Australia: The Land Where Time Began
Kangaroos - foregut fermentation
Foregut fermentation, the fermenting of plant material in the front part of the gut, has a number of advantages in the mammals using it, the main one being the breakdown of cellulose from plant cell walls by the bacteria in the the foregut, releasing the cell contents more effectively than the mechanical breakdown by teeth. Another important advantage is that the anaerobic fermentation of cellulose produces short chain fatty acids, SCFA, a rich source of energy. Non-fermenting herbivores can't make use of this energy source because mammals don't produce the enzymes necessary to hydrolyse the cellulose. Another advantage is that urea can be utilised by the bacteria in the foregut to obtain the nitrogen they need to synthesise their protein, which eventually becomes available to the mammal when it digests the bacteria as they pass to the small intestine, resulting in 2 advantages for the mammal, the excess nitrogen that would be excreted as urea in urine is conserved, with the consequence that less water is required than would be needed to excrete the urea in the urine. The macropods in Australia, as well as ruminants on other continents, have gained great economies in the conservation of water, nitrogen and energy, as a result of forming symbiotic relations with microbes in the foregut.
As with the stomachs of other mammals, such as ruminants and camels, using bacteria to digest plant material by fermentation, macropods have a large stomach that can comprise 15 % of total body mass when full. The anatomy of the macropod stomach differs greatly from that of other fermenters like sheep and cattle. The macropod sumach is in the form of a curved, elongated structure, the outer curvature of which is deeply indented, and the inner, shorter side, is smooth. On the external surface, there are 4 sections, each of which has a distinct function. The anterior 2 parts are found only in macropods, the 2 posterior parts correspond to the stomach in other marsupials. The oesophagus opens into a region with a funnel shape, extending along the inner curvature as a spiral groove, that is partly closed, and is lined with the same squamous epithelium as that lining the oesophagus. This groove separates the fine from the coarse plant material, directing the fine material to the posterior part of the stomach, the lining of which secretes hydrochloric acid, producing an acid pH of 1.8-3.0, as well as proteolytic enzymes that break down the protein from both the plants and the bacteria.
The coarse material is directed to the forestomach where it is fermented by the bacteria. The largest part of a macropod stomach, it is divided into an anterior sacciform forestomach, and posterior tubiform forestomach, by a deep, permanent fold. A glandular epithelium secreting mucus, but no acid or proteolytic enzymes, lines both sections of the forestomach. The pH is about 4.6 before feeding, rising to about 8.0 after feeding, buffering maintains this range by mucus secretion and saliva produced by the parotid salivary glands during chewing. There are high concentrations of bicarbonate, phosphate and sodium ions in the copious parotid saliva, that buffer the fluid, to maintain an alkaline pH, supporting bacterial growth in the forestomach. There are dense populations of bacteria in both sections of the forestomach, 1010/mL of bacteria, and 106/mL of ciliated protozoa. The cellulose of the plant cell walls is digested anaerobically to SCFA, releasing the cell contents in the process, which are then digested by the host macropod and the bacteria.
The different habits and food preferences of different species is reflected in the parts comprising the forestomach of the different species. The stomach of the musky rat kangaroo is simple and the contents are kept at a low pH. It lacks bacterial fermentation, the regions of the forestomach not developing. The sacciform forestomach is much larger then the tubiform forestomach in the rat kangaroo, tree kangaroos and pademelons. This is believed to result from the digestible nature of their browse. Food entering the stomach of the pademelon is moved preferentially to the sacciform forestomach, and after several hours, being moved to the tubiform forestomach. Their preferred diet of coarse material consisting mostly of grasses, is moved to the tubiform forestomach, remaining there for many hours, being thoroughly mixed, before contractions of the partitions between the pockets, and stomach wall muscles, pass it along to the next compartment. A food bolus moves to the hindstomach, where there is a very low pH and proteolytic enzymes, from the tubiform forestomach. The protein of both the bacteria and plant material is digested, the digestion products passing into the small intestine where assimilation takes place and they enter the bloodstream.
The caecum and proximal colon of the macropods are relatively small, compared to the same structures in the koala, wombats and possums, in which fermentation of plant material occurs in the hindgut. The caecum and proximal colon contribute little to the economy of the animal, though they contain fermentative bacteria. Water absorption from the faeces takes place in the distal colon, as in other herbivores, its length varying depending of the habitat of the particular species. Species such as pademelons, forest dwellers, have a short distal colon, and their faecal pellets have a high water content. In species such as the euro, adapted for desert conditions, the distal colon is long, resulting in very low water content of the faecal pellets (54 %). The southern hairy nosed wombat, Lasiorhinus latifrons, also produces dung with a low water content, as does the camel, Camelus dromedarrius.
In young macropods that are still in the pouch, and haven't started eating solid food, the stomach regions all have a low, variable, pH, and are proteolytic (Griffiths & Barton, 1966). The forestomach has a neutral pH as it is prepared to function as a fermentation chamber. Colonisation of the forestomach by bacteria and protozoa is believed to be from its mother. At this age, the young can often be seen making contact with its mother's muzzle (Russell, 1973, Croft, 1981b). Mothers have been observed passing chewed material to their young. In young koalas and wombats, caecal contents are passed from the mother to the young when the young first start eating herbage. It is believed to be the method used to introduce the bacteria and protozoa to the young.
Energy from cellulose
The environment of the forestomach is low in oxygen, so the bacteria cannot hydrolyse the cellulose of the plant cell walls to simple sugars, producing only the intermediate products by anaerobic fermentation. These fermentation products are short chain fatty acids, acetic acid, propionic acid and n-butyric acid, as well as ammonia, methane, carbon dioxide and hydrogen. The same SCFAs are found in the hindgut of koalas, wombats, and the greater glider, Petauroides volans. Based on studies on the tammar wallaby, the production of SCFA begins in the sacciform forestomach, continuing as the bolus moves along the tubiform forestomach, but at a reducing rat. As the bolus passes through the forestomach the SCFA produced is being absorbed across the forestomach walls, less than 20 % of the total SCFA produced being present by the time the bolus reaches the hind stomach. The epithelial cells of the stomach walls power the transport of other fatty acids across the stomach wall to the bloodstream by using the butyric acid for energy. The other fatty acids are transported to the liver in the blood, where they are metabolised to glucose, that can be detected in the blood soon after feeding.
A crucial factor in the bacterial fermentation of the cellulose is the rate at which the plant material passes through the macropod's tubular stomach. Less nutritious food is required if the food passes along slowly, giving the bacteria more time to work on the bolus, breaking down a higher proportion of the available cellulose. The food passes through the macropod's stomach faster than through the chambered stomach of ruminants, the use of low-grade grasses is superior in kangaroos, as the coarser material is fermented more rapidly, the coarser material continuing on to the caecum and proximal colon. In large macropods, the forage quality affects their intake to a lesser extent than it does in sheep. When euros and sheep were compared, on a low fibre diet the sheep ate 30 % more than the euros, because of the lower metabolic rate of the euros. The euros could consume a higher fibre diet than the sheep (Hume, 1999). This aspect of euro food processing is similar to that found in the southern hairy-nosed wombat, where food is fermented in the hindgut. In large macropods, the advantage afforded by the tubiform forestomach does not occur in the smaller species that have a large sacciform forestomach, as their processing of poor quality forage is too slow to be of benefit to them. The large body size required to take advantage of the tubiform forestomach may give a clue to the reason for large size of the herbivorous marsupial megafauna of the Pleistocene, when the climate was very arid and much of the available food could be expected to be of poor quality, large body size favouring bulk feeding (Tyndale-Biscoe, 2005).
Nitrogen and urea conservation
Nitrogen conservation is greatly favoured by fermentation in the forestomach. It differs from hindgut fermentation in that the protein that has been synthesised by the bacteria is easily available for digestion as soon as it leaves the forestomach. This enables the nitrogenous waste products of the mammal, ammonia and urea, to be recycled, as well as providing an additional source of protein. Excess amino acids are converted to ammonia in the liver, which is converted to the non-toxic urea, as amino acids cannot be stored in the body. This would normally be excreted in the urine. In ruminants and kangaroos, the urea in the blood can be passed to the forestomach where it is used by the bacteria to synthesise their protein, thereby increasing the level of hydrolysis of cellulose, especially for processing low protein forage. As in ruminants, the parotid saliva of macropods contains urea, which is delivered to the forestomach with food. In the sacciform forestomach, the contents can be higher in protein than was present in the food, as a result of the synthesis of new bacterial protein by using the urea (Hume, 1999).
When kangaroos and wallabies eat high nitrogen food, such as legumes, less urea is used by the bacteria and more is secreted in the urine, requiring the excretion of more water. Much less urea is excreted when they have a low-protein diet, selective reabsorption of urea taking place in the kidney (Lintern & Barker, 1969). This is an important adaptation for nitrogen conservation, as well as water conservation. Kangaroos and wallabies often occupy arid and semiarid environments with irregular and low rainfall, which makes this adaptation more important for their survival.
Some macropods have much lower nitrogen requirements in their food than arboreal marsupials, such as the greater glider. The daily nitrogen requirement for the tammar wallaby, 230 mg N/kg0.75, that is similar to that of ringtail possums that re-ingest, and half that of the greater glider that does not re-ingest. In the pademelon, a forest dweller, the daily nitrogen requirement is similar to that of the greater glider, 530 mg N/kg0.75, while those of the euro, a desert kangaroo, are 160 mg N/kg0.75 (Hume, 1999). From this it is apparent that there can be wide variation in the macropod digestion pattern, depending on the environment and the available food source. The abundance of nutritious forage in temperate climates results in rapid passage through the gut and increased urea excretion. In areas with high-fibre, low protein forage, the passage of the food through the gut is slower, and most urea and water is conserved. This is more apparent in individual species.
Tyndale-Biscoe, Hugh, 2005, Life of Marsupials, CSIRO Publishing.
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