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Australia: The Land Where Time Began |
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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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Author: M.H.Monroe Email: admin@austhrutime.com Sources & Further reading |