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First published online November 28, 2008
Journal of Experimental Biology 211, 3767-3774 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.023754
Commentary |
Digestive physiology of the Burmese python: broad regulation of integrated performance
Department of Biological Sciences, The University of Alabama, Tuscaloosa, AL 35405, USA
e-mail: ssecor{at}biology.as.ua.edu
Accepted 10 October 2008
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Summary |
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 TOP Summary IntroductionThe ups and downs...Mechanisms of regulationWhy regulate?An integrated effortInsights into the python...References |
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Key words: cardiovascular, digestion, gastrointestinal, postprandial response, python model, Python molurus, regulation, specific dynamic action
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Introduction |
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TOPSummaryIntroductionThe ups and downs...Mechanisms of regulationWhy regulate?An integrated effortInsights into the python...References |
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). This foraging
mode successfully balances low foraging costs with modest rates of energy
intake; as such, snakes repeatedly spend weeks and even months between meals
(Slip and Shine, 1988;
Secor and Nagy, 1994;
Wilson, 2007). For the Burmese
python, native to southeastern Asia, the next meal could range from a monitor
lizard or ground-dwelling bird to a prey as formidable as a pangolin, deer or
leopard (Wall, 1912;
Murphy and Henderson, 1997).
When it does eventually capture a prey and feed, the python's previously
dormant gut rapidly resumes function to tackle the difficult task of digesting
a prey that may exceed half of the python's own body mass. Once digestion is
complete, the python's gut and associated organs return to their previous
quiescent state, where they remain until the next meal.
For the past 15 years, the Burmese python as well as other species of
sit-and-wait foraging snakes (rattlesnakes, boas and other pythons) have been
the subject of physiological study, especially of their digestive and
cardiovascular systems (Secor et al.,
1994; Secor and Diamond,
1995; Overgaard et al.,
1999; Secor et al.,
2000b; Andrade et al.,
2004; Starck and Wimmer,
2005; Ott and Secor,
2007). The attention that Burmese pythons and these other snakes
have received stems from the unprecedented magnitude of their morphological
and physiological responses to feeding and fasting. This trait potentially
allows the many mechanisms underlying digestive responses to be easily studied
and identified (Secor and Diamond,
1998). The attractiveness of the Burmese python as a research
model is also aided by the ease of procurement through the commercial animal
trade, and the fact that they are generally very docile and easy to maintain,
and are amenable to a variety of different experimental treatments.
The aim of this Commentary is to provide an updated and comprehensive narrative of the digestive responses of the Burmese python. The findings described originate from studies that used pythons raised in captivity (usually 400–1000 g) that were fed a rodent meal weighing approximately 20–25% of the snake's body mass. While much of the information presented originates from published articles, I have also included findings recently presented at scientific meetings. In covering the responses of different tissues, I shall illustrate the integrated nature of the Burmese python's feeding and fasting responses.
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The ups and downs of python digestion |
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TOPSummaryIntroductionThe ups and downs...Mechanisms of regulationWhy regulate?An integrated effortInsights into the python...References |
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; Starck and Beese,
2001; Secor, 2003;
Lignot et al., 2005;
Cox and Secor, 2008). The
activity of other organs is also reduced and is associated with a reduction in
the mass of the heart, liver, pancreas and kidneys, and a suppressed cardiac
output (Secor and Diamond,
1995; Starck and Beese,
2001; Secor et al.,
2000b; Cox and Secor,
2008).
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).
Once the prey is within the snake's stomach, the real challenge begins, for
the dead intact prey begins to putrefy. Gas produced by the prey's resident
bacteria distends the prey, further expanding the snake's girth
(Fig. 1B). While it is
inconceivable that the snake's stomach and body wall would rupture from this
pressure, the compression that the expanded stomach and lower esophagus exert
on the lungs and vascularization may interfere with ventilation and blood
flow. Therefore it is necessary for the python to rapidly initiate breakdown
of the prey to both relieve this pressure and move the meal into the small
intestine. However, in the absence of a steady baseline rate of fasting acid
production, which is characteristic of mammals, the oxyntopeptic cells of the
python's gastric mucosa must rapidly begin pumping H+ while
releasing the inactive protease pepsinogen and Cl– into the
lumen of the gastric pits (Forte et al.,
1980).
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)
(Fig. 2). Pythons continue HCl
production at a rate that maintains a luminal pH of 1.5–2 in spite of
the large buffering capacity of the meal itself
(Fig. 2). To fuel the
H+/K+-ATPase (proton pumps), the python's oxyntopeptic
cells are packed with mitochondria (40–50% by volume). By day 3 of
digestion, only 25% of the ingested meal remains within the stomach, and it is
largely composed of portions of trunk vertebrae, hind limbs, tail and hair.
After 6 days, all that may remain within the stomach is a mat of hair
(Cox and Secor, 2008)
(Fig. 2).
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). Upon entry into the small intestine, the acidic chyme is
rapidly neutralized, presumably by secreted HCO
–3, such that the chyme pH increases from 2.5 to
6.5 within several centimeters (Secor et
al., 2006). The chyme is also immediately joined by bile released
by the gall bladder and amylase, lipase and a slew of inactive proteases
released by the pancreas. Bile release is associated with a 64% decrease in
gall bladder contents after feeding, and the enzyme release is associated with
the rapid postprandial appearance of zymogen granules (storage depots of
active and inactive enzymes) within pancreatic acinar cells and activated
trypsin within the intestinal lumen (Secor
and Diamond, 1995; Cox and
Secor, 2008).
Even before the chyme has entered the small intestine, this previously
dormant tissue has already begun to upregulate form and function. Within 6 h
of feeding, with the prey still intact within the stomach, the small intestine
has responded by doubling microvillus length, amino acid uptake rates, and
aminopeptidase-N activity (Secor and
Diamond, 1995; Lignot et al.,
2005; Cox and Secor,
2008) (Figs 3 and
4). Twenty-four hours after
feeding, 17–27% of the prey has entered the small intestine, which has
increased in mass by 70%, quadrupled in microvillus length, and increased
nutrient uptake and hydrolase activity 3- to 10-fold
(Secor and Diamond, 1995;
Lignot et al., 2005;
Cox and Secor, 2008). Peaks in
intestinal form and function are usually observed at day 2 or 3 of digestion
when as much as 75% of the prey has passed out of the stomach
(Secor and Diamond, 1995;
Lignot et al., 2005;
Cox and Secor, 2008) (Figs
3 and
4). At this time, the small
intestine has dramatically increased its synthesis of oleoylethanolamide, a
lipid mediator known to induce satiety, more than 300-fold
(Astarita et al., 2006).
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). With
each continuing day of digestion, the cecum and large intestine fill with more
unabsorbed material. In addition, there is an accumulation in the distal end
of the large intestine of white chalky deposits of urate that has passed from
the kidneys via the ureters. Burmese pythons often pass a bolus of
urate between 3 and 7 days after feeding, and follow this a week or two later
by passing a combined bolus of urate and feces.
As the last of the meal exits the stomach and transverses the small
intestine, 6 to 7 days after feeding, these organs begin to downregulate. By
day 10, stomach pH has risen beyond 6, pancreatic trypsin and amylase activity
have dropped by 50%, the intestine has decreased in mass by 35%, microvillus
length has been reduced by 50%, and intestinal nutrient uptake rates and
hydrolase activities have returned to levels not significantly different from
those prior to feeding (Secor et al.,
2006; Cox and Secor,
2008) (Figs 2,
3,
4,
5). At this time, other organs
have begun to reverse their postprandial response: notable is the 23% decrease
in liver and kidney mass. Thus, just as pythons rapidly upregulate the
structure and function of tissues and organs after feeding begins, so they
downregulate tissue mass and performance at a similar pace with the final
passage of the meal.
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Mechanisms of regulation |
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TOPSummaryIntroductionThe ups and downs...Mechanisms of regulationWhy regulate?An integrated effortInsights into the python...References |
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). Another
piece of evidence for a hormonal role is the observation that intestinal
segments isolated from contact with luminal nutrients, but still maintaining a
vascular supply, can with time upregulate function after feeding
(Secor et al., 2000a). The
importance of a luminal signal in triggering the initial intestinal response
was identified from the direct infusion of different nutrient solutions into
the python's small intestine. In response to the direct infusion of a mixed
amino acid or protein solution, the small intestine upregulates function and
experiences hypertrophy of the epithelium
(Secor et al., 2002). In
contrast, the infusion of a saline, glucose or lipid solution into the small
intestine does not elicit any increase in function
(Secor et al., 2002).
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). For enterocytes that populate the tips and edges of
the villi in the anterior small intestine, their increase in width is
contributed in part by the absorption of lipids originating from the meal
(Starck and Beese, 2001;
Lignot et al., 2005). A
postprandial increase in the rate of enterocyte replication has been observed
for Burmese pythons using several different techniques
(Secor et al., 2000a;
Starck and Beese, 2001;
Lignot and Secor, 2003).
Python enterocytes continue to replicate during fasting, although after
feeding rates of replication increase severalfold
(Secor et al., 2000a;
Starck and Beese, 2001;
Lignot and Secor, 2003). The
extent to which hyperplasia contributes to mucosal growth appears to be
dampened by the concurrent increase in apoptosis, programmed cell death
(Lignot and Secor, 2003). This
suggests that the intestinal epithelium of the Burmese python experiences a
postprandial increase in the rate of cell turnover, which may stem from the
greater activity of the cells and their increased exposure to luminal
contents.
The capacity of the python's intestine to modulate nutrient uptake and
enzyme activities stems from one or several different cellular mechanisms. We
could imagine that apical membrane nutrient transporters and enzymes simply
increase or decrease their rates of activity, as proposed for developmental
changes in intestinal function associated with ontogenetic shifts in diet
(Buddington and Diamond, 1992;
Toloza and Diamond, 1990).
Alternatively, python enterocytes could increase the synthesis of transporters
and enzymes with feeding, and increase the density of these apical proteins,
thereby increasing mass-specific function. This mechanism has been used to
explain the increase in glucose uptake for mice switched from a low to a high
carbohydrate diet (Ferraris et al.,
1992). A third mechanism would involve an increase in the apical
surface area of enterocytes. Pythons actually experience such a response with
the postprandial lengthening of their microvilli. By assuming that membrane
transporter and enzyme densities remain unchanged, the 5-fold length change of
the microvilli would generate a similar relative increase in function. In
general, intestinal uptake rates and enzyme activities increase by 3- to
8-fold with feeding (Secor and Diamond,
1995; Cox and Secor,
2008). The shortening of the microvilli once digestion is complete
would therefore explain the concurrent downregulation of intestinal nutrient
transport and enzyme activities.
Whilst we can explain much of the regulation of intestinal function by the modulation of microvillus length, what we cannot explain at present is the means by which the microvilli lengthen and shorten so quickly. Because this response in pythons is unprecedented in the literature, there are no prior descriptions of the cellular mechanisms that result in rapid lengthening of intestinal microvilli. The most parsimonious scenario is that all of the individual components of the microvilli are sequestered within the enterocyte cytoplasm and feeding triggers a signaling cascade that results in the trafficking of these components to the apical edge. There they are assembled on the tips of the pre-existing microvilli in a similar fashion to the construction of a skyscraper (Fig. 7). The polymerization of monomeric G-actin into filamentous F-actin, which forms the microvillus internal skeleton, is important in this process. Evidence for this process includes our observation of a shift from G-actin-laden enterocytes in fasted pythons to a dense concentration of apical F-actin after feeding. Additionally, we have found in preliminary studies that the postprandial growth of the python's microvilli is stunted by the direct administration of cytochalasin D, an inhibitor of actin polymerization, into the small intestine.
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Why regulate? |
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TOPSummaryIntroductionThe ups and downs...Mechanisms of regulationWhy regulate?An integrated effortInsights into the python...References |
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; Secor and
Diamond, 2000; McWilliams and
Karasov, 2001; Kroghdahl and Bakke-Mckellep, 2005;
Secor, 2005a). What sets
pythons, and other infrequently feeding snakes, apart is the sheer magnitude
of their regulatory response. Instead of a 25–50% increase in intestinal
mass and a 50–100% increase in mass-specific nutrient uptake rates
commonly observed with feeding or a change in diet, pythons double the mass of
their small intestine and increase nutrient uptake rates by 5- to 10-fold
(Secor, 2005b;
Ott and Secor, 2007). When
integrated for the complete small intestine, the capacity to hydrolyze and
absorb nutrients with an increase in demand may at best double for most
vertebrates. For the python, however, intestine functional capacity increases
as much as 10- to 20-fold after feeding, before declining after digestion is
completed (Secor, 2005b;
Ott and Secor, 2007).
Inquiries into why pythons regulate GI performance so dramatically have
focused our attention on the postdigestive downregulatory responses rather
than on the impressive postfeeding upregulatory responses. Any organism that
is predestined to feed infrequently due to their particular feeding habits or
strict seasonality of food would benefit from the selection for a reduced rate
of basal energy expenditure. Of all the tissues of the body, those of the gut
are relatively expensive to maintain due in part to the costs of acid
production, pancreatic and intestinal secretion, nutrient transport, ion
homeostasis and epithelial turnover
(Reenstra and Forte, 1981;
Cant et al., 1996;
Nyachoti et al., 2000). Hence,
selection would favor the depression of GI activity during long periods of
fasting, especially if these periods are predictable. Although the energy
expended by an idling snake gut has not been quantified, we have found that
species of snakes that downregulate their guts with fasting possess standard
metabolic rates that are almost 50% lower than rates characteristic of snakes
species that feed more frequently and only modestly regulate their guts with
fasting (Secor and Diamond,
2000; Ott and Secor,
2007). The downregulation of GI form and function by pythons and
other infrequently feeding snakes after completing digestion can therefore be
envisaged as an adaptive response that serves to conserve energy during
predictable long episodes of fasting
(Secor and Diamond, 2000b;
Secor, 2005b). On the other
side of the coin, the preferred adaptive strategy for frequently feeding
snakes is to maintain an idling intestinal tract during their short bouts of
fasting (Secor and Diamond,
2000; Secor,
2005b). Testing the validity of these adaptive scenarios for
snakes, other reptiles and even amphibians will require further examination of
the fasting and feeding responses of the GI tract over a broader range of
lineages and feeding habits.
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An integrated effort |
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TOPSummaryIntroductionThe ups and downs...Mechanisms of regulationWhy regulate?An integrated effortInsights into the python...References |
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). For the
Burmese python, the profile of the SDA response is quite similar to that of
other animals, being characterized by a rapid postfeeding increase in
metabolic rate followed by a slower return to basal rates
(Secor, 2009). Although
similar in profile, it is the magnitude of the python's postprandial metabolic
response that is eye-catching, highlighted by as much as a 44-fold increase in
metabolic rate and equal to as much as 37% of the ingested meal's energy
(Secor and Diamond, 1997b)
(Fig. 8). Assumed to be
entirely aerobic (plasma lactate <0.5 mmol l–1), the
python postprandial metabolic response can be significantly affected by body
temperature, meal composition and size
(Overgaard et al., 1999).
Decreasing body temperature prolongs the metabolic response while increasing
the protein content or the size of the meal generates a larger SDA response
(Secor and Diamond, 1997b;
Wang et al., 2003;
McCue et al., 2005)
(Fig. 8).
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; Powolny et al.,
2007). Endogenous as well as ingested lipids and glucose are
suspected to fuel the elevated tissue performance as suggested by the
postfeeding increase in plasma levels and, specifically for glucose, the
increased concentration of injected 2-[18F]fluoro-2-deoxyglucose
within tissues observed using positron emission tomography
(Secor and Diamond, 1997b;
Secor and Diamond, 1998;
Starck et al., 2004)
(Fig. 9).
The Burmese python coordinates feeding and fasting responses across organs
and tissues and this is reflected in the collective changes in their mass and
function. With feeding, the pancreas doubles in mass and experiences
significant increases in enzyme activities, while the gall bladder declines in
mass as bile is secreted into the small intestine
(Secor and Diamond, 1995;
Cox and Secor, 2008)
(Fig. 10). The python's liver
and kidneys can double in mass after feeding, which suggests matched
upregulation of hepatic and renal performance in response to feeding
(Secor and Diamond, 1995;
Starck and Beese, 2001)
(Fig. 10). Driven by the
increase in tissue metabolism, the python responds with a 5-fold increase in
ventilation and cardiac output, the latter being a function of a 3- to 4-fold
increase in heart rate and a 50% increase in stroke volume
(Secor et al., 2000b;
Secor and White, 2007). The
increase in stroke volume is due in part to a 40% increase in cardiac mass
(Secor and Diamond, 1995;
Andersen et al., 2005)
(Fig. 10). As predicted,
pythons experience a very large postprandial increase in intestinal blood
flow, highlighted by an 11-fold increase in flow through the superior
mesenteric artery (Secor and White,
2007). The Burmese python's postprandial intestinal hyperemia
appears in part to be mediated (via vasodilatation) by the regulatory
peptide neurotensin, whose plasma concentration increases 3.3-fold with
feeding (Secor et al., 2001;
Skovgaard et al., 2007).
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; Secor et al., 2000). Whilst they do not experience any
postprandial change in arterial PO2, arterial
PCO2 does increase by approximately 30%
(Overgaard et al., 1999;
Overgaard and Wang, 2002).
Digestion also generates an increase (35%) in plasma [HCO
–3] and a decrease (13%) in plasma
[Cl–] due to the exchange between the circulation and the
gastric epithelium of Cl– for HCO
–3; the former is channeled into HCl production
(Secor and Diamond, 1997a;
Overgaard et al., 1999;
Overgaard and Wang, 2002). The
potential for a postprandial metabolic alkalosis, an `alkaline tide',
resulting from increased blood [HCO –3] is
lessened by the concurrent increase in PCO2, such that
there is no significant change in arterial pH (7.45–7.62) with feeding
(Overgaard et al., 1999;
Overgaard and Wang, 2002).
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Insights into the python model |
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"When we summon a physician to the house or consult him at his office, we do not stop to realize that many a lowly animal, such as the snake, has indirectly contributed its small share to the learning possessed by the physician."Francis Benedict (Benedict, 1932a
Burmese pythons, and other sit-and-wait foraging snakes, possess a
tremendous capacity to alter GI form and function with feeding and fasting
(Secor and Diamond, 2000;
Ott and Secor, 2007). Each
meal triggers dramatic increases in metabolism, upregulation of tissue
function and tissue growth. Upon the completion of digestion, these
postprandial responses are thrown into reverse; tissue function is
collectively downregulated and tissues undergo atrophy. The extreme plasticity
of their GI tissue enables pythons to be very tractable research models to
experimentally investigate the signaling and cellular mechanisms that underlie
the regulation of digestive tissues (Secor
and Diamond, 1998; Secor, 2005). In 1929, August Krogh wrote, `For
such a large number of problems there will be some animal of choice or a few
such animals on which it can be most conveniently studied'
(Krogh, 1929). Krogh was
probably not thinking of the python when he penned his renowned Krogh
Principle, though it is certain that the python exemplifies his sentiments. It
was not that much later that the python was introduced in print as a valuable
animal for research and training by Francis Benedict, the author of the quote
that begins this section and the first to document the python's large
postprandial metabolic response (Benedict,
1932a; Benedict,
1932b).
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; Pope et al.,
2007) (Fig. 11);
(4) the fate of the intestinal microbial community during long episodes of
fasting and their role during digestion; and (5) the signals and mechanisms
that underlie the postprandial hypertrophy of python heart, liver, pancreas
and kidneys (Secor and Diamond,
1995; Starck and Beese,
2001; Andersen et al.,
2005). In securing their place as a model of the Krogh Principle,
pythons will continue to generate new discoveries in physiology. |
Acknowledgments |
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References |
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TOPSummaryIntroductionThe ups and downs...Mechanisms of regulationWhy regulate?An integrated effortInsights into the python...References |
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