The physiological response to digestion in snakes: A feast for the integrative physiologist

doi:10.1016/j.cbpa.2020.110891

Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology

Volume 254, April 2021, 110891

https://doi.org/10.1016/j.cbpa.2020.110891 Get rights and content

Highlights

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All animals must eat to derive chemical energy in the food to fuel metabolic processes.
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Many snakes have extreme feeding biology with prolonged fasting and ingestion of enormous meals.
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The rise in metabolism during digestion is most likely due to increased rates of protein synthesis.
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Gastric acid secretion leads to an alkaline tide (increased plasma HCO₃^-) attended by hypoventilation to maintain pH.
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The SDA response is supported by large increases in heart rate and stroke volume.

Abstract

Many snakes can subdue and swallow very large prey after many months of fasting. The functional capacity and the mass of the gastrointestinal organs regress during fasting, but are quickly restored upon feeding. This phenotypic flexibility appears to be energetically inexpensive, and represents a key adaptation that enables snakes to match digestive performance without compromising bodily energy stores prior to nutrient absorption. The reorganization of the intestines resembles the unfolding of an accordion where the individual enterocytes expand, primarily in response to luminal presence of nutrients. The very large rise in postprandial metabolism (specific dynamic action), where the rate of oxygen consumption can increase four- to six-fold, is likely due to a global rise in protein synthesis in all tissues. The rise in oxygen consumption is sustained by a pronounced tachycardia that, in part, is caused by un-identified humoral factor(s) with positive chronotropic effects, and a rise in stroke volume, where venous return may be augmented by a rise in venous tone. The immediate stimulation of gastric acid secretion causes a metabolic alkalosis (the alkaline tide), but pH remains unchanged due to a rise in arterial PCO₂ caused by a proportionally smaller elevation of ventilation than for CO₂ production (i.e., hypoventilation). Given the magnitude of the physiological responses to feast and famine, snakes provide a unique animal model to study regulation of organ function in response to rapid transitions in demands as well as an avenue to study a multitude of functional interactions among organ systems.

Graphical abstract

Introduction

Life costs energy and all animals must eat to fuel basal metabolic rate, physical work, growth and reproduction. Before being able to absorb the energy-rich nutrients across the small intestine, vertebrates rely on a combination of mechanical and enzymatic degradation within the gastrointestinal system. This mechanical work, synthesis and secretion of enzymes and digestive juices as well as the post-absorptive processes, including growth, incurs an energetic cost. The increase of metabolism with digestion, typically referred to as specific dynamic action of food (or SDA response), precedes nutrient absorption and must be fueled by existing bodily energy stores.

Vertebrates typically exhibit considerable changes in both form and function of the gastrointestinal organs as they transition between fasting and digestion. This reversible phenotypic flexibility is particularly pronounced in animals that experience prolonged fasting and ingest large meals under natural conditions, such as many species of snakes (Fig. 1). The down-regulation of digestive processes during fasting is believed to reduce energy expenditure for tissue maintenance and thereby serves to prolong the period where internal energy stores can provide for energy expenditure. However, this strategy is only viable as long as the animal can restore adequate digestive function to absorb the nutrient from the meal when food is available. It is therefore likely that natural selection has favored energetically inexpensive solutions to the rapid upregulation of digestive processes in animals that normally experience prolonged fasting.

The regulation of the many digestive processes begins with cephalic feed-forward regulation, followed by mechanical, luminal, and humoral signals as food moves through the gastrointestinal organs. The individual physiological processes involve many organ systems and require coordinated regulation. For example, the rise in metabolism must be provided by adequate cardiorespiratory functions involving a rise in ventilation that also serves to regulate pH as well as increased heart rate and stroke volume while maintaining blood pressure. These responses involve a variety of afferent feed-back mechanisms from various chemo- and mechanoreceptors, humoral and endocrine regulation, as well as efferent autonomic innervation of the viscera.

Many snakes endure months of fasting, but retain the capacity to subdue large meals. As pointed out in the pioneering studies of Secor and Diamond (e.g., 1995, 1998), the extreme natural history of feast and famine elicits enormous physiological responses in pythons that can provide insight to the general physiological mechanisms that govern digestive and cardiorespiratory functions in animals.

Section snippets

What are the costs of digestion?

The SDA response reflects the many physiological and biochemical processes that are stimulated or initiated by digestion (Fig. 2A), and include prey handling, secretions by the digestive organs, synthesis of enzymes, growth of visceral organs, nutrient assimilation and the post-absorptive stimulation of protein synthesis in various organs (Andrade et al., 2005; McCue et al., 2005; McCue, 2006; Secor, 2009). The quantitative importance of each process remains elusive and controversial.

The SDA

Phenotypic flexibility: what is restructured, when and how?

Digestion leads to large structural changes in the gastrointestinal organs. The mucosa in the small intestine unfolds as the enterocytes swell (Starck and Beese, 2001), and both villi and microvilli expand (Lignot et al., 2005) providing for a much larger surface area for nutrient absorption. There is also a marked rise in the physiological capacity for nutrient absorption (Secor et al., 2000a,2000b) that probably reflects increased number of nutrient transporters on the luminal side of the

How can the cardiovascular system support the rise in metabolism during digestion?

The rise in oxygen consumption (VO₂) during digestion is supported by increased oxygen delivery by a rise in heart rate (HR) and stroke volume (Vs) as well as increased oxygen extraction (the difference between arterial and venous oxygen concentrations, [O₂]a and [O₂]v, respectively) as described by the Fick principle: ${VO}_{2} = HR \times Vs \times ([O_{2}] a - [O_{2}] v)$

There is no indication of increased hematocrit during digestion and both arterial PO₂ and [O₂]a remains high, while the increased extraction lowers [O₂]v (Fig. 4

Acid-base regulation during digestion: the alkaline tide

Ingestion of food immediately stimulates gastric acid secretion (Secor, 2003) provided by the oxyntopeptic cells that secrete both HCl and pepsinogen (Helmstetter et al., 2009). The net acid and Cl⁻ secretion into the stomach lumen elevates plasma HCO₃⁻ concentration and create a metabolic alkalosis, known as the “alkaline tide” (Fig. 5). There is very little change in arterial pH because the metabolic alkalosis (the rise in HCO₃⁻) is accompanied by an elevation in arterial PCO₂ that stems from

Conclusions and perspectives

Given the enormous prey that can be subdued digested by many snakes, it is not surprising that digestion elicits large physiological and metabolic responses in comparison with other vertebrates. The magnitude of these responses are likely to reveal general principles for physiological regulation and can address hierarchies of physiological regulation where for example the need for acid-base regulation leads to a paradoxical hypoventilation in a situation where metabolic rate is increased. No

Declaration of Competing Interest

We declare no conflicts of interest.

Acknowledgements

The authors are grateful for continuous support from the Danish Council for Independent Research (Det Frie Forskningsråd|Natur og Univers) to study integrative vertebrate physiology.

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Graphical ReviewThe physiological response to digestion in snakes: A feast for the integrative physiologist

Highlights

Abstract

Graphical abstract

Introduction

Section snippets

What are the costs of digestion?

Phenotypic flexibility: what is restructured, when and how?

How can the cardiovascular system support the rise in metabolism during digestion?

Acid-base regulation during digestion: the alkaline tide

Conclusions and perspectives

Declaration of Competing Interest

Acknowledgements

Comp. Biochem. Physiol.

Comp. Biochem. Physiol.

Comp. Biochem. Physiol.

Comp. Biochem. Physiol.

Comp. Biochem. Physiol.

Comp. Biochem. Physiol.

Ventilatory compensation of the alkaline tide during digestion in the snake Boa constrictor

J. Exp. Biol.

Specific dynamic action in ectothermic vertebrates: a review of the determinants of postprandial metabolic response in fishes, amphibians, and reptiles

Improved cardiac filling facilitates the postprandial elevation of stroke volume in Python regius

J. Exp. Biol.

Digestive physiology of pythons with reference to other reptiles

Magnetic Resonance Imaging volumetry for noninvasive measures of phenotypic flexibility during digestion in Burmese pythons

Physiol. Biochem. Zool.

The effects of feeding on cell morphology and proliferation of the gastrointestinal tract of juvenile pythons (Python molurus)

Can. J. Zool.

What determines systemic blood flow in vertebrates?

J. Exp. Biol.

The effect of meal composition on specific dynamic action in burmese pythons (Python molurus)

Physiol. Biochem. Zool.

Graphical Review
The physiological response to digestion in snakes: A feast for the integrative physiologist