Foregut fermentation is best known from the ruminants, such as cattle, deer and giraffes, that regurgitate and rechew their food to aid microbial digestion. However, they are not the only mammals to have evolved this digestive strategy...

Foregut fermentation has evolved several times independently in herbivorous mammals. Most famous are, of course, the ruminants of the order Artiodactyla, such as cattle, sheep, deer, giraffes and antelope. But also sloths, colobine monkeys, some rodents and two families of marsupials are foregut fermenters. Microbial fermentation arose in large reptiles that opened up new niches by eating plants. The evolution of foregut fermentation in mammals from carnivorous ancestors could have occurred via omnivory, with the modification of the foregut into a new fermentation chamber following the development of the hindgut.

Even-toed ungulates

Most of the foregut-fermenters in the order Artiodactyla – about 150 species – are ruminants. The suborder Ruminantia includes cattle, goats, sheep, deer, antelope, giraffes and others. Ruminants are named after the process of rumination (from Latin “ruminare”, meaning to chew over again), which entails a slightly stomach-churning combination of regurgitation, remastication, resalivation and reswallowing of semi-digested material (known as cud) and is essential for efficient digestion. The ruminant stomach consists of four separate compartments divided by sphincters. Rumen and reticulum represent one functional space (so often called the reticulorumen). Here, microbial fermentation takes place, producing the nourishing volatile fatty acids as well as gases, such as carbon dioxide and methane. The reticulorumen is followed by the so-called omasum, where water and minerals are absorbed, and finally the abomasum, which secretes enzymes and is functionally similar to the “true stomach” of monogastric animals. This digestive system differs considerably from that of other mammals and is particularly efficient at digesting plant material high in cellulose. A peculiarity of the ruminant forestomach is its efficient particle sorting mechanism – larger food particles are selectively rechewed, while the gut is cleared from digested smaller ones. This feeding mode might have evolved because it facilitates escape from predators (with food being ingested quickly and then rechewed later), but microbial detoxification of secondary plant substances is probably of similar importance.

Confusingly, not all ruminants are included in the Rumimantia. Also camels, llamas and alpacas of the suborder Tylopoda ruminate. Their stomach, however, consists of only three compartments and has evolved independently from that of the Ruminantia. Finally, there are also some non-ruminating artiodactyls with multi-chambered stomachs, namely the herbivorous hippopotamuses (Hippopotamidae) and peccaries (Tayassuidae). Peccaries, which are often confused with the closely related monogastric pigs (Suidae), possess the smallest relative stomach of all foregut fermenters. Thus, fermentative capacity and forage digestibility are rather low, and the relevance of foregut fermentation to peccaries is still mysterious. It could allow them to deal with plant toxins such as oxalic acid.

Sloths

Sloths are notorious for their extremely low metabolic rate and slow movements. Most of their day is spent resting in trees, which likely includes deep sleep. The main reason for this is that they feed almost exclusively on leaves (as indicated by their Latin name Folivora), a low-quality diet, which is actually highly unusual for Neotropical arboreal mammals. Sloths have complex stomachs with multiple compartments, where symbiotic microbes ferment the leaves. Lysozyme, an antibacterial enzyme that has been recruited to aid digestion in many foregut fermenters, seems to have a different, more primary role in these animals, probably protecting the gut microflora from foreign bacteria. Although sloths mainly feed on young leaves that are nutritious and comparatively easy to digest, their fermentation rate is considerably slower than that of other relatively small mammalian foregut fermenters. This is probably related to their lower body temperature (28-35?C). The thermoregulatory capacities of sloths are rather poor, limiting their range to not too cool environments and relatively low altitudes. A study on a population of three-toed sloths (Bradypus variegatus flaccidus) in montane Venezuelan forests showed that the animals’ feeding activity increased during hotter parts of the day and that the weather affected their posture. In sunny conditions, they exposed their belly, but otherwise adopted heat-conserving postures (and contrary to common belief, they rather sit in trees than hang from branches, as the former is probably less energetically costly and might also help with the sorting of food particles in the stomach). This behavioural thermoregulation is reminiscent of that in mousebirds which also feed on leaves and seem to employ foregut fermentation. However, sun exposure not only serves to increase body temperature, but it is likely that it also speeds up microbial fermentation.

Colobine monkeys

Colobine Old World monkeys (such as langurs, colobus monkeys and proboscis monkeys) are unique among primates in that they have adapted to a diet consisting mainly of leaves by evolving a complex stomach and foregut fermentation. Some colobines, however, do not eat leaves but other food high in fibre. The Yunnan snub-nosed monkey (Rhinopithecus bieti) feeds primarily on lichens, a rather unusual food for mammals. And many species also take fruit, which is higher-quality, lower-fibre food albeit with potentially toxic seeds. While other primates either spit the seeds out or swallow them intact, colobines chew and digest them, detoxifying any harmful substances in their fermentation chamber. This different feeding ecology has also led to differences in behaviour – compared with their omnivorous baboon and macaque relatives, colobines have small home ranges and are not particularly aggressive over food.

Unlike ruminants, the stomach of colobine monkeys is not separated into discrete chambers. It is tubular in shape and thus more similar to that of marsupial foregut fermenters. But the digestive strategy of at least some colobines is, in fact, unique among mammalian folivores in that they have not only one but two fermentation chambers. Equally important as the forestomach is the large segmented colon, where digesta are also retained for a prolonged time (in other foregut fermenters, hindgut fermentation is only of secondary importance). Such gastro-colic fermentation was demonstrated in some Asian species of the genus Trachypithecus as well as in the mantled guereza (Colobus guereza) and Thomas’s langur (Presbytis thomasi). It has been suggested that the body size of colobines might be too small for them to rely exclusively on foregut fermentation. It is considered likely that colobine monkeys have developed a foregut fermentation chamber secondarily, in addition to the more primitive hindgut fermentation chamber present in the other subfamily of Old World monkeys, the Cercopithecinae.

Like ruminants, colobines have recruited the RNA-cutting enzyme pancreatic ribonuclease (pRNase) for digestive purposes. Molecular analysis of gene sequences showed that colobine monkeys have actually duplicated the pRNase gene, and it has been suggested that they possess two functionally distinct pRNases, one of which functions as a digestive enzyme.

Rodents

Most herbivorous rodents are hindgut fermenters, but some employ foregut fermentation. One example is the folivorous black-tailed tree rat (Thallomys nigricauda), an arboreal species that inhabits Acacia woodlands in dry regions of Southern Africa. These rats mainly consume leaves, seeds and other parts of Acacia trees, which contain high levels of condensed tannins. Tannins are anti-herbivore defences that reduce dietary quality in several ways – for example, they are potentially toxic and bind to proteins, thus reducing their digestibility. One advantage of foregut fermentation is microbial detoxification early in the digestive process, but no significant detoxification of tannins seems to occur in the foregut of tree rats. Experiments suggested that the rats behaviourally avoid a high-tannin diet, even at the cost of decreased body mass. They might be able to detect tannins by taste, which could hint at a close co-evolutionary relationship with Acacia trees.

Marsupials

Marsupial foregut fermenters, which are the macropods (kangaroos, wallabies, tree-kangaroos and pademelons) and potoroids (bettongs, potoroos and rat-kangaroos), evolved in regions of poor forage quality. Foregut fermentation, which allowed them to extract nutrients from high-fibre plant material, was probably the key to their success, just like in ruminants. However, they have evolved herbivory independent of the placental mammals and their digestive system is actually quite different. Kangaroos possess a basically tubiform forestomach, in contrast to the four-chambered stomach of ruminants, and it is more similar to the colon of hindgut-fermenting horses. And while regurgitation may be observed in marsupials, it is not analogous to rumination (and referred to as merycism). It is probably not necessary for digestion, but might help to stimulate saliva production. Interestingly, as kangaroos produce no methane gas, the gut microflora does not seem to include methanogenic bacteria. Marsupials generally have a lower metabolic rate than the placentals and, consequently, exhibit lower body temperature and energy requirements. While this has several negative consequences, it also means that their energy reserves last longer under adverse conditions, such as droughts, during which low-quality, high-fibre food is most abundant.