THE DIGESTIVE SYSTEM OF VERTEBRATES
1University
Esther J. Finegan, PhD1 and C. Edward Stevens, PhD, DVM2
of Guelph, Ontario, N1G 2W1 Canada; 2Department of Molecular Biomedical Sciences, College of Veterinary
Medicine, North Carolina State University, Raleigh, NC, 27606 USA.
Evolution of the digestive system
Introduction:
This section summarizes the adaptations of the digestive system to the habitat, diet and other
physiological characteristics of vertebrates and speculates on how these may have evolved.
Speculations on the digestive system of early vertebrates are based mostly on comparisons of
their skeletal remains, habitat, and environment with those of present-day species. Although our
discussion has been limited to vertebrates, they represent less than 5% of the species in the
Animal Kingdom. As Barnes (1987) pointed out, a taxonomist less biased than Man might have
divided these animals into arthropods (over 75% of the species) and non-arthropods. Separation
of the Animal kingdom into vertebrates and invertebrates is based on one characteristic of a
single subphylum, and many characteristics of the vertebrate digestive system are found among
the invertebrates. Therefore, a brief discussion of the invertebrate digestive systems provides
some necessary perspectives.
Digestive System - Invertebrates:
The structural and functional variations in the invertebrate digestive system are discussed by
Barnard and Prosser (1973), Barnes (1974; 1987), Wigglesworth (1984), and Vonk and Western
(1984). Although it is convenient to use the terms primitive, advanced, lower, higher, and
specialized in discussions of phylogenetic relations, this tends to create the erroneous
impression that evolution progressed toward an ideal goal. Lower and higher generally refer to
the level at which species have stemmed from a main line of evolution. Primitive species are
those believed to possess many or the greatest number of characteristics of the ancestral stock
within a particular group of animals. Advanced species are those that have changed
considerably as a result of different environments or modes of existence. The term specialized
refers to characteristics that are especially adapted to a particulate ecological niche. However, as
Barnes (1974) points out, the terms advanced and specialized should not be interpreted as more
perfect or better, and some species with primitive characteristics are specialized in other
respects.
The general pattern of invertebrate evolution is illustrated in Figure 12.1. Protozoa (flagellates,
sarcodinians, and ciliates), which are believed to have originated as singled-celled organisms in
the Archeozoic oceans long before the first fossil records, have no digestive tract. Some presentday species absorb nutrients across their cell membrane, but many protozoa ingest food by
phagocytosis at a specific site or various points on the cell membrane (Fig. 12.2). Ingested
material is taken up by food vacuoles, which are passed through the cell with digestion of their
contents, absorption of nutrients, and the eventual
evacuation of waste products. Some of the digestive
enzymes found in vertebrates have been isolated from
protozoa (Vonk and Western 1984) and intervacuolar
digestion can be accompanied by a similar cycle of
acidification and alkalization in some species.
Figure 12.1. Phylogeny of the Animal Kingdom as
reflected by the views of L. Hyman. (From Barnes
1987).
Figure 12.2. Formation of food vacuoles and digestion in a
ciliated protozoa, such as Tetrahymena. (From Barnes 1987)
A number of primitive metazoans, such as the Cnidaderian
hydra, have a mouth and a blind gastrovascular cavity, which is
lined with phagocytic, secretory, and ciliated, cells (Fig. 12.3).
However, most free-living advanced invertebrates have a
digestive tract that terminates in an anus. Movement of food and digesta is accomplished by
cilia in some species, but this is aided by muscular activity in most of the more advanced
invertebrates and cilia are absent in the nematodes and insects. The digestive tract of annelids,
mollusks, and arthropods can be divided into a headgut, foregut, and an intestine. The headgut
may be designed for a variety of functions, including filter-feeding, chewing, sucking, or
piercing. Scorpions and mites regurgitate enzymes into their prey, and some echinoderms evert
their stomach to engulf their prey.
Figure 12.3. Body form (A) and body wall (B)
of a hydra. (From Barnes 1987)
The advanced invertebrates show an increasing
dependence on extracellular digestion and the
replacement of phagocytosis by absorption into
the cells (Barrington 1962). Secretion of
enzymes, absorption of nutrients, and food
storage, which are carried out by multipurpose cells in the lower forms of invertebrates, become
the properties of specialized cells. The intestinal ceca of free-living flatworms in Phylum
Platyhelminthes, which are considered the most primitive bilateral animals, contain both
secretory cells that release mucus and enzymes, and absorptive cells that lack food vacuoles and
have microvilli on their lumen-facing membranes.
Phylum Annelida is comprised of 8700 species of segmented worms, including the familiar
earthworms. The digestive tract of lumbricid earthworms consists of a headgut (mouth, buccal
cavity, and muscular pharynx), foregut (esophagus, crop, and gizzard), and intestine (Fig. 12.4).
The anterior half of the intestine is the principal site of secretion and digestion, and the posterior
half is the principal site of absorption. The intestinal absorptive cells of Arenicola marina, a
burrowing annelid that ingests much sand along with organic matter, phagocytize food particles
and transfer them to wandering amoebocytes in a manner similar to that of primitive metazoa
(Barrington 1962). However, the midgut absorptive cells of most annelids lack food vacuoles
and demonstrate microvilli or a brush border on their lumen-facing membranes.
Figure 12.4. Anterior internal structures of the earthworm
Lumbricus. (From Barnes 1987)
Phylum Mollusca contains the clams, oysters, snails, slugs, squid,
and octopods, and the largest number of species (80,000) of any
phylum other than Arthropoda. The mollusks include carnivores,
omnivores, scavengers, and parasites that inhabit marine, freshwater,
and terrestrial environments. Digestion is at least partly extracellular
in all mollusks, and enzymes may be secreted by salivary glands,
esophageal pouches, portions of the stomach, intestinal glands, or a
combination of these. A chitinous radula in the headgut of many mollusks grinds food into
smaller particles (Fig. 12.5). Cilia in the stomach or style sac of some mollusks rotate its
contents into a mucous mass (protostyle) and direct
finer particles of food into digestive glands for
digestion and absorption. The remainder is directed
into the intestine for absorption of water and
excretion of waste material.
Figure 12.5. Lateral view of internal structures a
generalized mollusk. (From Barnes 1987)
Diverticula in the stomach of some mollusks
contain phagocytic vacuolated cells (Barrington 1962). However, the absorptive cells in the
digestive glands of others have microvilli and the digestive glands of the snail Helix secrete a
variety of digestive enzymes but have little absorptive capacity. The digestive glands of some
mollusks contain cells that can function for absorption, intracellular digestion, food storage,
secretion, or excretion, and are often referred to as the hepatopancreas or the pancreas and liver
in squid (Fig. 12.6). The squid and octopods have well developed salivary and digestive glands.
The pancreas of squid produces aminopeptidase, dipeptidase, and lipase. The liver produces
aminopeptidase, dipeptidase. and carboxypeptidase. Although cell vacuoles of the pancreas
contain food particles, nutrients must be absorbed into the circulatory system to reach the liver
cells. The pancreatic and liver ducts combine to form a common duct that can direct its flow
into the stomach or the cecum, and a sphincter at
the terminus of the liver duct prevents the backflow of lumen contents.
Figure 12.6. Digestive tract of the squid
Loglaga and octopus Octopus vulgaris. (From
Barnes 1987)
Phylum Arthropoda (horseshoe crabs,
crustaceans, arachnids, and insects) includes over 75% of the animal species. Most crustaceans
are filter feeders. Their foregut is often enlarged and lined with chitinous ridges to provide a
triturating stomach. Their midgut contains glandular ceca that are modified into large digestive
glands in some species and provide the principal source of extracellular digestive enzymes.
Digestion in arthropods is principally extracellular. The "hepatic ceca" of horseshoe crabs
consists of two large glands that function for both absorption and secretion of digestive
enzymes. The "hepatopancreas" of the crustacean midgut consists of a pair of ceca and secretory
ducts, which serve for absorption, secretion of digestive enzymes, and storage of glycogen, fat,
and calcium (Fig. 12.7). Many advanced invertebrates
produce emulsifying agents that serve functions
similar to those of the vertebrate bile salts (Haslewood
1967).
Figure 12.7. Digestive system of a crustacean
crayfish. (From Barnes 1987)
Van Weel (1974) concluded that the terms
hepatopancreas, pancreas, and liver are inappropriate
when applied to mollusks or crustaceans and they
should be referred to simply as digestive glands.
Bidder (1976) agreed and proposed the substitution of "digestive glands" and "digestive gland
appendages" for the "liver" and "pancreas" of the cephalopods. However, Gibson and Barker
(1979) concluded that the digestive glands of decapod crustaceans "are rightly and properly
named the hepatopancreas”.
The largest group of arthropods is the insects, which contain more than 750,000 species that
have adapted to all types of habitats and are the most successful of all terrestrial animals. The
digestive tract of most insects consists of a headgut, foregut (esophagus, crop, proventriculus,
and gastric ceca), midgut, and hindgut (Fig. 12.8 and 12.9). Their headgut is designed for a
variety of functions, including chewing, sucking, or piercing. Salivary glands are highly
developed in many insects. They secrete mucus, enzymes, anticoagulants, agglutinins,
venomous spreading agents or silk in various species. The crop serves for food storage and the
proventriculus controls the passage of food into the midgut and contains teeth for the crushing
or grinding of food in some species. The midgut is the principal site of digestion and absorption.
Cells in the anterior midgut of many insects generate a thin sheath of peritrophic membrane,
which protects it against physical damage but is permeable to nutrients. Malpighian tubules,
which are analogous to the kidneys of vertebrates, release electrolytes, waste products, and
water into the midgut.
Figure 12.8. Schematic diagram of the digestive tract of an insect. (Modified from
Wigglesworth 1962)
Figure 12.9.
Modifications of the
gastrointestinal tract
of insects. The foregut
and hindgut are
indicated by a red highlight. (From Wigglesworth 1962)
The hindgut of insects aids in the recovery of electrolytes,
water, and nitrogen (Fig. 12.10). The Malpighian tubules of the
desert locust secrete Na+, K+, Cl-, ammonia-urate, proline and
water, which are released into the intestinal contents at the
juncture of the midgut and hindgut (Phillips et al. 1988). The
rectal pad of their hindgut absorbs Na+ in cotransport with
proline and in exchange for H+ or NH4+ (Fig. 12.11). Absorption of electrolytes and water from
the rectum of cockroaches can produce extremely hypertonic solutions
in the lumen (Wall 1971), and the hindgut is extremely voluminous in
some herbivorous insects.
Figure 12.10. Enterocirculation of water by the alimentary tract of
insects. Letters indicate the midgut (a), Malpighian tubules (b),
hindgut (c), and rectum (d). (From Wigglesworth 1962)
Figure 12.11. Transport mechanisms in the apical and
basolateral membranes of the locust rectal pad
epithelium. Arrows through solid circles indicate carriermediated transport. Thick arrows indicate major ion
pumps. Sodium is transported across the apical
membrane in cotransport with amino acids and in
exchange for intracellular H+ and the intercellular NH4+.
(From Phillips et al. 1988)
Many of the digestive enzymes of vertebrates have been
demonstrated in various species of invertebrates (Vonk and Western 1984), and nutrients may
be assimilated by similar mechanisms. For example, Na+ was absorbed electrogenically from
the gut of the mollusk Alplysia californica (Gerencser 1988), and the rectal pad locusts
demonstrated both Na+-dependent absorption of amino acids and Na+ - H+ exchange (Phillips et
al. 1988). However, the electrogenic Cl- transport reported in the gut of the mollusk Alplysia
californica (Gerencser 1988) and electrogenic exchange of two Na+ for one H+ described in the
hepatopancreas brush border membranes of the freshwater prawn Macrobrachium rosenbergii
and marine lobster Homarus americanus (Ahern et al. 1990) appear to be unique to
invertebrates.
Digestive System - Vertebrates:
The chronology of terrestrial vertebrate evolution is illustrated in Figure 12.12. Amphibians are
believed to have evolved from predacious lobe-finned fishes (Crossopteygii). Amniotic
tetrapods appear to have evolved from amphibian anthrocosaurs, over 300 million years ago
(mya). The reptiles evolved into the dinosaurs, which were the dominant terrestrial vertebrates
from the mid-Triassic to the end of the Cretaceous period, and present-day chelonians, snakes,
lizards and crocodilians. Birds are believed to be the modern-day descendants of carnivorous
theropod dinosaurs (Gauthier 1986). Mammals appeared about 200 mya in the Late Triassic
period of the Mesozoic Era (Lillegraven et al. 1979) and evolved into the Prototheria
(monotremes) and, via the Pantotheria, into the Metatheria (marsupials) and Eutheria (placental
mammals). The earliest Mesozoic mammals were small (20-30 g) carnivores that fed on
invertebrates and other vertebrates (Crompton 1980). The Insectivora are regarded as their most
direct modern descendants (Romer 1966). However, the major expansion and diversification of
birds and mammals did not occur until after the end of Mesozoic (70 mya) and demise of the
dinosaurs and most other vertebrates over 10 kg in body weight.
Figure 12.12.
Phylogenetic origins of
various groups of
vertebrates. A) Urodela,
B) Lepospondylii, C)
Apoda, D) Anura, E)
Labyrinthodontia, F)
Apisidospondylii, G)
Chelonia, H) Anapsida,
I) Cotylosauria, J)
Eurapsida, K) Diapsida,
L) Eosuchia, M)
Squamata, N)
Rhyncocephalia, O)
Ornithischia, P)Thecodontia, Q) Synapsida, R) Parapsida, S) Pelycosauria, T) Pterosauria,
U) Crocodilia, V) Aves, W) Saurischia, X) Prototheria, Y) Metatheria, Z) Pantotheria,
AA) Therapsida, BB) Eutheria, CC) Ichthyosauria. (Modified from Torrey 1971)
The digestive tract of vertebrates shows many features that are analogous to those of advanced
invertebrates. Filter-feeders are found among fish (basking sharks, paddlefish), larval
amphibians, birds (flamingos), and mammals (baleen whales). A beak is used for cutting,
tearing, or crushing in the chelonians (turtles, terrapins, and tortoises) and birds. However, teeth
are used for this purpose in most other vertebrates. Teeth are located in the jaws, other
mouthparts, or the pharynx of fish, but confined to jaws of most vertebrates. Food can be
ground to small particles by pharyngeal teeth or gizzard-like stomach in some fish, the gizzard
of birds, or a combination of large cheek teeth and lateral or anterior-posterior movements of the
mandible in most mammals.
A stomach is absent in cyclostomes, some advanced species of fish, and the larval amphibians,
but present in all other vertebrates. The stomach of most vertebrates is a unilateral dilatation of
the digestive tract that serves for the storage of food and initial stages of digestion. However,
the crop and proventriculus perform these functions in birds. Eight of the 20 mammalian orders
include species with a stomach that is expanded and either haustrated or divided into permanent
compartments. The stomach of most vertebrates contains regions of proper gastric glandular
mucosa, pyloric glandular mucosa, and an additional region of cardiac mucosa in reptiles, some
adult amphibians, and most mammals. It also includes a region of stratified squamous
epithelium in species belonging to half of the mammalian orders. This led Oppel (1897) and
Bensley (1902-1903) to the conclusion that the appearance of cardiac glandular and stratified
squamous epithelium represented a regression of highly specialized proper gastric glandular
mucosa to a less complex cardiac glandular mucosa, and then to a nonglandular stratified
squamous epithelium.
The presence of stratified squamous epithelium in the stomachs of ant and termite-eaters, and
many herbivores suggests that it serves a protective function against physical damage from
food, analogous to chitin in the foregut of mollusks and insects, or the peritrophic membrane in
the midgut of insects. However, the absorption and buffering of SCFA by the stratified
squamous region of the ruminant forestomach also protects gastric epithelium against the
damaging effects of rapid SCFA absorption at the low pH produced by the proper gastric
glandular region of the stomach. Therefore, expansion of the stratified squamous epithelial
region may have been the most parsimonious response to the need for gastric expansion in
herbivores.
As with many of the advanced invertebrates, the intestines of fish, larval amphibians, and some
mammals lack a distinct hindgut. However, the intestine of most terrestrial insects and
vertebrates consists of a midgut and hindgut. The midgut of these animals is the principal site
for digestion and absorption. The hindgut aids in the recovery of electrolytes, nitrogen, and
water and serves as the principal site of microbial digestion in most species. The kidneys of
vertebrates carry out the excretory functions of the insect’s Malpighian tubules. However, these
excretions enter the gut at the cloaca of the adult amphibians, reptiles, and birds, which may
account for the appearance of antiperistalis in the hindgut of terrestrial vertebrates.
Endothermy required a more rapid processing of food and digesta by birds and mammals, and
additional mechanisms for the selective retention of bacteria and plant material by the
herbivores. Haustra in the hindgut of many and the foregut of some herbivorous mammals aid in
digesta retention. The colonic separation mechanisms of avian and mammalian cecum
fermenters and compartmentalization of the stomach of many mammalian foregut fermenters
provided another means for the selective retention of bacteria and plant fiber.
Other than the phagocytic properties of midgut cells in some mammalian neonates, food is
digested initially by extracellular enzymes secreted by the salivary, gastric, or pancreatic glands
of vertebrates and reduced to smaller units by enzymes in the brush border and cytosol of
midgut absorptive cells. Many of the digestive enzymes and mechanisms of nutrient absorption
appear to have first evolved in the invertebrates. Although the exocrine pancreatic glands are
distributed along the midgut of cyclostomes and some of the more advanced species of fish,
they are consolidated in a compact pancreas in most vertebrates. The liver is also a compact
organ in all vertebrates and no longer serves as a site for digestion or absorption of nutrients.
However, the midgut functions as the principal site of digestion and absorption, and the hindgut
conserves electrolytes, water, and nitrogen much as they do in the insects.
Neuroendocrine Control:
Neurotransmitter-like substances, peptides, and other messenger molecules are found in
protozoa, and a nervous system is present in sponges and well developed in annelids, mollusks,
arthropods, and vertebrates (Fig. 12.13). The motor, secretory, digestive and absorptive
functions of the vertebrate digestive system are controlled and integrated by a variety of
peptides and other substances secreted by neurons and endocrine cells. The neurons of
vertebrates secrete purines, amines, peptides and other agents that either modulate the release of
neurotransmitters by other neurons or have a direct effect on muscle, secretory, or absorptive
cells. Extrinsic innervation of the gastrointestinal tract by vagal (cranial) nerves is limited to the
stomach of fish (Fig. 11.4). The sacral cholinergic nerve supply to the hindgut seems to have
appeared with the evolution of a distinct hindgut in the adult amphibians (Fig, 11.5).
Figure 12.13. Evolution of biochemical elements of
the nervous and endocrine systems. (Modified
from Le Roith et al. 1982)
Figure 11.4. Diagrammatic representation of the autonomic
cholinergic excitatory (red line), adrenergic (yellow line) and
nonadrenergic inhibitory (blue line) nerves to the stomach of
vertebrates. (From Burnstock 1969). (From CD Chapter 11)
Figure 11.5. Diagrammatic representation
of the autonomic cholinergic excitatory (red line), adrenergic
(yellow line) and nonadrenergic inhibitory (blue line) nerves to
the intestine of vertebrates. (From Burnstock 1969). (From CD
Chapter 11)
The motor, secretory, digestive, and absorptive activities of the digestive system are affected by
a variety of peptides secreted by endocrine cells. Many of these peptides are released by both
nerves and endocrine glands and serve as neurotransmitters, neuromodulators, hormones, or
paracrine agents. This led to the theory that hormones evolved from neuroectodermal tissue
(Pearse 1969). Barrington (1962) advised caution in interpreting fragmentary evidence collected
from a few species and pointed out that many adaptations are determined by the evolution of
receptors and the modulation of programming by receptor cells, rather than changes in the
structure of these peptides. However, some families of hormones appear to have evolved from
ancestral peptides that served initially as neurotransmitters or modulating agents.
Pancreatic polypeptide-like activity has been reported in the nervous system of earthworms,
mollusks, and insects, and substance P has been identified in the nervous system of
coelenterates, prochordates, and all classes of vertebrates (Stevens and Hume 1995). Vasoactive
intestinal polypeptide (VIP) is considered the ancestral form of peptide in the secretin family,
because of its presence in the nervous tissue of prochordates, but secretin activity was also
reported in prochordates and mollusks. The CCK/gastrin family of peptides is believed to have
evolved from an ancestral peptide rather than through parallel evolution (Vigna 1983; 1986).
CCK-like peptides are found in all classes of vertebrates and it is the only member of this family
found in cyclostomes. Although, extracts of the hagfish intestine stimulated contraction of the
guinea pig gallbladder, the hagfish gallbladder was not stimulated by either these extracts or
mammalian CCK, suggesting the absence of appropriate receptors. Vigna (1986) concluded that
a CCK-like agent was present in prochordates and persisted in mammals, but its regulation of
gallbladder contraction did not appear until after the evolution of cyclostomes.
A CCK-gastrin like hormone stimulates HCl secretion in chondricthyean fish, but appears to
have been lost in present-day osteicthyeans and possibly replaced by bombesin. Bioassay
procedures that discriminate between CCK and gastrin suggest their divergence between the
evolution of elasmobranch and teleost fish. However, the gallbladder of coho salmon responded
to both CCK and gastrin (Vigna and Gorbman 1977), and radioimmunoassay and
immunostaining studies indicate the appearance of a separate gastrin-like peptide at the
divergence of amphibians and reptiles. Therefore, Vigna (1986) concluded that the functional
evolution of these hormones involved recruitment of new targets for old hormones, new cellular
sources for old hormones, and old targets for new hormones.
Evolution of herbivores:
One of the major advances in evolution was the advent of animals that can derive a substantial
amount of their nutritional requirements from the leaves, petioles, or stems of plants. The
abundance and availability of this plant material throughout the year opened the way to a much
wider range of diets and ecological niches. However, the ability to derive nutrients from these
fibrous portions of the plant, requires the ingestion of large quantities of plant material, its
breakdown into small particles, and either its rapid passage through the gut or its retention for
microbial fermentation of the cell walls. The first option was adopted by some invertebrates,
most fish, the larval amphibians, emu, and panda. The second option requires cellulytic
enzymes of either endogenous or microbial origin.
Evolution of herbivores - Invertebrates:
Buchner (1965) discussed the widespread distribution of endosymbiosis among invertebrates.
Algae in the cells of Paramecium bursa provide their host with O2 and carbohydrates, and allow
its survival in the absence of a normal food supply if there is sufficient light for photosynthesis.
Bacteria in the endoplasm of the amoebae Pelomyxa are believed to be responsible for their
ability to digest filter paper. A similar inclusion of bacteria has been observed in cells lining the
digestive tract of some invertebrates, and large numbers of bacteria (and sometimes, protozoa)
are found in the lumen of the digestive tract of many advanced species. Methanogenic bacteria
were found in the digestive tracts of cockroaches, termites, millipedes, and scarab beetles
(Hackstein and Stumm 1994). Microbial fermentation has been demonstrated in the gut of
annelids, mollusks, echinoderms, and insects. The microbes are most concentrated in the crop of
cockroaches, the midgut or midgut ceca of some herbivores, and in the expanded hindgut of
termites (Fig, 12.14).
Figure 12.14. Alimentary tract of termite Eutermes; a) esophagus, b)
crop, c) proventriculus, d) midgut, e) Malpighian tubules, f) hindgut,
g) rectal valve, h) rectal pouch, i) terminal rectum. (Modified from
Wigglesworth 1962)
Although cellulose digestion is well documented in a number of insects,
there is disagreement over how it is accomplished. Wigglesworth (1984)
stated that protozoa are the chief agents of cellulose digestion in woodeating termites. Martin (1991) contended that cellulose is digested by bacteria and protozoa,
based partly on the assumption that the complete cellulase complex of exo-1,4-glucanase and
endo-1,4-glucanase is required and insects are unable to synthesize the exo-glucanase
(cellobiohydrolase). However, Slaytor (1992) concluded that there is no evidence that an exo1,4-glucanase is either involved in or required for cellulose digestion in termites or wood-eating
cockroaches, and endo-1,4-glucanase is found in the salivary glands, foregut, and midgut of
these insects. He concluded that although there is evidence that bacteria are involved in
cellulose digestion in the gut of these and other invertebrates, the evidence is often weak.
Evolution of herbivores - Vertebrate herbivores:
The earliest vertebrate herbivores were probably fish that adopted pharyngeal teeth, a gizzardlike stomach, or microfiltration for the reduction of aquatic plants to a smaller particle size and
used their midgut as the principal site for microbial fermentation. However, the expansion of
vertebrates into terrestrial habitats required a larger gut capacity and longer retention time for
the fermentation of plants that contained higher levels of structural carbohydrates. Although gut
capacity increases with body mass, an increase in body mass also requires the ingestion of
larger quantities of the more readily available but less readily fermentable forage. Evolution of
the hindgut for the conservation of electrolytes and water by terrestrial vertebrates provided a
site for the more prolonged retention of digesta and multiplication of larger populations of
indigenous bacteria.
Figure 12.12.
Phylogenetic origins of
various groups of
vertebrates. A) Urodela,
B) Lepospondylii, C)
Apoda, D) Anura, E)
Labyrinthodontia, F)
Apisidospondylii, G)
Chelonia, H) Anapsida, I)
Cotylosauria, J)
Eurapsida, K) Diapsida,
L) Eosuchia, M)
Squamata, N)
Rhyncocephalia, O)
Ornithischia,
P)Thecodontia, Q)
Synapsida, R) Parapsida, S) Pelycosauria, T) Pterosauria, U) Crocodilia, V) Aves, W)
Saurischia, X) Prototheria, Y) Metatheria, Z) Pantotheria, AA) Therapsida, BB) Eutheria,
CC) Ichthyosauria. (Modified from Torrey 1971)
Dinosaurs: The appearance of herbivorous prosauropods in the Late Triassic was followed by
the rapid radiation of two major groups; the saurischians and ornithiscia (Fig. 12.12).
Saurischian dinosaurs included a wide range of herbivorous species and the ornithiscians appear
to have been exclusively herbivores (Fastovsky and Weishampel 1996). Gymnosperms (cycads,
cycadoids and conifers) and pteridophytes (ferns and other free-sporing plants) were the
predominant terrestrial plants during the Triassic and Jurassic, but angiosperms (flowering
plants) became the predominant plants during the Cretaceous Period (Coe et al. 1985; Taggart
and Cross 1997). The body masses of species in 220 dinosaur genera were estimated to have
ranged from 1-70,000 kg on nearly every continent and during most stages of the Mesozoic
(Peczkis 1994). Although the Jurassic ornithischians were relatively small, the herbivorous
sauropods of the late Jurassic included the largest terrestrial vertebrates of all time. The largest
sauropods peaked in diversity during the Late Jurassic, but by the late Cretaceous the dominant
herbivores were ornithischians of intermediate body weight.
Studies of bone histology and growth rates, and other characteristics indicate that the dinosaurs
were endotherms (Bakker 1971; Robertshaw 1984; Barrick and Showers 1994; Chinsamy and
Dodson 1995; Fisher et al. 2000). However, Chinsamy and Dodson (1995) concluded that
elevated growth rates and endothermy may have arisen independently in different groups of
dinosaurs, and the general consensus is that the metabolic rate of dinosaurs fell between that of
modern reptiles and mammals (Fastovsky and Weishampel 1996).
The saurischian herbivores had cropping teeth, and the presence of polished stones with their
fossil remains suggests that they used a gastric mill for the breakdown of plant material (Bakker
1987; Barrett and Upchurch 1995; Currie 1997) in a manner similar to that seen in the modern
day mullet, birds, and some reptiles. However, the Cretaceous ornithiscians included two
diverse groups of herbivores with a jaw musculature and dental batteries suitable for the
reduction of plant material to a small particle size (Fastovsky and Weishampel 1996). The
hadrosaur masticatory apparatus included cheek teeth that formed oblique shearing blades and a
jaw articulation that allowed lateral rotation of the jaws (Fig. 12.15). The masticatory apparatus
of ceratopsians consisted of a dense cluster of cheek teeth with uneven occluding surfaces and
massive jaw muscles.
Figure. 12.15. Unlike mammals (A), ornithopod dinosaurs
(B) had jaws of equal width and cheek teeth that
interlocked to form oblique, shearing surfaces. (From
Norman and Weishampel 1985)
Marshall and Stevens (2000) concluded that the large body
size of most sauropod herbivores and the rarity and inherent
inefficiency of foregut fermentation in present-day herbivores
with a gastric mill suggest that the sauropod herbivores were
colon fermenters. However, the masticatory apparatus of the ornithiscian hadrosaurs and
ceratopsians would have satisfied the requirements for foregut fermentation, and the body mass
of many species (Tables 12.1a,b) was less than that of the largest modern-day hippos or Tertiary
ground sloths. Furthermore, the maximum body weight of hadrosaur and ceratopsian foregut
fermenters could have exceeded that of present-day mammalian foregut fermenters if they had a
lower rate of metabolism or a kangaroo-like forestomach less restrictive on forage intake.
Table 12.1a.
Body masses calculated
from scale model (M),
pelvic height (P), femur
diameter (F), or
humerus diameter (H).
Asterisk denotes body
mass cited by authors,
all other values are
estimates from
information provided by
authors. (modified from
Peczkis 1994)
Table 12.1b.
Body masses calculated from scale
model (M), pelvic height (P), femur
diameter (F), or humerus diameter
(H). Asterisk denotes body mass
cited by authors, all other values
are estimates from information
provided by authors. (modified
from Peczkis 1994)
A hadrosaur dinosaur Gryptosaurus from the
late Cretaceous of Alberta, Canada.
(Weishampel & Young 1996)
A ceratopsian dinosaur Styracosaurus of western America from the late Cretaceous of
western America. (Weishampel & Young 1996)
Farlow (1987) concluded that foregut fermentation would be of little advantage to herbivorous
dinosaurs beyond its ability to remove plant toxins that interfere with metabolism. However, a
more complete extraction of energy from forage and greater ability to conserve water would
have allowed their adaptation to climates and habitats far less suitable to other herbivores.
Therefore, evolution of foregut fermenters may have contributed to the diversification and
distribution of the Cretaceous ornithiscians.
The digestive strategies of ornithiscians could be explored by studies of microbial fermentation
of the present-day angiosperms, gymnosperms, and pteridophytes that were listed by Taggart
and Cross (1997) as similar to those of the Cretaceous Period. Bacteria could be collected from
the hindgut or foregut of modern-day herbivores, including those that have adapted to high
levels of tannin in their diet, such as the koalas (Osawa et al. 1993), spruce grouse (Pendergast
and Boad 1973), and some tortoises (Swain 1976). Viable cultures can be maintained for up to
four weeks to determine their
adaptability to substrates and measure
microbial fermentation over a range of
temperatures and retention times (Dr.
Vivek Fellner, Department of Animal
Science, North Carolina State
University - personal
communication). Models based on
chemical reactor theory could then be
employed to estimate the optimal
digestive strategy of herbivorous
dinosaurs as a function of their gut
capacity (body mass), body
temperature, and the digestibility of
their diet.
The massive extinction of plants and animals at the end of the Cretaceous Period removed the
dinosaurs (Fig. 12.12) and the other terrestrial vertebrates over 10 kg in body weight. The
paucity of present-day reptilian herbivores has been attributed to an inefficient masticatory
apparatus and the small body mass (gut capacity) of most species. A small body size provides a
greater ratio between surface area and body mass for rapid equilibration between the body and
environmental temperature. However, the fact that the largest present-day reptilian herbivores
are an arboreal lizard and tortoises with a protective carapace suggests that their size may also
have been limited by predation by mammals.
Figure 12.12. Phylogenetic
origins of various groups of
vertebrates. A) Urodela, B)
Lepospondylii, C) Apoda, D)
Anura, E) Labyrinthodontia, F)
Apisidospondylii, G) Chelonia,
H) Anapsida, I) Cotylosauria,
J) Eurapsida, K) Diapsida, L)
Eosuchia, M) Squamata, N)
Rhyncocephalia, O)
Ornithischia, P)Thecodontia,
Q) Synapsida, R) Parapsida, S) Pelycosauria, T) Pterosauria, U) Crocodilia, V) Aves, W)
Saurischia, X) Prototheria, Y) Metatheria, Z) Pantotheria, AA) Therapsida, BB) Eutheria,
CC) Ichthyosauria. (Modified from Torrey 1971)
Birds and mammals: The earliest mammals are believed to have been small carnivores that
appeared in the Jurassic Period (Crompton and Parker 1978). Marsupial and eutherian mammals
diverged during the Early Cretaceous and the ancestors of modern-day eutherian herbivores had
appeared by the Late Cretaceous (Fig. 12.12). The earliest herbivores may have been
multituberculates, which were abundant during the Mesozoic and persisted into the Cenozoic
(Krause 1982; Carroll 1988; Wall and Krause 1992). Figure 12.16 shows the evolution of
angiosperms, rodents, artiodactyls, perissodactyls, and macropod marsupials during the Tertiary
Period of the Cenozoic. Artiodactyls, perissodactyls, proboscideans, hyracoids, and sirenians
stemmed from a common source of Cretaceous ungulates or hoofed animals (Prothero 1994).
The climate of the Paleocene and Eocene Epochs of the Tertiary was warmer and wetter than
that of today, and rain forests extended over much of the globe. However, a gradual cooling
since the beginning of the Eocene was accompanied by the diversification of ungulates, rodents,
and lagomorphs (Carroll 1987; Prothero 1994).
Figure 12.16. Diversification of angiosperms, rodents, ungulates, and macropod
marsupials during the Tertiary. The width of columns is a compromise between species
diversity and density. (data on angiosperms: Van Soest 1994; data on rodents: Romer
1966; data on ungulates: Janis 1976; data on macropod marsupials: Hume 1978)
(Modified from Stevens and Hume 1995)
The Oligocene saw the appearance of grasslands, with a higher cellulose-lignin ratio, and
further diversification of rodents, artiodactyls, perissodactyls, and macropod marsupials (Fig.
12.16). It was also accompanied by the diversification of cetaceans, which are closely related to
the artiodactyls (Árnason et al. 1991; Adachi et al. 1993; Milinkovitch et al. 1993) and may
have originated from terrestrial herbivores. This could account for the multicompartmental
forestomach and high concentrations of bacteria and SCFA in both toothed and baleen
cetaceans. Separation of the camelids and ruminants in the Middle Eocene suggests that
rumination had already evolved in this lineage, but the appearance of the omasum as an
important functional organ in the advanced ruminants seems to have occurred after their
separation from tragulids in the Late Oligocene.
The cooler, drier climates of the Miocene were accompanied by an expansion of grasslands and
diversification of the perrisodactyls, proboscideans, hyracoids, sirenians, and lagomorphs
(Romer 1966; Prothero 1994). However, the most pronounced diversification and radiation was
seen in the advanced ruminants, rodents, and macropod marsupials (Fig. 12.16).
The Cricetidae, which includes lemmings, voles, and many of the other herbivorous rodents,
underwent a major expansion. The earliest fossils of macropod Potoridae were small ratkangaroos, with a dentition that was adapted to nonabrasive materials and has changed
relatively little since (Bartholomai 1972; Sanson 1989). The earliest Macropodidae (wallabies
and kangaroos) inhabited wet forests (Flannery 1984) and were probably similar to extant small
(2-8 kg) wallabies, with lophodont dentition suitable for soft, nonabrasive forage (Hume 1978;
Freudenberger et al. 1989).
The latter half of the Tertiary saw a reduction in global temperatures and an increase in the body
size of many mammals. Some became megaherbivores, over 1000 kg in body weight. The
eutherian megaherbivores included hippos, camelids, bison, rhinoceroses, mammoths,
mastodons, sirenians, and giant ground sloths (Owen-Smith 1988). The giant ground sloth
Megatherium reached weights of 3400 kg. Baluchiterium, a rhinoscerotid that appeared in Asia
during the Oligocene and early Miocene, had a shoulder height of 5 m and is believed to have
been the largest terrestrial mammal of all time. The marsupial herbivores of Australasia
included the giant wombat Phascolonus (150 kg), tapir-like Palorchestes (300 kg), wallaby
Protomodon (50 kg), browsing, short-faced kangaroo Procoptodon, and Diprotodon the largest
(1150 kg) marsupial herbivore (Hume 1999). The lower body weights of the largest marsupials,
in contrast to eutherian mammals, has been attributed to the arid climates and poor
replenishment of soil nutrients by tectonic activity in this region over the past 60 million years
(Flannery 1994). By the end of the Pleistocene Epoch of glaciations most of the megaherbivores
were extinct. The final extinction of most megaherbivores is attributed to a combination of
climatic change and human predation (Owen-Smith 1988). The only modern-day
megaherbivores are the elephants, white rhinos, giraffes, and hippos.
Figure 12.16 shows that the diversification of mammalian herbivores since the beginning of the
Miocene was greatly influenced by the evolution of rodent cecum fermenters and the artiodactyl
and marsupial foregut fermenters. This would be further supported by the inclusion of the
modern day cecum fermenting lagomorphs and arboreal marsupials, and foregut fermenting
sloths and colobid monkeys. Therefore, the evolution of cecum and foregut fermenters played
an important role in the diversification and distribution of mammalian herbivores.
Fossil records of ptarmigan and ostriches were found in the Miocene (Johnsgard 1983; MourerChauviré et al. 1996). However, rhea and emu fossils date back only to the Pliocene, and fossil
records of New Zealand moas and Madagascar elephant birds extend only to the Pleistocene
(Carroll 1988).
Figure 12.16. Diversification of
angiosperms, rodents, ungulates,
and macropod marsupials
during the Tertiary. The width
of columns is a compromise
between species diversity and
density. (data on angiosperms:
Van Soest 1994; data on rodents:
Romer 1966; data on ungulates:
Janis 1976; data on macropod
marsupials: Hume 1978)
(Modified from Stevens and
Hume 1995)
The earliest mammalian herbivores may have been colon fermenters, as suggested by Hume and
Warner (1980). However, the appearance of cecum fermenters would have allowed an earlier
evolution of herbivory in smaller species. The earliest cecum fermenters may have fed on
invertebrates and used cecal bacteria to break down chitin, the structural carbohydrate in the
integument of many invertebrates. Chitinolytic bacteria are found in the midgut of fish, large
ceca of many, and forestomach of baleen whales that feed on invertebrates (Stevens and Hume
1995). Evolution of a colonic separation mechanism allowed the selective retention of smaller,
more rapidly digestible plant particles in the cecum and rapid transit of larger digesta particles
through a relatively short colon. Periodic release of cecal contents (cecotrophy) would provide
highly nutritious feces and enhance the advantages of the coprophagy, which is seen in most
other mammals only on nutrient deficient diets (Stevens and Hume 1995). Lagomorphs,
herbivorous rodents and arboreal marsupials, some herbivorous primates, and most avian
herbivores have retained this strategy.
Expansion in the body size of many herbivores may have increased the diameter of the colon,
and reduced the effectiveness of the colonic separation mechanism. An increase in the length of
the colon would also increase its absorptive and microbial digestive capacity, which would
reduce the nutritional value of coprophagy. Therefore, the colon became the principal site of
microbial fermentation in the largest avian and mammalian herbivores. Forestomach
fermentation probably evolved in a series of changes that began with its expansion for food
storage and use as a secondary site to cecum fermentation, as seen in the present-day hyracoids
and some herbivorous rodents. This would be followed by further foregut expansion in species
that fed on a mixture of plant concentrates and fiber, such as the present-day peccaries that
inhabit Amazon forests (Bodmer 1989) and the smallest ruminants.
Cooler, drier climates during the Miocene reduced the rapid rate of plant growth and
lignification, and increased the spread of grasslands with a higher cellulose/lignin ratio. Cooler
climates also encouraged the evolution of larger species, including the megaherbivores. A
longer digesta retention time set limits on the forage intake and body mass of foregut
fermenters. However, foregut fermentation allowed the recovery of microbial protein and Bvitamins and adaptation to regions where the climates were more arid, the forage was less
digestible, or the plants were more toxic. This proved especially effective when combined with
rumination and omasal filtration of digesta in the advanced ruminants.
The diversification and distribution of vertebrates were influenced by many factors, including
reproductive efficiency and defenses against predation. However, the advent of herbivores that
could subsist on the fibrous portion of plants played a major role in the diversification and
distribution of mammals and dinosaurs. The success of herbivorous mammals can be attributed
to an efficient masticatory apparatus, and to the evolution of a colonic separation mechanism
and expanded cecum in the smallest herbivores and an expanded proximal colon or forestomach
in the larger herbivores. Convergence on the strategies of cecum and forestomach fermentation
allowed the evolution of small and intermediate sized endothermic herbivores, and their
distribution to a wider range of habitats. An evolution of foregut fermenters may have played a
similar role in the diversification and distribution of Cretaceous dinosaurs.
Summary & Conclusions:
The digestive system of vertebrates consists of a headgut (mouthparts and pharynx), foregut
(esophagus and stomach), midgut, hindgut, exocrine pancreas, and biliary system. The headgut
serves for the procurement and physical breakdown of food. Food is passed through the
esophagus to the stomach, where it is stored and undergoes the initial stages of digestion by HCl
and pepsin. The midgut is principal site of digestion, which is aided by enzymes secreted by the
pancreas and located in the lumen-facing membranes and contents of the midgut epithelial cells,
and by bile salts that are secreted by the liver and stored in the gall bladder. The midgut is also
the principal site for the absorption of nutrients by passive diffusion or carrier-mediated
transport across its epithelial cells. Digestion is aided by large quantities of electrolytes and
water secreted by the oral glands, pancreas, biliary system and gastrointestinal tract. Most of the
electrolytes and water are reabsorbed by the midgut and hindgut. The hindgut is also the
principal site for the microbial production and conservation of nutrients in most species. All of
these activities are integrated and controlled by the nervous system, hormones and paracrine
agents. The effectiveness and efficiency of this basic design is demonstrated by a n analogous
arrangement in the digestive system of many advanced invertebrates.
Despite these common characteristics, the vertebrate digestive system shows a wide range of
adaptations to the diet, habitat, or other characteristics of the species. Food can be reduced to a
smaller particle size by teeth that are located in the jaws, oral cavity, or pharynx, or by
microfiltration, a beak, or a gastric mill. The stomach is absent in cyclostomes, some advanced
species of fish, and the larval amphibians, and its functions are served by the crop and
proventriculus in birds. The stomach secretes neither HCl nor pepsinogen in a few species of
mammals, and it includes an expanded, haustrated or compartmentalized forestomach in a few
others. Pancreatic tissue is distributed along the intestine of some fish, and a gall bladder is
absent in some fish and mammals. The hindgut varies from a short segment of intestine that is
difficult to distinguish from the midgut in most fish, the larval amphibians, and some birds and
mammals, to a voluminous, haustrated, and compartmentalized large intestine in some
mammals. The hindgut of amphibians, reptiles and birds aids in the recovery of electrolytes,
nitrogen, and water from the urinary excretions, as well as the secretions of the digestive
system. Although many of the endogenous enzymes, indigenous microbes, mechanisms for
secretion and absorption, and neuroendocrine agents are found in all classes of vertebrates, they
can vary in their presence, composition, or location.
Many adaptations of the digestive system are related to the habitat or diet of the species. Gill
rakers or pharyngeal teeth allow some fish to swallow smaller particles of food without loss
through the gills. Absorption of Na+ and Cl- by the esophagus aids others in their adaptation to a
marine environment. Retention of digesta in a more highly developed hindgut allows terrestrial
vertebrates to conserve electrolytes and water. A longer hindgut allows the more efficient
conservation of water in species that inhabit arid environments. The digestive tract of carnivores
and animals that feed on plant concentrates tend to be relatively simple in structure, with a rapid
rate of digesta passage and episodic release of digestive fluids and enzymes. Omnivores tend to
have a more complex digestive tract and longer digesta retention time. The high fiber diet of
herbivores requires the ingestion of large quantities of plant material, a larger gut capacity, a
longer digesta retention time, and a more continuous and voluminous secretion of electrolytes
and water.
The evolution of herbivores played an important role in the diversification and distribution of
vertebrates, especially the mammals and dinosaurs. The success of mammalian herbivores can
be attributed to an improved masticatory apparatus and the appearance of cecum and foregut
fermenters. The success of the herbivorous dinosaurs also can be attributed to an effective
masticatory apparatus or gastric mill and, possibly, the appearance of foregut fermenting
ornithiscians.
The previous sections include many examples of the contributions of comparative physiology to
the understanding of basic physiological mechanisms. Many of these contributions have derived
from the differences rather than the similarities among species. The nonglandular, stratified
squamous epithelium of the frog skin and ruminant forestomach offered a much simpler system
for the study of electrolyte and short-chain fatty acid transport mechanisms. Relationships
between the rates of metabolism, food intake, digesta passage, digestion, and absorption are best
studied in either ectotherms or endotherms with a temperature span wider than that of most
birds and mammals. The ability to access and sample the forestomach contents of ruminants
provided the basic information on the composition of indigenous gut bacteria and their
contribution to the production and conservation of nutrients. The equine large intestine provided
a unique model for the compartmental analysis of secretion, absorption, and digesta flow.
Variations in the neurotransmitters, neuromodulators, hormones and paracrine agents of
different classes of vertebrates helped describe their functions and how they evolved.
One of the most compelling reasons for the study of comparative physiology of the digestive
system is the information it provides for the maintenance of domesticated and captive animals,
conservation of wildlife, and preservation of endangered species. Many diseases of
domesticated and captive animals can be traced to an improper diet or feeding schedule, and the
survival of free-ranging species rests on a delicate balance between plants, herbivores,
omnivores, and carnivores. Interruption of the food chain at any level can affect their survival.
Removal or poisoning of their natural habitat can guarantee their extinction.
The digestive tract is the major portal of entry for both nutrients and the toxic agents. Yet the
digestive systems of many mammalian species have received little or no study. Birds and
reptiles have received less study, and the amphibians and fish that comprise almost half of the
vertebrate species have received the least attention. Although survival of these animals is
dependent on the food chain, we know very little about the composition of the diet of many of
these species and how it changes with the seasons or migration. For example, how do the
endogenous and microbial enzymes match the storage carbohydrates of algae or the wax esters
of plankton in the diet of many animals at the base of the food chain? Do the endogenous and
microbial chitinases play a significant role in the many species that feed on marine or terrestrial
invertebrates? Is the ability of the hindgut of some birds to switch from Na+ - H+ exchange to
eletrogenic Na+ absorption on low Na+ diets shared by some reptiles or other vertebrates?
The renewed interest in the comparative physiology of the digestive system and the application
of new methods and techniques to a wider range of species is encouraging. These studies should
provide a better understanding of the basic mechanisms and how they are disrupted by abnormal
diets, unnatural feeding practices, and digestive diseases. They will also provide information
that is needed for the maintenance of domesticated and captive animals, conservation of
wildlife, and preservation of endangered species.