Ever tried eating a newspaper? Don't. Plant cell walls contain cellulose, which is notoriously difficult to digest. Considering that all vertebrates lack the enzymes to attack this polysaccharide, how do so many of them manage to survive on a plant diet?

Plant eating certainly has its advantages. Leaves in particular are easily and widely available and in contrast to animal prey plants neither need to be hunted nor do they try to escape. And although many plants defend themselves against herbivores, these defences are not exactly violent. However, herbivory comes with a big disadvantage. Leaves are rather low-quality food, because they have only little cellular content and consist mainly of cellulosic fibre, which is notoriously difficult to break down. Young leaves and fruit are more nutritious, but much of their tissue is still cellulose. Considering that all vertebrates lack the enzymes to digest this polysaccharide, how do so many of them manage to survive on a herbivorous diet?

As so often the answer lies in a symbiosis with microorganisms, such as bacteria, protozoans and fungi, that are able to convert the indigestible cellulose into digestible nutrients via the process of fermentation. To maximise digestive efficiency, most herbivores have evolved specialised guts with fermentation chambers, where the plant material is subject to prolonged microbial attack. The by-products of fermentation, mainly volatile fatty acids (VFAs), can then be utilised by the animal host and constitute an important energy source. However, this does not come without costs. The energy from plant material is released relatively slowly, and particularly leaf-eating animals need to adopt a physiological and behavioural lifestyle that minimises energy expenditure. As huge quantities of food need to be ingested, the fermentation chamber has to be large. This adds considerable weight, which might be a disadvantage if a predator approaches. For efficient nutrient production, the food needs to be retained in the fermentation chamber for hours, so the transit time of food in the gut is significantly increased. Gut fermentation might furthermore impose limits on an animal’s body size. Smaller animals require more energy per unit body mass and have a higher mass-specific metabolic rate, but as their gut capacity is restricted, they might not obtain enough energy from fermenting high-fibre low-quality food.

Foregut and hindgut fermentation

Depending on the position of the fermentation chamber relative to the stomach, two types of gut fermentation can be distinguished. In foregut fermenters, the fermentation chamber is anterior to the stomach (e.g. rumen or crop), whereas it is posterior to the stomach (e.g. colon or caecum) in hindgut fermenters. Both digestive methods have advantages and disadvantages. Foregut fermenters are more efficient at breaking down cellulose, and bacteria lost from the chamber can be digested and serve as a source of protein. Fermentative digestion in the foregut furthermore allows for microbial detoxification early in the digestive process, so that enzymatic digestion in subsequent parts of the gut is not impeded by toxins. However, it is a slow process and the easily digestible cellular contents of the food are largely lost to the fermenting microbes before being exposed to the animal’s own digestion, making foregut fermentation less suitable for high-quality forages. Additionally, the intake of food is limited and particle size has to be reduced before it can be passed on to the stomach, which ruminants achieve by regurgitating and re-chewing their food.

Hindgut fermentation is assumed to be the phylogenetically older method and is found in many mammals (e.g. horses, elephants, rhinoceroses, rabbits, some rodents and koalas), herbivorous birds, such as grouse, and some reptiles (e.g. iguanines and the green turtle Chelonia mydas). It has been suggested that also most (if not all) herbivorous dinosaurs (e.g. Triceratops, brachiosaurs and hadrosaurs) were hindgut fermenters. Foregut fermentation is a prime example of evolutionary convergence as it has arisen independently in different animal groups. While it is best known from ruminant mammals, such as cattle, giraffes and camels, it also occurs in sloths, colobine monkeys (including the langurs), some rodents and macropodid and potoroid marsupials (kangaroos and their relatives). Intriguingly, foregut fermentation is not unique to mammals, but is employed by some birds as well. It has been extensively studied in the hoatzin (Opisthocomus hoazin), a curious South American bird, while its occurrence in two other birds (the green-rumped parrotlet Forpus passerinus and the speckled mousebird Colius striatus) is somewhat less well known. The convergence also has an important molecular context in the repeated recruitment of lysozyme as a digestive enzyme.

It should be noted, however, that such modifications of the digestive system are not necessarily a must for herbivorous animals. The giant panda (Ailuropoda melanoleuca), for instance, eats huge amounts of bamboo and probably utilises gut microbes to help with digestion, but it possesses the digestive system of its carnivorous relatives and lacks the gut specialisations found in other herbivores. The takahe (Porphyrio hochstetteri), an endangered flightless bird endemic to New Zealand, takes up large quantities of grass and shows no obvious gut specialisations either.