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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
J. Matthias Starck
, Patrick Moser
, Roland A. Werner
and Petra Linke
Department of Biology II, University of Munich (LMU), Luisenstrasse 14–16, D-80333 Munich, Germany
Institute of Zoology and Evolutionary Biology, University of Jena, Erbertstrasse 1, D-07743 Jena, Germany
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 (
C). For
two weeks after feeding we quantified the CO
exhaled by pythons and determined its isotopic
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
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
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 (
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
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
C and
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
C signature distinctly different
from that of the snake, then analysis of the
904 J. M. Starck and others Source of fuel for SDA
signature of the exhaled CO
could determine the source
of the catabolized fuel—the meal or the snake. The analy-
sis of ratios of stable isotopes of carbon (
C and
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
C signature of exhaled CO
is a reliable estimator of the isotopic composition of the
substrates catabolized by an animal (Tieszen & Fagre
1993). We fed
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
to be
enriched in
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
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
C signature of the exhaled
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
C signature in exhaled breath is not
expected to change immediately after feeding.
(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
from mice reared on the corn diet showed that
they were clearly enriched in
C of –16.26 ± 2.05‰)
relative to mice fed on standard rodent pellets (δ
C of –25.89 ±
0.189‰; difference in δ
C of 9.63‰). Five snakes were fed on
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
) 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
) was bubbled through a solution
of concentrated KOH to scrub off CO
and dried (silica gel blue;
Roth GmbH, Germany) before entering the metabolic chamber.
The air stream vented from the metabolic chamber to the O
analyser was re-dried before entering the oxygen analyser. We
calculated mass-specific V
(ml g
), corrected for standard
temperature and pressure, by taking the lowest 10 min interval
that did not change by more than 0.01% O
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
C of exhaled CO
and tissue samples
from the snakes and performed post-run off-line calculation and
blank correction for assigning the final δ
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
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
residual breath air. Usually, seven injections were done from one
sample. The resulting CO
peaks were evaluated isotopically and
placed on the V-PDB scale using laboratory air standards.
(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:
= 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:
= 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)
mucosal thickness (mm)
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).
oxygen consumption (ml h
4 2 024681012
time from feedin
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
(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
C values of tissues and exhaled air.
(Three to five repeats were measured for n individuals.)
source δ
C (‰) n
snake adipose tissue, –25.06 ± 1.42 2
snake muscle tissue, –23.99 ± 0.11 2
snake liver tissue, –23.32 ± 1.63 2
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
, 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
= 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
C ‰) for the
exhaled CO
of fasting snakes (n = 8) was
24.30 ± 0.03‰. This value is within the 95% confidence
limits of the δ
C in the adipose tissue of snakes (of
25.06 ± 1.42‰; table 1). Although we lack statistical
power in this comparison, the
C signature of the
exhaled CO
of fasting snakes is closest to the isotopic
composition of their adipose tissue. The snakes’ exhaled
had a lower δ
C (by 1.8‰) than the exhaled CO
of mice fed on conventional pellets, reflecting the isotopic
fractionation of bulk diet to breath CO
in the snake.
Within 24 h after feeding, the
C signature of exhaled
breath of snakes fed
C-enriched mice (n = 5) rose rapidly
to peak ratios of –15.5 ± 1.32‰ at 48 h after feeding.
Thus, the δ
C of snakes exceeded the –16.26 ± 2.05‰
measured for the exhaled CO
of mice fed on corn diet
(figure 3). From the third day after feeding, the isotope
ratio of the exhaled CO
of snakes declined slowly towards
more depleted values. By the end of measurements,
14 days after feeding, the snakes had not reached fasting
C values.
In snakes that were fed mice raised on standard pellet
food the δ
C of exhaled CO
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
C in the exhaled breath occurred
within 24 h after feeding. The dynamics of the δ
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
= 99.17, p = 0.002); body mass was not significant
as a covariate (F
= 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
C values before feeding were significantly lower
than those after feeding (ANOVA with Tukey–HSD post
hoc: p 0.05).
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
; 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
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
in other vertebrates (Tieszen & Fagre 1993; Hatch et al.
2002). Twenty-four hours after feeding snakes with iso-
topically enriched mice, the CO
of the exhaled air of the
snakes was enriched in
C. This shows unambiguously
that the snakes switched the source of fuel. No other
source is possible, which shows that the snakes have meta-
bolized the prey to fuel the postprandial metabolism. The
peak in
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
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
2 0 2 4 6 8 10 12 14
C (‰)
C of exhaled breath from ‘enriched’ mouse
C of exhaled breath from ‘normal’ mouse
time from feeding (days)
Figure 3. The
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
C (pure corn diet);
white symbols are from those fed with mice raised on standard rodent pellets. The horizontal upper line at δ
C = –16 is the
mean of the exhaled air of mice fed with
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
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
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
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
C profile of exhaled breath from the depleted values of
adipose tissue to the less depleted values of mouse. After
feeding, the δ
C ratios of the exhaled air of control snakes
were constant over the entire period of measurements. We
did not observe declining δ
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 first 36 h following ingestion of a meal are characterized by a rapid increase in oxygen consumption, which matches the rate when the python moves at its maximum speed of 1.5 km/hour (Secor et al. 2000a;Hicks and Bennett 2004). Oxygen consumption then gradually declines to fasted rates by one to two weeks postfeeding Starck et al. 2004;McCue et al. 2005;Wang and Rindom 2021). In parallel with increased oxygen consumption, Burmese python organs (except for the brain) also undergo massive increases in size, including the intestines, liver, kidneys, pancreas, lungs and heart in the first 72 h following meal ingestion (Andersen et al. 2005;Lignot et al. 2005;Andrew et al. 2017). ...
... Interestingly, a study of another closely related species, the Ball python (Python regius), found that these predators do not withdraw from their own energy stores to pay off the debt. Instead, Ball pythons use energy from their digesting prey to fuel metabolism (Starck et al. 2004). Given these findings, the analogy between python SDA and automobile fueling may be better revised to 'pay-while-pumping'. ...
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Non-traditional animal models present an opportunity to discover novel biology that has evolved to allow such animals to survive in extreme environments. One striking example is the Burmese python (Python molurus bivittatus), which exhibits extreme physiological adaptation in various metabolic organs after consuming a large meal following long periods of fasting. The response to such a large meal in pythons involves a dramatic surge in metabolic rate, lipid overload in plasma, and massive but reversible organ growth through the course of digestion. Multiple studies have reported the physiological responses in post-prandial pythons, while the specific molecular control of these processes is less well-studied. Investigating the mechanisms that coordinate organ growth and adaptive responses offers the opportunity to gain novel insight that may be able to treat various pathologies in humans. Here, we summarize past research on the post-prandial physiological changes in the Burmese python with a focus on the gastrointestinal tract, heart, and liver. Specifically, we address our recent molecular discoveries in the post-prandial python liver which demonstrate transient adaptations that may reveal new therapeutic targets. Lastly, we explore new biology of the aquaporin 7 gene that is potently upregulated in mammalian cardiac myocytes by circulating factors in post-prandial python plasma.
... Pythons can ingest prey exceeding half of their own body mass (Secor, 2008), stimulating a massive, systemic upregulation of metabolic rate and digestive function within 24 h of the meal (Cox and Secor, 2008;Lignot et al., 2005;Secor and Diamond, 1995). To support the dramatically increased demands, the cardiovascular system is also upregulated at this time, with up to 5-fold increases in ventilation rate, cardiac output and heart rate (Starck et al., 2004), and metabolic rate may increase as much as 44-fold to support the energetic demands of digestion, assimilation and organ growth (Secor, 2008;Secor and Diamond, 1997). ...
... During a python's SDA response, when significant postprandial metabolic regulation is necessary, brain cell proliferation is low or similar to baseline levels. It is possible that brain cell proliferation may not increase at this point because most of the python's energy is focused toward the immediate need: the energetically expensive process of digesting and absorbing a large meal, in which both body reserves and nutrients from the ingested meal are used to 'pay' for the metabolic costs of feeding (Secor and Diamond, 1995;Starck et al., 2004). Visceral organs of pythons respond to feeding by upregulating many genes related to metabolic processes, cell growth and proliferation, and protective responses to oxidative stress (Andrew et al., 2015(Andrew et al., , 2017Duan et al., 2017), in keeping with the fact that proliferation of cells in these organs occurs during the SDA window. ...
Pythons are model organisms for investigating physiological responses to food intake. While systemic growth in response to food consumption is well documented, what occurs in the brain is currently unexplored. In this study, male ball pythons (Python regius) were used to test the hypothesis that food consumption stimulates cell proliferation in the brain. We used 5-bromo-12'-deoxyuridine as a cell-birth marker to quantify and compare cell proliferation in the brain of fasted snakes and those at two and six days after a meal. Throughout the telencephalon, cell proliferation was significantly increased in the six-day group, with no difference between the two-day group and controls. Systemic postprandial plasticity occurs quickly after a meal is ingested, during the period of active digestion; however, the brain displays a surge of cell proliferation after most digestion and absorption is complete.
... Pythons show highly elevated (up to 160-fold) levels of plasma triglycerides following a meal (Secor & Diamond, 1995;Secor & Nagy, 2000). These elevated plasma triglyceride levels were originally attributed to some form of mobilisation of endogenous lipid stores (Secor & Diamond, 1995;Secor & Nagy, 2000), but later studies showed that prey items underwent rapid digestion and absorption (Starck et al., 2004;Fig. 1. Major lipid transport processes in reptiles during feeding. ...
... During feeding, levels of triglycerides should rise in the plasma due to the input of enteromicrons from the gut and the input of VLDL from the liver due to lipogenesis from glucose or amino acids (Fig. 1). Unlike the rapid digestive processing of birds, reptiles have slow digestion, and some species can take several weeks to become post-absorptive (Starck et al., 2004;Amorocho & Reina, 2008). Thus the pulse of plasma triglycerides is likely to be dampened and long compared to birds. ...
Lipid metabolism is central to understanding whole-animal energetics. Reptiles store most excess energy in lipid form, mobilise those lipids when needed to meet energetic demands, and invest lipids in eggs to provide the primary source of energy to developing embryos. Here, I review the mechanisms by which non-avian reptiles store, transport, and use lipids. Many aspects of lipid absorption, transport, and storage appear to be similar to birds, including the hepatic synthesis of lipids from glucose substrates, the transport of triglycerides in lipoproteins, and the storage of lipids in adipose tissue, although adipose tissue in non-avian reptiles is usually concentrated in abdominal fat bodies or the tail. Seasonal changes in fat stores suggest that lipid storage is primarily for reproduction in most species, rather than for maintenance during aphagic periods. The effects of fasting on plasma lipid metabolites can differ from mammals and birds due to the ability of non-avian reptiles to reduce their metabolism drastically during extended fasts. The effect of fasting on levels of plasma ketones is species specific: β-hydroxybutyrate concentration may rise or fall during fasting. I also describe the process by which the bulk of lipids are deposited into oocytes during vitellogenesis. Although this process is sometimes ascribed to vitellogenin-based transport in reptiles, the majority of lipid deposition occurs via triglycerides packaged in very-low-density lipoproteins (VLDLs), based on physiological, histological, biochemical, comparative, and genomic evidence. I also discuss the evidence for non-avian reptiles using 'yolk-targeted' VLDLs during vitellogenesis. The major physiological states - feeding, fasting, and vitellogenesis - have different effects on plasma lipid metabolites, and I discuss the possibilities and potential problems of using plasma metabolites to diagnose feeding condition in non-avian reptiles.
... Riquelme et al., 2011;Slay et al., 2014), and metabolism (e.g. Castoe et al., 2013;Secor and Diamond, 1997;Starck et al., 2004). Additionally, the biology of Burmese pythons is of interest because, though they are endangered in parts of their native range (Jiang et al., 2016), they have proliferated in and caused severe damage to the Greater Everglades Ecosystem as an invasive species (e.g. ...
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Identifying which environmental and genetic factors affect growth pattern phenotypes can help biologists predict how organisms distribute finite energy resources in response to varying environmental conditions and physiological states. This information may be useful for monitoring and managing populations of cryptic, endangered, and invasive species. Consequently, we assessed the effects of food availability, clutch, and sex on the growth of invasive Burmese pythons (Python bivittatus Kuhl) from the Greater Everglades Ecosystem in Florida, USA. Though little is known from the wild, Burmese pythons have been physiological model organisms for decades, with most experimental research sourcing individuals from the pet trade. Here, we used 60 hatchlings collected as eggs from the nests of two wild pythons, assigned them to High or Low feeding treatments, and monitored growth and meal consumption for 12 weeks, a period when pythons are thought to grow very rapidly. None of the 30 hatchlings that were offered food prior to their fourth week post-hatching consumed it, presumably because they were relying on internal yolk stores. Although only two clutches were used in the experiment, we found that nearly all phenotypic variation was explained by clutch rather than feeding treatment or sex. Hatchlings from clutch 1 (C1) grew faster and were longer, heavier, in better body condition, ate more frequently, and were bolder than hatchlings from clutch 2 (C2), regardless of food availability. On average, C1 and C2 hatchling snout-vent length (SVL) and weight grew 0.15 cm d−1 and 0.10 cm d−1, and 0.20 g d−1 and 0.03 g d−1, respectively. Additional research may be warranted to determine whether these effects remain with larger clutch sample sizes and to identify the underlying mechanisms and fitness implications of this variation to help inform risk assessments and management. This article has an associated First Person interview with the first author of the paper.
... In fact, during high energetic demanding processes, BKA tends to decline, as demonstrated in pregnant pygmy rattlesnakes (S. miliarius) and during the absorptive meal period in bullfrogs (Lind et al., 2020;Figueiredo et al., in press). Meanwhile, snakes are able to obtain energy from prey to support part of the digestion processes (Starck et al., 2004;Waas et al., 2010). In this way, it is possible that we did not find any conclusive evidence of a tradeoff between immune function and feeding in boas because these animals were not energetically limited. ...
Feeding upregulates immune function and the systemic and local (gastrointestinal tract) concentrations of some immunoregulatory hormones, as corticosterone (CORT) and melatonin (MEL), in mammals and anurans. However, little is known about the immune and hormonal regulation in response to feeding in other ectothermic vertebrates, especially snakes, in which the postprandial metabolic changes are pronounced. Here, we investigated the effects feeding have on hormonal and innate immune responses in the snake, Boa constrictor. We divided juvenile males into two groups: fasting and fed with mice (30% of body mass). We measured the rates of oxygen consumption, plasma CORT levels, heterophil/lymphocyte ratio (HL ratio), plasma bacterial killing ability (BKA), and stomach and intestine MEL in fasting snakes and 48 h after meal intake. We observed increased rates of oxygen consumption, plasma CORT levels, and HL ratio, along with a tendency of decreased stomach and intestine MEL in fed snakes compared to fasting ones. BKA was not affected by feeding. Overall, we found that feeding modulates metabolic rates, CORT levels, and immune cell distribution in boas. Increased baseline CORT may be important to mobilize energy to support the metabolic increment during the postprandial period. Increased HL ratio might be an immunoregulatory effect of increased CORT, which has been shown in different physiological situations such as in response to immune challenge. Our results suggest that feeding activates the hypothalamic-pituitary-adrenal axis and modulates immune cell redistribution, possibly contributing to fighting potential injuries and infections derived from predation and from pathogens present in ingested food.
... Differences in MS among Bothrops species however were not correlated to the decrease in energy amount employed in digestion (assessed by the SDA values), and the interpretation of these results remains elusive. Accepting that at least a part of the energy employed during SDA is actually obtained from the actual meal (Starck et al., 2004), lower MS but equal SDA values could represent different pre-prandial energetic reserves of the animals. Thus, a snake with low energetic reserves could, in theory, invest less energy in digestion before start using the energy provided directly from the meal to support the remaining digestion. ...
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Feeding specialization is a recurrent issue in the evolution of snakes and is sometimes associated to morphological and/or behavioral adaptations that improve snake performance to exploit a particular food type. Despite its importance for animal fitness, the role of physiological traits has been much less studied than morphological and behavioral traits in the evolution of feeding specialization in snakes. In this context, the energetic cost of post-prandial period is an important physiological factor due to the remarkable effect on the snake energy budget. We collected data on post-prandial metabolic rate (SDA) in five species of pit vipers from the genus Bothrops with different degrees of mammal feeding specialization to test the hypothesis that feeding specialist species have lower energy costs during the digestion of their regular food item when compared to species with a more generalist diet. Our results support this hypothesis and suggest that ontogenetic changes in diet can be accompanied by changes in energy cost of the digestion process.
... Ectothermic animals have accordingly proven convenient for studies on the mechanisms that underlie the SDA response. Nevertheless, even though the metabolic stimulation of food has been studied since the time of Lavoisier, many aspects remain uncertain and there has been considerable controversy about the respective metabolic costs of intestinal growth, protein synthesis, gastric acid secretion, etc. (Secor, 2001(Secor, , 2003Beese, 2001, 2002;Starck et al. 2004). Given that the metabolic costs associated with feeding and digestion are an integral part of organismal function and permeate virtually all aspects of an organism's physiology and ecology, it is important to understand these mechanisms. ...
... The increased heart rate and stroke volume of the postprandial snakes, a hallmark of the specific dynamic action response in pythons Secor et al., 2000;Starck et al., 2004), clearly persisted during anaesthesia, giving credence to the experimental approach of using anaesthetized animals to unravel the physiological mechanisms underlying the rise in stroke volume during digestion. In the present study, we provide evidence supporting an unchanged contractile force during digestion, which only leaves an increased cardiac filling as the underlying cause for an increased postprandial stroke volume. ...
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To accommodate the pronounced metabolic response to digestion, pythons increase heart rate and elevate stroke volume, where the latter has been ascribed to a massive and fast cardiac hypertrophy. However, numerous recent studies show that heart mass rarely increases, even upon ingestion of large meals, and we therefore explored the possibility that a rise in mean circulatory filling pressure (MCFP) serves to elevate venous pressure and cardiac filling during digestion. To this end, we measured blood flows and pressures in anaesthetized Python regius. The anaesthetized snakes exhibited the archetypal tachycardia as well as a rise in both venous pressure and MCFP that fully account for the approximate doubling of stroke volume. There was no rise in blood volume and the elevated MCFP must therefore stem from increased vascular tone, possibly by means of increased sympathetic tone on the veins. Furthermore, although both venous pressure and MCFP increased during volume loading, there was no evidence that postprandial hearts were endowed with an additional capacity to elevate stroke volume. In vitro measurements of force development of paced ventricular strips also failed to reveal signs of increased contractility, but the postprandial hearts had higher activities of cytochrome oxidase and pyruvate kinase, which probably serves to sustain the rise in cardiac work during digestion.
... Research into the SDA of vertebrates known to digest relatively large meals at relatively infrequent intervals, has revealed that SDA is fuelled using a mixture of endogenous and exogenous nutrients (Starck et al., 2004;Waas et al., 2010), but those studies were not able to identify which classes of nutrients (e.g., carbohydrates, lipids, and amino acids) provided this energy. Indeed, the postprandial oxidative kinetics of different classes of nutrients have been studied in other animals including humans (Hoekstra et al., 1996;Labayen et al., 2004a;Labayen et al., 2004b), rodents (McCue et al., 2014), reptiles (McCue et al., 2015a), and birds (Swennen et al., 2007;McCue et al., 2010;McCue et al., 2011). ...
The energetics of processing a meal is crucial for understanding energy budgets of animals in the wild. Given that digestion and its associated costs may be dependent on environmental conditions, it is crucial to obtain a better understanding of these costs under diverse conditions and identify resulting behavioural or physiological trade-offs. This study examines the speed and metabolic costs - in cumulative, absolute, and relative energetic terms - of processing a bloodmeal for a major zoonotic disease vector, the tsetse flyGlossina brevipalpis, across a range of ecologically-relevant temperatures (25°C, 30°C & 35°C). Respirometry showed that flies used less energy digesting meals faster at higher temperatures but that their starvation tolerance was reduced supporting the prediction that warmer temperatures are optimal for bloodmeal digestion while cooler temperatures should be preferred for unfed or post-absorptive flies.(13)C-Breath testing revealed that the flies oxidized dietary glucose and amino acids within the first couple of hours of feeding and overall oxidized more dietary nutrients at the cooler temperatures supporting the premise that warmer digestion temperatures are preferred because they maximise speed and minimise costs. An independent test of these predictions using a thermal gradient confirmed that recently fed flies selected warmer temperatures and then selected cooler temperatures as they became postabsorptive, presumably to maximize starvation resistance. Collectively these results suggest there are at least two thermal optima in a given population at any time and flies switch dynamically between optima throughout feeding cycles.
The postprandial period is characterized by a modification of the gastrointestinal activity after food intake, accompanied by an increase in metabolic rate, secretion of acids, and absorption of nutrients. For ectothermic vertebrates, those changes are particularly prominent given the relatively low metabolic cost and the low frequency of food uptake. However, prolonged fasting periods decrease energy reserves and may compromise the upregulation of costly processes, such as the increase in metabolic rate after resuming the meal intake. Assuming that the main source of energy needed to support such events is provided from the animal's own body reserves, our aim with this study is to test the hypothesis that the longer the period of fasting, the smaller the metabolic rate increase during the postprandial period, since lesser energy reserves trigger these increases. For this, we measured the oxygen consumption rates (V̇O2) of red‐eared slider turtles, Trachemys scripta elegans, submitted to different periods of fasting (47 and 102 days), before and after the ingestion of meals equivalent to 5% of their body masses. Despite the longer fasting period, which led to a reduction of 10.77% in the body mass of the turtles, there were no differences between the two experimental groups regarding maximum V̇O2 values after food intake (V̇O2 peak), postprandial metabolic scope, mean time to V̇O2 peak, and postprandial duration. Results indicate that 102 fasting days does not compromise aerobic metabolic increase during postprandial period and does not impair digestive process of the turtles, even with a loss of body mass. Highlights • 102 Days of fasting reduced body mass of the turtles Trachemys scripta elegans but not impair the metabolic increase after a new meal intake. The turtles use their energy reserves to sustain the postprandial metabolism.
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SYNOPSIS Analysis of natural stable isotope ratios has created a methodological upheaval in animal ecology. Because the distribution of stable isotopes in organisms follows reliable patterns, their analyses have become established useful methods for animal ecologists. However, because animal ecologists have adopted a phenomenological approach to the use of stable isotopes, the mechanisms that create isotope variation patterns remain unexplored. The mass-balance models that can provide a mechanistic, and hence predictive foundation for animal isotopic ecology are presented here. We review and elaborate the current mixing models used to reconstruct animal diets and develop new mathematical models to explain one of the most widely used patterns in animal isotopic ecology: enrichment in 15 N observed across trophic levels. Construction of element and isotope budgets is central to testing the mass-balance models described herein. Because the concept of a budget is central to all animal physiological ecology, development of a mechanistic and predictive framework for isotopic animal ecology falls naturally on physiological ecologists. We argue that progress in isotopic animal ecology hinges on laboratory experiments that explore mechanism, documentation of pattern in the field, and theoretical integration of mechanism and pattern.
A newly developed interface coupling a CHN combustion device (elemental analyser ‘EA’) to an isotope ratio mass spectrometer is described and evaluated. The purpose of the device is to extend the dynamic range of δ¹³C and δ¹⁵N analysis from less than 2 orders of magnitude to more than 3 orders of magnitude. Carbon isotope ratio measurements of atropine as a model compound have been performed analysing between 1 µg to 5 mg C with acceptable to excellent precision (0.6 to 0.06‰, δ-notation). The correction due to the blank signal is critical for sample amounts smaller than 4 µg C. The maximum sample weight is determined by the combustion capacity of the EA. Larger sample amounts are measured using dilution of a small part of the EA effluent with helium. The dilution mechanism works virtually free of isotope fractionation. Copyright © 1999 John Wiley & Sons, Ltd.
The isotopic ratios of common light elements often provide useful information about past geologic, environmental, or biologic history. Bender’s (1968) clear identification of two distinct isotopic values for carbon from C3 and C4 plant organic matter led to the experiments which showed that animal δ13C values were closely related to dietary values (DeNiro and Epstein 1978a; Tieszen et al. 1983). Results from field applications (DeNiro and Epstein 1978b; Vogel 1978; Tieszen et al. 1979; Tieszen and Imbamba 1980) established the usefulness of these tracers and soon led to numerous archaeological studies. C and N, both present in bone collagen, have been most useful to suggest marine versus terrestrial dependence, to establish maize utilization or dependence on legumes, and to identify relative trophic-level positions or carnivory versus herbivory. Recently, attention has been focused on the use of bioapatite CO3 (Lee-Thorp et al. 1989a, 1989b; Lee-Thorp and van der Merwe 1991) as a supplement to collagen, especially in bones older than 10000 years, and as an adjunct to collagen for estimates of carnivory. The 180 signal in bioapatite also has the potential to provide information on the water status of the individual or the environment. Sulfur isotopes δ 34 S), when present in sufficient quantities, as in hair or skin, are also useful and in some cases can distinguish clearly between marine and terrestrial dietary sources (Krouse and Herbert 1988).
The pivotal role played by fat in suppyling energy for migration in birds has been appreciated for nearly 4 decades and reviewed extensively (Odum and Perkinson 1951; King and Farner 1956; Berthold 1976; Blem 1976, 1980; Dawson et al. 1983). The basic biochemistry, physiology, and bioenergetics of migratory fattening have been identified; yet, the regulatory mechanisms involved remain obscure. On the one hand, the behavioral and physiological functions associated with migration are thought by some to be an expression of an endogenous (genetic) program that relies little upon cues from the environment (Berthold 1985). Conversely, environmental information is regarded by others as playing an instrumental role in the regulation of such migratory functions as hyperphagia, fattening, and Zugunruhe (nocturnal restlessness) (Stetson and Erickson 1972; Schwabl and Farner 1989a,b; Wingfield, this Vol.). Recently, Wingfield et al. (this Vol.) proposed a scheme for classifying environmental and endogenous factors that regulate migratory phenomenon. Specifically, vernal (spring) fattening is triggered by initial predictive factors that include an increase in photoperiod and endogenous programs (Wingfield et al., this Vol.). However, the supplementary factors that guide the progression and termination of both vernal and autumnal fattening are not well understood.
Compared with other reptiles, pythons have a relatively low standard metabolic rate (SMR) when post-absorptive, but metabolism increases substantially after feeding. This study examined the effects of feeding and fasting on adult and hatchling water pythons (Liasis fuscus). We compared ratios of peak digestive metabolic rate (PDMR) after feeding with the metabolic rate of both post-absorptive (SMR) and fasted water pythons. If metabolic rate of a fasting snake is taken as ‘SMR’, then the ratio PDMR/SMR becomes increasingly exaggerated as fasting continues. After 56 days of fasting in adults, or after 45 days in hatchlings, the metabolic rate of water pythons was significantly lower than that of post-absorptive animals. Peak digestive metabolic rate of post-absorptive adult water pythons was only 6.3–12.0 times SMR, but the ratio was twice that if fasted (metabolically depressed) animals were used to determine the ‘SMR’ denominator. Thus, this ratio should be used with caution. Peak digestive metabolic rate after feeding increased with increasing meal size for meals less than 20% of body mass, but PDMR did not increase for meals between 20% and 39% of body mass for adult water pythons. Similarly, the PDMR did not increase signif icantly between 25% and 50% meal sizes for hatchlings. The digestive physiology of water pythons is apparently better suited to frequent meals of relatively small prey compared with the digestive physiology of some other pythons.
Plasma fat metabolites were measured during the nocturnal migratory flight in three species of small passerines. The birds had higher free fatty acid (FFA) and glycerol levels than resting birds that had been fasted overnight. In contrast to exercising mammals and large birds, they also had elevated levels of triglyceride and the very low density lipoprotein (VLDL) fraction. It is hypothesized that FFA reesterification in the liver and delivery of triglyceride-VLDL to the flight muscles helps to circumvent constraints in energy supply during endurance locomotion in animals with very high mass-specific metabolic rates.
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.