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Vertebrate Gastrointestinal System

William H. Karasov, Ian D. Hume

10.1002/cphy.cp130107

Source: Supplement 30: Handbook of Physiology, Comparative Physiology

Originally published: 1997

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Matching Food Intake, Throughput, Breakdown, and Absorption: Integrative Models
1.1 Utility of the Modeling Approach
1.2 General Features of Reactor‐Based Models
1.3 Reactor Models Applied to Animal Guts
2 Optimizing Retention Time to Rate and Efficiency of Nutrient Extraction
2.1 Matching Overall Digesta Retention Time to Metabolic Needs
2.2 Matching Pulsatile Patterns of Food Intake to Continuous‐Flow Digestive Systems
3 Chemical Breakdown
3.1 Survey of Chemical Breakdown of Food Components across Vertebrate Species
3.2 Specific Modulation of Catalytic Enzymes within Species in Relation to Diet
3.3 Modulation of Catalytic Enzymes during Development
4 Microbial Fermentation
4.1 Microbial Habitats in the Gut
4.2 Rates of Fermentation
4.3 Models of Fermentation Systems
4.4 Modulation of Fermentation Capacity and Digesta Retention
4.5 Modulation of Retention Times of Digesta Components
5 Absorption
5.1 Pathways for Absorption of Organic Solutes
5.2 Mechanistic Bases for Differences in Absorption within and between Species
5.3 Nutrient Absorption and Dietary Composition
5.4 Developmental Adaptation to Diet
5.5 Nutrient Absorption and Level of Food Intake
5.6 Absorption in Relation to other Digestive and Metabolic Processes
6 Water and Electrolytes
6.1 Mechanisms of Wafer and Ion Movement across Membranes
6.2 Quantitative Aspects and Adaptive Significance
7 Conclusion
7.1 Toward an Ecological Physiology of Food Exploitation
7.2 Areas for Future Research
Figure 1. Figure 1.

General characteristics of the vertebrate GI tract. In fish the stomach is usually present and the tract shows no external characteristics indicative of a large intestine. A wide range of fish, but not all, have pyloric ceca which vary in size, shape, and number (from one to thousands). Urine in fish is usually excreted via a separate orifice. In the adult amphibian there is a distinct enlargement of the hindgut into a large intestine, which terminates in a cloaca, a feature shared with reptiles and birds. The GI tract of reptiles is similar to that of amphibians, except that the most proximal segment of the large intestine may be dilated, especially in herbivores. Special characteristics of the avian digestive tract include division of the stomach's secretory and triturative functions into two distinct compartments (glandular stomach or proventriculus and ventriculus or gizzard) and the development of paired ceca, though some species have only a single cecum and others none.

adapted from ref. 504
Figure 2. Figure 2.

Simple model of digestion. The value on the ordinate is the net amount of energy or nutrient obtained, which is defined as the amount extracted minus the amount invested in extraction. The value on the abscissa is the retention time of food in the gut. The net amount obtained may initially decline with time between when food is ingested and when breakdown products are actually absorbed (signified by the letter A). Subsequently, material is rapidly absorbed (B), but eventually the rate of absorption declines when no more food can be digested (C). f(T) has the same shape as extraction efficiency plotted as a function of time. The net rate of extraction, f(T)/T, is maximized at retention time T″, whereas the efficiency of extraction is maximized at T″.

adapted from ref. 477
Figure 3. Figure 3.

Effect of time of day on luminal glucose concentration and osmolality in four regions of the GI tract of rats fed a 65% glucose ration. Each point represents means ±SE of four rats 160.
Figure 4. Figure 4.

Principal food components and endogenous digestive enzymes of vertebrates 506.
Figure 5. Figure 5.

A: Differential curves for aminopeptidase N (upper panel), microvillous membrane (middle panel), and isomaltase development (lower panel) in jejunal enterocytes. Rats were fed isoenergetic diets containing 20% or 5% protein (broken and continuous lines, respectively). Vertical lines: calculated times for maximal rates of expression of development function. Rates of change are given in absorbance unit·h–1 for isomaltase and aminopeptidase N activities and as μh–1 for increases in microvillous length 486. B: Microvillous elongation in migrating enterocytes. H‐pigs had been adapted to twice the food intake of L‐pigs. H‐ and L‐rats had been fed isoenergetic diets containing 20% or 5% protein, respectively. Environmental temperatures at which pigs were kept, in °C, indicated by 35 and 10—for example, Pig 10 H. 486.
Figure 6. Figure 6.

Fermentation of alfalfa components in the rumen of a cow fed once daily 389.
Figure 7. Figure 7.

Chemical reactors.

adapted from 403
Figure 8. Figure 8.

Forestomach of the kangaroo and proximal colon of the horse, which are best modeled as modified plug‐flow reactors 244.
Figure 9. Figure 9.

Predictions of optimal gut structure of herbivores eating three different quality diets at two different relative rates. Contours represent relative rates of energy gain. • Global maxima, ○ local maximum; NDF, neutral‐detergent fiber; PFR, plug‐flow reactor; CSTR, continuous‐flow, stirred‐tank reactor; FG, foregut; HG, hind‐gut (from ref. 9).
Figure 10. Figure 10.

Comparison between four mammalian species of rates of uptake of a homologous series of saturated fatty acid into discs of intact jejunum under conditions selected to vary the effective resistance of the unstirred water layer. Each point represents the means of values from nine to 12 mammals; S.E.M. was smaller than symbol size. Bulk phase was stirred at 600 rev/min (stirred) or unstirred (from ref. 529).
Figure 11. Figure 11.

Hypothetical models for short‐chain‐fatty‐acid (SCFA) transport. A: Proposed for mammalian rumen and colon, SCFA associates with H+ resulting from the luminal hydration of CO2 and diffuses nonionically into the cell. It exits the cell across the basolateral membrane by ionic or nonionic diffusion down a chemical gradient or becomes metabolized. Intracellular carbonic anhydrase (CA)–catalyzed hydration of CO2 results in the generation of bicarbonate and H+, which enter the lumen in exchange with Cl and Na, respectively, and subsequently aid in the continued diffusion of SCFA. Ac, acetate (from ref. 505). B: Proposed for tilapia small intestine, luminal SCFA enters across the brush border membrane in exchange for intracellular bicarbonate. At the basolateral membrane SCFA exits the cell by way of a low‐affinity SCFA–high‐affinity bicarbonate exchanger, whereby bicarbonate is transported against a gradient into the cell. Bicarbonate from blood, or formed by intracellular carbonic anhydrase, provides a substrate for the brush‐border SCFA–bicarbonate antiport mechanism. The resultant proton from the hydration reaction enters the lumen in exchange for luminal Na (not depicted) (from ref. 535).
Figure 12. Figure 12.

Relationships between intestinal surface area and body mass. Surface areas are nominal unless indicated otherwise and for fish and birds include ceca when present (see text). For the seven data sets, indicated as 1–7, there was no significant difference in slope, so the seven lines fit the data of each set to the common slope of 0.71. Calculated proportionality coefficients (intercept at unity) are fish, 1.06; amphibians, 0.63; reptiles, 1.08; birds, 1.43; mammals, 2.47; villous area of mammals, 16.44; microvillus area of mammals, 867. Sources of data: on mammals—269; on birds—143,254,277,281,284,286,386, (Afik and Karasov, unpublished data); on reptiles—290 (Karasov, unpublished data); on amphibians—56,538 (Buddington, personal communication); on fish—55,57.
Figure 13. Figure 13.

Observed modulation patterns for activities of intestinal nutrient transporters (ordinate) as a function of dietary levels or body stores of their substrates (abscissa). A: Glucose and fructose transporters of mouse intestine. B: Transporters for biotin, choline, thiamine, ascorbic acid, and pantothenic acid in intestine of rat, rat, rat, guinea pig, and mouse, respectively. C: Aspartate, proline, and peptide (carnosine) transporters of mouse intestine. AAs, amino acids. D: Iron, zinc, calcium, phosphate, and copper transporters of rat intestine. E: Transport of the amino acids lysine and histidine by mouse intestine 156.
Figure 14. Figure 14.

The intestine's summed uptake capacity for glucose divided by that for proline (ordinate) as a function of the percentage of protein or carbohydrate in the natural diet (abscissa). A: For eight species of fish: carnivores, closed circles; omnivores, open squares; herbivores, closed triangles; a species (monkeyface prickleback) that is carnivorous while small (open circle) but herbivorous when large (open triangle). Note that the ratio of glucose to proline uptake decreases with the proportion of protein in the natural diet, even though all eight species were studied while eating the same artificial diet 55. B: For eight species of bird. Note that the ratio of glucose to proline uptake increases with the proportion of carbohydrate in the natural diet, both in species from different orders maintained in captivity on different foods (open and closed symbols) and in species from the same order that eat the same ration (closed symbols) 284.
Figure 15. Figure 15.

Total L‐proline uptake (top) and carrier‐mediated D‐glucose uptake (bottom) by intact intestinal tissue in vertebrates. Uptake rates were measured by the everted sleeve method at saturating concentrations (25–50 mM). Incubation temperatures were 20°C for fish and 37°–40°C for all others. Tissues were taken from the region where transport activity was greatest (proximal or mid‐intestine). Open bars are carnivores and cross‐hatched bars are herbivore/omnivores (also includes frugivores and nectarivores in the case of birds). Standard errors are designated by vertical lines. Data for fish and reptiles were extracted from the literature by Karasov 268 and for birds were taken from references 143,277,284,286, and 385. Note that tissue‐specific uptake is similar among the taxonomic groups (lower in fish due to lower assay temperature) but that glucose uptake is lower in the carnivores.
Figure 16. Figure 16.

A: Model proposed for secretion of HCl by gastric parietal cells. Apical membrane contains an Na–H exchange pump and conductive pathways for passive transport of K and Cl. Basolateral membrane contains an Na–K pump, a K conductance, and separate Na–H and Cl–HCO3 exchange mechanisms.

adapted from ref. 424. B, C: Ileal transport pathways demonstrated in membrane vesicle studies (adapted from ref. 514). D: Model for coupled NaCl absorption in the proximal colon (adapted from ref. 202). E: Model for electrogenic Na absorption in distal colon. Schematic shows epithelium separating mucosal solution from serosal solution adapted from ref. 202
Figure 17. Figure 17.

Rates of hydrolysis and glucose transport as a function of assay temperature. A: Specific activity of trypsin from pyloric ceca of giant bluefin tuna. Specific activity of chymotrypsin as a function of temperature showed a similar pattern 508. B: Relative carrier‐mediated D‐glucose uptake at 50 mM, calculated as uptake at given temperature divided by uptake at 37°C measured in an adjacent intestinal sleeve from same animal (from ref. 290).


Figure 1.

General characteristics of the vertebrate GI tract. In fish the stomach is usually present and the tract shows no external characteristics indicative of a large intestine. A wide range of fish, but not all, have pyloric ceca which vary in size, shape, and number (from one to thousands). Urine in fish is usually excreted via a separate orifice. In the adult amphibian there is a distinct enlargement of the hindgut into a large intestine, which terminates in a cloaca, a feature shared with reptiles and birds. The GI tract of reptiles is similar to that of amphibians, except that the most proximal segment of the large intestine may be dilated, especially in herbivores. Special characteristics of the avian digestive tract include division of the stomach's secretory and triturative functions into two distinct compartments (glandular stomach or proventriculus and ventriculus or gizzard) and the development of paired ceca, though some species have only a single cecum and others none.

adapted from ref. 504


Figure 2.

Simple model of digestion. The value on the ordinate is the net amount of energy or nutrient obtained, which is defined as the amount extracted minus the amount invested in extraction. The value on the abscissa is the retention time of food in the gut. The net amount obtained may initially decline with time between when food is ingested and when breakdown products are actually absorbed (signified by the letter A). Subsequently, material is rapidly absorbed (B), but eventually the rate of absorption declines when no more food can be digested (C). f(T) has the same shape as extraction efficiency plotted as a function of time. The net rate of extraction, f(T)/T, is maximized at retention time T″, whereas the efficiency of extraction is maximized at T″.

adapted from ref. 477


Figure 3.

Effect of time of day on luminal glucose concentration and osmolality in four regions of the GI tract of rats fed a 65% glucose ration. Each point represents means ±SE of four rats 160.



Figure 4.

Principal food components and endogenous digestive enzymes of vertebrates 506.



Figure 5.

A: Differential curves for aminopeptidase N (upper panel), microvillous membrane (middle panel), and isomaltase development (lower panel) in jejunal enterocytes. Rats were fed isoenergetic diets containing 20% or 5% protein (broken and continuous lines, respectively). Vertical lines: calculated times for maximal rates of expression of development function. Rates of change are given in absorbance unit·h–1 for isomaltase and aminopeptidase N activities and as μh–1 for increases in microvillous length 486. B: Microvillous elongation in migrating enterocytes. H‐pigs had been adapted to twice the food intake of L‐pigs. H‐ and L‐rats had been fed isoenergetic diets containing 20% or 5% protein, respectively. Environmental temperatures at which pigs were kept, in °C, indicated by 35 and 10—for example, Pig 10 H. 486.



Figure 6.

Fermentation of alfalfa components in the rumen of a cow fed once daily 389.



Figure 7.

Chemical reactors.

adapted from 403


Figure 8.

Forestomach of the kangaroo and proximal colon of the horse, which are best modeled as modified plug‐flow reactors 244.



Figure 9.

Predictions of optimal gut structure of herbivores eating three different quality diets at two different relative rates. Contours represent relative rates of energy gain. • Global maxima, ○ local maximum; NDF, neutral‐detergent fiber; PFR, plug‐flow reactor; CSTR, continuous‐flow, stirred‐tank reactor; FG, foregut; HG, hind‐gut (from ref. 9).



Figure 10.

Comparison between four mammalian species of rates of uptake of a homologous series of saturated fatty acid into discs of intact jejunum under conditions selected to vary the effective resistance of the unstirred water layer. Each point represents the means of values from nine to 12 mammals; S.E.M. was smaller than symbol size. Bulk phase was stirred at 600 rev/min (stirred) or unstirred (from ref. 529).



Figure 11.

Hypothetical models for short‐chain‐fatty‐acid (SCFA) transport. A: Proposed for mammalian rumen and colon, SCFA associates with H+ resulting from the luminal hydration of CO2 and diffuses nonionically into the cell. It exits the cell across the basolateral membrane by ionic or nonionic diffusion down a chemical gradient or becomes metabolized. Intracellular carbonic anhydrase (CA)–catalyzed hydration of CO2 results in the generation of bicarbonate and H+, which enter the lumen in exchange with Cl and Na, respectively, and subsequently aid in the continued diffusion of SCFA. Ac, acetate (from ref. 505). B: Proposed for tilapia small intestine, luminal SCFA enters across the brush border membrane in exchange for intracellular bicarbonate. At the basolateral membrane SCFA exits the cell by way of a low‐affinity SCFA–high‐affinity bicarbonate exchanger, whereby bicarbonate is transported against a gradient into the cell. Bicarbonate from blood, or formed by intracellular carbonic anhydrase, provides a substrate for the brush‐border SCFA–bicarbonate antiport mechanism. The resultant proton from the hydration reaction enters the lumen in exchange for luminal Na (not depicted) (from ref. 535).



Figure 12.

Relationships between intestinal surface area and body mass. Surface areas are nominal unless indicated otherwise and for fish and birds include ceca when present (see text). For the seven data sets, indicated as 1–7, there was no significant difference in slope, so the seven lines fit the data of each set to the common slope of 0.71. Calculated proportionality coefficients (intercept at unity) are fish, 1.06; amphibians, 0.63; reptiles, 1.08; birds, 1.43; mammals, 2.47; villous area of mammals, 16.44; microvillus area of mammals, 867. Sources of data: on mammals—269; on birds—143,254,277,281,284,286,386, (Afik and Karasov, unpublished data); on reptiles—290 (Karasov, unpublished data); on amphibians—56,538 (Buddington, personal communication); on fish—55,57.



Figure 13.

Observed modulation patterns for activities of intestinal nutrient transporters (ordinate) as a function of dietary levels or body stores of their substrates (abscissa). A: Glucose and fructose transporters of mouse intestine. B: Transporters for biotin, choline, thiamine, ascorbic acid, and pantothenic acid in intestine of rat, rat, rat, guinea pig, and mouse, respectively. C: Aspartate, proline, and peptide (carnosine) transporters of mouse intestine. AAs, amino acids. D: Iron, zinc, calcium, phosphate, and copper transporters of rat intestine. E: Transport of the amino acids lysine and histidine by mouse intestine 156.



Figure 14.

The intestine's summed uptake capacity for glucose divided by that for proline (ordinate) as a function of the percentage of protein or carbohydrate in the natural diet (abscissa). A: For eight species of fish: carnivores, closed circles; omnivores, open squares; herbivores, closed triangles; a species (monkeyface prickleback) that is carnivorous while small (open circle) but herbivorous when large (open triangle). Note that the ratio of glucose to proline uptake decreases with the proportion of protein in the natural diet, even though all eight species were studied while eating the same artificial diet 55. B: For eight species of bird. Note that the ratio of glucose to proline uptake increases with the proportion of carbohydrate in the natural diet, both in species from different orders maintained in captivity on different foods (open and closed symbols) and in species from the same order that eat the same ration (closed symbols) 284.



Figure 15.

Total L‐proline uptake (top) and carrier‐mediated D‐glucose uptake (bottom) by intact intestinal tissue in vertebrates. Uptake rates were measured by the everted sleeve method at saturating concentrations (25–50 mM). Incubation temperatures were 20°C for fish and 37°–40°C for all others. Tissues were taken from the region where transport activity was greatest (proximal or mid‐intestine). Open bars are carnivores and cross‐hatched bars are herbivore/omnivores (also includes frugivores and nectarivores in the case of birds). Standard errors are designated by vertical lines. Data for fish and reptiles were extracted from the literature by Karasov 268 and for birds were taken from references 143,277,284,286, and 385. Note that tissue‐specific uptake is similar among the taxonomic groups (lower in fish due to lower assay temperature) but that glucose uptake is lower in the carnivores.



Figure 16.

A: Model proposed for secretion of HCl by gastric parietal cells. Apical membrane contains an Na–H exchange pump and conductive pathways for passive transport of K and Cl. Basolateral membrane contains an Na–K pump, a K conductance, and separate Na–H and Cl–HCO3 exchange mechanisms.

adapted from ref. 424. B, C: Ileal transport pathways demonstrated in membrane vesicle studies (adapted from ref. 514). D: Model for coupled NaCl absorption in the proximal colon (adapted from ref. 202). E: Model for electrogenic Na absorption in distal colon. Schematic shows epithelium separating mucosal solution from serosal solution adapted from ref. 202


Figure 17.

Rates of hydrolysis and glucose transport as a function of assay temperature. A: Specific activity of trypsin from pyloric ceca of giant bluefin tuna. Specific activity of chymotrypsin as a function of temperature showed a similar pattern 508. B: Relative carrier‐mediated D‐glucose uptake at 50 mM, calculated as uptake at given temperature divided by uptake at 37°C measured in an adjacent intestinal sleeve from same animal (from ref. 290).

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Article Title: Vertebrate Gastrointestinal System
 

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William H. Karasov, Ian D. Hume. Vertebrate Gastrointestinal System. Compr Physiol 2011, Supplement 30: Handbook of Physiology, Comparative Physiology: 409-480. First published in print 1997. doi: 10.1002/cphy.cp130107