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THE DIGESTIVE SYSTEM OF
VERTEBRATES: CD 
7. Digesta transit and retention:
Introduction:
The length of time that food and digesta are retained in the gastrointestinal tract helps determine the degrees of digestion and absorption. Although their passage can be measured by the gut emptying or the transit time (first appearance of food in the feces), fluid and particles travel at different rates and the relative rate of passage varies with species and diet. Therefore, the best measure of digesta passage is the mean retention time (MRT) of fluid and particulate digesta markers that are not normally present in gut contents and neither digested, absorbed or adsorbed during their travel through the gut. The most commonly used fluid markers are polyethylene glycol (PEG) and Cr++-EDTA. Particulate markers can consist of glass beads, plastic, or rubber of various dimensions, but one of the best markers is chromium fixed to food particles by a mordant that renders them indigestible. Digesta retention time is reduced by an increase in the mass-specific metabolic rate, body temperature, or the percentage of plant fiber in the diet. It is also determined by the structural and functional characteristics of the gastrointestinal tract (Stevens and Hume 1995).
Digesta transit and retention time - Fish:
Horn (1989) reviewed a variety of studies on the rate of passage of food particles through the digestive tract of fish. The total gut emptying time ranged from 10 to 158 hours for carnivores, but was less than 10 hours in most herbivores. Omnivorous hemiramphids, which feed on seagrass during the day and crustaceans at night, passed seagrass through their gut at about twice the rate of crustaceans. Therefore, the rapid passage in herbivores appears to be due to the high fiber content of their diet. Digesta transit and food intake increase with an increase in body temperature. Fange and Grove (1979) found that body temperature had an average Q10 effect of about 2.6 on the gut emptying time of a number of species, and the stomach was the principal site of digesta retention. However, a similar Q10 was recorded for the transit of food through the digestive tract of the herbivorous freshwater grass carp (Table 7.1), which lacks a stomach, and the midgut is the principal site for microbial fermentation in most herbivorous fish.
Table 7.1. Effect of body temperature on digesta transit in fish
Digesta transit and retention time - Reptiles:
The digesta retention time in reptiles is generally longer than that of fish. The stomach is the principal site of digesta retention in carnivorous reptiles that swallow their entire prey, and the midgut is the principal site in the herbivorous Florida red-bellied turtle. However, the colon is a major site of digesta retention in most herbivorous reptiles. The mean retention times of fluid and particulate digesta markers by the gastrointestinal tract of a carnivorous caiman, omnivorous painted turtle, and two herbivorous reptiles at similar body temperatures are illustrated in Table 7.2. Particles were retained longer than fluid by all of these species. Their retention time was longest in herbivores and this increased with an increase in particle size, due to their selective retention in a more highly developed hindgut (Fig. 5.4).
Table 7.2. Mean digesta retention time in reptiles
Liquid marker was polyethylene glycol or BaSO4. Particulate markers were segments of polyethylene tubing.
Figure 5.4. Gastrointestinal tracts of a carnivorous caiman and snake, an omnivorous turtle, and a herbivorous tortoise and lizard. Note the cecum, larger volume, and greater relative length of the herbivore hindgut, and the baffles provided by projections of tissue into the cecum and colon of the iguana. (From Stevens & Hume 1995.)
A reduction in body temperature reduced the rate of food intake and increased the digesta transit time in snakes and lizards, with Q10 values of 2.7-3.8 (Skoczylas 1978; Waldschmidt et al. 1986). However, it had no effect on gross energy digestibility in the herbivorous chuckwalla Sauromalus obesus (Zimmerman and Tracy 1989) or green iguana Iguana iguana (Baer 1996). Therefore, the increase in digesta retention time at lower body temperatures appeared to compensate for the accompanying reduction in the rates of digestion and absorption of end products.
Digesta transit and retention time - Birds:
Due to the lower gut capacity and higher metabolic rate required for flight, the mean retention times for fluid and particles tends to be short in most birds. The MRTs for fluid markers ranged from 0.8 to 0.9 hours in the gastrointestinal tracts of the rufus hummingbird, cedar waxwing, European starling, and American robin (Stevens and Hume 1995). The foregut (crop and gizzard) is the principal site of digesta retention in the small passerine species, and raptors such as hawks, eaglkes, and owls. The crop and distal esophagus are also the major site of digesta retention in the herbivorous hoatzin. However, the midgut is the major site in the emu, the ceca are major sites in the herbivorous grouse, partridge and rheas, and the colon is the principal site in the ostrich (Fig. 5.6).
Figure 5.6. Gastrointestinal tracts of avian herbivores. The crop is absent in the ostrich, but expanded in the grouse and rhea, and both the crop and distal esophagus are expanded in the hoatzin. Note the well-developed ceca in the grouse and rhea, and extremely long colon of the ostrich. (From Stevens & Hume 1995.)
The MRTs for fluid and particulate markers in a rock ptarmigan, albatross, penguin, and emu are shown in Table 7.3. Their digesta retention times were unrelated to body mass and could be attributed largely to differences in their diet and gastrointestinal tract. The long retention time of fluid and brief retention time of particles by the herbivorous ptarmigan can be attributed to the selective retention of fluid and small particles in their large ceca. Studies of the Alaskan rock ptarmigan showed that while larger particles of digesta were rapidly excreted in the feces, fluid and small particles of digesta were selectively retained in the ceca and released for fecal excretion at about eight hour intervals, with an average discharge of 56% of the cecal contents (Gasaway et al. 1975). This compensates for the higher mass-specific metabolic rare of small herbivores by minimizing the gut-filling effects of large particles and concentrating the fermentative effort on the more readily digestible small particles. The piscivorous sooty albatross and rockhopper penguin, and herbivorous emu showed much shorter retention times for fluid and longer times for the retention of particulate markers.
Table 7.3. Mean digesta retention time in birds
Digesta transit time of birds tend to be short, and particles are generally retained longer than fluid digesta, but fluid was selectively retained in the ceca of the herbivorous ptarmigan. (From Stevens & Hume 1995)
Digesta transit and retention time - Mammals:
The stomach is the principal site of digesta retention in many mammalian carnivores and species that feed on plant concentrates, and this is prolonged in the expanded stomachs of vampire bats (Fig. 5.12b). The proximal colon is the principal site in some carnivores and omnivores, and mant herbivores. However, an expanded cecum is a principal site in a few small carnivores such as the elephant shrew (Fig. 5.11d), omnivores such as the Norway rat (Fig. 5.14b), and bandicoot (Fig. 5.15d), and most small herbivorous mammals.
Figure 5.12b Vampire bat (Desmodus rufus) digestive tract (Stevens & Hume 1995)
Figure 5.11d Elephant shrew (Rhynchoyon chrysopygus) digestive tract (Stevens & Hume 1995)
Figure 5.14b Norway rat (Rattus norvegicus) digestive tract (Stevens & Hume 1995)
Figure 5.15d Short-nosed bandicoot (Isoodon macrourus) digestive tract (Stevens & Hume 1995)
Figure 7.1a. Percentage of digesta fluid and particulate markers (+/- SE) recovered from the gastrointestinal tract of the dog at various times following their oral administration during feeding. Fluid markers consisted of PEG or 51Cr-EDTA. Plastic markers consisted of polyethylene tubing with an outside diameter of 2 mm, cut into lengths of 2 mm. S = stomach; SI = small intestine; C = colon; Fe = feces. Particles were selectively retained by the stomach and the large intestine. (Modified from Banta et al. 1979.)
Figure 7.1b. Percentage of digesta fluid and particulate markers (+/- SE) recovered from the gastrointestinal tract of the pig at various times following their oral administration during feeding. Fluid markers consisted of PEG or 51Cr-EDTA. Plastic markers consisted of polyethylene tubing with an outside diameter of 2 mm, cut into lengths of 2 mm. S = stomach; SI = small intestine; Ce = cecum; PC = proximal colon; C = colon; TC = terminal colon. Particles were selectively retained by the stomach and the large intestine. (Modified from Clemens et al. 1975a.)
Figure 7.1c. Percentage of digesta fluid and particulate markers recovered from the gastrointestinal tract of the rabbit at various times following their oral administration during feeding. Fluid markers consisted of PEG or 51Cr-EDTA. Plastic markers consisted of polyethylene tubing with an outside diameter of 2 mm, cut into lengths of 2 mm. S = stomach; SI = small intestine; Ce = cecum; C = colon; Fe = feces. Particles were selectively retained by the stomach, but fluid was selectively retained by the cecum of rabbits, with a more rapid excretion of particles. (Modified from Pickard & Stevens 1972.)
Figure 5.12e Dog (Canis familiaris) digestive tract (Stevens & Hume 1995)
Figure 5.16e Pig (Sus scrofa) digestive tract (Stevens & Hume 1995)
Figure 5.18c European rabbit (Oryctolagus cuniculus) digestive tract (Stevens & Hume 1995)
Strategies for digesta retention:
Therefore, the major sites for the prolonged retention of fluid or particulate digesta in the digestive tract of vertebrates are the foregut, midgut, cecum, or colon. The mechanisms or strategies for digesta retention have been examined most extensively in the herbivores, where they play a major role in the retention and microbial fermentation of plant material.
Strategies for digesta retention - midgut fermenters:
The midgut is the principal site of digesta retention and microbial fermentation in herbivorous fish (Fig. 5.2), larval amphibians, Florida red-bellied turtles, emus, and pandas. Substantial concentrations of SCFA were reported in the midgut of many herbivorous fish (Clements and Choat 1995) and high concentrations were found in the midgut of the Florida red-bellied turtle (Bjorndal and Bolten 1990) and emu (Herd and Dawson 1984). Although the contribution of SCFA to the maintenance energy of fish is unknown, their rate of production in the midgut of the red-bellied turtle indicated that they could provide 100% of the maintenance energy requirements. However, SCFA provided only 11% of the maintenance energy of emus (Herd and Dawson 1984), and a brief digesta retention time and low degree of cellulose digestibility suggests that microbial fermentation also plays a minor role in the production of nutrients in the giant panda (Dierenfeld et al 1982). Therefore, the effective use of the midgut as the principal site of digesta retention and microbial fermentation appears to be limited to herbivorous ectotherms that feed on more readily fermentable aquatic plants.
Figure 5.2. Digestive strategies of herbivorous marine fish. Surgeonfish and parrotfish are browsers. Mullet and sea bass are grazers. Shaded areas indicate the gizzard-like stomach of the mullet, pyloric ceca of surgeonfish and sea bass, and two regions of sphincters in distal intestine the sea bass (Modified from Horn 1989.)
Strategies for digesta retention - colon fermenters:
The colon is the major site of digesta retention and microbial fermentation in most reptilian herbivores, and the ostrich, wombats, herbivorous apes, perissodactyls, and elephants (Fig. 7.2). The mean retention times for fluid digesta markers and the ratio of the particle/fluid retention times for a number of colon fermenters are given in Table 7.4. Colon fermenters retain digesta particles as long or longer than fluid and their retention time increases with particle size. The prolonged retention of hindgut digesta is accomplished in part by the antiperistaltic waves of muscular contraction, that are generated by a pacemaker located in the cloacal region of some reptiles, most birds, and at least some marsupials, and at the termination of the proximal colon of eutherian mammals.
Digesta retention is further aided by projections of the mucosa into the hindgut lumen of herbivorous lizards or by sacculations (haustra) formed by contractions of circular and longitudinal bands of muscle in the hindgut of mammals (Fig. 7.2). The proximal colon is greatly expanded in elephants and perissodactyls. It is further divided into two compartments in the perissodactyls, each with its own pacemaker (Sellers et al. 1982). Therefore, perissodactyls appear to represent the most complex example of this digestive strategy. Although the gut capacity of herbivores is related to body weight, there was no relationship between the body weight and retention time. This can be attributed to differences in the metabolic rate, body temperature, diet, or structural and functional characteristic of the hindgut.
Figure 7.2 Gastrointestinal tracts of reptilian, avian, and mammalian colon fermenters. The principal site(s) of microbial fermentation in these gut drawings are denoted by darker lines. Tortoise, ostrich, and pony from Stevens & Hume 1995; wombat from Harrop & Hume 1980; rhino and elephant from Clemens & Maloiy 1982.
Table 7.4. Mean digesta retention time for herbivorous colon fermenters
Although digesta retention times are affected by differences in the diet, and in the body temperatures of the reptiles, marsupial, and eutherian mammals, colon fermenters retain particulate digesta as long or longer than fluid digesta. The effects of colonic retention of particles can be muted in animals with a relatively large cecum such as the chimpanzee, orangutan and gorilla. (modified from Stevens & Hume 1995)
Strategies for digesta retention - cecum fermenters:
The cecum is the principal site of digesta retention and microbial fermentation in most small avian and mammalian herbivores (Fig. 7.3). Cecum fermenters overcome the limitations of a high mass-specific metabolic weight on gut capacity and digesta retention time by rapid excretion of large digesta particles and selective retention of fluid, bacteria, and very small particles of digesta in the cecum (Table 7.5). Cecal retention of fluid and small particles is accomplished by a colonic separation mechanism (CSM). The degree of selectivity varies from an extremely complex CSM that returns mucus and bacteria to the cecum of lemmings and voles, to less selective mechanisms in rabbits, koalas, greater gliders and ringtail possums, and the least selective CSM of cavomorph rodents (Björnhag 1994). The longer digesta retention time of marsupials in contrast to the eutherian mammals and ptarmigan can be attributed largely to their lower body temperature.
Figure 7.3 Gastrointestinal tracts of avian and mammalian cecum fermenters. The principal site(s) of microbial fermentation in these gut drawings are denoted by darker lines. Grouse, rhea, guinea pig, and greater glider from Stevens & Hume 1995; rabbit from Stevens 1977; koala from Harrop & Hume 1980.
Table 7.5. Mean digesta retention time for herbivorous cecum fermenters
Although digesta retention times are affected by differences in the diet, and in the body temperatures of the bird, marsupials, and eutherian mammals, cecum fermenters retain fluid digesta as long or longer than particulate digesta. Fluid and small digesta particles are selectively retained by the cecum of small mammals with a large cecum, especially in herbivores with a well-developed colonic separation mechanism. The longer digesta retention times of the marsupials are due, partly, to their lower rate of metabolism. (modified from Stevens & Hume 1995)
The digesta retention time of most cecum fermenting herbivores is further prolonged by coprophagy (ingestion of feces), which gives the upper digestive tract access to the protein and B-vitamins synthesized by hindgut bacteria. Although difficult to detect without close and continuous observation, coprophagy has been witnessed in lagomorphs, rodents (guinea pigs, chinchilla, voles, lemmings, capybara, and nutria), ringtail possums, and a folivorous lemur (Lepilemur mustelinus leucopus). The nutritional value of coprophagy is improved in many of these species by cecotrophy; the selective ingestion of highly nutritious feces that are derived from a periodic release of cecal contents (Hörnicke and Björnhag 1980; Björnhag 1987; 1994). A fecal discharge of over 50% of the cecal contents at 8.6 hour intervals suggests that the Alaskan rock ptarmigan also may be cecotrophic (Gasaway et al. 1975). Cecotrophs contain high levels of SCFA, microbial protein, B vitamins, Na+, K+, and water. Their B-vitamin and nitrogen content can exceed that of the diet and normal feces, and much of the nitrogen is in the form of high-quality microbial protein.
Strategies for digesta retention - foregut fermenters:
The foregut is the principal site of digesta retention and microbial fermentation in the hoatzin, and some small and most intermediate-sized mammalian herbivores (Fig. 7.4). The crop and distal esophagus are the main sites in the foregut of hoatzins. Weight limitations of a fermentation chamber on their ability to fly and its inefficient location cranial to the trituration organ (gizzard) could account for the rarity of avian foregut fermenters. Digesta retention is aided by permanent compartmentalization of the sloth, hippopotamus, camelid, and ruminant forestomachs, and by haustra-like sacculations in the forestomach of colobid monkeys and tubular segment of the kangaroo and wallaby forestomach. Like the coprophagy of cecum fermenters, foregut fermentation allows the recovery of the microbial protein and B-vitamins.
Figure 7.4 Gastrointestinal tracts of avian and mammalian foregut fermenters. The principal site(s) of microbial fermentation in these gut drawings are denoted by darker lines. Hoatzin from Grajal & Parra 1995; sloth from Stevens 1980; colobus from Stevens 1983; kangaroo from Stevens 1977; sheep from Stevens & Hume 1995.
The MRT for fluid and particulate digesta in an hoatzin, sloth, rat kangaroo, colobus monkey, eastern gray kangaroo, sheep, llama, and ox are listed in Table 7.6. Like colon fermenters, foregut fermenters retain particles as long or longer than fluid and the retention time increases with particle size. The prolonged digesta retention time of sloths can be attributed partly to storage in the rectum and infrequent defecation. However, it is also the result of large fluctuations in the body temperature with changes in ambient temperature (Britton 1941) and a voluminous highly compartmentalized forestomach. Despite a lower metabolic rate and body temperature, the digesta retention time of the eastern gray kangaroo was less than that of the sheep, llama, and ox, suggesting that its haustrated forestomach is less retentive than the compartmentalized forestomach of the sloths, hippos, camelids and ruminants (Fig. 5.9).
Table 7.6. Mean digesta retention time for herbivorous forestomach fermenters
Although digesta retention times are affected by differences in the diet, and in the body temperatures of the bird, sloth and other eutherian mammals, foregut fermenters retain particulate digesta as long or longer than fluid digesta. Most small forestomach fermenters retain fluid and particles for equal lengths of time, but particles are selectively retained by the forestomach of large species and this tends to increase with an increase in dietary fiber. (modified from Stevens & Hume 1995)
Figure 5.9. Examples of mammals with an expanded forestomach. E designates esophageal entrance, P designates pylorus, 1 designates omasum, and 2 designates abomasum. (Modified from Stevens & Hume 1995.)
The forestomach of asdvanced ruminants has received the most extensive study and is often used as the standard for foregut fermenters. Some authors categorize all herbivores as simply ruminants and hindgut fermenters. However, as mentioned in the previous section, the advanced ruminants (pecora) have the unique combination of cyclic contractions of the forestomach, rumination, and an omasal filtration system (Figs. 6.4, 6.6, and 6.7). Rumination increases the efficiency of mastication and reduces the digesta retention time (Pearce and Moir 1964). The omasum prevents the exodus of plant material from the reticulorumen until it is reduced to a small enough particle size. The omasum is only a rudimentary organ in the African genus of tragulids, Hyemoshu, and absent in the Asian genus of Tragulus (Moir 1968), camelids, and and all other artiodactyls.
Figure 6.4 A six-minute recording of reticuloruminal cycles and associated events in the esophagus and omasum. Note the relationship between the contractions of the rumen and omasal canal, and the prolonged, acyclic contractions of the omasal body pressure during primary contraction of the dorsal rumen and omasal canal. Upper traces show eructation as a biphasic wave occurring during secondary rumen contractions and the frequent waves of deglutition associated with the swallowing of saliva. (From Sellers & Stevens 1966.)
Figure 6.6 Movement of digesta through the bovine omasum. Closed arrows show movement of digesta and open arrows show movement of forestomach walls. Diagrammatic axial section (see Fig. 5.3) shows the cranial reticulum (1), reticulo-omasal orifice (2), omasal leaf portion of omasal body (3), omasal canal (4) and cranial abomasum (5). A: All structures are relaxed during much of the cyclic contraction of the forestomach. B: During the second reticular contraction, the reticulo-omasal orifice and omasal canal are pulled ventrally, producing a negative pressure in the canal and a closing and then opening of the orifice, which results in aspiration of digesta from the base of the reticulum. C: Primary contraction of the rumen is associated with a primary contraction of the reticulo-omasal orifice and omasal canal, forcing fluid and small digesta particles between the leaves of the omasal body and into the abomasum. These events are followed by relaxation of these structures (D), and repeated if the forestomach undergoes a secondary contraction. E: At intervals that vary and are unrelated to the cyclic contractions of the forestomach, a wave of contraction passes over the omasal body, releasing its contents into the abomasum. (From Stevens & Hume 1995.)
Figure 6.7 Reticuloruminal cycles during rumination in cattle. Numbers 1 and 2 mark first and second reticular contractions seen with every cycle and the x marks the extra reticular cycle at the regurgitation stage (R) of rumination. The remasticated bolus is swallowed (D) just prior to the next reticulorumen cycle. The AP on the reticular tracing is a registration of abdominal press at the time of eructation (E). (From Stevens & Sellers 1968.)
Strategies for digesta retention - combinations of strategies:
Some mammals use a combination of digestive strategies. A partially compartmentalized stomach serves as a secondary site for microbial fermentation in some rodents, such as hamsters and voles, and the hyracoids and sirenians (Fig. 7.5). The gastrointestinal tract of hyracoids, has the unique combination of a forestomach, cecum and pair of colonic appendages that serve as sites for microbial fermentation. The cecum and colonic appendages are the major sites of microbial fermentation (Rubsamen et al. 1982; Eloff and van Hoven 1985). Their small body mass ( 2.5 to 3.5 kg) would predict the strategy of cecum fermentation. However, hyracoids do not appear to be coprophagic (Bjornhag 1994), and MRTs for fluid and particles of the rock hyrax on an alfalfa diet were approximately 28 and 50 hours, respectively (Rubsamen et al. 1982; Bjornhag et al 1994). Their large gut capacity and long digesta retention time can be attributed to a BMR 40% less than that of the average eutherian mammal and a body temperature that ranged between 32 and 35 oC (Rubsamen and Kettembeil 1980).
Although dugongs and manatees have a partially compartmentalized stomach and a pair of duodenal appendages (Fig. 7.5), their long colon serves as the principal site for microbial fermentation (Murray et al. 1977). The relative importance of the forestomach and cecum fermentation also varies among ruminants. Concentrate selectors such as the dik-dik have a smaller forestomach and larger cecum than bulk roughage feeders such as sheep (Fig. 5.19). The Arctic muskoxen have both a large forestomach, which serves as the principal site of microbial fermentation during winter months (Adamczewski et al. 1994), and a large cecum that serves as the principal site during the summer (Staaland and Thing 1991).
Figure 7.5 Gastrointestinal tracts of herbivores with a combination of digestive strategies. The principal site(s) of microbial fermentation in these gut drawings are denoted by darker lines. Hyrax from Clemens 1977; hamster, dugong, and dik-dik from Stevens & Hume 1995.
Figure 5.19d Sheep (Ovis aries) digestive tract (Stevens & Hume 1995)
Models of digestive strategies:
Penry and Jumars (1987) used the principles of chemical reactor theory to formulate three models to describe the constraints on optimal digestion. They consisted of plug-flow reactors, batch reactors, and continuous-flow, stirred-tank reactors (Fig 7.6). Plug-flow reactors mimic the midgut fermenters and batch reactors resemble the cecum of cecotrophic cecum fermenters. The continuous-flow, stirred-tank reactors (CSTR) resemble the forestomach of ruminants, camelids, and sloths, cranial segment of the macropod marsupial stomach, and cecum of most birds and mammals. Dello et al. (1983) suggested that the haustrated segments of the macropod marsupial and collobid monkey forestomach, and colon of mammalian herbivores are best described by a fourth model that consists of plug-flow reactors modified by a series of CSTRs with considerable radial and axial mixing. The optimal configuration of CSTR and plug-flow reactors has been examined in ruminants (Illius and Gordon 1992; Spalinger and Robbins 1992), other mammalian herbivores (Hume 1989; Justice and Smith 1992) and herbivorous fish (Horn and Messer 1992). Alexander (1991) assessed the relative advantages of a foregut and hindgut CSTRs as a function of the level of intake and fiber content of the diet.
Figure 7.6. Chemical reactor models homologous to fermentation in the digestive tract of vertebrates. They consist of a batch reactor (A), plug flow reactor (B), continuous-flow, stirred-tank reactor (C), and a modified plug flow reactor (D), with pulsed inputs (PI) and outputs ((PO), or continuous inputs (CI) and outputs (CO). (From Stevens & Hume 1995.)
Effect of diet on the digesta retention time:
An elevation in the percentage of fiber in the diet reduces the retention time of fluid and particles by midgut, colon, and cecum fermenters. This appears to be due to the physical or bulk effect of the plant fiber, because the retention time is relatively unaffected by the degree of fiber digestibility and increased by the grinding and pelleting of high fiber diets. The reduction in retention time on high fiber diets is accompanied by an increase in food intake, which allows the processing of larger quantities of forage for the recovery of soluble nutrients from the midgut prior to their less efficient microbial fermentation. However, an increase in dietary fiber increases the digesta retention time of foregut fermenters, which results in the more complete digestion of plant fiber but a reduction in food intake.
The different response of foregut and colon fermenters to changes in the percentage of fiber in their diet was illustrated by a studied of captive (zoo) animals conducted by Foose (1982). The digestibility for plant cell walls by foregut fermenters (ruminants, camels, and hippos) and colon fermenters (tapirs, zebra, asses, rhinos, and elephants) on diets of alfalfa or grass hay increased with retention time. This was most pronounced on the more fibrous grass hay diet (Fig. 7.7). However, ruminants and camels demonstrated longer digesta retention times than the colon fermenters and a greater efficiency in cell wall digestion. The greater digestive efficiency of ruminants and camels was attributed to the masticatory advantages of rumination. Hippos digested cell walls as efficiently as the ruminants and camelids on the more readily digestible alfalfa diet. However, on the grass hay diet, their retention time was much longer than that of the ruminants and camelids, and their digestive efficiency was reduced to that of the colon fermenters. The longer retention time of hippos could be due to a lower core body temperature of 35.4 +/- 0.7 oC (Wright 1987), and their lower digestive efficiency was attributed to the absence of rumination.
Conversion from alfalfa hay to the more fibrous grass hay reduced the rate of food intake by ruminants, camels, and hippos, but increased the intake of the colon fermenters. Therefore, despite their lower digestive efficiency, the equids, elephants, and rhinos satisfied their metabolic requirements as well as most bovids, and better than the giraffes or hippos. Although the retention time tended to increase with body weight, the retention time of camels was longer than that of ruminants of higher body weights and the retention time of rhinos was longer than that of elephants. This may be due to differences in body temperature. The body temperature of camels can undergo daily variations of up to 5 oC (Schmidt Nielsen et al. 1967) and, although the mean body temperature of elephants (Benedict 1936) and white rhinos (Allbrook et al. 1958) were similar, the body temperature of the rhinos ranged from 33.6 to 37.5 oC. The longer digesta retention time of rhinos also may be due to the unique structural and functional characteristics of the perissodactyl proximal colon.
Figure 7.7. Relationship between cell wall digestibility and mean retention time (MRT) of fiber by foregut and colon fermenters on a grass hay diet. Red circles represent foregut fermenting ruminants and camels; a) barasingha, b) eland, c) nilgae, d) wapiti, e) water buck, f) gaur, g) giraffe, h) gemsbok, i) African buffalo, j) American bison, k) dromedary camel, and l) bactrian camel. Blue circles represent colon fermenting a) Grevy’s zebra, b) mountain zebra, c) plains zebra, d) Asian tapir, e) American tapir, f) Asian wild ass, g) African elephant, h) Asian elephant, i) black rhino, j) Indian rhino, and k) white rhino. R2 = 0.66 for the ruminants and camels and 0.26 for colon fermenters. Yellow triangles represent; (1) red kangaroos on an alfalfa diet, river hippos on an (2) alfalfa hay or (3) grass diet, and (4) sloths on a diet of Ceropia palmata foliage. Data for ruminants, camels, hippos, and colon fermenters are from Foose (1982). Data on red kangaroos are from Hume (1999) and data on the three-toed sloth are from Foley et al. (1995) and Foley (personal communication.)
The effect of fiber digestibility on digesta retention time also varies with the digestive strategy. Both the black Bedouin goats and donkeys (Equus asinus asinus) of Mideastern desert tribesmen maintained their body weight after conversion from a diet of alfalfa hay to a much less readily digestible diet of wheat straw (Izraely et al 1989 a,b; Brosh et al. 1986). This was aided by a reduction in the metabolic rate of both species. However, the goats also increased their digesta retention time on the wheat straw diet, while the digesta retention time of the donkeys remained constant. When converted from alfalfa hay to a poorly digestible diet of Panicum grass, the Levantine vole (Microtus quentheri) was unable to increase its digesta retention time or maintain its body weight. However, the Fat jird (Merionus crassus), a cavomorph desert rodent with a much less efficient CSM, maintained its body weight by doubling its cecal retention time of plant fiber (Chosniak and Yahov 1987).
Therefore, ruminants can survive on poorly digestible, high fiber forage by increasing their digestion retention time at the expense of a lower rate of food intake. Sloths also satisfied their metabolic requirements on poorly digestible Cecropia palmata foliage with an extremely long digesta retention time (Fig. 7.7), because of a metabolic rate much lower than that of most eutherian mammals (Nagy and Montgomery 1980) and a body temperature that ranged between 32 and 35 oC (Foley et al. 1995). The low cell wall digestibility of red kangaroos (Macropus rufus) on a diet alfalfa hay (Fig. 7.7) can be similarly attributed to the lower metabolic rate and body temperature of marsupials. However, their digesta retention time was less than that of ruminants of equivalent body size, and the food intake of kangaroos and wallabies was less affected by either an elevation in the percentage of dietary fiber or a decrease in fiber digestibility (Foot and Romberg 1965; Hume 1999). Therefore, the haustrated forestomach of these animals appears to set less stringent limits on digesta retention time and food intake.
Cork et al. (1999) reviewed the variations within each of these digestive strategies and the many factors that must be considered in the development of mechanistic models for their study. They point out that the studies of hindgut fermenters have concentrated on the refractory polysaccharides (cellulose, hemicellulose, and lignin) in the diet with less attention to the protein, and other carbohydrates, such as pectin or the non-starch storage carbohydrates in roots, rhizomes, stolons, corms, bulbs, and tubers consumed by rat kangaroos and burrowing animals. Yet the ability of cecum fermenters to adapt to diets with different levels of protein, fermentable solutes, and refractory polysaccharides varies with the type or degree of colonic separation. They concluded that cecum fermenters with a colonic separation mechanism can adapt to higher levels of refractory polysaccharides and lower levels of dietary protein, and those that are cecotrophic can adapt to the lowest levels of dietary protein (Fig. 7.8). However, none of the cecum fermenters could compete with large ruminants or colon fermenters on diets that contained high levels of refractory polysaccharides.
Figure 7.8. Variations in digestive strategy with respect to dietary combinations of refractory carbohydrates (cellulose, hemicellulose, and lignin), and protein (A) or fermentable solutes (B). The size and shape of the boxes represent the range of diets within which each digestive strategy is postulated to be effective. (From Cork et al. 1999.)
Relationships between digestive strategies and body mass:
Figure 7.9 shows the relationship between digestive strategies and body mass. Herbivorous colon fermenters include 0.1 to 250-kg reptiles, the largest bird (ostrich), and mammals that range from 30-kg wombats to 10,000-kg elephants. Their minimum body weight can be attributed to the limitations of a high mass-specific rate of metabolism on gut capacity and retention time. The limitations on the maximum weight of herbivorous reptiles have been attributed to the advantages of large surface area for temperature equilibration. However, the fact that the largest herbivores are 250-kg tortoises (Mlynarski and Wermuth 1975) and 13-kg arboreal lizards (Kastle 1975) suggests that their maximum size also may have been limited by mammalian predation. The body weight of cecum fermenters range from the 6-g voles to 49-kg capybara. Their maximum body weight is reduced to about 25 kg by removal of species that feed on less fibrous aquatic diets. Their minimal body weight appears to be determined by the efficiency of the colon separation mechanism and their maximum weight may be limited by a decrease in its efficiency with an increase in colon diameter.
The body mass of foregut fermenters ranges from the 750-g hoatzin to 3500-kg hippos, but it is also reduced to about 1900 kg (giraffes) by removal of the amphibious hippos, which feed on a less fibrous diet (Fig. 7.9). Demment and Van Soest (1985) reviewed the relationship between body weight and gut capacity in East African ruminants. They noted that the smallest ruminants compensate for a limited gut capacity by supplementing their diet with seeds or fruit. However, an increase in total metabolic requirements with body size required adaptation to more plentiful, high-fiber diets. Although rumination reduces their digesta retention time, it was limited to a maximum time of 10 hours in sheep and cattle on high fiber diets. In vitro studies of rumen bacteria showed that the optimal retention for cell wall digestibility would range from 30 to 45 hours, regardless of the diet or location of the fermentation chamber (Smith et al. 1972). Therefore, Demment and Van Soest concluded that the maximum body size of bulk-feeding, grazing ruminants was limited to about 1200 kg by the restrictions of digesta retention time on food intake (Fig. 7.10).
Figure 7.9. Relationships between digestive strategies and the body mass of reptilian, avian and mammalian herbivores. Dark, shaded areas include cecum and forestomach fermenters that feed on less fibrous aquatic plants (From Stevens 1998)
Figure 7.10. Relationship between digestive retention time and the body mass of grazing ruminants. Retention time is plotted against body mass for forages of different degrees of digestibility. Shaded area indicates the retention time necessary for digestion of most of the energy by rumen bacteria. A 120 kg animal at a body temperature of 38 'C would achieve maximum efficiency of microbial fermentation for forage of 50% digestibility within 45 hours, regardless of the site or mechanism of digesta retention. (From Demment & Van Soest 1985.)
Relative advantages of digestive strategies:
The restrictions of digesta retention time on the body size of ruminants are often assumed to apply to all foregut fermenting herbivores. However, the hippos greatly exceed the body weight of ruminants by means of a lower body temperature and access to more readily fermentable forage, and kangaroos and wallabies process high-fiber and poorly digestible forage more rapidly than ruminants and with less of a reduction in forage intake. Modern-day sloths also subsist on a poorly digestible diet because of low metabolic requirements, a low body temperature, and large gut capacity, and the giant ground sloth (Megatherium) of the Tertiary Period is said to have reached weights of 3400 kg (Owen-Smith 1988). Therefore, the digesta retention time appears to have a less limiting effect on the body mass of foregut fermenters with a haustrated forestomach or a low body temperature and metabolic rate.
The relative advantages of midgut, colon, cecum, and foregut fermentation are summarized in Table 7.7. The efficiency of midgut fermentation is limited by a brief digesta retention time and the competition between and mutual destruction of gut bacteria and endogenous digestive enzymes (Mackie and Wilkins 1988: Clements 1991). Although this is an effective strategy in ectotherms that feed on aquatic plants with a low cellulose and lignin content, most reptiles, mammals and birds are colon, cecum, or foregut fermenters. Colon and cecum fermenters can utilize the soluble nutrients in the diet and, with the exception of some cecum fermenters, increase their rates of digesta passage, food intake, and and recovery of soluble nutrients on high-fiber diets. Coprophagic cecum fermenters can also utilize the protein and B vitamins synthesized by gut bacteria, and some cecum fermenters can adapt to poorly fermentable diets by an increase in fiber retention time.
Foregut fermenters sacrifice the advantage of recovering soluble nutrients prior to their microbial digestion and increasing their rate of food intake on high fiber diets. However, they can utilize the protein and B-vitamins synthesized by the indigenous bacteria, and the bacteria can remove or reduce the toxicity of plant defense compounds (McSweeney and Mackie 1997). Foregut fermenters can also adapt more readily to arid conditions (Table 7.7). Microbial fermentation requires the secretion of large amounts of fluid into the digestive tract. The daily volume of salivary, pancreatic, biliary and intestinal fluids secreted into the digestive tract of sheep and ponies is equivalent to over twice their extracellular fluid volume (see Section 13). Ninety-eight percent of this fluid was reabsorbed from the digestive tract of each of these species. Most of these fluids were reabsorbed by the forestomach and small intestine of sheep. However, the large intestine had to serve as the major site for both microbial fermentation and fluid absorption in the pony. The forestomach can also store water for slow release during periods of dehydration. Dehydrated cattle can replace an 18% loss in their body weight in one drinking period (Silanikove 1989). Black Bedouin goats can graze for several days without access to water, by increasing their forestomach retention time, and replace 40% of their body weight by doubling their reticuloruminal volume during one drinking period (Shkolnik et al. 1980).
Table 7.7. Characteristics of digestive strategies
Plus symbols represent the presence of a characteristic. Arrows represent an increase or decrease in retention time. Minus symbols represent either the absence of a characteristic or no change in the retention time. (modified from Stevens & Hume 1995)
The relative advantages of these digestive strategies are reflected by the distribution of colon, cecum, and foregut fermenters into the harsher regions of the world (Table 7.8). Deserts are inhabited by herbivorous colon fermenters (lizards, tortoises, and ostriches), cecum fermenters (lagomorphs and rodents) and foregut fermenters (camels and a number of advanced ruminants). However, cecum and foregut fermenters have also adapted to altitudes of over 3000 m (partridge, rodents, lagomorphs, New World camelids, mountain sheep and goats, and the langur monkey Presbytis entellus schistceus), and the arctic (ptarmigan, lemmings, arctic hares, moose, elk, reindeer, and muskoxen). Therefore, adoption of the cecum or forestomach as the principal site of microbial fermentation allowed both the expansion of herbivory into smaller species of birds and mammals and the adaptation of herbivores to regions where forage and/or water are sparse.
Table 7.8. Adaptations of digestive strategies to environment
(Stevens 1998)
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