A foregut-fermenting bird was long considered a paradox. But what about the hoatzin, a curious South American bird known locally as the "stinking pheasant" thanks to its smell of fresh cow manure?

A foregut-fermenting bird was long considered a paradox. Compared to mammalian foregut fermenters such as ruminants, birds are much smaller and small body size is not particularly compatible with foregut fermentation. For efficient digestion, the fermentation chamber needs to be large, but the gut capacity of small animals is limited. However, they require more energy per unit body mass and have a higher mass-specific metabolic rate than larger animals, meaning that they might not obtain enough energy from slowly fermenting high-fibre low-quality food. In birds, the energy demands are even higher, because they have a higher body temperature than mammals and most of them fly. Indeed, only about 3% of all bird species eat leaves and very few of them are obligate folivores. Not surprisingly, almost all herbivorous birds are hindgut fermenters, where microbial fermentation occurs in the caeca or colon (e.g. in ratites, anatids and grouse).

So why should foregut fermentation have evolved in flying birds at all? Flight allows for increased food selectivity, thus the bird can seek out highly fermentable and patchy resources that might not be available to other herbivores and then digest them efficiently. Furthermore, foregut fermentation has the added advantages of utilising the fermenting microbes as a source of protein and enabling microbial detoxification of secondary plant compounds.

There is one well-documented case of foregut fermentation in birds. This is the hoatzin (Opisthocomus hoazin), a curious South American bird that feeds on the leaves of many different plants and ferments them in its massively enlarged crop. Some evidence suggests that two other (and, interestingly, much smaller) species also rely on foregut fermentation to at least some extent. These are the green-rumped parrotlet (Forpus passerinus), the smallest Neotropical psittacid, and the speckled mousebird (Colius striatus), which is endemic to sub-Saharan Africa. But knowledge of the crop microflora of birds is limited and it has been suggested that microbial activity in the crop could be more important for digestion in leaf- and seed-eating species than currently assumed.

Hoatzin

For quite some time it had been suggested that the crop might be of particular importance for digestion in this species and people had noticed the bird’s rather unpleasant smell (that is pretty similar to fresh cow manure), as reflected in its local name “stinking pheasant”. But it was not until 1989 that foregut fermentation was reported in the hoatzin and this finding provided new insights into the evolution of this digestive system. Because of the evolutionary distance between the Aves and the Artiodactyla, it is considered a prime example of evolutionary convergence. Hoatzins show morphological, microbiological and behavioural adaptations to their diet of leaves that are analogous to those found in ruminants.

Fermentative digestion takes place in the well-developed double-chambered crop and multi-chambered lower oesophagus. These two structures account for about 70% of the bird’s digestive tract and up to 17% of an adult’s body mass. The large size of the foregut is necessary for effective fermentation as it allows for high intake of food and long retention times of plant material (despite its much smaller body size, the hoatzin retains food in its crop for as long as sheep do). The crop is not only large but also highly muscular and equipped with cornified epithelial ridges that help to reduce food particle size, thus increasing the surface for digestion. This is functionally similar to the rumination process. What is highly unusual for birds, which normally grind food internally in their muscular gizzard, is that some food processing seems to take place in the bill (which possesses some unique adaptations) and the hoatzin has been referred to as a “chewing bird”.

The fermentation chambers harbour a wide array of microorganisms, including anaerobic eubacteria, methanogenic archaea, ciliate protozoa and fungi, in concentrations similar to those of ruminants. This complex microbial community is characterised by greater diversity than the more intensely sampled human colon and a surprisingly high degree of novelty. A characterisation of the crop bacterial population showed that more than 90% of phylotypes were unclassified at the species level and phylogenetically distinct from those found in the rumen. However, the methanogens in the hoatzin crop are more similar to those from ruminant mammals than to those isolated from the caeca of hindgut-fermenting birds. Differences in the microbial community between the hoatzin and ruminants could be linked with the higher body temperature of birds compared to mammals. As in the rumen, fermentation generates high levels of volatile fatty acids that nourish the bird. However, cellulolytic activity, which is elevated in the mammalian rumen, seems to be reduced in the crop. But perhaps the explanation lies in the fact that the hoatzin (like colobine monkeys) is a selective browser and preferentially chooses the more nutritious young leaves that contain less lignin and cellulose and more hemicellulose (that is easier to hydrolyse). Apart from breaking down the plant material, the gut microbes have another function, which is to detoxify plant chemicals (the food plants of hoatzins often contain toxic secondary compounds). In chicks, the crop microflora is established by transfer of microbes with partially fermented plant material regurgitated to them by adults. Interestingly, the structure of the microbial gut community changes with age, probably in relation to dietary changes as chicks become less dependent on adult crop liquids and progressively browse foliage themselves. Like foregut-fermenting mammals, the hoatzin has also recruited lysozyme as a digestive enzyme, but it is of the calcium-binding instead of the conventional type, thus representing an intriguing case of molecular convergence.

All these adaptations maximise digestive efficiency and the hoatzin is as efficient at digesting plant material as ruminants. However, compared with other birds, hoatzins are very inactive. And since the massive crop has led to a reduction in the size of the sternum and, correspondingly, of the attached flight muscles, they are also poor flyers. The chicks need a long time to learn how to fly and their wing claws and unusual predator-escape mechanism (which can not only involve shinning up trees, but also swimming) have been interpreted as developmental costs of folivory and foregut fermentation.

Green-rumped parrotlet

During reproduction, this species feeds almost exclusively on unripe seeds of the euphorbian plant Croton hirtus, which are rich in starch and thus hard to digest. An analysis of the microbial flora of this bird’s crop showed that it contains facultatively anaerobic bacteria, predominantly Streptococcus and Lactobacillus, in densities comparable to those found in the crop of hoatzins and the foregut of several herbivorous mammals. These bacteria produce the starch-digesting enzyme amylase, which is present in human saliva but is absent from the saliva of most birds. The efficiency of microbial fermentation is enhanced by the unusually long retention time of seeds in the crop, which furthermore facilitates hydration of the starch. In addition to this presumably important role in the nutritional physiology of this bird, the crop-associated bacteria could also constitute a source of protein, thus enhancing the parrotlet’s nitrogen supply.

Speckled mousebird

In contrast to the hoatzin and green-rumped parrotlet, the speckled mousebird does not possess an enlarged crop. It has, however, a well-developed proventriculus and prominent ventriculus that contain various bacteria. These seem to help with the digestion of leaves, producing the volatile fatty acids that have been recorded in the foregut of this bird at levels similar to those measured in the hoatzin. However, mousebirds are not obligate folivores, but have rather flexible dietary habits. While leaves are easily obtainable and form a major part of their diet, they switch to higher-quality food such as fruit when available. This allows them to adjust to seasonal fluctuations in food abundance and they deal with the low nutritional value of leaves by reducing their energy demands, for example through basking in the sun, huddling together at night and apparently gliding instead of flying. The sunning behaviour of mousebirds might furthermore have a digestive function (like in sloths), possibly accelerating starch hydrolysis.