Sterile Bowel Theory

Dr Rob Marshall has written this article to explain his thoughts on the sterile bowel theory.

At an Association of Avian Veterinarian International Conference held in 1989 I was surprised when first hearing that both Dr Gerry Dorrestein and Dr Helga Gerlach believed the bowel of healthy finches and canaries was sterile. At Veterinary school I had been taught that bacteria played a vital role in the continuing health of the animals we studied (dogs, cats, cows, horses as well as poultry). I instantly accepted the opinions of these two eminent bird pathologists and immediately used this new found knowledge to help me understand the special nature of Passerines in general and finches in particular.

The Sterile Bowel Theory is supported by the following facts:

1. Finches belong to the most advanced order of birds: Oscine passerines.
2. Oscine passerines have developed specialized adaptive anatomical and physiological systems that are different from the more primitive bird orders (eg Galliformes)
3. The high metabolic rate of Oscine Passerines (eg finches) requires much more additional energy. In passerines more advanced and improved chemical digestion and intestinal absorption provide this additional energy.
4. Bacterial fermentation is an inefficient source of energy. Birds with caeca utilise bacteria to help digest fibrous matter. Finches have no caeca.
5. Finches have no resident bowel or so-called "friendly bacteria". "Friendly Bacteria" is a concept that explains the theory of probiotics.

Knowledge of the special position Passerines hold in the bird world should help you understand the notion of a sterile bowel in these birds.

Passerines are the most recent and advanced order of bird species. They account for approximately three fifths of all living birds, or some 5,739 of the 9,702 species of 1,168 genera. Other birds such as poultry (Galliformes) belong to much older and more primitive orders of birds.

Passerines broke away from the normal avian (more primitive bird orders) mould to become the most successful group of birds. They appeared in force by adaptive radiation after the Paleogene time period moving them into unexploited and unrestricted ecological zones largely because their complex nest building behaviour released them from the limited resource of cavity nesting. Passerines were so successful during the late Tertiary period that lines of demarcation among families and higher groups are poorly defined, so that differences among many passerine families are not as great as those among non-passerine genera. Almost all recent workers have considered the order Passeriniformes to be monophyletic sharing many anatomic and physiological similarities (a special type of palate and syringeal anatomy, bundled spermatozoa, the distinctive passerine foot and an elevated metabolic rate).

The elevated basal metabolic rates of Passerines compared to other birds are an indication of the uniqueness of this group of birds. This finding also supports a view that their bowel is sterile. The basal (at rest) metabolic rates of Passerines average some 50-60% higher than non-passerines of equivalent size. This feature found in Passerines reflects a significant move away from the physiology established in more primitive bird forms such as Galliformes (poultry).

Passerines can be divided into two broad groups: Suboscines and Oscines. The Oscines constitute about four fifths of the Passerine birds and are extremely uniform in their morphology. They are referred to as the "songbirds" that largely inhabit temperate zones of the world. Finches are a part of the Oscine group of Passerines. The suboscines are slightly less morphological uniformity and are prominent in neo tropical regions. The Australian Lyrebird and scrub birds do not fit into the classical definition of suboscines or Oscines.

Our interest lies in the Oscines that occupy temperate zones of the world. The Oscines represent an absolute extreme among birds and perhaps all living vertebrates in their morphological uniformity. Most are small land birds primarily adapted for feeding on insects, small fruits and seeds and therefore many of the differences we do see among them are in the feeding mechanism and bill structures that are often convergent rather than indicative of any evolutionary link. Similarly the digestive tract of the seed-eating finches should be viewed as an adaptive change with no evolutionary link to more primitive orders of birds.

The lack of major gaps among many Oscine families suggest the adaptive radiation of modern, advanced Oscines is probably quite recent perhaps dating to the Medial to late Tertiary period of time. For this reason we should not assume any evolutionary link between the digestive physiology of primitive birds forms such as Galliformes (poultry) and the most advanced and recent birds; the Passerine Oscines.

Current knowledge of the digestion of food in birds is the result of scientific studies performed on poultry. Poultry belong the Galliformes a most primitive form of birds. In these birds the crop, proventriculus, gizzard, small intestine and caeca are all involved in the digestive process. The gastric apparatus includes the proventriculus (secretes acid gastric juice and pepsin) and gizzard action (grinding action and acid proteolysis). The principle organ for chemical digestion and absorption takes place in the small intestine. Here the chyme from the gizzard is neutralised by the highly buffered bile, pancreas juice and succus entricus so the pH especially in the ileum is between 6-8. Chemical digestion of starch is effected largely in the small intestine through activities of pancreatic amylase and of intestinal and pancreatic maltase. Lactose and sucrose are hydrolysed by lactase and maltase respectively in the succus entricus.

In birds that must digest fibrous plant foods the caeca (birds have paired caeca) are well developed and the combined length of the caeca may be the length of the small intestine. The caeca harbour bacteria that help breakdown plant cellulose into simple digestible carbohydrates. Food reaches the caeca by anti-peristaltic movements of the rectum. Recent research has shown that bacterial fermentation in the caeca supplies only a small fraction of the total energy requirements of birds, so the real importance of the caeca in the domestic fowl is in doubt3. Finches have no caeca.

Although microbiological digestion and fermentation of cellulose occur in the caeca of some Galliform species, the frequently repeated suggestions that these processes also occur in granivore species such as parrots, pigeons and finches which have no functional caeca has not been experimentally substantiated. Passerines have no caeca and therefore no intestinal flora for microbiological digestion.

Food eaten by finches is digested chemically and then absorbed in the small intestine without the presence of symbiotic bacteria. Passerines are not considered to have a permanent gut flora. The microscopic examination of faecal smears from healthy finches does not reveal bacteria or other organisms. Routine aerobic microbiological cultures taken from droppings of passerine birds do not produce any bacterial growth.

Discussion
It is commonly accepted that Oscine Passerines are the most modern and advanced of birds. Their small size and high metabolic rate (65% greater than for non-passerine birds) that has allowed them to occupy their dominant numerical position in the bird world has meant that further physiological adaptations have also become necessary. The Oscines require an increased source of energy to maintain their high body temperature (2 degrees Celsius higher than other birds). They must eat (up to 30% of their body weight daily) and drink (25-30mls per 100grams body weight daily) relatively enormous amounts to maintain their energy levels. As well the food must be digested and absorbed as quickly as possible. Death from haemorrhagic diathesis that occurs in finch species that have not eaten within 48 hours is testament to the vascularity and highly efficient absorption mechanism of the small intestines of finches.

Bacteria present in the bowel of the more primitive bird forms (eg Galliformes) that help with digestion and also produce vitamins and other metabolites are not required in Passerines. The extremely high-energy requirements of these small birds are covered by an increased activity of the enzymes lipase and amylase. Refined chemical (enzymes) digestion and enhanced absorption capabilities present in finches is a far more efficient method of energy production. The environmental niches occupied by the more mobile oscines are also more likely to provide the required dietary vitamins and other metabolites.

Resident bacteria exist in many bird species. They help repel potentially harmful environmental bacteria. These "friendly bacteria" vary from one bird species to another and relate to their natural environment, for example, my studies on the wild Budgerigar have revealed the presence of Streptococcus faecalis as a normal inhabitant the bowel. Under adverse conditions this normal bacteria may produce disease. Poultry have a wide range of normal gut bacteria as they have adapted to an environment rich in these bacteria and germs. Probiotics have been produced mainly for poultry species in order to counteract the potential harmful effects of normally encountered bacteria. In order to work properly, probiotics must colonise the bowel and to do so they must be part of the normal gut microflora.

Consequently, probiotics designed for poultry will not be effective for parrots or paserines. The acidifying effect of Lactobacillus acidophillus, a common ingredient of probiotics, is responsible for a beneficial effect experienced with "generic" probiotic use. Probiotics do not apply to Oscine Passerines (finches) because it is commonly agreed that the healthy finch has no resident gut bacteria.

The notion that finches have a sterile gut is important but often misunderstood. Autolysis that occurs after death does not require the presence of bacteria in the bowel. The proteolytic tissue damage that results following death allows anaerobic bacteria to colonise these tissues from the outside to the body. Resident bacteria found in the more primitive bird species play a part in preventing bowel infections but the more conventional immune modulators remain the main barriers to infection from environmental germs in these species. The role of the very high body temperature of finches should not be underestimated as an important supporting role in preventing colonisation of the bowel with harmful bacteria.

References

1. Seminars in Avian & Exotic Pet Medicine Volume 12 Number 1 Jan 2003, pages 12-22
2. Origin & Evolution of Birds. Feduccia, pages 346ff
3. Birds: Structure and Function. King and McLelland, pages 104,105
4. Disease of Cage and Aviary Birds. Petrak Edition 2, page 189
5. Manual of Ornithology: Avian Structure and Function. Proctor and Lynch, page 18
6. Avian Medicine Principles and Application Ritchie, Harrison and Harrison, page 1187

Copyright © 2010 Rob Marshall, All Rights Reserved.