Digestive enzymes, and end product assimilation

Section Introduction:

The digestive tract is the principle portal of entry for both the nutrients required by vertebrates and many toxic and infectious agents. Some harmful agents may be rejected by highly developed senses of taste and smell, ejected by emesis (vomiting), or eliminated by rapid passage through the gut (diarrhea). However, one of the most effective protection against the assimilation of harmful agents is the breakdown of ingesta by endogenous digestive enzymes and selective absorption of end products. Digestion is initiated with the aid of enzymes released into the digestive tract in response to the presence of food or digesta. The mechanisms that stimulate the release of these enzymes are discussed in the section on Neuroendocrine Control of the Digestive System. The end products of this digestion are reduced to absorbable nutrients by enzymes in the lumen-facing membranes and cytosol of midgut epithelial cells.

The digestive system produces a variety of enzymes that catalyze the conversion of food into a limited number of absorbable end products. Although many digestive enzymes are found in the digestive tract, their origin is often difficult to assess (Vonk and Western 1984). Some of these enzymes are present in food or released from desquaminated gut cells, where they are involved only in cellular metabolism. Their presence at a given site along the digestive tract does not necessarily indicate the site of release, and their presence in tissue homogenates can be the result of adsorption to the lumen surface of cells. Comparative studies are further complicated by the fact that some enzymes act on more than one substrate and the levels of enzyme activity and nutrient absorption are modulated by the diet, body temperature, and stage of development. Therefore, each of these factors must be considered in the comparisons among species.

Digestion - Carbohydrates:

The carbohydrates in the plants or animals that make up the diet of vertebrates consist of individual monosaccharides or monosaccharides linked by glycosidic bonds into two (disaccharides), three to ten (oligosaccharides), or more than ten (polysaccharides) units. Most of the carbohydrates are polysaccharides, which either serve for the intracellular storage of energy (starches) or provide structural support for the cells of plants (cellulose, hemicellulose, pectin) or the integument of many invertebrates (chitin). The principal storage carbohydrates are amylose and amylopectin in terrestrial plants, and glycogen in animals. Amylose consists almost entirely of a-1,4 - linked glucose units. Amylopectin consists of these same chains with branches formed by a-1,6 linkages. Glycogen is similar to amylopectin, but with shorter (10-14 unit) chains between a-1,6 linkages. The principal storage carbohydrates in algae are Floridean starch, which is similar to amylopectin, and laminaran - a polymer of b-1,3 - linked glucose (Vonk and Western 1984). The major disaccharides are sucrose (glucose-fructose), lactose (glucose-galactose), and trehalose (glucose-glucose). Sucrose is the principal transport carbohydrate of plants, trehalose is the blood transport carbohydrate of insects, and lactose is the principal carbohydrate in the milk of most mammals. The only free monosaccharides that are found in any quantity are glucose, the transport carbohydrate of vertebrates, and the fructose found in some plants. 

The monosaccharide linkages of cellulose, hemicellulose, pectin, pectin, or chitin are illustrated in Figure 8.1. The b-1,4 linkage of cellulose and hemicellulose cannot be hydrolyzed by the endogenous enzymes of vertebrates and the axial position of the a-1,4 linkage of pectin makes it highly resistant to enzymatic attack. However, a chitinase that hydrolyses the b-1,4 linkage of chitin (Fig. 8.1) was found in the gastric mucosa of many adult amphibians and reptiles (Table 8.1), birds (Table 8.2), and mammals (Table 8.3), and the pancreas of some of these species. Its distribution suggests that endogenous chitinase appeared early in the evolution of vertebrates that fed on insects or other invertebrates, and it has been conserved in many species that no longer feed on these diets.

<img alt="Cellulose, hemicellulose, pectin &amp; chitin" src="../images/dsv/GITFigures/EnzymesCelluloseHemiPectinChitin%20F8_03.gif">

Figure 8.1. Haworth projections of cellulose, xylan, pectin (Van Soest 1982), and chitin (Fruton & Simmonds 1958). The linkage in pectic acid is alpha-1,4. Haworth formulae are misleading in that xylan and pectin appear to have a conformation similar to cellulose, while they actually differ. Pectin, like starch, cannot exist in a linear conformation and must form kinks or coils. However, the axial position of carbon 4 in galacturonic acid results in a different configuration, as compared to starch.

Table 8.1.

<img alt="Chitinase activity in amphibians &amp; reptiles" src="../images/dsv/Tables/EnzymesChitinaseAmphibReptiles%20T8_01.gif">

(From Stevens & Hume 1995)

Table 8.2.

<img alt="Chitinase activity in birds" src="../images/dsv/Tables/EnzymesChitinaseBirds%20T8_02.gif">

(From Stevens & Hume 1995)

Table 8.3.

<img alt="Chitinase activity in mammals" src="../images/dsv/Tables/EnzymesChitinaseMammals%20T8_03.gif">

(From Stevens & Hume 1995)

Table 8-4 lists the principal dietary carbohydrates that are digested by the endogenous enzymes of vertebrates, the principal enzymes responsible for their digestion, and the end products of their digestion. All vertebrates produce pancreatic a-amylase, which hydrolyzes the a-1,4 linkages of amylose, amylopectin, glycogen and Floridean starch to form maltose, isomaltose (a-limited dextrose), maltotriose, and other a-1,4 oligosaccharides (Fig. 8.2). Salivary secretion of a-amylase was also reported in echidnas, dogs, rabbits, mice, guinea pigs, voles, squirrels, rabbits, possums Trichosurus), artiodactyls (pigs, sheep, goats, cattle, deer), and primates (Vonk and Western 1984). An intestinal g-amylase that releases the terminal glucose from starches and oligosaccharides has also been described (Alpers and Solin 1970), but Vonk and Western (1984) attributed this to a lysosomal enzyme.

Table 8.4. Digestion of the principal dietary carbohydrates by the endogenous enzymes of vertebrates (Modified from Stevens & Hume 1995.)

<img alt="Carbohydrate digestion" src="../images/dsv/GITFigures/EnzymesCarbohydrateDigestion%20F8_01.gif">

<img alt="Starch hydrolysis" src="../images/dsv/GITFigures/EnzymesStarchHydrolysis%20F8_02.gif">

Figure 8.2. The structure of starch. Hydrolysis catalyzed by pancreatic amylase occurs at the alpha-1,4-linkage, and the products of hydrolysis are straight-chain oligosaccharides. Further hydrolysis is catalyzed by the maltases and isomaltase of the brush border of intestinal epithelial cells (Davenport 1982)

Oligosaccharides and disaccharides are further reduced to monosaccharides by enzymes in the brush border membranes of intestinal absorptive cells (Table 8.4). Brush border disaccharidases can be present in a number of combinations, which vary with species (Vonk and Western 1984; Stevens and Hume 1995). Maltase-isomaltase activity has been identified in the intestinal mucosa of all classes of vertebrates, but sucrase activity was low or absent in fish, amphibians, and reptiles, and a number of mammals and birds whose intestines are not usually exposed to sucrose. Trehalase activity was found in a number of mammals and reptiles. Lactase is present in the intestinal brush border of most mammals, where it is found in highest concentrations at birth and decreases or disappears in adults. However, only trace amounts were found in the intestine of neonate pinnipeds (seals, walruses and sea lions), which have little or no lactose in their milk, and lactase was absent in adult echidnas, bandicoots, ringtail possums, and elephants (Vonk and Western 1984). The principal end products of digestion by these enzymes are glucose, galactose, and fructose. 

The intestinal disaccharidase activities of a number of mammals are listed in Tables 8.5 and 8.6a and b. Although the levels of enzyme activity can be influenced by the diet, the results of these studies suggest considerable species variation in maltose and isomaltose activity. Sucrase and lactase levels are low or absent in the pinnepeds (seals, sea lions, and walruses) and trehalase activity is low or absent in both the pinnepeds and feline species. Low levels of cellobiose activity were reported in the intestinal mucosa of many of these species. However, cellobiose is a a-glucosidase that can hydrolyze the a-1,4 linkage of cellobiose, the end product of cellulose hydrolysis by C1 and Cx cellulytic enzymes. Therefore, the absence of endogenous cellulytic enzymes in vertebrates led Vonk and Western (1984) to the conclusion that the cellobiase may be of bacterial or lysosomal origin.

Table 8.5.

<img alt="Intestinal disaccharidase activity in prototherian and metatherian mammals" src="../images/dsv/Tables/EnzymesDisaccharidasesMonotremesMarsupials%20T8_04.gif">

All data on adult specimens are expressed in µmoles substrate/minute per gram (wet weight) of mucosa. (modified from Vonk & Western 1984)

Table 8.6a.

<img alt="Intestinal disaccharidase activity in eutherian mammals" src="../images/dsv/Tables/EnzymesDisaccharidasesEutheriansA%20T8_05.gif">

Enzymatic activity is designated as + (present), trace or 0 (absent). Results in brackets indicate use of and alternate substrate. All data from adult specimens. * suckling animals. (from Vonk & Western 1984)

Table 8.6b.

<img alt="Intestinal disaccharidase activity in eutherian mammals" src="../images/dsv/Tables/EnzymesDisaccharidasesEutheriansB%20T8_06.gif">

Enzymatic activity is designated as + (present), trace or 0 (absent). Results in brackets indicate use of and alternate substrate. All data from adult specimens. (from Vonk and Western 1984, plus perissodactyla data from Roberts 1975)

Digestion - Lipids:

Lipids serve as the major energy reserve in plants and animals. Those found in greatest quantity are the triglycerides, phospholipids, cholesterol, glycolipids, and waxes, which consist principally of alcohol-fatty acid esters (Table 8.7). Triglycerides are the major form of lipid storage in most animals. However, wax-esters constitute the major form of lipid storage in the marine mesopelagic and bathopelagic zooplankton and fish. They are stored or utilized by all organisms examined from depths of 1000 m (Benson et al. 1972) and constituted 20% of the lipids in copepods (small crustaceans) in cold, deep water and in Antarctic planktonic crustaceans at depths of 0 to 300 m (Lee et al. 1972; Bottino 1975). Benson and Lee (1975) estimated that 50% of the organic material synthesized by phytoplankton was stored temporarily as waxes by marine animals. Phospholipids are major components of cellular and cell organelle membranes, and cholesterol esters are the main form of the cholesterol found in vertebrates. Glycolipids are found mainly in the photosynthetic tissue of plants.

Table 8.7. Digestion of the principle dietary lipids by endogenous enzymes of vertebrates (Modified from Stevens & Hume 1995.)

<img alt="Lipid digestion" src="../images/dsv/GITFigures/EnzymesLipidDigestion%20F8_04.gif">

Lipids are hydrolyzed by lipases, which can act only at a lipid-water interface, and esterases which can only hydrolyze lipids that are in solution. Therefore, lipids must be emulsified to provide the surface area necessary for their efficient digestion. The principal agents responsible for emulsification are the bile salts, which are secreted by the liver and consist of sulfated alcohols in fish, amphibians, and a few mammals, and taurine and glycine conjugates of bile acids in reptiles, birds, and most mammals (Hagey 1992). Bile is secreted by the liver, and stored in the gallbladder of most vertebrates for release when high concentrations of lipid reach the midgut, but a gallbladder is absent in some fish and mammals. Pancreatic lipase appears to be the most important enzyme for lipid digestion in all vertebrates. However, lipases are also present in the salivary, pharyngeal, or gastric secretions of some species, and a number of esterases have been identified in the pancreatic secretions of rats, pigs, and humans (Stevens and Hume 1995).

Benson and Lee (1975) concluded that despite a dietary wax ester content that ranged from 5% in five species of tropical reef fish to 70% in anchovies, all of these fish hydrolyzed wax-esters, oxidized the alcohols, and incorporated the fatty acids into acyl lipids. A correlation between digestibility and digesta retention time suggested that wax esters were stored in the pyloric ceca of anchovy. Wax-esters provided up to 63% of the digestible energy in the diet of the chicks of five species of planktivorous sea birds (Roby et al. 1986). Place (1992) concluded that their efficient digestion and assimilation by sea birds was due to high concentrations of bile salts and triglycerides in their bile, a long retention time, and the efficient oxidation of fatty alcohols by enterocytes.

Digestion – Proteins and nucleic acids:

Plant and animal protein consist of up to 20 L-amino or -imino acids linked together with peptide bonds into a variety of different amino acid sequences, cross-linkages, and tertiary structures that result in a wide variety of dietary proteins. The protein levels in plants tends to be highest in seeds and lowest in leaves and stems, and they vary with both the stage of growth and the species. Protein is also added to the digestive tract by the secretion of enzymes, escape of plasma protein, desquamation of epithelial cells, and synthesis by indigenous gut microbes.

Protein hydrolysis is illustrated in Table 8.8. Proteins are hydrolyzed by endopeptidases, which attack peptide bonds along the protein chain, and exopeptidases that split off terminal amino acids. The endopeptidases are secreted by the stomach (pepsin) and pancreas (trypsin, chymotrypsin, elastase, collagenase) as inactive zymogens, which prevent the autodigestion of secretory cells. The low pH of stomach contents activates pepsinogen to pepsin, which serves as an autocatalyst for its further release. Enterokinase released from the intestinal mucosa activates the conversion of trypsinogen into trypsin, which catalyzes the release of additional trypsin and the remaining pancreatic endo- and exopeptidases.

Table 8.8. Digestion of proteins and nucleic acids by the endogenous enzymes of vertebrates (Modified from Stevens & Hume 1995.)

<img alt="Protein digestion" src="../images/dsv/GITFigures/EnzymesProteinDigestion%20F8_05.gif">

Pepsinogens are secreted by all vertebrates that have a stomach, other than monotremes (echidna and platypuses) and armadillos. Pepsin is most active at a pH of 2 to 4. They hydrolyze the peptide bonds of aromatic amino acids (Fruton and Simmonds 1958). The principal end products are large polypeptides and oligopeptides. The glandular stomach of calves also secretes chymosin (rennin), which has a proteolytic activity similar to, but weaker than, pepsin and aids in the clotting of milk. There is also immunological evidence for the presence of chymosin in the stomach of dogs, cats, rats. horses and kangaroos, but it is absent in humans (Vonk and Western 1984). Trypsin and chymotrypsin appear to be secreted by the pancreas of all classes of vertebrates (Tables 8.9 and 8.10). Elastase, which attacks the fibrous protein of arteries and ligaments, has been found in mammals, birds and fish. Collagenase, which has been found in the pancreas of dogs and chimaera fish, attacks the fibrous protein of connective tissues.

Table 8.9.

<img alt="Proteinase activity in the pancreas of fish and amphibians" src="../images/dsv/Tables/EnzymesProteinasesFishAmphib%20T8_07.gif">

Enzyme activities expressed as the equivalent amount of bovine trypsin (casein or BAEE) or chymotrypsin (BTEE) under the same conditions. a measurements of enzyme activity in the pyloric cecal tissue may account for the lower values, b frogs were fed, c frogs fasted at 5 C, * group C: 0-20 µg RNase per gram of pancreatic tissue. (from Vonk & Western 1984)

Table 8.10.

<img alt="Proteinase activity in the pancreas of reptiles, birds and mammals" src="../images/dsv/Tables/EnzymesProteinasesReptilesBirdsMammals%20T8_08.gif">

Enzyme activities expressed as the equivalent amount of bovine trypsin (casein or BAEE) or chymotrypsin (BTEE) under the same conditions. *A: 200-1,200 g RNase per gram pancreatic tissue; B: 20-100 g per gram pancreatic tissue; C: 0-20 µg RNase per gram pancreatic tissue. (from Vonk & Western 1984)

The exopeptidases are secreted by the pancreas and present in the membranes and cytosol of midgut absorptive cells. The pancreatic exopeptidases are C-terminal carboxypeptidases. Carboxypeptidase A was found in the pancreas of humans, cattle, pigs, turtles and terrapins, as well as the pancreatic tissue of teleosts, elasmobranches, and cyclosomes (Vonk and Western 1984). Carboxypeptidase B has been reported in the pancreas of humans, cattle, pigs, dogs, rats, dogfish, and lungfish, and in the pyloric ceca of cod, bass, mullet, and carp. There is also evidence for carboxypeptidase in the pancreas of chickens and adult amphibians. 

The brush border and cytosol of intestinal absorptive cells contain aminopeptidases, dipeptidases, and oligopeptidases. Brush border enzymes have greater activity on tetra- and larger oligopetides, but much of the tri- and dipeptidase activity resides in the cytosol. The concentration of these enzymes increased from the duodenum to mid-ileum and then decreased along the remainder of the small intestine in the rat (Robinson 1960) and pig (Josefsson and Lindberg 1965). Four brush-border and seven cytosolic enzymes that hydrolyze small peptides were reported in humans (Tobey et al 1985), and Vonk and Western (1984) listed seven exopeptidases in the intestinal cells of mammals. Hydrolysis of glycine dipeptides was demonstrated in intestinal mucosal extracts from teleosts, chimaeras and hagfish. Leucine aminopeptidase activity was reported in the intestinal cells of reptiles and intestinal microvilli of chimaeras and hagfish. Aminopeptidases were also reported in the intestinal cells of teleost, cartilaginous, and cyclostome fish. 

The cells of all plants and animals contain ribonucleic acid (RNA) and deoxyribonucleic acid (DNA), which consist of pentose sugars (ribose and deoxyribose), phosphate, and purine or pyrimidine bases. RNA is present in the cytosol and some nuclei. DNA is found in the nucleus and mitochondria of plant and animal cells, and packaged separately in the cell contents of prokaryotes. With the exception of bacteria and virus, most of the nucleic acids are bound to protein. Hydrolysis of nucleoproteins releases the nucleic acids, which are hydrolyzed by pancreatic ribo- and deoxyribonucleases into polynucleotides (Table 8.8 above). Pancreatic ribonuclease has been reported in all classes of vertebrate (Tables 8.9 and 8.10 above). The highest levels were found in the intestines of ruminants and kangaroos, which receive large numbers of bacteria from the forestomach. Smith and McAllan (1971) estimated that 20% of the microbial protein nitrogen and up to 75 to 80% of the microbial RNA and DNA that left the forestomach of cattle in the form of bacterial polynucleotides were digested in the duodenum.

Digestion - Vitamins: 

Vitamins are organic compound required in small amounts in the diet as catalysts for biochemical reactions. They consist of the lipid-soluble vitamins (A, D, E, and K) and water-soluble vitamins, such as biotin, choline, riboflavin, nicotinic acid, and pantothenic acid. Ascorbic acid (vitamin C) is also required in the diet of fish, some passerine birds, bats, guinea pigs, and some primates. Some vitamins must be released from complexes with other substances prior to their absorption.

Absorption of end products:

Absorption of the end products of carbohydrate and protein hydrolysis is limited mainly to a few monosaccharides (glucose, galactose, and fructose) and the amino acids. Glucose, galactose, amino acids, and the B-vitamins, biotin, choline, nicotinic acid, pantothenic acid, and riboflavin are transported across the apical membranes of midgut absorptive cells by a variety of different carrier-mediated transport mechanisms that are dependent on the simultaneous absorption of Na+ (Fig. 8.3). Sodium-dependent, carrier-mediated mechanisms have also been described for the transport of Vitamin C (ascorbic acid) in primates, guinea pigs and the European eel, and the transport of dipeptides in talapia fish, chickens, and a number of mammals (Stevens and Hume 1995). Monosaccharides, amino acids, and the water-soluble vitamins are also transferred across the basolateral cell membranes by carrier-mediated transport.

<img alt="Absorption of carbohydrates, amino acids &amp; B vitamins" src="../images/dsv/GITFigures/EnzymesAbsorptionCarbsAminoAcidsBVits%20F8_06.gif">

Figure 8.3. Absorption of monosaccharides, amino acids, and B-vitamins (Stevens 2001.)

Although carrier-mediated uptake of monosaccharides and amino acids appears to be absent in the hindgut of mammals, carrier-mediated transport of glucose, amino acids, and vitamin B6 was reported in the cecum of birds (Moreto and Planas 1989; Heard and Annison 1986). It was also present in the colon of chickens, but disappeared in birds on a Na+-deficient diet (Skadhauge 1993).

The end products of lipid digestion are absorbed by passive diffusion into the midgut intestinal epithelial cells. The epithelial cells then resynthesize triglycerides and phospholipids, and assemble them into chylomicrons, which are coated with a mixture of protein, cholesterol, and triglycerides for intracellular passage and released into the intercellular space and lymphatic system. Fat-soluble vitamins are also absorbed by passive diffusion. 

Interspecies comparisons of nutrient absorption are complicated by differences in the total absorptive surface area and the absorptive capacity of different segments of the intestine. Absorptive capacity is dependent on the surface area of the intestinal absorptive cells, which is the product of the intestinal length and diameter (nominal surface) plus the surface area of microvilli and that of the villi in mammals, birds, and some adult amphibians. Absorption of sugars, amino acids, and dipeptides, and the re-esterfication of fatty acids are confined principally to the cells near the tip of the villus. 

Figure 4.4 compares the log of the nominal surface area of the midgut (length x diameter) of the midgut, plus the ceca of fish and birds, in the various classes of vertebrates to the log of their body weight. Although there were no differences in the slope, the surface area increased with body mass. Differences in the intercept indicated that the nominal surface of endotherms exceeded that of ectotherms, and the nominal surface of mammals exceeded that of birds. It also shows the major effect of villi and microvilli on the intestinal surface area of mammals. The multiplication factor for microvilli to the nominal surface area ranged from 18 to 80 in nine species of mammal (Karasov 1988). The multiplication factor for villi ranged from 3 to 21 among 16 mammalian species, as compared to 8 for pigeons and 3.4 for the desert iguana.

<img alt="Relationship between lumen surface area of the midgut or small intestine, and body mass" src="../images/dsv/Graphs/CharacteristicsLumenSurfaceBodyMass%20F4_04.gif">

Figure 4.4. Relationship between lumen surface area of the midgut or small intestine, and body mass. Surface areas are nominal (length x diameter) except where otherwise indicated, and include ceca when present in fish and birds (From Karasov & Hume 1997.)

The levels of digestive enzyme activity and nutrient absorption are affected by the diet, time of measurement, and body temperature of a species. Karasov and Hume (1997) reviewed the results from a large number of studies on the effects of diet on the amylase, trypsin, chymotrypsin, lipase, sucrase, maltase, isomaltase, aminopeptidase and dipeptidase activity in a variety of mammals, birds, and fish. In almost every study, the enzyme activity increase with an increase in the level of its substrate in the diet. Addition of carbohydrate, protein, or lipid to the diet of rats resulted in a 500 to 800 % increase the levels of pancreatic amylase, trypsinogen, chymotrypsin, or lipase. Addition of sucrose to the diet increased the activities of brush border sucrase, isomaltase, and lactase activities along the entire length of the villus within three hours after a meal (Koldovsky 1981). Disaccharidase activities of the rat intestine also showed a circadian rhythm, which peaked in the dark and were lowest in the light hours of the day.

The rates of nutrient absorption are also affected by the diet. The relative rates of sugar versus amino acid absorption were lowest in carnivores and highest in herbivores in all classes of vertebrate (Fig. 8.4). Ferraris and Diamond (1989) examined the effects of an increase in the dietary levels on the intestinal uptake of sugars, amino acids, vitamins, and minerals in laboratory rodents. The uptake of sugars, amino acids, and peptides increased with an increase in the level of each substrate in the diet. However, absorption of vitamins tended to decrease, and the uptake of choline and ascorbic acid did not even increase in animals on diets deficient in these vitamins. The uptake of iron, calcium, copper, and phosphate were reduced with an increase in their dietary levels, as might be predicted by their toxic effects in high concentrations.

<img alt="Sugar &amp; amino acid transport" src="../images/dsv/Graphs/EnzymesSugarsAminoAcidsTransport%20F8_07.gif">

Figure 8.4. Relative rates of sugar and amino acid absorption in carnivorous, omnivorous, and herbivorous vertebrates on either their natural diet or one of similar nutrient composition. The ordinate is the ratio of the uptake capacity for D-glucose/ L-proline for the midgut or total intestine. Ratios appeared to be independent of body weight; therefore horizontal lines depict average values. Note that this ratio is highest for herbivores and lowest for carnivores in all classes. Glucose uptake showed a greater variation (herbivores > omnivores > carnivores) than proline. (From Karasov & Diamond 1988.)

Effects of diet and body temperature: 

As mentioned earlier, a decrease in body temperature reduces the rates of food intake, digesta passage, digestion, and absorption, and the utilization of nutrients. Coulson et al. (1990) examined the effects of ambient temperatures of 31oC ,25oC , 20oC , and 10oC on protein digestion, amino acid absorption and assimilation, heart rate, and oxygen consumption in alligators. Each of these parameters decreased to a roughly proportional degree with a reduction in temperature. They pointed out that the rates of digestion, absorption, and assimilation must be closely integrated by animals whose mass-specific metabolic rates can differ over a range of 4000 times between the largest crocodile and smallest shrew, and concluded that the rate of digestion may be controlled by the rate of villus blood perfusion. Peterson et al. (1990) also suggested that the absorptive capacity of the digestive system was the most proximate cause of the metabolic ceiling of a species.

Ontogeny of digestive enzymes and absorptive mechanisms:

The presence and activities of digestive enzymes and the mechanisms of nutrient absorption can also change with the stages of development in a species. Although the digestive system can undergo major changes during the early development in all vertebrates, the most extensive changes are seen in metamorphosis of amphibians (see section on Anatomy of the Digestive Tract), and the neonatal development of mammals. Mammals differ from other vertebrates in that they are born at a more precocious stage of development and suckle their young. Oftedal (1984) listed the milk composition of 57 species. On the basis of dry matter, the fat content of milk ranged from 2% in black rhinos to 82% in the harp seal. Protein content varied from 7% in humans to 40% in the dog and raccoon. The sugar content ranged from 7% in lagomorphs to 66% in the horse. Lactose was the major carbohydrate in most species, but it was absent or present in low concentrations in the milk of pinnipeds (seals, sea lions, and walruses). The milk of some mammals that nurse their young for prolonged periods of time also undergoes major changes in its composition. Therefore, survival of orphan neonates often requires the preparation of an artificial diet by dilution of or additions to cow’s milk. Some species such as rabbits can be easily killed by overfeeding. The diet following weaning contains little or no lactose, lower of lipids, and higher levels of carbohydrates in most species. These dietary changes are preceded by the eruption of teeth, major changes in digestive enzymes, and changes in the absorptive mechanisms.

Prenatal and neonatal development of the digestive system have been studied most extensively in the rat (Henning 1985,1987; Henning et al. 1994). The gastrointestinal tract of rats is functionally immature at birth and during the first two postnatal weeks of life. Lipids are digested by lingual and, possibly, gastric lipase, but there is no gastric secretion of HCl or pepsinogen and little secretion of pancreatic enzymes or bile. Brush border enzymes are limited mainly to lactase. Most macromolecules, including the immunoglobulins and nutrient proteins in the milk, are absorbed by pinocytosis. Immunoglobulins are absorbed by jejunal mucosa and transferred intact to the blood. Other proteins are absorbed by ileal mucosa and digested by lysosomal cathepsins and peptidases in the cytosol of these cells. 

The third and fourth weeks in the postnatal development of rats are accompanied by a dramatic increase in the secretion of salivary amylase, gastric pepsinogen and HCl, and pancreatic amylase, lipase, trypsin, and chymotrypsin. Brush border lactase declines with a reciprocal increase in maltase and sucrase activity, and pinocytosis and cathepsin activities are reduced to adult levels. These developments are stimulated by a rise in plasma cortisone and thyroxin levels and relatively unaffected by a delay in weaning, which normally begins at 17 days and is completed 26 days after birth. Therefore, they represent an inherent, or “hard wired”, series of postnatal events that are independent of the diet. 

Although the general patterns of development are similar in other mammals, there are some major differences among species (Koldovsky 1981; Janssens and Messer 1988). For example, the human digestive system is more mature than that of rat at the time of birth. Pancreatic amylase and lipase activities are low or absent. However, pepsinogen, HCl and pancreatic proteases are secreted at 50% of the adult levels, and salivary amylase, intestinal maltase, and lipase activities are equivalent to those of adults. The ability of mammals to transfer immunoglobulins in milk appears to be inversely related to their ability to transfer them across the placenta (Table 8.11). The transfer of immunoglobulins from dam to progeny via the digestive tract is limited by their ability to survive digestion and the ability of the intestine to absorb them intact. Gastric secretion of HCl is well-developed before the birth of guinea pigs and increases rapidly during the first day following the birth of humans. Trypsin activity increases during the first week following the birth of humans, sheep, cattle, and horses (Koldovsky 1970), although a trypsin inhibitor is present in the pancreatic juice of humans and the colostrum of calves. Intact protein can be absorbed from the intestine during the first 24 to 36 hours following the birth of cats, pigs, sheep, goats, and cattle. However, they are absorbed for a longer period of time by dogs, up to three weeks by rats and mice, and for as long as six weeks after the birth of hedgehogs.

Table 8.11.

<img alt="Transmission of passive immunity" src="../images/dsv/Tables/EnzymesPassiveImmunity%20T8_11.gif">

0, no absorption or transfer; + to +++, degrees of absorption or transfer. (from Brambell 1970)

The mechanisms for carrier-mediated absorption of glucose and amino acids appear to be present at the time of birth in all mammals (Buddington and Diamond 1989, 1990; Buddington 1992). Glucose absorption by the small intestine of lambs increased to a maximum two weeks after birth and declined to much lower levels in adults (Shirazt-Beechey et al. 1991a, b). However, it was increased 40-80% by a prolonged intestinal infusion of glucose, suggesting that the reduction was due to the absence of glucose in the intestine of mature ruminants. Buddington (1992) compared the ontogeny of glucose and amino acid absorption in eight species of mammal to that of a bird, amphibian, and two species of fish. Age-related changes in nutrient uptake corresponded to changes in the diet and the need to absorb greater quantities of food. Although mechanisms for glucose and amino acid transport were present in all species before their appearance in the diet, they responded to alterations in the diet by changes in the density, distribution, and type of carriers for different nutrients, and the physicochemical properties of the brush border.