Mammalian strategies for utilizing high fibre diets.

Abstract

8 3 MAMMALIAN STRATEGIES FOR UTILIZING HIGH FIBRE DIETS . I.D. HUME* SUMMARY A number of different strategies have evolved,among mammals for utilizing fibrous diets. The Ruminantia are best equipped for fibre digestion, but on very' high fibre diets their nutrient intake is severely limited by a slow rate of.passage of food residues out of the reticula- ' rumen. Foregut fermenters such as the macropod marsupials and hindgut fermenters do not. suffer from this limitation on very high fibre diets, . but fibre digestion is 1es.s complete. The relative advantages and disadvantages of these'alternative strategies are discussed in relation . to feeds of different fibre concentrations. INTRODUCTION . The Fifth International Symposium on Ruminant Physiologv held in France in 1979 contained a section on comparative ,digestive physiology .of herbivores. This was a new development ;.and reflectsthe recent increase in interest incomparative studies of digestive physiology in several centres around the world, including the University of New '. England. Many of these studies have been. concerned with alternative strategies found among mammals in their ,utilization of poor quality, high fibre roughage diets. Ruminants . There is no doubt that among the various groups of mamals the' This is basically Ruminantia 'are best equipped far fibre .digestion. because of a physiological mechanism at the reticulo-omasal orifice which has been shown to selectively retain within the reticulorumen the larger food particles (Stevenset al. 1960). This mechanism has only ' been demonstrated in the domestic.ruminants,'but similar anatomy suggests its presence in at least some. of .the other bovids (i.e. sheep, cattle, goat,' gazelle) and probably the cervids (deer), giraffids (giraffe, okapi) and antilocaprids (oronghorn antelope). The .came'lids (camel, llama) have -an. apparently analogous constriction between the second and third'compartments of the stomach (Vallenas et al. 1971), but it is not known whether an analogous function exists. No. similar structure or function is known in any other foregut fermenter, passage from the fermentative to the acidic part of the stomach being- little if at all impeded.. *. Department of Biochemistry and Nutrition, University of New England, . *Armidale, N.S.W. 2351 84 The mechanism whereby the larger feed particles are selectively retained in the, reticulorumen has several important consequences'for I ruminants. First; there is efficient separation of the fermentative from the acid-secreting region of the stomach. This has allowed develcpment of the, most obvious special feature of the ruminants, rumination, whereby forestomach digesta are regurgitated, rechewed and reswallowed in a frequent, regular pattern.. .This pattern may be.repeated,some 5'30. . times a day, occupying a total of more than 8 hours, and involving more than 25,000 chews (Gordon 1968). Rumination occurs in all the Ruminantia and the Camelidae. While it is claimed that some other herbivores ruminate (Hendricks 1965), this is incorrect. The second consequence of importance is that retention times of coarse feed particles in the reticulorumen can be quite long, with mean residence times exceeding 60 hours. This, in combination with the mechanical breakdown achieved by rumination, results in the efficient - digestion of fibre which+ characteristic of the ruminants. However, a further consequence of this mechanism at the reticula-omasal orifice is that on the most highly fibrous feeds retention is so long that undigested material accumulates in the. rumenand food intake and therefore nutrient supply is reduced,. The relationship between food intake ' by ruminantsand increasing content of cell-wall constituents, one 'measure of fibre, isshown in Fig. 1. . FIGURE 1' Relationship between dry matter intake by ruminants and ,' * fibre content of forages measured as cell-wall' constituents. From: Van Soest (1965). . Hume and Warner (1980) consider that maximal efficiency of fibre digestion by this strategy' would be adaptively important only if the as quantity of food was limiting, .and that food poorly digested. T h i s suggests that the special features of ruminant digestion evolved in regions where.`both quality and quantity,of forage were either . irregularly or seasonally Jimiting, such as in hot deserts, cold deserts (tundra) or deciduous forests. Relatively few modern ruminants live in the mrt of environment for which their special-: ruminant .adaptations evolved,` due either to migration or to .a change of climate. These.adaptations are of no great disadvantage except at very high fibre .. concentrations in. the food (Janis 1976); the ruminant is still a very 85 efficient foregut fermenter with all its advantages. It qeems likely that the camelids, with their similar digestive physiology, evolved in a similar way, though all the modem wild representatives remainin. arid environments similar to those postulated for the origin of their special adaptive features. Hindgut fermenters Compared with ruminants, fibre digestion is less efficient in all However, among the hindgutfermenters the hindgut f ermenterk,studied. there are significant differences'in ,efficiency of fibre digestion. There is much .less information available on fibre digestion in the caecum and colon than in the reticulorumen,, but it appears that, among the hindgut fermenters, at least two alternative strategies have. evolved. Hume and Warner (1980) refer to these as 'colon fermentation' and 'caecum fermentation'. Colon fermentation In colon fermenters the primary expansion of the .hindgut is in -. the proximal colon; expansion of the caecum is also usual, but a few exceptions exist, such as the wombat and the giant panda, which rely entirely on a colonic fermentation to utilize fibre. The caecum, if . developed, appears to .function simply as an extension of the proximal colon as the site of fermentation, with,the ,contents of the two organs mixing together with little, if any, separation of fluid and particles. In the horse, particulate digesta pass through the digestive tract a 'little moreslowly than fluid (Argenzio et al. 1974), but this appears to be a simple mechanical functionof the haustrations of the hindgut, without any special mechanism for separation as found in caecum *fermenters or in the ruminant forestimach. The overall faster rate of passage of digesta through the horse is the main reason for the lower efficiency of fibre digestion in this and other colon fermenters. All large (over about 30 kg) hindgut fermenters appear to be colon fermenters. This is probably due .in part to the increased ability of a larger animal to tolerate a poorer quality diet because it needs less energy andless protein per unit of body weight, in part because' digesta can be retained in the gut of larger animals for longer periods, allowing more-extensive'fermentation (Parra 1978). Thus amonghindgutfermenters . the horse and other colon fermenters are generdlly more efficient fibre digesters than the smaller ,caecum fermenters -(Table 'l)- 8 6 TABLE 1 Crude fibre digestion in two types of hindgut fermenters, large 'colon fermenters' and a small *caecum fermenter' The other important advantage of the colon fermentation strategy, at least in the Equidae (horses, zebra), is the ability to increase greatly their dry matter intake as the fibre content of the food. at increases,, the expense of efficiency of digestion (Janis 1976), SO that they occupy a niche at the extreme end of the range of food fibre content, though it is uncertain what proportion of their energv comes L from fibre as distinct from cell contents. Thus zebra have been sh&n to Select plant species'and plant parts of'higher fibre'content than ruminants (wildebeest) grazing the same low quality herbage, despite the,presumed lower digestibility ofthe more fibrous mater,ial (Bell 1969, Owaga 1975,). This tvpe of hindgut fermentation seems to be the most primitive. It is also found as a secondary fermentation in the hindsut of . ruminants, macropods, and probably other foregut fermenters. Caecum fermentation The best known caecum fermenter is the rabbit. In this strategy the enlarged caecum is used in a different wav, not as a simple -a extension .of the proximal colon, *but as a fermentation chamber specifically for the solutes and small digesta particles, rather than the coarse, high fibre, high lignin particles. These latter, the less digestible components o.f the diet, pass rapidly through the hindgut,,. while the potentially more digestible components are .retained for fermentation (Bjornhag 1972; Pickard and Stevens 1972). This is a e ' means of* utilizing fibrous diets without the encumbrance of an overlarge gut; and is more important for small animals than for large because.of the effect of body size on nutrient requirements. It'is therefore no surprise that all animals known to have adopted this strategy are relatively.smal-1, the largest being perhaps the koala (about 10 kg), although the capybara and other large rodents' (up to 50 kg) may also be ofthis type. : L 87 : A few animals have adopted caecum fermentation in its simple form. For example, the koala retains, presumably in the extremely'long caecum; the fluid part of the digesta with overall retention times of 8-9 days, compared with 5-6 days for particles (Cork et al. 1977). However, many other caecum fermenters combine selective retention of fluid and small particles with coprophagy (eating of faeces) in some form. This allows easier assimilation of microbially synthesised vitamins and also makes microbial,protein available for digestion by the host animal. Thus, amonghindgut fermenters, colon fermentation allows retention of a large .mass of digesta, with retention of particles for a longer time than fluid digesta, SO that fibre digestion is maximal, although generally less than in ruminants because of shorter overall retention times. The smaller caecum fermenters, however, avoid the coarse ,fibrous portion of the.food by passing itthroughthe gut more rapidly, and concentrate instead on the more digestible solutes and fine particles.. Consequently fibre digestion isoftenpoor (Table 1). . . . ~~~acropods We have recently completed a comprehensive study of digestive ' function and digest& flow through the gut of kangaroos and wallabies (i.e. members ofthe ,subfamily *?acropodinae within the marsupial family t Eacropodidae). The macropodines are foregut fermenters as are ruminants, but their stomach differs from the ruminant stomach in that it is esgentially tubular, rather'than saccular, and in many resp.ects resembles in structure the proximal colon (Fig. 2). There is no obvious. anatomical constriction or physioldgical mechanism to selectively. retain coarse feed particles as in the ruminant. The differentialflow of .particles and fluid is the result of the tubular flow of digesta along the stomach, assisted by'contractions of the haustra of the gastric wall: this results in the caudal extrusion of liquid through the particulate digesta (Dellow 1979). The anatomical arrangement of the macropodine stomach (Fig. 2) results in several important differsnces in digestion from ruminants. 88 First, overall retention'times of both fluid and particulate diq'esta . . are shorter than in the ruminant. Consequently fibre digestion is generally less efficient (Table 2), although .one exception to this has . been found in the euro, Macropus robustus (Hume 1974). Second, macropods do not ruminate, perhaps as a~ consequence of the lack of a well-defined sphincte,r separating the fermentative and acidic regions of the stomach. They do regurgitate, but the act is much more irregular and .infrequent than in rumination, and involves much less chewing; Barker et al. (1963) recommend that this process be termed 'merycism'. Instead of. ruminating, macropodines chew their food more finely initially, and consequently eat more slowly than .do ruminants.. . TABLE 2 Fibre digesti0n.i.n two types of foregut fetienters, the ruminant and the macropod Finally, as in maintain its intake thereby maintaining than would otherwise efficiency. the horse/ the kangaroo appears to be able to '. on highly fibrous diets'betterthan can ruminants, its digestible nutrient supply at a higher level be possible, at the expense of high unit digestive' Thi's conclusion is based on limited data: The often reported finding ,that mature kangaroos . eat no more of high fibre diets than do., sheep does not destroy the argument. This is because the.maintenance energy requirement of macropodines is at least 20% below that of sheep . . (Hume ,1974). Only if the total energy requirement of the macropodine was greater than that of the ruminant would a higher .digestible,energy intake, be expected. Only one experiment hasbeen reported'which compares intake of a high fibre diet between mature ruminants and growing 'kangaroos, when the,total energy ,requirement of the, kangaroos the may .be'expected to be substantially higher than maintenance. I n .89 study'of Foot and Romberg (1965) (Table 3) young red kangaroos, I.lacropus ruf usI consumed less of the high quality chopped lucerne hay However, on the poor quality diet than did mature Corridale wethers. chopped oaten straw. diet, although dry matter intake by both herbivores declined, intake by the young red kangaroos was 40% 'greater than by the sheep,. Thus it appears that at least the red kangaroo is able to'better maintain its intake of a high fibre diet than is the Similar studies with other ,macrogodid species would be . sheep. necessary to fully testthis idea. TABLE 3 Intak'e and digestion by three young red kangaroos and three mature sheep From Foot and Romberg (1965) CONCLUSIOr;rS Herbivores, both foregutand hindgut fermenters, appear.to have evolved a number of different strategies for utilizing high fibre diets. Among the foregut fermenters the ruminant system is the best equiDped to maximise fibre d%gestion, but suffers from the' disadvantage that on very high fibre diets dry'matter intake is severely limited by slow passage out of the rumen of coarse feed particles. The macropodines, which have a stomach more like the proximal c&on than the rumen in gross morphology, do not suffer from this intake limitation to the same degree but are generally less efficient in their digestion of fibre. Among the hindgut f,ermenters the. colon fermentation system is generally superior to the caecum fermentation system in fibre digestion. but it can only be adopted by herbivores of large body size.' 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