Australia: The Land Where Time Began
Sauropod Biology - Functional Gut Flora – Evidence
1. Among taxa of extant large herbivore lineages a fermentation chamber within their guts is the rule and not the exception. Diverse taxa, such as artiodactyls, perissodactyls, proboscideans, lagomorphs, rodents, a variety of marsupials, as well as other mammals (Stevens & Hume, 1995); birds such as ostrich, rhea, and galliformes (Klasing, 1998); tortoises, iguanids (Bjorndal, 1997); and tadpoles (Pryor & Bjorndal, 2005) and several lineages of fish (Clements, 1997). There are still different degrees to which fibre is digested among the extant large herbivores. A classic example of a herbivore that, though it depends on its gut flora, employs a strategy of high intake and low digestibility when compared to other herbivores (Clauss et al., 2003), is the elephant, though still with more efficient digestion than geese or the panda.
2. The microbial groups responsible for degrading fibre are among the evolutionarily earliest, originating about 1 Gyr before the opening of the Mesozoic (Hume & Warner, 1980; Van Soest, 1994). It is believed the Carboniferous/Permian was the time when terrestrial vertebrates that had symbiotic gut microbiota that degraded fibre first appeared in the fossil record. Colonising of the gut of these herbivores by fibre-degrading microbes is suggested to have occurred by the ingestion of detritus and/or herbivorous insects (Horton et al., 1997; Sues & Reisz, 1998; Reisz & Sues, 2000). The prerequisite for making use of a functioning symbiotic gut flora therefore existed long before the rise of the large herbivorous sauropods.
3. Evidence has been found that among ruminants when calves are isolated it may prevent colonisation of their guts by protists, microbes that are not considered to be essential for the function of the gut flora of the host, (Van Soest, 1994), though it has been found that even without direct contact with other animals bacteria that degrade fibre still colonise the gut of these isolated animals. Colonisation of the rumen/gut cannot be completely prevented even under extremely severe isolation, which includes food sterilisation (Males, 1993). Under such extremely unnatural circumstances significant populations that are atypical may develop that exhibits the relevant fibre-degrading capacities, with the digestion of dry matter being reduced by 2-10 %, and the digestion of cellulose being down by 15-40 %, as stated by Males (1973, cited in Dehority & Orpin, 1997).
Gut microbe acquisition
Hummel & Clauss suggest that as a consequence of the above evidence the acquisition of a functional gut flora may not have been as big a problem on an evolutionary level as has often been supposed. Symbiotic gut microbe acquisition, e.g., is considered to have occurred independently in several lineages in the late Palaeozoic (Sues & Reisz, 1998). As long as there is a chamber of large volume in the gut is available inoculation by suitable gut microbes may not necessarily be considered to be limiting, in line with Hotton et al., (1997).
This does not suggest that active inoculation from conspecifics during the ontogenetic development of an individual is not beneficial. It will represent an advantage if a young animal can acquire a microbial flora from its mother or by mouth-to-mouth contact from conspecifics or by ingestion of faeces, this will represent a digestive advantage, as the flora so acquired in probably already adapted to the respective food sources. Though it should be considered that particular behavioural adaptations for the acquisition of gut fauna should be considered to be more of an improvement of the acquisition mechanism than as a prerequisite, according to Hummel & Clauss (Troyer, 1982), is often cited here as evidence supporting obligatory sociality among herbivorous dinosaurs).
Given the broad distribution of symbiotic gut microbes among extant specialised herbivores, Hummel & Clauss suggest it is safe to consider that herbivorous dinosaurs may have also harboured a symbiotic fibre digesting gut flora (Farlow, 1987; Van Soest 1994).
Heat of fermentation
It has been hypothesised that an extensive population of microbes in a large fermentation chamber would contribute significantly to temperature regulation, which is the basis for the comparison of sauropods being compared to giant compost heaps (Farlow, 1987). It is yet to be analysed in detail if heat from fermentation contributes significantly to thermoregulation in herbivores. There is, however, a limited amount of evidence contradicting this suggestion: body temperature across a large variety of herbivorous mammal species which concluded that there is not a general pattern indicating either increasing or decreasing body temperature with increasing or decreasing body mass that is evident, which led to the conclusion that there is not a consistent pattern of contribution to overall temperature regulation of heat generated by fermentation. This does not rule out such compensation occurring in other groups such as dinosaurs.
Fermentation in foregut versus hindgut
Basically there are 2 main sites for fermentation chambers that are known of among vertebrate herbivores (Stevens & Hume, 1995). The hindgut is the most basic site where a population of microbes is hosted as it is in the hindgut that some degree of fermentation occurs, in a species such as humans that are lightly specialised. Taxa which employ this strategy are unable to use this huge amount of microbial mass developing in their gut, these microbes being a significant source of protein, which can only be excreted, though fatty acids, the products of their fermentation, can be absorbed as short-chain fatty acids. Diverse groups such as tortoises, iguanas, agamids, sea turtles, herbivorous skinks, perissodactyls, such as horses, rhinos and tapirs), elephants, sirenians, koalas and wombats, which is concentrated considerably in the colon of these animals. Other hindgut sites that are found to be used as fermentation chambers are the paired blindsacs in birds, such as ostrich and grouse, the caecum in rodents, such as the capybara, nutria, guinea pigs, as well as many others, and lagomorphs such as rabbits. The strategy of fermentation in these taxa of mammals is often coupled with coprophagy (eating of excrement) which allows these animals to utilise the microbial protein that has accumulated in the gut.
The microbial fermentation chamber is located in the foregut among another herbivore group, the foregut fermenters. In these animals the microbes are utilised as an important source of protein, as well as producers of short-chain fatty acids for use by the animal; as they are washed out of the foregut into the stomach and small intestine where they are digested. It can be considered to be a slightly more complicated process, which occurs almost exclusively among specialised mammalian herbivores, such as camelids, hippos, peccaries, colobus monkeys, sloths, kangaroos, and to a certain extent, hamsters and voles. The hoatzin, a bird, is known to carry on intensive fermentation in its crop, which makes it a foregut fermenter, and the only bird known to use fermentation, otherwise it is a strategy that has been restricted to mammals (Grajal et al., 1969). There is no known evidence of foregut fermentation in reptiles.
It is believed by most authors that sauropods used hindgut fermentation, as is used by elephants and rhinos, taking the view that this is the most likely option. Hummel & Clauss suggest the sauropods could have used large blindsacs like the paired caecum of ostriches, given the relatedness of birds to dinosaurs. Hummel & Clauss suggests the solution being a foregut cannot be discarded completely on the rough basis of analogy as among the extant megaherbivores the hippo has fermentation being carried out in an extensive forestomach (Clauss et al., 2004). Both systems, hindgut fermentation in, e.g., howler monkeys, and foregut fermentation in, e.g., colobines, have evolved, which demonstrates that even in 1 taxonomic unit, the primates, 2 types of fermentation can evolve (Chivers & Hladik, 1980). The foregut fermentation system appears to be more complicated to evolve, Hummel & Clauss suggesting it should be noted that the majority of extinct and extant mammalian taxa are considered to have been, or are, hindgut fermenters. It is only when the physiological mechanism of rumination, regurgitation of the sorted contents of the forestomach which are then chewed again, did a high degree of species diversification result from the foregut fermentation system (ruminants and camelids) (Langer, 1994; Schwarm et al., 2009). According to Hummel & Clauss the foregut fermentation option is much less likely in sauropods without an efficient system of mastication.
Foregut fermentation in sauropods, the arguments against it
A number of authors (Farlow, 1987; Marshall & Stevens, 2000) have worked on the occurrence of foregut or hindgut fermentation in the dinosaurs. Hummel & Clauss have presented additional arguments that support their view that foregut fermentation among sauropods is particularly unlikely to have evolved.
An important restraint linked to the differential speed at which plant fibre on the one hand and soluble carbohydrates and other nutrients such as protein and fat on the other can be digested is represented by foregut fermentation. Bacterial fermentation and enzymatic digestions of soluble carbohydrates and fat are rapid processes (Hummel et al., 2006a). The bacterial fermentation of these substances represents a loss in energetic terms when compared to autoenzymatic digestion (Stevens & Hume, 1998). Bacterial fermentation of plant fibre, the major source of energy in obligate herbivores, in contrast to these rapid processes, requires a long time; therefore a longer retention time of ingesta is a characteristic of most herbivorous species (Stevens & Hume, 1998; Hummel et al., 2006b).
For any given gut system the retention time of ingesta is a function of food intake and the fraction that is indigestible; the more food that is ingested, the faster the food is moved through the gut (Clauss et al., 2007a, 2007b). In this respect a hindgut fermentation system is flexible, allowing for a low intake of food in, e.g., the rhinoceros, or a high food intake as in, e.g., the elephant (Clauss et al., 2008b). At any level of intake autoenzymatic digestion of soluble carbohydrates, proteins, fats in the small intestine will take place efficiently at any level of food intake, only the digestion of plant fibre in the large intestine will be affected by the level of intake, being higher at lower food intake levels, i.e., longer retention time, or at high food intake levels, i.e., shorter times of retention. In the latter case the lower digestibility of food can be compensated for by an intake of food that is generally higher. In contrast, a foregut fermentation system is limited to a relatively low intake of food. The bacterial flora of the forestomach will first ferment any ingested nutrient. The result of this is a lower energetic efficiency compared to autoenzymatic digestion in the case of soluble carbohydrate, protein or fat.
Whether the intake of food is high or low there will always be comparative energetic losses, as these easily digestible components are fermented rapidly. Plant fibre will be fermented less efficiently given a high food intake, and therefore a shorter retention time in the forestomach. A foregut fermenter that had a high intake of food would have the worst of both worlds: substrates that are easily digestible are lost to fermentation in the foregut, as fermentation is less efficient, so the short time of retention results in the plant fibre being used less efficiently. As a result of this the only logical option for foregut fermenters is having a food intake that is relatively low. Foregut fermentation is restricted to 1 of these options: low food intake and efficient use of fibre (Clauss et al., 2008b, 2010), though hindgut fermentation allows for the flexibility of either strategy: In regards to foregut fermenters only those that have also evolved rumination can achieve food intakes that are relatively high (Clauss et al., 2007a; Schwarm et al., 2009) because the forestomach can clear the fine (digested) particles of food selectively, while the larger food particles are still being digested.
Fats are saturated in the foregut before being absorbed
An important constraint linked to the differential speed of digestion of plant fibre on the one hand and soluble carbohydrates and other nutrients such as proteins or fat on the other is represented by foregut fermentation. Both enzymatic digestion and bacterial fermentation of soluble carbohydrates, protein and fats is a rapid process (Hummel et al, 2006a). Though in energetic terms, however, the fermentation of these substances by bacteria represents a loss when compared to autoenzymatic digestion (Stevens & Hume, 1998). Contrasting with these processes that are comparatively rapid, fermentation of plant fibre by bacteria, which is the major source of energy in obligate herbivores, is a slower process requiring more time, therefore a long retention of ingesta is characteristic of most species of herbivore (Stevens & Hume, 1998; Hummel et al., 2006b).
The time for which ingesta is retained for any give system is a function of food intake and the indigestible fraction: the more food ingested the faster the food is moved through the gut (Clauss et al., 007a; 2007b). In this respect a hindgut fermenting system is flexible, allowing for a low level of feed intake, rhinoceros, or a high level, such as the elephant, (Clauss et al., 2008b). Autoenzymatic digestion of soluble carbohydrates, proteins, and fat in the small intestine will operate efficiently whatever the level of food intake, and only the digestion of plant fibre in the large intestine will be affected by the level of food intake – higher at lower levels of intake (longer retention) or lower at higher food intake levels (shorter retention time). In the case of lower intake levels, the lower digestibility of fibre can be compensated for by a level of food intake that is generally higher. By contrast, a foregut fermentation system is limited to a relatively low intake of food, and any nutrient that is ingested will be fermented first by the bacteria in the forestomach, and therefore the result is a reduction of energetic efficiency compared to autoenzymatic digestion.
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