone and collagen,
which becomes available only after several days of
digestion; for example, the bones of a rat in a
python’s stomach remain intact for 24–48 h after
feeding (Blain & Campbell 1942; Secor 2003).
Source of fuel for SDA J. M. Starck and others 907
feeding
a
α
α
α
α
a
a
a
b
bc
bc
bc
bc
bc
bc
bc
bc
β
β
βββ
β
ββ
β
β
β
β
bc
bc
bc
bc
bc
12
2 0 2 4 6 8 10 12 14
14
16
18
20
22
24
26
28
δ
13
C (‰)
δ
13
C of exhaled breath from ‘enriched’ mouse
δ
13
C of exhaled breath from ‘normal’ mouse
time from feeding (days)
Figure 3. The
13
C/
12
C signatures of the exhaled air of pythons during fasting (days –2–0) and after feeding a prey equivalent
to ca. 25% of body mass. Black symbols are means ± s.d. of pythons fed mice that were enriched in
13
C (pure corn diet);
white symbols are from those fed with mice raised on standard rodent pellets. The horizontal upper line at δ
13
C = –16 is the
mean of the exhaled air of mice fed with
13
C-enriched food. The lower horizontal line indicates the mean value for exhaled
breath of mice fed standard rodent food. Tukey–HSD test for differences among means: means in the same curve labelled
with different letters are significantly different (
= 0.05).
Thus, during the first days of SDA, the snake fuels
its metabolism predominantly from the soft tissues
of its prey, which are generally more enriched in
13
C
than are bone and collagen (Martinez del Rio
´
&
Wolf 2004).
(ii) Alternatively, the declining isotope ratio may indi-
cate that snakes increasingly mix different sources of
fuel, i.e. prey and the snake’s own body resources.
The results of the control experiment in which snakes
were fed mice raised on standard rodent pellets support
the view that snakes metabolize the prey to fuel SDA.
Within 24 h after feeding we observed a significant
increase in δ
13
C towards more enriched values, even when
snakes were fed mice raised on standard food (figure 3).
As pointed out in § 3c, the fasting snakes fuel their metab-
olism from adipose tissue, which is depleted in
13
C relative
to other tissues (table 1) owing to isotopic fractionation
(Hatch et al. 2002). After feeding, the snakes switch to
fuelling their metabolism from prey, thereby shifting the
13
C profile of exhaled breath from the depleted values of
adipose tissue to the less depleted values of mouse. After
feeding, the δ
13
C ratios of the exhaled air of control snakes
were constant over the entire period of measurements. We
did not observe declining δ
13
C values from differential
digestion of control mice, presumably because differences
in isotope ratios between different tissues were less than
in artificially enriched mice. This suggests to us that no
source mixing occurred and that snakes fuelled the entire
SDA by catabolizing the prey.
The results of our study support the hypothesis that
snakes fuel SDA by metabolizing their prey. The results
presented do not exclude ‘pay before pumping’ (Secor &
Diamond 1995; Secor 2001, 2003), which may hold as a
general principle of energy allocation for pre-absorptive
costs. As shown in this study, the ‘pay’ period in pythons
is short because within a day after feeding they switch to
Proc. R. Soc. Lond. B (2004)
fuelling the metabolic upregulation by metabolizing the
prey. We suggest that cytoplasmic fuel depots (glycogen
or lipids) are large enough to pay the pre-absorptive costs
of digestion and that the remaining costs of digestion are
paid from the prey. Elevated levels of triglycerides 24 h
after feeding in the blood plasma of Burmese pythons have
been cited as evidence for the mobilization of energy
depots from the snakes’ tissues (Secor & Diamond 1995,
1998; Secor & Nagy 2000). Free fatty acids as mobilized
from adipose tissue might undergo re-esterification to
triglycerides in the liver, as for example described in long-
distance migrating song birds (Ramenofsky 1990; Jenni-
Eiermann & Jenni 1992; Tso 1994). However, elevated
levels of plasma triglycerides together with ‘milky white
plasma’ (Secor & Diamond 1998, p. 660) are not
unequivocal evidence for lipid mobilization from adipose
tissue because plasma triglycerides also increase after
digestion and release from the gut. Thus, the observation
of elevated plasma triglycerides does not discriminate
between sources of fuel.
This study profited tremendously from many discussions with
C. Martinez del
´
o. The authors thank S. McWilliams, S.
Jenni-Eiermann and B. Helm for discussions and comments
on an earlier version of this paper. The authors gratefully
acknowledge W. Brandt for granting access to the stable iso-
tope facilities at the MPI in Jena. They thank S. Koch and H.
Geilmann for technical help in the laboratory.
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The standard metabolic rate for juvenile carpet pythons, Morelia spilota imbricata, with a mean body mass of 129.6 g (range 57.7–253 g) increased from 6.75 ± 0.96 (s.e.) mL h–1 to 42.6 ± 12.40 (s.e.) mL h–1 in 48 h after ingesting mice equal to approximately 23% of their body mass, at a temperature of 30°C. Sloughing increased metabolic rate to approximately 146% of standard metabolic rate at 30°C. Metabolic rate is elevated before the eyes become opaque and other visual signs indicate that a slough is imminent. The implications of these two factors when measuring standard metabolic rate are discussed.