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动物学报 48 (1) :1~19 , 2002A cta Zoologica S inica
综 述
DIGESTIVE STRATEGIES OF MAMMALS
Ian D. Hume( School of Biological Sciences A 08 , U niversity of Sydney , NS W 2006 , A ust ralia)
Abstract Understanding an animal’s nutritional niche is fundamental to a full appreciation of its ecology , and is
important for both pest control and species conservation purposes. Carnivores have digestive systems dominated by the
small intestine , which can be related to the generally high digestibility of their food. Omnivores have more complex
gastrointestinal tracts , with a hindgut caecum in which some microbial fermentation takes place , and they have longer
mean retention times (MRTs) of digesta. The longest MRTs are found in herbivores , in which digesta are retained and
fermented by dense microbial populations in one or more regions of relative stasis. However , not all herbivores have
digestive systems that maximise fibre digestibility ; only ruminants , camelids and very large hindgut fermenters (rhinos ,
elephants) achieve this. Instead , many other herbivores (foregut fermenters such as kangaroos and small hindgut
fermenters such as rabbits , voles and possums) have digestive systems that sacrifice maximal fibre digestibility for a
capacity to process large amounts of forage , even when forage fibre content becomes very high. These different digestive
strategies result in the wide range of nutritional niches found among mammals.
Key words Carnivore , Herbivore , Omnivore , Caecum fermenter , Colon fermenter , Foregut fermenter , Mean
retention time , Digestive strategies
Received 19 May , 2001 ; revised 24 Oct . , 2001
Brief introduction to the f irst author Dr. Ian D. Hume , Challis Professor of Biology. Research interests : digestive physiology and nutritional
ecology of mammals and birds. E2mail : ianhume @bio. usyd. edu. au
1 Introduction
A fundamental aspect of an animal’s ecology is
its nutritional niche. The nutritional niche occupied
by any animal has two basic components : (a) what
it needs in the way of energy and specific nutrients
(i. e. its nutrient requirements) ; and ( b) how it
harvests and extracts those needed nutrients f rom the
food resources available to it ( its foraging and
digestive strategies) .
It is important to determine both the nutrient
requirements of a species and its digestive strategy in
order to gain a full understanding of its nutritional
ecology. With sound knowledge of its nutritional
niche and ecology , the manager is in a good position
from which to plan for either the conservation of a
threatened species or the population control of a pest
species. This paper reviews recent developments in
our understanding of the range of digestive strategies
found amongst the mammals.
Biologists have long been interested in the
concepts of optimal foraging strategies in animals (e.
g. Belovsky , 1978 ; Townsend et al . , 1981) and
optimal defence strategies against predation ( e. g.
Janzen , 1981 ; Rhoades , 1985 ) . Comparative
physiologists have more recently become interested in
optimal digestive strategies. Sibly (1981) was one of
the first to formalise the relationship between the rate
of net energy gain from a food with the time it is
retained in an animal’s gastrointestinal t ract . Hume
(1989) showed how this simple model of digestion
applied to high versus low quality foods ( Fig. 1) . In
the model , the net energy released is initially negative
until the food’s defences , such as the chitinous
exoskeleton of invertebrates or the lignified cell walls
of plants , are overcome (e. g. by mastication) . Then
follows a period of rapid digestion (of haemolymph
and the soft tissues of invertebrates , and the contents
of plant cells) , but eventually digestion rate declines
as digestion is progressively confined to less t ractable
dietary components such as the structural proteins of
animal tissues and the structural carbohydrates of
plant cell walls.
The mean retention time (MRT) of food in the
Fig. 1 Model of digestion in a continuous2flow system
A. A high quality B. A low quality food
Modified from Sibly (1981) by Hume (1989)
digestive tract is all important . MRT is measured
with inert , indigestible markers that associate with a
particular phase of the digesta , and is the average
time taken for a pulse dose of marker given by mouth
to appear in the faeces. It is the best single measure
of the rate of passage of food through the gut
(Warner , 1981) . If the MRT is too short the energy
spent by the animal in cracking the food’s defence
may not be recovered through digestion of the
animal’s soft tissues or the contents of plant cells. If
the MRT is too long the space in the animal’s gut
may be occupied by indigestible residues of a meal ,
inhibiting further food intake and limiting the rate of
net energy gain. Optimal MRT [ optimal digestion
time in Sibly’s (1981) model ] is given by the straight
line from the origin tangential to the curve. It is shorter
for high quality (easily digested) foods and longer for
lower quality foods. Therefore animals that utilise low
quality foods should have longer , more complex digestive
systems. They may also have lower metabolic rates
(McNab , 1986) and thus lower food requirements. Low
food intakes are usually associated with slow passage
through the gut (i. e. longer MRTs) .
2 Application of chemical reactor
theory to digestion
Although linear models of digesta passage have
been used by ruminant nutritionists for some time
(e. g. Waldo et al . , 1972 ; Mertens et al . , 1979 ;
Spalinger et al . , 1992) , it was the approach used by
Penry et al . (1986 , 1987) based on chemical reactor
theory that stimulated interest by comparative
physiologists in gut performance across a wide range
of animal taxa , including fish ( Horn et al . , 1992) ,
nectar2and fruit2eating birds ( Martinez del Rio et
al . , 1990 ) and mammalian herbivores ( Hume ,
1989) . The organisms of primary interest to Penry et
al . ( 1987 ) were various marine deposit feeders ,
which ingest and pass considerable quantities of
indigestible mud through their gut . This mud dilutes
nutrient concentrations and occupies a significant
proportion of total gut volume. Little of the ingested
volume is actually digested. Models developed for
such digestive systems find ready application in
mammalian herbivores as well , in which the time
taken to process the indigestible bulk of plant cell
walls can be a major constraint to rates of energy
acquisition.
Three basic types of chemical reactors have been
applied to animal digestive systems : batch reactors
(BR) , plug2flow reactors ( PFR) and mixed2flow or
continuous2flow , stirred2tank reactors ( CSTR )
( Fig. 2) . Batch reactors feature discontinuous flow
because they process reactants ( ingested food) in
discrete batches. In ideal batch reactors ( those thatcan be described accurately by simple equations) all
reactants are added simultaneously and are
continuously mixed. The reaction is allowed to
2 动 物 学 报 48 卷
proceed for a set period , after which reaction products
and un2reacted materials are all removed. The reactor
may then remain empty for a period or be refilled.
Extent of reaction can be high , depending on the time
Fig. 2 Models of three types of chemical reactors that have analogues in the mammalian digestive tract
A. Batch reactor , which describes the functioning of the carnivore stomach and other regions of the gut in which filling is discontinuous
B. Plug2flow reactor , which most closely describes performance of the small intestine
C. continuous2flow , stirred tank reactor (or mixed2flow reactor) , which is useful in modelling regions of microbial fermentation
From Hume (1999)
reactants are left in the reactor (i. e. the MRT) , but
material flow is interrupted and low overall , which
results in low production rate capabilities , unless
reactor volume is very high. Batch reactors usually
have only one opening , and many invertebrates such
as cnidarians like sea anemones have guts of this type.
Prey are ingested through the oral opening into the
gastrovascular cavity , where digestion occurs.
Undigested remnants are then ejected back through
the oral opening. However , batch processing can be
found in animals with complete digestive systems
(i. e. with two openings) as well. For instance , the
stomach of carnivores may operate more as a batch
reactor than any other type ; often , a large prey item
will be ingested and partially digested in the stomach.
Indigestible bones and hair may then be regurgitated
and expelled through the mouth , as seen in owls and
diurnal raptors. Batch2reactor guts may be flexible
under conditions of varying food supply , and can be
emptied and refilled quickly when better quality food
becomes available.
Cochran (1987) applied batch2reactor theory to
the problem of optimal MRT for carnivores that
partially consume individual prey. As the rate of net
energy uptake from an individual prey begins to
decline , a point is reached when it becomes more
profitable to search for and consume fresh prey. This
point is likely to increase as the mean interval
between meals increases. That is , how long a meal
should be retained depends on the availability of
subsequent meals. When food is continuously
available , optimal retention time is determined by the
energy invested in food acquisition and initial
processing. When food is scarce (i. e. the probability
31 期 Ian D. Hume : Digestive strategies of mammals
of obtaining a subsequent meal before the first is
completely digested is low) , the first meal should be
retained until the rate of net energy uptake falls close
to the rate of energy expenditure needed to maintain
an empty gut . The stomach of a carnivore that can be
emptied by regurgitation and refilled at intervals that
are related to prey availability operates as a batch
reactor.
Semi2batch reactors , which feature pulsed inputs
but continuous output ( Penry , 1993) , may be more
applicable to parts of the herbivore digestive system.
One type of semi2batch reactor , the partially
emptying batch reactor ( PEBR) has been suggested
by R. G. Lentle (pers. comm. ) to be particularly
applicable to the sacciform forestomach of kangaroos.
PEBRs empty only to a certain minimal level , which
ensures that an active inoculum of microbes is always
available to initiate digestion of incoming food.
Complete emptying of a herbivore’s fermentation
region would be inappropriate.
Of the two types of continuous2flow models
applied to the digestive tract of mammals , plug2flow
reactors ( PFRs) most closely approximate digesta
processing in the small intestine. PFRs feature
continuous , orderly flow of material through a usually
tubular reaction vessel. In ideal PFRs , material does
not mix along the flow axis , but there is perfect radial
mixing. Consequently , incoming food passes along
the tubular reactor as a plug which changes in
composition during its passage. At steady state there
is a continuous decline in reactant concentrations from
the inlet along the reactor to the outlet , and a
continuous increase in concentration of products. Plug
flow provides the greatest rate of digestive product
formation in the minimum of time and volume under
most conditions ( Penry et al . , 1987 ) , although
extent of digestion may be low unless the PFR is very
long. For these reasons PFRs are best suited to food
of high quality. Thus we find that animals that feed
on easily digested food , such as carnivores and
exudivores (animals that feed on plant exudates such
as sap and nectar) have digestive tracts dominated by
the small intestine (Caton et al . , 2000) . Generally ,
the more easily digested is the food the shorter is the
small intestine. The shortest small intestines are
found in nectar2feeding hummingbirds ( Karasov et
al . , 1986) and fruit bats ( Tedman et al . , 1985) .
Extremely long small intestines are found in sperm
whales ( that feed mainly on cephalopods ) and
dolphins (that feed on fish) (Stevens et al . , 1995) .
The small intestine deviates f rom an ideal PFR in
that digesta flow is pulsatile rather than continuous ,
radial mixing is not perfect , and there is considerable
axial mixing by alternate waves of antiperistaltic and
peristaltic contractions of the wall ( Weems , 1987) .
There is also secretion across the reactor wall f rom
blood to lumen , and absorption of water and solutes
f rom lumen into the portal blood ( Stevens et al . ,
1995) . J umars ( 2000) has modelled some of these
deviations from an ideal PFR.
The other type of continuous2flow chemical
reactor model , the continuous2flow , stirred2tank
reactor (CSTR) , features continuous flow through a
usually spherical reaction vessel of minimal volume.
In an ideal CSTR mixing is continuous. At steady
state , reactant concentrations are uniform throughout
the vessel and with time. Reactant concentration is
diluted immediately upon entry into the vessel by
materials recirculating in the reactor. This reduces
reaction rate , but extent of reaction can be high if
material flow through the reactor is slow enough (i.
e. if MRT is long enough) . CSTR2type gut regions
are particularly suited to processing of plant material ,
since the microbial fermentation required for the
digestion of plant cell walls is inherently slow. The
sacciform morphology of the ruminant forestomach
maximises MRT of digesta for fermentation and
results in high digestibilities of plant cell walls.
The disadvantage of a large single CSTR is the
dilution of incoming substrate by materials
recirculating in the reactor. This can be partially
overcome by dividing the same total volume among
several smaller CSTRs arranged in series ( Fig. 3) .
Incoming food is then diluted by a smaller quantity of
recirculating materials in the first CSTR , resulting in
higher rates of reaction. Reaction rate declines along
the series of CSTRs. The forestomach of kangaroos
and wallabies has a morphology that suggests such a
4 动 物 学 报 48 卷
Fig. 3 A linear series of continuous2flow, stirred2tank reactors ( CSTRs) reduces the problem of initial
dilution of incoming reactants with material re2circulating in the reactor , a limitation of large single
CSTRs. Such a reactor arrangement is seen in the forestomach of kangaroos and the proximal
colon of large hindgut fermenters such as the horse
reactor arrangement (Dellow et al . , 1983) . These
authors measured rates of fermentation along the
forestomach of two species of wallabies by assuming
that their forestomach consisted of four CSTRs in
series. Fermentation rate was highest in the first
CSTR (the sacciform region of the forestomach) , and
progressively declined distally along the tubiform
region. As the number of CSTRs in series increases
the performance of the system approaches that of a
PFR with significant axial mixing ( Martinez del Rio
et al . , 1994) . J umars (2000) calculated that there
is little difference in extent of hydrolysis or absorption
between a PFR and 10 CSTRs in series.
Although chemical reactor2based models of
digestive tract performance do not yet take account of
numerous important physiological and ecological
aspects of digestive strategies of animals , they are
fruitful analogies for digestive systems and provide a
sound conceptual base for examining and comparing
gut function across a wide range of animal taxa.
3 Digestive strategies of mammalian
carnivores
Carnivores are distinguished from other feeding
modes by their dentition and their relatively simple
digestive tract ( Fig. 4 ) . The carnivore dentition
usually emphasises the canines and premolars for
tearing and shearing of meat respectively. Incisors
may also be prominent (Stevens et al . , 1995) . The
canines of the upper jaw are usually enlarged , the
premolars tend to be tricuspidate and the molars
quadritubercular. The cheek teeth ( premolars and
molars) of small insectivores may be more complex ,
with many small cutting edges because of the effort
required to breach the barrier of the tough arthropod
exoskeleton.
The carnivore stomach is simple , without
diverticula , but can often be expanded to
accommodate large items of prey. The small intestine
is short , but nevertheless is the dominant feature of
the carnivore gut in most species ( Stevens et al . ,
1995) . The large intestine or hindgut is also short ,
with a small caecum and short , non2sacculated but
often wide colon. A hindgut caecum is absent in all
marsupial carnivores ( Hume , 1999 ) . Marine
carnivores differ f rom terrest rial carnivores by having
a much longer small intestine , but the reason for this
is unclear ( Stevens et al . , 1995) . In all carnivores
the main substrates for the gut microbes that
comprise the normal gut flora are endogenous
secretions ( mucus , sloughed mucosal cells , spent
digestive enzymes) . Although the end2products of
microbial fermentation in the carnivore gut are
probably unimportant in terms of their contribution to
the energy and nutrient status of the animal , the
indigenous microbes play an important role in
protecting the carnivore gut f rom invasion by
pathogenic species (Mackie , 1997) .
51 期 Ian D. Hume : Digestive strategies of mammals
Fig. 4 The gastrointestinal tracts of two carnivores , the cat and dog
From Stevens et al . (1995)
The relatively simple morphology of the digestive
tract of carnivores correlates with the generally high
digestibility of their food. If rate of digestion is high ,
MRT of food should be short ( Fig. 1 ) and the
optimal chemical reactor is a PFR , most closely
approximated in the digestive tract by the small
intestine ( Fig. 2) . A large stomach may be required
for storage of food , particularly in those species that
feed on large prey at infrequent intervals. Here the
stomach acts as a header tank , helping to maintain
continuous flow through the small intestine despite
pulsatile patterns of food ingestion. Total passage
times of 3 ~ 4 hours were recorded for 6 ~ 9 g
marsupial planigales (Read , 1987) , and for eutherian
shrews of similar size ( Pernetta , 1976) . Within the
marsupial carnivores , MRT increases with increasing
species adult body mass ( Table 1 ) , reflecting a
common gastrointestinal t ract plan but increasing
total t ract length with increasing body size. A similar
relationship is assumed to hold among eutherian
carnivores but few MRT data have been published.
Carnivores are distinguished not only by their
relatively simple digestive system but also by a suite
of metabolic adaptations to diets that are always high
in protein and in which vitamins are present in their
active metabolic form ( Morris , 1994 ) . Thus the
maintenance protein requirement of adult cats is 13 %
of the diet compared with 6 %~8 % for most adult non2carnivores; for maximal growth of kittens it is 20 %~
30 % of the diet . The higher protein requirement is to
supply nit rogen because the activities of urea2cycle
enzymes and amino2t ransferases are always high in
cats and do not respond to diets low in protein in
order to conserve nit rogen ( Rogers et al . , 1977) .
The low carbohydrate content of carnivorous diets
means that little hexose is normally absorbed from the
gut , and instead the animal’s requirements for
glucose are met largely from amino acids. Thus
hepatic activities of the enzymes involved in
gluconeogenesis are also always high.
Because of the high activity of their urea cycle ,
cats and dogs cannot synthesise enough arginine to
6 动 物 学 报 48 卷
Table 1 Mean retention time ( MRT) of fluid and particle markers in the
digestive tracts of carnivorous and omnivorous mammals
SpeciesBody mass
(kg)Diet
MRT (h)
Fluid ParticlesRef .
A. Carnivores
S mi nthopsis crassicaudata 0102 Insect - 019 1
( Fat2tailed dunnart)
S mi nthopsis douglasi 0107 Insect/ mincemeat 313 317 2
(J ulia Creek dunnart)
Dasycercus byrnei 0114 Insect - 115 1
( Kowari)
Dasyurus viverri nus 019~113 Insect/ small carnivore mix 1012 1012 3
( Eastern quoll)
B. Omnivores
U romys caudi maculat us 016~017 Rodent chow 4514 5515 4
( Giant white2tailed rat)
Perameles nasuta 017~018 Insect 2316 1112 3 5
(Long2nosed bandicoot) Plant 3311 2710 3
Macrotis lagotis 019~111 Insect 1719 2315 6
(Bilby) Seed 3012 3310
Isoodon macrourus 110~113 Insect 3014 2417 3 7
(Northern brown bandicoot) Plant 2714 1010 3
3 Selective retention of the fluid marker by a colonic separation mechanism (CSM) 2 see Section 7 (caecum fermenters) . References : 11 Dawson and
Paizs , in Hume (1999) 21 Hume , et al . (2000) 31 Moyle , in Hume (1999) 41 Comport et al . (1998) 51Moyle et al . (1995) 61Gibson
et al . (2000) 71 McClelland et al . (1999)
supply the urea cycle and thus arginine is an essential
amino acid for them ; most non2carnivores do not
require arginine in the diet as adults , although for
maximal growth a dietary source is needed. Another
requirement of cats is for taurine ( Hayes et al . ,
1975) . This amino acid is a metabolite of cysteine
oxidation and is present in all animal tissues. Cats and
dogs use taurine exclusively to conjugate bile acids ;
the taurine is excreted in the bile and degraded by
bacteria in the gut . This taurine must be replaced ,
but the rate of taurine synthesis in cats is limited , and
some is needed in the diet .
4 Digestive strategies of mammalian
omnivores
Omnivory means the ingestion of both animal
and plant ( and fungal ) material , with greater
amounts of indigestible residues being consumed.
This has at least two important nutritional
consequences. The first is the need for greater
lubrication to protect the mucosal lining of the
gastrointestinal t ract f rom physical damage during
passage of plant residues ( Hume et al . , 1980) . The
second is that plant residues provide an additional
substrate for bacteria and other microbes in the gut ,
primarily in the hindgut caecum. Thus , compared
with carnivores , the omnivore digestive tract usually
features an increased caecal capacity , as well as an
increase in length of the small intestine and in length
and diameter of the colon ( Fig. 5) .
The dentition of most omnivores reflects the
need to grind plant material as well as to tear animal
tissue. In some species that feed on non2st ructural
plant products such as nectar and pollen , sap and
gum , the emphasis on stabbing of invertebrate prey
results in a dentition that resembles that of
71 期 Ian D. Hume : Digestive strategies of mammals
Fig. 5 The gastrointestinal tract of an omnivore , the rat
From Stevens et al . (1995)
insectivores. In others , particularly primates , that
feed on plant leaves , petioles and stems as well as
meat there is a need for crushing ( when blunt
surfaces oppose each other) and grinding (crushing
with a translational motion) . This is reflected in
premolars and molars that are longer , higher crowned
and more heavily enamelled.
The longer and more complex gastrointestinal
t ract of most mammalian omnivores is reflected in
slower passage of digesta. The principal site of
digesta retention is usually the hindgut caecum ,
where microbial fermentation yields short2chain fatty
acids ( SCFA ) , microbial protein and B2vitamins.
Compared with herbivores , there is little quantitative
information available on microbial digestion in
mammalian omnivores. The MRT of inert fluid and
particulate markers in 200 g rats ranges from 12 to 35
hours , depending on diet ; the shorter MRTs are
associated with high2fibre forage diets , the longer
with low2fibre purified diets (Stevens et al . , 1995) .
Roughage stimulates gut motility ( Stevens et al . ,
1998) . Irrespective of diet , the passage of digesta
through the omnivore gastrointestinal t ract is
generally much slower than through that of a
carnivore of similar body size ( Table 1) .
5 Digestive strategies of mammalian
herbivores
Herbivory was defined by Stevens et al . (1995)
as the derivation of a significant proportion of an
animal’s energy and nutrient requirements f rom
structural components of plants (leaves , petioles and
stems) by the microbial fermentation of fibre. Fibre
is that f raction of plants that is resistant to digestion
and has a gut2filling effect while it is being processed
by the herbivore. It consists of lignin , cellulose and
hemicelluloses of plant cell walls that cannot be
digested by vertebrate enzymes. Instead , it is
digested by microbial fermentation at a slow rate
relative to other diet f ractions. This process takes
place in parts of the digestive tract where digesta are
retained for considerable periods , which allows time
for microbial growth to proceed.
However , there are several small mammals that
feed on plant leaves , stems and petioles yet do not
derive much energy from their st ructural
components. There are others that feed on other parts
of plants such as roots , bulbs , tubers , f ruit and
seeds. Although lower in fibre , some of these parts
contain non2st ructural polysaccharides that are
resistant to digestion in the small intestine , and
provide substrates for microbial fermentation in the
hindgut (large intestine) . These plant constituents ,
such as resistant starch and nonstarch storage
polysaccharides , are fermented at a faster rate than
refractory structural carbohydrates. Other plant
products that are generally readily digested in the
small intestine are also eaten by mammals ; these
products include nectar , pollen , sap and gums. Thus
the definition of herbivory can be much broader than
that of Stevens et al . (1995) .
8 动 物 学 报 48 卷
Table 2 Mammalian foregut fermenters ( digesta retention mainly in an expanded forestomach)
Order Family ExampleBody mass
(kg)
No.
species
Artiodactyla Tragulidae Chevrotains , mouse deer 2~17 4
Bovidae Antelope , cattle , sheep , goats 2~1 200 126
Giraffidae Giraffe , okapi 210~1 930 2
Cervidae Deer 8~800 36
Moschidae Musk deer 7~17 3
Tayassuidae Peccaries 17~43 3
Hippopotomidae Hippopotomus 180~3 200 2
Camelidae Camels and llamas 45~650 6
Marsupialia Potoroidae Rat2kangaroos 017~315 8
Macropodidae Kangaroos and wallabies 018~85 46
Edentata Megalonychidae Two2toed sloths 4~8 2
Bradypodidae Three2toed sloths 315~415 3
Primates Cercopithecidae
(Subfamily Colobinae) Colobus and leaf monkeys 3~24 37
Classification after Macdonald (1984) , body mass data from Macdonald (1984) (eutherians) and Strahan (1995) (marsupials)
6 Foregut fermenters
The main site of microbial fermentation in
relation to the small intestine is a natural basis on
which to group mammalian herbivores. The two
primary groups are foregut fermenters and hindgut
fermenters. In foregut fermenters the main site of
digesta retention , and therefore of microbial
fermentation , is an expanded fore2stomach. The
main groups of foregut fermenters are listed in Table
2. In nearly all foregut fermenters there is a
secondary site of microbial fermentation in the
proximal colon and/ or caecum of the hindgut , but the
hindgut makes only a minor contribution to the
energy economy of the animal compared to that made
by the foregut ( Hume et al . , 1980) .
Foregut fermenters can be subdivided on the
basis of the gross morphology of the forestomach. In
the artiodactyls ( the ruminants and camelids ,
peccaries and hippos ) , the forestomach consists
grossly of one or more sac2like diverticula. This
sacciform morphology maximises retention of digesta
for fermentation and results in high digestibility of
plant cell walls ( Freudenberger et al . , 1989 ) .
These are characteristics of a CSTR. However , only
in animals of at least 100 kg body mass are the energy
requirements for maintenance likely to be met by the
SCFA produced by the forestomach fermentation.
This is because small herbivores have high mass2specific metabolic rates but low absolute gut capacities
(Demment et al . , 1985) . Thus there is a need to
maintain high rates of fermentation and turnover of
the contents of the fermentation chamber. This need
dictates that the plant material selected must have a
high ratio of cell contents to cell walls. Even on such
rich diets , daily SCFA production in small ruminants
fails to meet the calculated maintenance energy
requirement of the animal ( Fig. 6) , let alone the
energy costs of growth and reproduction.
There are two possible explanations , not
mutually exclusive , for the obvious success of small
concentrate selectors of the Artiodactyl families
Tragulidae , Bovidae , Cervidae and Moschidae ( Table
1) . These small foregut fermenters must have lower
energy requirements than those calculated by Parra
(1978) ( see Fig. 6) or have alternative sources of
digestible energy. Maintenance energy requirements
have not been established experimentally for many
small wild ruminants , but Hofmann ( 1973 , 1988)
showed that in small ruminants there was opportunity
91 期 Ian D. Hume : Digestive strategies of mammals
Fig. 6 The relationship between fermentation rate ( Hoppe
1977) and body mass in ruminants compared with
the fermentation rate calculated by Parra ( 1978)
to be required to meet maintenance energy
requirements
Adapted by Hume (1989) from Van Soest (1982)
for significant amounts of ingested food to escape
microbial attack in the rumen. Among the Bovidae
the reticulomasal orifice of small concentrate selectors
such as duikers is wider , and the omasum is smaller
and with fewer laminae than in larger bulk and
roughage feeders ( grazers ) . In the even smaller
mouse deer (family Tragulidae) there is little if any
omasal tissue at all (Langer , 1988 ; Richardson et
al . , 1988) . These anatomical features allow ingesta
to bypass the rumen and pass rapidly through the
omasum to the abomasum and small intestine where
plant cell contents can be more efficiently digested by
the animal ’s own enzymes and absorbed as
monosaccharides and amino acids. This results in
significant increases in rates of net energy gain , and
helps to fill the gap in Fig. 6 between the rates of
energy release from forestomach fermentation
measured by Hoppe ( 1977 ) and calculated
maintenance energy requirements.
Large body size removes the problem of a
shortfall between rate of SCFA production and
estimated maintenance energy requirements and thus
the need for additional sources of absorbed energy and
nutrients. However , although mass2specific energy
requirements are lower , total energy and nutrient
requirements increase with increasing body mass.
These large total requirements cannot be met by
highly selective feeding behaviours because of the
wide spatial dist ribution of high cell content plant
material and the time that would be needed to harvest
it . For this reason large herbivores cannot afford to be
selective concentrate feeders. Instead , they need to
handle bulk plant material that is high in cell walls
but is more abundant and is more readily harvested.
A large fermentation chamber is consistent with the
need for prolonged retention of slowly fermenting
plant material that consists mainly of cell walls. This
cannot be achieved in a PFR , requiring instead some
form of CSTR ( Penry and J umars , 1987) or partially
emptying batch reactor ( PEBR) ( R. G. Lentle ,
pers. comm. ) .
Among the large foregut fermenters there appear
to be two alternative strategies for utilising plant
material of high cell wall content . Which strategy is
optimal depends primarily on the abundance of the
plant material. The first st rategy is that of the
ruminant system , which is designed for maximal cell
wall degradation in a minimal volume but not
necessarily for maximal material flow ( the single
CSTR or PEBR strategy) . These features of the
ruminant system are enhanced by the physiological
mechanism that involves the reticulo2omasal orifice
and results in prolonged retention of particles in the
reticulo2rumen until they have been broken down to a
certain size by rumination. An analogous large
particle retention system is found in the camelids ; it
involves the second and third compartments of the
stomach , and it is interesting that the camelids are
the only other foregut fermenters that ruminate
( Engelhardt et al . , 1987 ) . The strategy of
maximising extent rather than rate of cell wall
digestion would seem to be best suited to ecosystems
in which food availability is sometimes limited. Hume
et al . (1980) suggested that the special features of
the ruminant system , as opposed to the general
features shared by all foregut fermenters , evolved in
regions where quality and quantity of forage are either
seasonally or irregularly limiting , as in deciduous
forests and in hot and cold deserts. Foose ( 1982)
01 动 物 学 报 48 卷
added temperate grasslands to this list . Few present2day ruminants live in the sort of environments for
which their special ruminant adaptations evolved. In
contrast , all the modern representatives of the
Camelidae remain in either hot or cold arid
environments.
The second strategy of foregut fermenters is seen
in the large kangaroos , which are primarily grazers
( Hume , 1999) . In these herbivores the forestomach
is mainly tubiform rather than sacciform ( Fig. 7) ,
and is better compared to a series of smaller CSTRs
rather than a single large CSTR. The first reactor is
the sacciform region of the forestomach. This region
has been described by R. G. Lentle (pers. comm. )
as being more like a PEBR because of the
discontinuous pattern of food intake of kangaroos
(foraging activity peaks occur at dusk and dawn) and
changing levels of forestomach fill related to this
foraging strategy. Sequential CSTRs are found along
the length of the tubiform region of the forestomach.
Importantly , the special features of the ruminant
forestomach designed to maximise retention of large
particles are absent . The kangaroo strategy appears to
be designed for maximising material flow through the
fermentation chamber and maximising rate of
fermentation at the cost of plant cell wall digestion.
MRTs of particles are lower than in ruminants of
similar body size ( Hume , 1999) , and consequently
cell wall digestion is usually less complete. However ,
it means that food intake is less limited on forages of
high cell wall (fibre) content , as illust rated in the
model of food intake regulation in Fig. 81 In studies
by Foot and Romberg ( 1965) and Hollis ( 1984) ,
food intake fell significantly less in kangaroos than in
sheep as the quality of the forage was reduced. The
lower food intake by kangaroos on the higher quality
forage reflects their lower maintenance energy
requirements ( Hume , 1999) .
Another possible factor involved is nit rogen ; as
the fibre content increases as forages mature ,
nit rogen levels fall. Freudenberger et al . ( 1992 )
examined the effects of both increasing fibre content
and decreasing nit rogen content on food intake of
kangaroos and goats. Nit rogen had only a secondary
influence on food intake in both herbivores.
However , the effects of fibre content predicted by the
model in Fig. 8 were only seen when the diets were
ground and pelleted , and not when coarsely chopped.
They concluded that kangaroos can maintain higher
rates of intake of increasingly fibrous forages if the
constraint of mastication is removed by grinding and/
or pelleting the food offered. Many other factors
influence forage intake by the grazing animal through
their effects on such parameters as bite size , bite rate
and chewing time. Lentle et al . ( 1998 , 1999 )
examined some of these factors in small wallabies , but
more comparative studies in this area are needed.
Digestive strategies that emphasise the
maintenance of passage rate rather than maximising
extent of digestion are best suited to environments in
which forage is often of low quality but only rarely is
limiting in quantity. Such environments developed in
Australia in the Miocene (25~10 million years ago)
as the climate became drier and cooler and extensive
grasslands replaced forests ( Frakes et al . , 1987) .
Kangaroos appeared in the fossil record at the same
time. Similar changes occurred in the African
savannah (Janis , 1976) .
Like the smaller ruminants , small wallabies tend
to be concentrate selectors rather than grazers , and
have a relatively larger sacciform and a smaller
tubiform region of the forestomach than the large
kangaroos. A combination of higher mass2specific
energy requirements and smaller absolute forestomach
capacity rest ricts these herbivores to higher quality
forage.
7 Hindgut fermenters
In hindgut fermenters ingested food is first
subjected to digestion in a simple stomach and the
small intestine. Fermentation is largely confined to
the hindgut or large intestine. If there is any
fermentation in the stomach it is of a highly
specialised nature and limited in its nutritional
significance to the animal.
Hindgut fermenters can be divided into either
colon fermenters or caecum fermenters. In colon
fermenters ( Table 3) , all of which tend to be large
111 期 Ian D. Hume : Digestive strategies of mammals
Fig. 7 The gastrointestinal tracts of two foregut fermenters , the sheep and the kangaroo
From Stevens et al . (1995)
Fig. 8 The relationship between dry matter intake by
ruminants ( solid line ) and wallaroos or hill
kangaroos ( Macropus robustus ) ( broken line)
and cell wall content of chopped forages
Ruminant line from Van Soest ( 1965 ) . Sheep ( squares ) and
wallaroo (circles) data from Hollis (1984)
(more than 10 kg adult body mass) , the main site of
digesta retention is the proximal colon ( Fig. 9) . A
caecum may or may not be present ( Hume , 1989) . If
it is present , the caecum appears to function more2or2less as a simple extension of the proximal colon ; there
is mixing of digesta between the two regions , and
surgical removal of the caecum results in hypert rophy
of the proximal colon to compensate for the loss
(Sauer et al . , 1979 ; Wellard and Hume , 1981) .
The digestive strategy of the colon fermenters appears
to be similar in many respects to that adopted by the
large kangaroos. This is not unexpected , because the
principal fermentation chamber in each case is a
haustrated tubiform organ with characteristics of a
linear series of small CSTRs , albeit in the
forestomach of kangaroos but the colon of the large
hindgut fermenters ( Hume , 1989) .
Because of their low mass2specific energy and
nutrient requirements , colon fermenters can satisfy
most of their requirements for protein and other
specific nutrients by catalytic digestion in the small
intestine. Energy absorbed as hexoses , amino acids
and long2chain fatty acids from the small intestine is
supplemented by SCFA absorbed from the hindgut
after auto2catalytic digestion (microbial fermentation)
of plant cell walls. Extent of digestion of the cell
walls is usually less than in a ruminant of similar body
21 动 物 学 报 48 卷
Table 3 Mammalian colon fermenters ( digesta retention mainly in an expanded proximal colon)
Order Family ExampleBody mass
(kg)
No.
species
Artiodactyla Suidae Wild pigs and boars 6~275 9
Perissodactyla Equidae Horse , ass , zebra 275~405 7
Tapiridae Tapirs 225~300 4
Rhinocerotidae Rhinoceros 800~2 300 5
Proboscidea Elephantidae Elephants 3 000~6 000 2
Marsupialia Vombatidae Wombats 19~39 3
Sirenia Dugongidae Dugong 230~900 1
Trichechidae Manatees 350~1 600 3
Primates Cercopithecidae Guenons , macaques , baboons 017~50 45
Hylobatidae Gibbons 515~1015 9
Pongidae Great apes 30~180 4
Hominidae Humans 1
Classification after Macdonald (1984) , primate information from Caton (1997) , body mass data from Macdonald (1984)
Fig. 9 The gastrointestinal tracts of two hindgut fermenters , the pony ( a colon fermenter)
and the rabbit ( a caecum fermenter)
From Stevens and Hume (1995)
311 期 Ian D. Hume : Digestive strategies of mammals
size , for the same reasons advanced for kangaroos.
That is , the digestive strategy of the colon fermenters
emphasises the maintenance of food intake at the
expense of extent of digestion. However , food intake
falls significantly less than in ruminants of similar size
as forage quality declines (Van Soest , 1965 and Fig.
8) , as seen in horses (Darlington et al . , 1968) and
zebras ( Foose , 1982) .
The MRT of particles is greater than that of
fluids and solutes because of the selective retention of
large digesta particles by the haustra that are
characteristic of the proximal colon and the caecum.
The MRT of both digesta f ractions increases with
increasing body size. At very large body sizes (those
of elephants and rhinos) , absolute gut capacity is so
great and MRTs so long that the difference in extent
of fibre digestion between colon fermenters and
ruminants of similar body size disappears.
In contrast to colon fermenters , caecum
fermenters are generally small , less than 10 kg adult
body mass ( Table 4) , although the capybara at 45 kg
(Stevens et al . , 1995 ) is an obvious exception.
Microbial fermentation is more2or2less confined to an
expanded and often structurally complex caecum
( Fig. 9) . This organ operates as a CSTR or a semi2batch reactor , depending on the pattern of digesta
movement ( see below) . There may or may not be
some extension of microbial fermentation into the
proximal colon. As can be seen from Table 4 , caecum
fermentation is a widespread digestive strategy among
small mammals , both herbivore and omnivore.
Also in contrast to colon fermenters , there is no
relationship between body size of caecum fermenters
and extent of fibre digestion. The MRT of solute
markers is either similar to or longer than that of
particle markers. This is because of a colonic
separation mechanism (CSM) located in the proximal
colon (BjÊrnhag , 1987 ) . This mechanism returns
solutes and/ or very small particles , including
bacteria , to the caecum. The result is selective
Table 4 Mammalian caecum fermenters ( digesta retention mainly in an expanded hindgut caecum)
Order Family ExampleBody mass
(kg)
No.
species
Rodentia
Suborder Sciuromorpha (7 families) Squirrels , beavers , pocket gophers 0101~30 377
Suborder Myomorpha (5 families) Rats , mice , dormice , jerboas 0101~2 1 137
Suborder Caviomorpha (18 families) Cavies (guinea pigs) , porcupines , capybara 0118~64 188
Lagomorpha Leporidae Rabbits , hares 013~215 41
Ochotonidae Pikas 0108~013 14
Hyracoidea Procaviidae Hyraxes 113~514 11
Marsupialia Peramelidae Bandicoots and bilbies 012~311 17
Phalangeridae Brushtail possums , cuscuses 114~419 14
Pseudocheiridae Ringtail possums , greater glider 0115~210 16
Phascolarctidae Koala 5~12 1
Primates Daubentoniidae Aye2aye 3 1
Lemuridae Lemurs 015~10 10
Indriidae Indri and sifakas 315~10 4
Cheirogaleidae Dwarf and mouse lemurs 0105~0145 7
Lorisidae Loris , pottos , bush babies 0106~112 11
Cebidae Howler monkeys , capuchins 016~12 30
Callitrichidae Marmosets and tamarins 0112~0171 21
Classification after Macdonald (1984) , primate information from Caton (1997) , body mass data from Macdonald (1984) (eutherians) and Strahan
(1995) and Flannery (1995) (marsupials)
41 动 物 学 报 48 卷
retention of the solutes and fine particles in the
caecum , with facilitated passage of larger particles
distally through the colon. Because the larger
particles reaching the hindgut contain mainly plant
cell walls , their relatively rapid passage through the
fermentation chamber limits their exposure to
microbial action , and this explains why extent of
fibre digestion is highly variable among caecum
fermenters , and often low.
So far as we know , in all caecum fermenters
most of the digesta leaving the ileum (the distal end
of the small intestine) enter the caecum. Peristaltic
and antiperistaltic contractions mix them with
material already in the caecum. Digesta leaving the
caecum enters the proximal colon , the site of the
CSM. Not all caecum fermenters have a CSM , but
we do not yet have enough information to know how
widespread digesta separation in the proximal colon of
caecum fermenters is. There is a wide variety of
caecum fermenters dist ributed across 40 families and
five orders of the Mammalia ( Table 4) . So far two
types of CSM have been identified , the“mucus2t rap”
and the“wash2back”systems. In the“wash2back”
CSM , there is net secretion of fluid from blood into
the proximal colon. This washes out solutes and fine
particles f rom the larger particles and moves them
toward the haustrated wall , a process aided by intense
muscular activity of the colon (BjÊrnhag , 1994) . The
contents of the haustra are carried along the walls of
the proximal colon , by retrograde movement of the
haustra , at about 1 mm per second in rabbits
(BjÊrnhag , 1981) , into the caecum. The muscular
activity of the wall of the proximal colon that forms
and moves the haustra originates at the fusus coli , the
pacemaker located at the junction between proximal
and distal colon. This activity results in the
accumulation of fluid , solutes , bacteria and very small
food particles in the caecum , which has been
variously modelled as a CSTR ( Hume , 1989) , batch
reactor or semi2batch reactor ( Hume , 1999) . Net
absorption of fluid from the caecum balances its
secretion in the proximal colon , and completes an
“internal water cycle”.
At the same time , the larger particles in the
proximal colon move slowly in the centre of the lumen
toward the distal colon , propelled largely by outflow
from the caecum. This completes the separation of
the two components of the digesta. Many caecum
fermenters with a wash2back CSM are coprophagic
(they eat a certain proportion of their faeces) or even
caecotrophic ( they eat one type of faeces called
caecotrophes that originate f rom accumulated caecal
contents) . In caecotrophic species , while the CSM is
operating , usually during the active phase of the
animal , the larger particles passing into the distal
colon form the hard faecal pellets , which are not
eaten ; these are easily observed on the ground.
Then , during the rest phase , the CSM is switched
off , the caecum partially empties and caecotrophes or
soft faecal pellets are produced during one or a few
periods per day and are eaten directly from the anus.
It must be remembered that because most ileal
contents first enter the caecum , both hard and soft
faeces are of caecal origin , but the composition of the
hard pellets is modified drastically during passage
through the proximal colon (BjÊrnhag , 1994) . In
caecum fermenters with a“wash2back”CSM digesta
flow into and out of the caecum may be best modelled
as a semi2batch reactor because of the partial
emptying of the organ once or a few times per day.
In caecum fermenters with a“mucus2t rap”CSM
the lumen of part of the proximal colon is often nearly
completely divided into a main channel and a narrow
channel by mucosal folds ( Sperber et al . , 1983 ;
Takahashi and Sakaguchi , 2000) . Mucus secreted by
the walls of the proximal colon trap mainly bacteria
by means of an aggregating action of the mucus , but
chemotasis may also be involved (BjÊrnhag , 1994) .
The ensuring mixture of bacteria and mucus is
t ransported into the narrow channel and eventually
back to the caecum by antiperistaltic movements of
the wall. The bacteria and mucus mix with the caecal
contents , while food residues are passed on to the
distal colon and are voided as faecal pellets. The CSM
ceases for several periods of variable duration , and
when the colon is nearly empty the caecum is partially
evacuated and caecotrophes may be formed and eaten
in caecotrophic species. Nearly all myomorph rodents
511 期 Ian D. Hume : Digestive strategies of mammals
( Table 4) show the anatomical modifications of the
proximal colon suggestive of a mucus2t rap CSM ; the
only exceptions appear to belong to two carnivorous
genera (Sperber et al . , 1983) . Digesta flow into and
out of the caecum in animals with a“mucus2t rap”
CSM may be best modelled as a CSTR because of its
more continuous nature than in wash2back CSM
animals.
Fig. 10 The nutritional niches of hindgut fermenters in relation to dietary combinations of f ibre ( refractory structural
polysaccharides) and ( a) protein , and ( b) fermentable solutes ( starch , non2starch storage polysaccharides , pectin) .
CSM = colonic separation mechanism in the proximal colon that results in the selective retention of digesta in caecum
fermenters. Two types of foregut fermenters ( ruminants and kangaroos) are included in broken lines in (a) for comparison
From Cork et al . (1999)
The nutritional consequence of a CSM is the
concentration in an enlarged caecum of bacteria and
proteinaceous mucus in the mucus2t rap system or
bacteria , very small food particles and solutes in the
wash2back system. At the same time , in both
systems the more intractable components of the
digesta entering the hindgut are cleared from the
colon relatively rapidly. This has the important
consequence of alleviating the gut2filling effects of
plant cell walls , and allowing much higher intakes of
forage diets by these small mammals than would be
predicted purely on the basis of body mass. The
efficiency of the caecal fermentation system is
enhanced and , at least in coprophagic and
caecotrophic species , cellular products of the
fermentation ( microbial protein and B2vitamins) are
recycled to the stomach and small intestine. All
caecum fermenters benefit by the direct absorption of
the SCFA produced in the hindgut . The main
substrates utilised in the fermentation are not plant
cell walls but cell contents , particularly resistant
starch , non2starch storage polysaccharides , and
oligosaccharides , that have escaped digestion in the
small intestine , as well as endogenous secretions and
sloughed mucosal cells f rom the small intestine.
8 Conclusion
The mammalian digestive system is generally
simplest in carnivores , more complex in omnivores ,
and of greatest complexity in herbivores. The
carnivore digestive tract is dominated by the small
intestine irrespective of body size , and thus there is a
direct relationship between passage time or mean
retention time (MRT) of digesta and body size of the
carnivore.
In omnivores there is usually greater complexity
of the stomach and/ or the hindgut . Consequently
there is no simple relationship between digesta MRT
and body size. However , MRTs are generally longer
in omnivores than in carnivores of similar body size.
Such a digestive strategy correlates with the inclusion
of plant as well as animal material in the diet , and
with the lower rate of digestion of plant material.
Each of the three groups of mammalian
herbivores (foregut fermenters , colon fermenters and
caecum fermenters) has a different digestive strategy ,
and consequently each fills a specific nutritional niche
( Fig. 10) . Many of the foregut fermenters and the
61 动 物 学 报 48 卷
colon fermenters specialise on digestion of plant fibre ,
and fit most closely Stevens and Hume’s ( 1995 )
definition of herbivores. On the other hand , the
caecum fermenters specialise on fermentation of non2fibre components of the digesta leaving the small
intestine. Their capacity to retain plant cell walls for
the extended periods necessary for substantial
breakdown of the fibre is limited by their small body
size and thus small absolute gut capacity. Therefore
they feed on plant species and plant parts of lower cell
wall content , digest most of the cell contents in a
simple stomach and small intestine , and ferment any
cell contents that are resistant to catalytic digestion in
an enlarged caecum. However , many caecum
fermenters have a colonic separation mechanism in the
proximal colon that leads to the selective retention of
bacteria , and in some species solutes and small food
particles as well , in the caecum. At the same time the
elimination of large food particles is facilitated , which
alleviates the gut filling effect of plant cell walls ,
allowing these small mammals to utilise forages of
much higher cell wall content than would be predicted
on the basis of their small body size.
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中 文 摘 要
哺乳动物的消化策略
Ian D. Hume(悉尼大学生物科学学院 , NSW 2006 , 澳大利亚)
理解动物的营养生态位是充分理解其整个生态学的基础 , 对于害兽控制和物种保护也很重要。食肉动
物的小肠很发达 , 这可能与对食物的高消化能力有关 ; 杂食性动物有更复杂的胃肠器官 , 其后端有可进行
发酵的盲肠 , 消化物的平均滞留时间 (mean retention times , MRTs) 更长 ; 最长的平均滞留时间见于食
草动物 , 其消化道内高密度的微生物种群对不同滞留区内的消化物进行发酵。但是 , 并不是所有的食草动
物都能够最大程度地消化植物纤维 , 只有反刍动物、骆驼和个体较大的后肠发酵动物 (hindgut fermenter)
能够具有这种能力。对比而言 , 许多其它的食草动物 , 如前肠发酵的有袋类和小型的后肠发酵动物如兔
子、田鼠和负鼠等 , 它们具备可以使植物纤维消化效率最大的消化系统 , 可以在食物中的纤维素含量非常
高的情况下仍能处理大量的食物。这些不同的消化策略使哺乳动物具有广幅的营养生态位。
关键词 食肉动物 食草动物 杂食性动物 盲肠发酵动物 结肠发酵动物 前肠发酵动物 消化物平均
滞留时间 消化策略
911 期 Ian D. Hume : Digestive strategies of mammals
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