A Nutritional Explanation for Body-Size Patterns of Ruminant and Nonruminant Herbivores

The gut capacity of mammalian herbivores increases linearly with body weight. This relationship, coupled with the change in basal metabolism with weight, produces an MR/GC ratio (metabolic requirement/gut capacity) that decreases with increasing body size. Since the retention of a food particle within the gut is proportional to this ratio, the extent to which food particles are digested will be related to body size. Plant material is made up of chemical components that react differently to digestive enzymes. The fiber fraction of plant material (i.e., cell wall) is digested slowly and exclusively by microbial symbiotes. A positive relationship probably exists between the fiber content of plant parts and their biomass in the environment. This relationship is used to describe a resource axis on which digestion rate is the scaling variable. In response to this resource axis and metabolic requirements, the fiber content of the diet of herbivores increases with body size. Ruminants are the predominant medium-sized herbivores in East Africa, while nonruminants are mainly small or very large animals. Small herbivores are constrained to rapid passage of ingesta by their high MR/GC ratio. In response, they have evolved hindgut fermentation and feed selectively on rapidly digestible (i.e., low-fiber) foods. Both responses contribute to loss of nutrients (synthesized by gut microbes) in the feces, and thus contribute to coprophagy in this group. To eat a diet higher in fiber, the herbivore must increase its body size. The reduced MR/GC ratio of medium-sized herbivores allows the evolution of gut structures that selectively delay the passage of ingesta. Selective delay results from the rumination process because the probability of passage is tied to particle size. This process produces more efficient fiber digestion in ruminants than that in nonruminants of similar size. Rumination, however, is advantageous over only a limited range of body sizes. The lower limits of ruminant body size are set by maximal fermentation rates. Foregut fermentation will not only digest the cell wall, but also use many of the soluble nutrients before their direct absorption is possible. Therefore, ruminants must rely almost entirely on the production of microbial volatile fatty acids (VFA) for energy and postruminal digestion of microbes for other nutrients. With decreasing body size, the increasing rate at which energy must be produced per unit volume of the rumen cannot be matched by a concomitant increase in the fermentation rate of forages. Nonruminants are favored by the more efficient energy transfer of enzymatic digestion in the foregut of the low-fiber foods often required by small animals. The upper limits may be imposed by two factors. First, rumination rates (g cell wall ruminated per unit time) increase with body size more slowly than does the cell-wall content of the diet. Using the case of the African buffalo, we arrived at calculations which suggest that sufficient intake of a high-fiber diet cannot be maintained to provide the energy necessary to support larger body sizes. Second, with increased body size the very low MR/GC ratio allows very long retention times. A point in body size is reached (600-1200 kg) at which retention times are sufficient to achieve relatively complete digestion of the potentially digestible component of forages, regardless of whether the herbivore possesses a selective delay mechanism of the rumen or the "perfect mixing" of the nonruminant model. Because of the small body size of early ruminants, the evolution of the rumen was probably initiated by selection for the detoxification or synthetic capabilities of foregut fermentation. The foregut then was preadapted for development as a structure for the selective delay of forages when the grasslands expanded. Changing body size is postulated as a mechanism for differentiating the feeding requirements of herbivores. The fiber composition of plant material is the scaling variable for a resource axis for herbivores. Large herbivores can extract more energy from plant material than can smaller herbivores, but cannot concentrate on the rapidly digestible foods used by small animals because these foods are rare. Therefore, if competition is important in structuring herbivore communities, then body size is probably a factor that contributes to feeding differences.