动物学报 48 ( 1) :1～19 , 2002
A ct a Zoologica S i nica 综 述
D IGESTIVE STRATEGIES OF MAMMALS
Ian D. Hume
( School of Biological Sciences A 08 , U niversity of S y dney , N S 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 bot h pest control and species conservation purposes. Carnivores have digestive systems dominated by t he
small intestine , which can be related to t he generally high digestibility of t heir food. Omnivores have more complex
gastrointestinal tracts , wit h a hindgut caecum in which some microbial fermentation takes place , and t hey have longer
mean retention times ( MR Ts) of digesta. The longest MR Ts 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 t hat maximise fibre digestibility ; only ruminants , camelids and very large hindgut fermenters ( rhinos ,
elep hants) achieve t his. Instead , many ot her herbivores ( foregut fermenters such as kangaroos and small hindgut
fermenters such as rabbits , voles and possums) have digestive systems t hat 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 t he wide range of nutritional niches found among mammals.
Key words Carnivore , Herbivore , Omnivore , Caecum fermenter , Colon fermenter , Foregut fermenter , Mean
retention time , Digestive strategies
g. Belovsky , 1978 ; Townsend et al . , 1981 ) and
optimal defence st rategies against predation ( e. g.
1 Int roduction
A f undamental aspect of an animal ’s ecology is
J anzen ,
1981 ;
Rhoades ,
1985 ) .
Comparative
it s nut ritional niche. The nut ritional niche occupied
by any animal has two basic component s : ( a ) what
p hysiologist s have more recently become interested in
optimal digestive st rategies. Sibly ( 1981) was one of
it needs in t he way of energy and specific nut rient s
(i. e. it s nut rient requirement s ) ; and ( b ) how it
t he first to formalise t he relationship between t he rate
of net energy gain f rom a food wit h t he time it is
harvest s and ext ract s t hose needed nut rient s f rom t he
food resources available to it ( it s foraging and
retained in an animal ’s gast rointestinal t ract . Hume
(1989 ) showed how t his simple model of digestion
digestive st rategies) .
applied to high versus low quality foods ( Fig. 1) . In
It is important to determine bot h t he nut rient
t he model , t he net energy released is initially negative
requirement s of a species and it s digestive st rategy in
until t he food ’s defences , such as t he chitinous
order to gain a f ull understanding of it s nut ritional
exoskeleton of invertebrates or t he lignified cell walls
of plant s , are overcome ( e. g. by mastication) . Then
follows a period of rapid digestion ( of haemolymp h
ecology. Wit h sound knowledge of it s nut ritional
niche and ecology , t he manager is in a good position
f rom which to plan for eit her t he conservation of a
t hreatened species or t he population cont rol of a pest
and t he soft tissues of invertebrates , and t he content s
of plant cells) , but event ually digestion rate declines
species. This paper reviews recent develop ment s in
as digestion is progressively confined to less t ractable
our understanding of t he range of digestive st rategies
dietary component s such as t he st ruct ural proteins of
found amongst t he mammals.
animal tissues and t he st ruct ural carbohydrates of
Biologist s have long been interested in t he
concept s of optimal foraging st rategies in animals ( e.
plant cell walls.
The mean retention time ( MR T) of food in t he
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
2
动 物 学 报
48 卷
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 t ract is all important . MR T is measured
Spalinger et al . , 1992) , it was t he approach used by
wit h inert , indigestible markers t hat associate wit h a
Penry et al . ( 1986 , 1987) based on chemical reactor
particular p hase of t he digesta , and is t he average
t heory t hat
time taken for a pulse dose of marker given by mout h
to appear in t he faeces. It is t he best single measure
p hysiologist s in gut performance across a wide range
of animal taxa , including fish ( Horn et al . , 1992 ) ,
of t he rate of passage of food t hrough t he gut
( Warner , 1981) . If t he MR T is too short t he energy
nectar2and f ruit2eating birds ( Martinez del Rio et
al . , 1990 ) and mammalian herbivores ( Hume ,
spent by t he animal in cracking t he food ’s defence
may not be recovered t hrough digestion of t he
1989 ) . The organisms of primary interest to Penry et
al . ( 1987 ) were various marine deposit feeders ,
animal’s soft tissues or t he content s of plant cells. If
which ingest and pass considerable quantities of
t he MR T is too long t he space in t he animal ’s gut
indigestible mud t hrough t heir gut . This mud dilutes
may be occupied by indigestible residues of a meal ,
nut rient concent rations and occupies a significant
inhibiting f urt her food intake and limiting t he rate of
proportion of total gut volume. Little of t he ingested
net energy gain. Optimal MR T [ optimal digestion
time in Sibly’s ( 1981) model ] is given by the straight
volume is act ually digested. Models developed for
line from the origin tangential to the curve. It is shorter
for high quality ( easily digested ) foods and longer for
mammalian herbivores as well , in which t he time
taken to process t he indigestible bulk of plant cell
lower quality foods. Therefore animals that utilise low
walls can be a major const raint to rates of energy
quality foods should have longer , more complex digestive
acquisition.
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
t heory to digestion
Alt hough linear models of digesta passage have
been used by ruminant nut ritionist s for some time
( e. g. Waldo et al . , 1972 ; Mertens et al . , 1979 ;
stimulated interest
by comparative
such digestive systems find ready application in
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 feat ure discontinuous flow
because t hey process reactant s ( ingested food ) in
discrete batches. In ideal batch reactors ( t hose t hat
can be described accurately by simple equations) all
reactant s
are
added
continuously mixed.
simultaneously
and
are
The reaction is allowed to
1期
Ian D. Hume : Digestive strategies of mammals
3
proceed for a set period , after which reaction product s
Indigestible bones and hair may t hen be regurgitated
and un2reacted materials are all removed. The reactor
and expelled t hrough t he mout h , as seen in owls and
may t hen remain empty for a period or be refilled.
diurnal raptors. Batch2reactor gut s may be flexible
Extent of reaction can be high , depending on t he time
under conditions of varying food supply , and can be
reactant s are left in t he reactor (i. e. t he MR T) , but
emptied and refilled quickly when better quality food
material flow is interrupted and low overall , which
becomes available.
result s in low production rate capabilities , unless
Cochran ( 1987 ) applied batch2reactor t heory to
reactor volume is very high. Batch reactors usually
t he problem of optimal MR T for carnivores t hat
have only one opening , and many invertebrates such
partially consume individual prey. As t he rate of net
as cnidarians like sea anemones have gut s of t his type.
energy uptake f rom an individual prey begins to
Prey are ingested t hrough t he oral opening into t he
decline , a point is reached when it becomes more
gast rovascular
occurs.
profitable to search for and consume f resh prey. This
U ndigested remnant s are t hen ejected back t hrough
point is likely to increase as t he mean interval
t he oral opening. However , batch processing can be
between meals increases. That is , how long a meal
found in animals wit h complete digestive systems
should be retained depends on t he availability of
(i. e. wit h two openings) as well. For instance , t he
subsequent
stomach of carnivores may operate more as a batch
available , optimal retention time is determined by t he
reactor t han any ot her type ; often , a large prey item
energy invested in food acquisition and initial
processing. When food is scarce (i. e. t he probability
cavity ,
where
digestion
will be ingested and partially digested in t he stomach.
meals.
When food
is
continuously
Fig. 2 Models of three types of chemical reactors that have analogues in the mammalian digestive tract
A. Batch reactor , which describes t he functioning of t he carnivore stomach and ot her regions of t he gut in which filling is discontinuous
B. Plug2flow reactor , which most closely describes performance of t he small intestine
C. continuous2flow , stirred tank reactor (or mixed2flow reactor) , which is useful in modelling regions of microbial fermentation
From Hume (1999)
动 物 学 报
4
48 卷
of obtaining a subsequent meal before t he first is
small intestine.
The shortest small intestines are
completely digested is low ) , t he first meal should be
found in nectar2feeding hummingbirds ( Karasov et
retained until t he rate of net energy uptake falls close
al . , 1986 ) and f ruit bat s ( Tedman et al . , 1985 ) .
to t he rate of energy expendit ure needed to maintain
Ext remely long small intestines are found in sperm
an empty gut . The stomach of a carnivore t hat can be
whales ( t hat feed mainly on cep halopods ) and
emptied by regurgitation and refilled at intervals t hat
dolp hins ( t hat feed on fish) ( Stevens et al . , 1995) .
are related to prey availability operates as a batch
The small intestine deviates f rom an ideal PFR in
t hat digesta flow is pulsatile rat her t han continuous ,
reactor.
Semi2batch reactors , which feat ure pulsed input s
radial mixing is not perfect , and t here is considerable
but continuous output ( Penry , 1993 ) , may be more
axial mixing by alternate waves of antiperistaltic and
applicable to part s of t he herbivore digestive system.
peristaltic cont ractions of t he wall ( Weems , 1987 ) .
semi2batch
t he partially
There is also secretion across t he reactor wall f rom
emptying batch reactor ( PEBR ) has been suggested
by R. G. Lentle ( pers. comm. ) to be particularly
blood to lumen , and absorption of water and solutes
f rom lumen into t he portal blood ( Stevens et al . ,
applicable to t he sacciform forestomach of kangaroos.
1995) . J umars ( 2000 ) has modelled some of t hese
PEBRs empty only to a certain minimal level , which
deviations f rom an ideal PFR.
One type of
reactor ,
ensures t hat an active inoculum of microbes is always
The ot her type of continuous2flow chemical
available to initiate digestion of incoming food.
Complete emptying of a herbivore ’s fermentation
reactor model , t he continuous2flow , stirred2tank
reactor ( CSTR) , feat ures continuous flow t hrough a
region would be inappropriate.
usually sp herical reaction vessel of minimal volume.
Of t he two types of continuous2flow models
In an ideal CSTR mixing is continuous. At steady
applied to t he digestive t ract of mammals , plug2flow
reactors ( PFRs ) most closely approximate digesta
state , reactant concent rations are uniform t hroughout
t he vessel and wit h time. Reactant concent ration is
processing in t he small intestine.
PFRs feat ure
diluted immediately upon ent ry into t he vessel by
continuous , orderly flow of material t hrough a usually
materials recirculating in t he reactor. This reduces
t ubular reaction vessel. In ideal PFRs , material does
reaction rate , but extent of reaction can be high if
not mix along t he flow axis , but t here is perfect radial
mixing. Consequently , incoming food passes along
material flow t hrough t he reactor is slow enough ( i.
e. if MR T is long enough ) . CSTR2type gut regions
t he t ubular reactor as a plug which changes in
are particularly suited to processing of plant material ,
composition during it s passage. At steady state t here
since t he microbial fermentation required for t he
is a continuous decline in reactant concent rations f rom
digestion of plant cell walls is inherently slow. The
t he inlet along t he reactor to t he outlet , and a
sacciform morp hology of t he ruminant forestomach
continuous increase in concent ration of product s. Plug
maximises MR T of digesta for fermentation and
flow provides t he greatest rate of digestive product
result s in high digestibilities of plant cell walls.
formation in t he minimum of time and volume under
The disadvantage of a large single CSTR is t he
most conditions ( Penry et al . , 1987 ) , alt hough
dilution
extent of digestion may be low unless t he PFR is very
recirculating in t he reactor. This can be partially
long. For t hese reasons PFRs are best suited to food
overcome by dividing t he same total volume among
several smaller CSTRs arranged in series ( Fig. 3 ) .
of high quality. Thus we find t hat animals t hat feed
on easily digested food , such as carnivores and
exudivores ( animals t hat feed on plant exudates such
of
incoming
subst rate
by
materials
Incoming food is t hen diluted by a smaller quantity of
recirculating materials in t he first CSTR , resulting in
as sap and nectar) have digestive t ract s dominated by
t he small intestine ( Caton et al . , 2000) . Generally ,
t he series of CSTRs. The forestomach of kangaroos
t he more easily digested is t he food t he shorter is t he
and wallabies has a morp hology t hat suggest s such a
higher rates of reaction. Reaction rate declines along
1期
Ian D. Hume : Digestive strategies of mammals
5
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
canines of t he upper jaw are usually enlarged , t he
aut hors measured rates of fermentation along t he
premolars tend to be t ricuspidate and t he molars
forestomach of two species of wallabies by assuming
quadrit ubercular. The cheek teet h ( premolars and
t hat t heir forestomach consisted of four CSTRs in
molars) of small insectivores may be more complex ,
series. Fermentation rate was highest in t he first
wit h many small cutting edges because of t he effort
CSTR ( t he sacciform region of t he forestomach) , and
required to breach t he barrier of t he tough art hropod
progressively declined distally along t he t ubiform
exoskeleton.
region. As t he number of CSTRs in series increases
The carnivore stomach is simple , wit hout
t he performance of t he system approaches t hat of a
diverticula ,
but
can
often
be
expanded
to
PFR wit h significant axial mixing ( Martinez del Rio
et al . , 1994 ) . J umars ( 2000 ) calculated t hat t here
accommodate large items of prey. The small intestine
is short , but nevert heless is t he dominant feat ure of
is little difference in extent of hydrolysis or absorption
t he carnivore gut in most species ( Stevens et al . ,
between a PFR and 10 CSTRs in series.
1995) . The large intestine or hindgut is also short ,
models of
wit h a small caecum and short , non2sacculated but
digestive t ract performance do not yet take account of
often wide colon. A hindgut caecum is absent in all
numerous important p hysiological and ecological
marsupial carnivores
aspect s of digestive st rategies of animals , t hey are
carnivores differ f rom terrest rial carnivores by having
f ruitf ul analogies for digestive systems and provide a
sound concept ual base for examining and comparing
a much longer small intestine , but t he reason for t his
is unclear ( Stevens et al . , 1995 ) . In all carnivores
gut f unction across a wide range of animal taxa.
t he main subst rates for t he gut microbes t hat
3 Digestive st rategies of mammalian
carnivores
comprise t he normal gut flora are endogenous
Carnivores are distinguished f rom ot her feeding
microbial fermentation in t he carnivore gut are
modes by t heir dentition and t heir relatively simple
probably unimportant in terms of t heir cont ribution to
digestive t ract ( Fig. 4 ) . The carnivore dentition
t he energy and nut rient stat us of t he animal , t he
usually emp hasises t he canines and premolars for
indigenous microbes play an important
tearing and shearing of meat respectively. Incisors
may also be prominent ( Stevens et al . , 1995 ) . The
protecting t he carnivore gut f rom invasion by
Alt hough chemical
reactor2based
( Hume ,
1999 ) .
Marine
secretions ( mucus , sloughed mucosal cells , spent
digestive enzymes ) . Alt hough t he end2product s of
pat hogenic species ( Mackie , 1997) .
role in
6
动 物 学 报
48 卷
Fig. 4 The gastrointestinal tracts of t wo carnivores , the cat and dog
From Stevens et al . (1995)
The relatively simple morp hology of t he digestive
Carnivores are distinguished not only by t heir
t ract of carnivores correlates wit h t he generally high
relatively simple digestive system but also by a suite
digestibility of t heir food. If rate of digestion is high ,
of metabolic adaptations to diet s t hat are always high
MR T of food should be short ( Fig. 1 ) and t he
in protein and in which vitamins are present in t heir
active metabolic form ( Morris , 1994 ) . Thus t he
optimal chemical reactor is a PFR , most closely
approximated in t he digestive t ract by t he small
maintenance protein requirement of adult cat s is 13 %
intestine ( Fig. 2) . A large stomach may be required
of the diet compared with 6 %～8 % for most adult non2
for storage of food , particularly in t hose species t hat
carnivores; for maximal growth of kittens it is 20 %～
feed on large prey at inf requent intervals. Here t he
30 % of the diet. The higher protein requirement is to
stomach act s as a header tank , helping to maintain
supply nit rogen because t he activities of urea2cycle
continuous flow t hrough t he small intestine despite
enzymes and amino2t ransferases are always high in
times of 3 ～ 4 hours were recorded for 6 ～ 9 g
cat s and do not respond to diet s low in protein in
order to conserve nit rogen ( Rogers et al . , 1977 ) .
marsupial planigales ( Read , 1987) , and for eut herian
The low carbohydrate content of carnivorous diet s
shrews of similar size ( Pernetta , 1976 ) . Wit hin t he
means t hat little hexose is normally absorbed f rom t he
marsupial carnivores , MR T increases wit h increasing
species adult body mass ( Table 1 ) , reflecting a
gut , and instead t he animal ’s requirement s for
glucose are met largely f rom amino acids.
common gast rointestinal t ract plan but increasing
hepatic activities of
total t ract lengt h wit h increasing body size. A similar
gluconeogenesis are also always high.
pulsatile patterns of food ingestion. Total passage
relationship is assumed to hold among eut herian
carnivores but few MR T data have been published.
t he
enzymes
Thus
involved
in
Because of t he high activity of t heir urea cycle ,
cat s and dogs cannot synt hesise enough arginine to
1期
Ian D. Hume : Digestive strategies of mammals
7
Table 1 Mean retention time ( MRT) of fluid and particle markers in the
digestive tracts of carnivorous and omnivorous mammals
Species
MRT ( h)
Body mass
( kg)
Diet
Ref .
Fluid
Particles
-
019
1
313
317
2
-
115
1
A. Carnivores
S mi nt hopsis crassicaudata
0102
Insect
0107
Insect/ mincemeat
0114
Insect
( Fat2tailed dunnart)
S mi nt hopsis douglasi
(J ulia Creek dunnart)
Dasycercus by rnei
( Kowari)
Dasy urus viverri nus
019～113
Insect/ small carnivore mix
1012
1012
3
016～017
Rodent chow
4514
5515
4
017～018
Insect
2316
1112 3
5
Plant
3311
3
Insect
1719
2315
Seed
3012
3310
Insect
3014
2417 3
2714
3
( Eastern quoll)
B. Omnivores
U romys caudi m aculat us
( Giant white2tailed rat)
Perameles nasuta
(Long2nosed bandicoot)
M acrotis lagotis
019～111
(Bilby)
Isoodon m acrourus
110～113
(Nort hern brown bandicoot)
Plant
2710
1010
6
7
3 Selective retention of t he 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) 51 Moyle et al . (1995) 61 Gibson
et al . (2000) 71 McClelland et al . (1999)
supply t he urea cycle and t hus arginine is an essential
This
amino acid for t hem ; most non2carnivores do not
consequences.
require arginine in t he diet as adult s , alt hough for
lubrication to protect t he mucosal lining of t he
maximal growt h a dietary source is needed. Anot her
gast rointestinal t ract f rom p hysical damage during
requirement of cat s is for taurine ( Hayes et al . ,
1975) . This amino acid is a metabolite of cysteine
passage of plant residues ( Hume et al . , 1980 ) . The
oxidation and is present in all animal tissues. Cat s and
subst rate for bacteria and ot her microbes in t he gut ,
dogs use taurine exclusively to conjugate bile acids ;
primarily in t he hindgut caecum. Thus , compared
t he taurine is excreted in t he bile and degraded by
wit h carnivores , t he omnivore digestive t ract usually
bacteria in t he gut . This taurine must be replaced ,
feat ures an increased caecal capacity , as well as an
but t he rate of taurine synt hesis in cat s is limited , and
increase in lengt h of t he small intestine and in lengt h
some is needed in t he diet .
and diameter of t he colon ( Fig. 5) .
4 Digestive st rategies of mammalian
omnivores
Omnivory means t he ingestion of bot h animal
and plant ( and f ungal ) material , wit h greater
amount s of indigestible residues being consumed.
has
at
least
two
important
nut ritional
The first is t he need for greater
second is t hat plant residues provide an additional
The dentition of most omnivores reflect s t he
need to grind plant material as well as to tear animal
tissue. In some species t hat feed on non2st ruct ural
plant product s such as nectar and pollen , sap and
gum , t he emp hasis on stabbing of invertebrate prey
result s in a
dentition
t hat
resembles t hat
of
动 物 学 报
8
48 卷
hours , depending on diet ; t he shorter MR Ts are
associated wit h high2fibre forage diet s , t he longer
wit h low2fibre purified diet s ( Stevens et al . , 1995) .
Roughage stimulates gut motility ( Stevens et al . ,
1998 ) . Irrespective of diet , t he passage of digesta
t hrough
t he
omnivore
gast rointestinal
t ract
is
generally much slower t han t hrough t hat of a
carnivore of similar body size ( Table 1) .
5 Digestive st rategies of mammalian
herbivores
Herbivory was defined by Stevens et al . ( 1995)
as t he derivation of a significant proportion of an
animal ’s energy and nut rient requirement s f rom
st ruct ural component s of plant s ( leaves , petioles and
stems) by t he microbial fermentation of fibre. Fibre
is t hat f raction of plant s t hat is resistant to digestion
and has a gut2filling effect while it is being processed
by t he herbivore. It consist s of lignin , cellulose and
hemicelluloses of plant cell walls t hat cannot be
digested by vertebrate enzymes.
Instead , it is
digested by microbial fermentation at a slow rate
relative to ot her diet f ractions. This process takes
place in part s of t he digestive t ract where digesta are
retained for considerable periods , which allows time
Fig. 5 The gastrointestinal tract of an omnivore , the rat
From Stevens et al . (1995)
for microbial growt h to proceed.
However , t here are several small mammals t hat
insectivores. In ot hers , particularly primates , t hat
feed on plant leaves , stems and petioles yet do not
feed on plant leaves , petioles and stems as well as
meat t here is a need for crushing ( when blunt
derive
much
energy
f rom
t heir
st ruct ural
component s. There are ot hers t hat feed on ot her part s
surfaces oppose each ot her ) and grinding ( crushing
wit h a t ranslational motion ) . This is reflected in
of plant s such as root s , bulbs , t ubers , f ruit and
premolars and molars t hat are longer , higher crowned
contain
seeds. Alt hough lower in fibre , some of t hese part s
non2st ruct ural
polysaccharides
t hat
are
resistant to digestion in t he small intestine , and
and more heavily enamelled.
The longer and more complex gast rointestinal
provide subst rates for microbial fermentation in t he
t ract of most mammalian omnivores is reflected in
hindgut ( large intestine ) . These plant constit uent s ,
slower passage of digesta.
such as resistant
The principal site of
starch and nonstarch storage
digesta retention is usually t he hindgut caecum ,
polysaccharides , are fermented at a faster rate t han
where microbial fermentation yields short2chain fatty
acids ( SCFA ) , microbial protein and B2vitamins.
ref ractory st ruct ural carbohydrates.
product s t hat are generally readily digested in t he
Compared wit h herbivores , t here is little quantitative
small intestine are also eaten by mammals ; t hese
information available on
digestion in
product s include nectar , pollen , sap and gums. Thus
mammalian omnivores. The MR T of inert fluid and
t he definition of herbivory can be much broader t han
particulate markers in 200 g rat s ranges f rom 12 to 35
t hat of Stevens et al . ( 1995) .
microbial
Ot her plant
1期
Ian D. Hume : Digestive strategies of mammals
9
Table 2 Mammalian foregut fermenters ( digesta retention mainly in an expanded forestomach)
Order
Family
Artiodactyla
Marsupialia
Edentata
Primates
Example
Body mass
No.
( kg)
species
2～17
4
2～1 200
126
210～1 930
2
Tragulidae
Chevrotains , mouse deer
Bovidae
Antelope , cattle , sheep , goats
Giraffidae
Giraffe , okapi
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
Potoroidae
Rat2kangaroos
017～315
8
Macropodidae
Kangaroos and wallabies
018～85
46
Megalonychidae
Two2toed slot hs
4～8
2
Bradypodidae
Three2toed slot hs
315～415
3
3～24
37
Cercopit hecidae
( Subfamily Colobinae)
Colobus and leaf monkeys
Classification after Macdonald (1984) , body mass data from Macdonald (1984) (eut herians) and Strahan (1995) ( marsupials)
in animals of at least 100 kg body mass are t he energy
6 Foregut fermenters
requirement s for maintenance likely to be met by t he
The main site of microbial fermentation in
SCFA produced by t he forestomach fermentation.
relation to t he small intestine is a nat ural basis on
This is because small herbivores have high mass2
which to group mammalian herbivores.
The two
specific metabolic rates but low absolute gut capacities
primary groups are foregut fermenters and hindgut
(Demment et al . , 1985 ) . Thus t here is a need to
fermenters. In foregut fermenters t he main site of
maintain high rates of fermentation and t urnover of
digesta
t he content s of t he fermentation chamber. This need
retention ,
and
t herefore
of
microbial
fermentation , is an expanded fore2stomach.
The
dictates t hat t he plant material selected must have a
main groups of foregut fermenters are listed in Table
high ratio of cell content s to cell walls. Even on such
2.
In nearly all foregut fermenters t here is a
rich diet s , daily SCFA production in small ruminant s
secondary site of microbial fermentation in t he
proximal colon and/ or caecum of t he hindgut , but t he
fails to meet t he calculated maintenance energy
requirement of t he animal ( Fig. 6 ) , let alone t he
hindgut makes only a minor cont ribution to t he
energy cost s of growt h and reproduction.
energy economy of t he animal compared to t hat made
by t he foregut ( Hume et al . , 1980) .
mut ually exclusive , for t he obvious success of small
Foregut fermenters can be subdivided on t he
concent rate selectors of t he Artiodactyl families
basis of t he gross morp hology of t he forestomach. In
t he artiodactyls ( t he ruminant s and camelids ,
peccaries and hippos ) , t he forestomach consist s
Tragulidae , Bovidae , Cervidae and Moschidae ( Table
1) . These small foregut fermenters must have lower
There are
two
possible
explanations ,
not
This
energy requirement s t han t hose calculated by Parra
(1978) ( see Fig. 6 ) or have alternative sources of
sacciform morp hology maximises retention of digesta
digestible energy. Maintenance energy requirement s
for fermentation and result s in high digestibility of
have not been established experimentally for many
plant cell walls ( Freudenberger et al . , 1989 ) .
small wild ruminant s , but Hof mann ( 1973 , 1988 )
These are characteristics of a CSTR. However , only
showed t hat in small ruminant s t here was opport unity
grossly of one or more sac2like diverticula.
动 物 学 报
10
48 卷
requirement s increase wit h increasing body mass.
These large total requirement s cannot be met by
highly selective feeding behaviours because of t he
wide spatial dist ribution of high cell content plant
material and t he time t hat would be needed to harvest
it . For t his reason large herbivores cannot afford to be
selective concent rate feeders. Instead , t hey need to
handle bulk plant material t hat is high in cell walls
but is more abundant and is more readily harvested.
A large fermentation chamber is consistent wit h t he
need for prolonged retention of slowly fermenting
plant material t hat consist s mainly of cell walls. This
Fig. 6 The relationship bet ween fermentation rate ( Hoppe
cannot be achieved in a PFR , requiring instead some
form of CSTR ( Penry and J umars , 1987) or partially
1977) and body mass in ruminants compared with
emptying batch reactor ( PEBR ) ( R.
the fermentation rate calculated by Parra ( 1978)
pers. comm. ) .
to be required to meet maintenance energy
requirements
G. Lentle ,
Among t he large foregut fermenters t here appear
to be two alternative st rategies for utilising plant
Adapted by Hume (1989) from Van Soest (1982)
for significant amount s of ingested food to escape
material of high cell wall content . Which st rategy is
optimal depends primarily on t he abundance of t he
microbial attack in t he rumen. Among t he Bovidae
plant material.
t he reticulomasal orifice of small concent rate selectors
ruminant system , which is designed for maximal cell
such as duikers is wider , and t he omasum is smaller
wall degradation in a minimal volume but not
and wit h fewer laminae t han in larger bulk and
roughage feeders ( grazers ) . In t he even smaller
necessarily for maximal material flow ( t he single
mouse deer ( family Tragulidae ) t here is little if any
omasal tissue at all ( Langer , 1988 ; Richardson et
al . , 1988 ) . These anatomical feat ures allow ingesta
The first st rategy is t hat of t he
CSTR or PEBR st rategy ) . These feat ures of t he
ruminant system are enhanced by t he p hysiological
mechanism t hat involves t he reticulo2omasal orifice
and result s in prolonged retention of particles in t he
to bypass t he rumen and pass rapidly t hrough t he
reticulo2rumen until t hey have been broken down to a
omasum to t he abomasum and small intestine where
certain size by rumination.
plant cell content s can be more efficiently digested by
particle retention system is found in t he camelids ; it
t he animal ’ s own enzymes and absorbed as
involves t he second and t hird compart ment s of t he
monosaccharides and amino acids. This result s in
stomach , and it is interesting t hat t he camelids are
significant increases in rates of net energy gain , and
t he only ot her foregut fermenters t hat ruminate
helps to fill t he gap in Fig. 6 between t he rates of
( Engelhardt
energy
maximising extent rat her t han rate of cell wall
measured
release
by
f rom
Hoppe
forestomach fermentation
( 1977 ) and calculated
maintenance energy requirement s.
et
An analogous large
al . , 1987 ) .
The st rategy of
digestion would seem to be best suited to ecosystems
in which food availability is sometimes limited. Hume
Large body size removes t he problem of a
et al . ( 1980 ) suggested t hat t he special feat ures of
shortfall between rate of SCFA production and
t he ruminant system , as opposed to t he general
estimated maintenance energy requirement s and t hus
feat ures shared by all foregut fermenters , evolved in
t he need for additional sources of absorbed energy and
regions where quality and quantity of forage are eit her
nut rient s. However , alt hough mass2specific energy
seasonally or irregularly limiting , as in deciduous
requirement s are lower , total energy and nut rient
forest s and in hot and cold desert s. Foose ( 1982 )
1期
Ian D. Hume : Digestive strategies of mammals
11
added temperate grasslands to t his list . Few present2
influence on food
day ruminant s live in t he sort of environment s for
However , t he effect s of fibre content predicted by t he
which t heir special ruminant adaptations evolved. In
model in Fig. 8 were only seen when t he diet s were
cont rast , all t he modern representatives of t he
ground and pelleted , and not when coarsely chopped.
Camelidae remain in eit her
hot
or
cold
arid
environment s.
intake
in
bot h
herbivores.
They concluded t hat kangaroos can maintain higher
rates of intake of increasingly fibrous forages if t he
The second st rategy of foregut fermenters is seen
const raint of mastication is removed by grinding and/
in t he large kangaroos , which are primarily grazers
or pelleting t he food offered. Many ot her factors
( Hume , 1999) . In t hese herbivores t he forestomach
is mainly t ubiform rat her t han sacciform ( Fig. 7 ) ,
influence forage intake by t he grazing animal t hrough
and is better compared to a series of smaller CSTRs
and chewing time. Lentle et al .
rat her t han a single large CSTR. The first reactor is
examined some of t hese factors in small wallabies , but
t he sacciform region of t he forestomach. This region
has been described by R. G. Lentle ( pers. comm. )
more comparative st udies in t his area are needed.
as being
t he
maintenance of passage rate rat her t han maximising
discontinuous pattern of food intake of kangaroos
(foraging activity peaks occur at dusk and dawn) and
extent of digestion are best suited to environment s in
changing levels of forestomach fill related to t his
foraging st rategy. Sequential CSTRs are found along
limiting in quantity. Such environment s developed in
Aust ralia in t he Miocene ( 25 ～ 10 million years ago )
t he lengt h of t he t ubiform region of t he forestomach.
as t he climate became drier and cooler and extensive
Importantly , t he special feat ures of t he ruminant
grasslands replaced forest s ( Frakes et al . , 1987 ) .
forestomach designed to maximise retention of large
Kangaroos appeared in t he fossil record at t he same
particles are absent . The kangaroo st rategy appears to
time.
be designed for maximising material flow t hrough t he
savannah (J anis , 1976) .
more like a
PEBR
because of
t heir effect s on such parameters as bite size , bite rate
Digestive
st rategies
t hat
( 1998 , 1999 )
emp hasise
t he
which forage is often of low quality but only rarely is
Similar changes occurred in t he Af rican
of
Like t he smaller ruminant s , small wallabies tend
fermentation at t he cost of plant cell wall digestion.
to be concent rate selectors rat her t han grazers , and
MR Ts of particles are lower t han in ruminant s of
similar body size ( Hume , 1999 ) , and consequently
have a relatively larger sacciform and a smaller
t ubiform region of t he forestomach t han t he large
cell wall digestion is usually less complete. However ,
kangaroos. A combination of higher mass2specific
it means t hat food intake is less limited on forages of
energy requirement s and smaller absolute forestomach
high cell wall ( fibre ) content , as illust rated in t he
capacity rest rict s t hese herbivores to higher quality
model of food intake regulation in Fig. 81 In st udies
by Foot and Romberg ( 1965 ) and Hollis ( 1984 ) ,
forage.
fermentation chamber
and
maximising
rate
food intake fell significantly less in kangaroos t han in
7 Hindgut fermenters
sheep as t he quality of t he forage was reduced. The
In hindgut fermenters ingested food is first
lower food intake by kangaroos on t he higher quality
subjected to digestion in a simple stomach and t he
forage reflect s t heir lower
requirement s ( Hume , 1999) .
small intestine. Fermentation is largely confined to
maintenance
energy
t he hindgut or large intestine.
If t here is any
Anot her possible factor involved is nit rogen ; as
fermentation in t he stomach it is of a highly
t he fibre content increases as forages mat ure ,
specialised nat ure and limited in it s nut ritional
nit rogen levels fall. Freudenberger et al . ( 1992 )
significance to t he animal.
examined t he effect s of bot h increasing fibre content
Hindgut fermenters can be divided into eit her
and decreasing nit rogen content on food intake of
colon fermenters or caecum fermenters.
In colon
kangaroos and goat s. Nit rogen had only a secondary
fermenters ( Table 3 ) , all of which tend to be large
动 物 学 报
12
48 卷
Fig. 7 The gastrointestinal tracts of t wo foregut fermenters , the sheep and the kangaroo
From Stevens et al . (1995)
surgical removal of t he caecum result s in hypert rop hy
of t he proximal colon to compensate for t he loss
( Sauer et al . , 1979 ; Wellard and Hume , 1981 ) .
The digestive st rategy of t he colon fermenters appears
to be similar in many respect s to t hat adopted by t he
large kangaroos. This is not unexpected , because t he
principal fermentation chamber in each case is a
haust rated t ubiform organ wit h characteristics of a
linear
Fig. 8 The relationship bet ween dry matter intake by
ruminants ( solid line ) and wallaroos or hill
kangaroos ( Macropus robust us ) ( broken line )
series of
small
CSTRs ,
albeit
in
t he
forestomach of kangaroos but t he colon of t he large
hindgut fermenters ( Hume , 1989) .
Because of t heir low mass2specific energy and
and cell wall content of chopped forages
nut rient requirement s , colon fermenters can satisfy
Ruminant line from Van Soest ( 1965 ) . Sheep ( squares ) and
most of t heir requirement s for protein and ot her
wallaroo (circles) data from Hollis (1984)
specific nut rient s by catalytic digestion in t he small
( more t han 10 kg adult body mass) , t he main site of
digesta retention is t he proximal colon ( Fig. 9 ) . A
intestine. Energy absorbed as hexoses , amino acids
caecum may or may not be present ( Hume , 1989) . If
supplemented by SCFA absorbed f rom t he hindgut
it is present , t he caecum appears to f unction more2or2
after auto2catalytic digestion ( microbial fermentation)
less as a simple extension of t he proximal colon ; t here
of plant cell walls. Extent of digestion of t he cell
is mixing of digesta between t he two regions , and
walls is usually less t han in a ruminant of similar body
and long2chain fatty acids f rom t he small intestine is
1期
Ian D. Hume : Digestive strategies of mammals
13
Table 3 Mammalian colon fermenters ( digesta retention mainly in an expanded proximal colon)
Order
Family
Example
Body mass
No.
( kg)
species
6～275
9
Artiodactyla
Suidae
Wild pigs and boars
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
Cercopit hecidae
Guenons , macaques , baboons
017～50
45
515～1015
9
30～180
4
Primates
Hylobatidae
Gibbons
Pongidae
Great apes
Hominidae
Humans
1
Classification after Macdonald (1984) , primate information from Caton (1997) , body mass data from Macdonald (1984)
Fig. 9 The gastrointestinal tracts of t wo hindgut fermenters , the pony ( a colon fermenter)
and the rabbit ( a caecum fermenter)
From Stevens and Hume (1995)
动 物 学 报
14
48 卷
That is , t he digestive st rategy of t he colon fermenters
body mass ( Table 4) , alt hough t he capybara at 45 kg
( Stevens et al . , 1995 ) is an obvious exception.
emp hasises t he maintenance of food intake at t he
Microbial fermentation is more2or2less confined to an
expense of extent of digestion. However , food intake
expanded and often st ruct urally complex caecum
falls significantly less t han in ruminant s of similar size
( Fig. 9) . This organ operates as a CSTR or a semi2
as forage quality declines ( Van Soest , 1965 and Fig.
batch reactor , depending on t he pattern of digesta
8) , as seen in horses ( Darlington et al . , 1968 ) and
zebras ( Foose , 1982) .
movement ( see below ) . There may or may not be
some extension of microbial fermentation into t he
The MR T of particles is greater t han t hat of
proximal colon. As can be seen f rom Table 4 , caecum
fluids and solutes because of t he selective retention of
fermentation is a widespread digestive st rategy among
large digesta particles by t he haust ra t hat are
small mammals , bot h herbivore and omnivore.
size , for t he same reasons advanced for kangaroos.
characteristic of t he proximal colon and t he caecum.
Also in cont rast to colon fermenters , t here is no
The MR T of bot h digesta f ractions increases wit h
increasing body size. At very large body sizes ( t hose
relationship between body size of caecum fermenters
and extent of fibre digestion. The MR T of solute
of elep hant s and rhinos) , absolute gut capacity is so
markers is eit her similar to or longer t han t hat of
great and MR Ts so long t hat t he difference in extent
particle markers.
of fibre digestion between colon fermenters and
separation mechanism ( CSM) located in t he proximal
ruminant s of similar body size disappears.
colon ( Bjgrnhag , 1987 ) . This mechanism ret urns
In
cont rast
to
colon
fermenters ,
caecum
fermenters are generally small , less t han 10 kg adult
solutes and/ or
This is because of a colonic
very
small
bacteria , to t he caecum.
particles ,
including
The result is selective
Table 4 Mammalian caecum fermenters ( digesta retention mainly in an expanded hindgut caecum)
Order
Family
Example
Body mass
No.
( kg)
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
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
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
Lagomorpha
Primates
Classification after Macdonald (1984) , primate information from Caton (1997) , body mass data from Macdonald ( 1984) (eut herians) and Strahan
(1995) and Flannery (1995) ( marsupials)
1期
Ian D. Hume : Digestive strategies of mammals
15
retention of t he solutes and fine particles in t he
proximal colon move slowly in t he cent re of t he lumen
caecum , wit h facilitated passage of larger particles
toward t he distal colon , propelled largely by outflow
distally t hrough t he colon.
Because t he larger
f rom t he caecum. This completes t he separation of
particles reaching t he hindgut contain mainly plant
t he two component s of t he digesta. Many caecum
cell walls , t heir relatively rapid passage t hrough t he
fermenters wit h a wash2back CSM are coprop hagic
fermentation chamber
to
( t hey eat a certain proportion of t heir faeces) or even
microbial action , and t his explains why extent of
caecot rop hic ( t hey eat one type of faeces called
fibre digestion is highly variable among caecum
caecot rop hes t hat originate f rom accumulated caecal
fermenters , and often low.
content s) . In caecot rop hic species , while t he CSM is
limit s
t heir
exposure
So far as we know , in all caecum fermenters
operating , usually during t he active p hase of t he
most of t he digesta leaving t he ileum ( t he distal end
animal , t he larger particles passing into t he distal
of t he small intestine ) enter t he caecum. Peristaltic
colon form t he hard faecal pellet s , which are not
and antiperistaltic cont ractions
wit h
eaten ; t hese are easily observed on t he ground.
material already in t he caecum. Digesta leaving t he
Then , during t he rest p hase , t he CSM is switched
caecum enters t he proximal colon , t he site of t he
off , t he caecum partially empties and caecot rop hes or
CSM. Not all caecum fermenters have a CSM , but
soft faecal pellet s are produced during one or a few
we do not yet have enough information to know how
periods per day and are eaten directly f rom t he anus.
widespread digesta separation in t he proximal colon of
It must be remembered t hat because most ileal
mix
t hem
caecum fermenters is. There is a wide variety of
content s first enter t he caecum , bot h hard and soft
caecum fermenters dist ributed across 40 families and
faeces are of caecal origin , but t he composition of t he
five orders of t he Mammalia ( Table 4 ) . So far two
hard pellet s is modified drastically during passage
types of CSM have been identified , t he“mucus2t rap ”
t hrough t he proximal colon ( Bjgrnhag , 1994 ) . In
and t he “wash2back ”systems. In t he “wash2back ”
caecum fermenters wit h a“wash2back ”CSM digesta
CSM , t here is net secretion of fluid f rom blood into
flow into and out of t he caecum may be best modelled
t he proximal colon. This washes out solutes and fine
as a semi2batch reactor because of t he partial
particles f rom t he larger particles and moves t hem
emptying of t he organ once or a few times per day.
toward t he haust rated wall , a process aided by intense
muscular activity of t he colon (Bjgrnhag , 1994) . The
content s of t he haust ra are carried along t he walls of
t he proximal colon , by ret rograde movement of t he
haust ra , at about 1 mm per second in rabbit s
( Bjgrnhag , 1981 ) , into t he caecum. The muscular
In caecum fermenters wit h a“mucus2t rap ”CSM
t he lumen of part of t he 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
t he walls of t he proximal colon t rap mainly bacteria
and moves t he haust ra originates at t he f usus coli , t he
by means of an aggregating action of t he mucus , but
chemotasis may also be involved ( Bjgrnhag , 1994 ) .
pacemaker located at t he junction between proximal
The ensuring mixt ure of bacteria and mucus is
and distal colon.
This activity result s in t he
t ransported into t he narrow channel and event ually
accumulation of fluid , solutes , bacteria and very small
back to t he caecum by antiperistaltic movement s of
food particles in t he caecum , which has been
variously modelled as a CSTR ( Hume , 1989) , batch
reactor or semi2batch reactor ( Hume , 1999 ) . Net
t he wall. The bacteria and mucus mix wit h t he caecal
content s , while food residues are passed on to t he
absorption of fluid f rom t he caecum balances it s
ceases for several periods of variable duration , and
secretion in t he proximal colon , and completes an
when t he colon is nearly empty t he caecum is partially
“internal water cycle”.
At t he same time , t he larger particles in t he
evacuated and caecot rop hes may be formed and eaten
activity of t he wall of t he proximal colon t hat forms
distal colon and are voided as faecal pellet s. The CSM
in caecot rop hic species. Nearly all myomorp h rodent s
动 物 学 报
16
48 卷
( Table 4 ) show t he anatomical modifications of t he
cell walls but cell content s , particularly resistant
proximal colon suggestive of a mucus2t rap CSM ; t he
starch ,
only exceptions appear to belong to two carnivorous
oligosaccharides , t hat have escaped digestion in t he
genera ( Sperber et al . , 1983) . Digesta flow into and
small intestine , as well as endogenous secretions and
out of t he caecum in animals wit h a “mucus2t rap ”
sloughed mucosal cells f rom t he small intestine.
CSM may be best modelled as a CSTR because of it s
8 Conclusion
more continuous nat ure t han in wash2back CSM
non2starch
storage polysaccharides ,
and
The mammalian digestive system is generally
animals.
The nut ritional consequence of a CSM is t he
simplest in carnivores , more complex in omnivores ,
concent ration in an enlarged caecum of bacteria and
and of greatest complexity in herbivores.
The
proteinaceous mucus in t he mucus2t rap system or
carnivore digestive t ract is dominated by t he small
bacteria , very small food particles and solutes in t he
intestine irrespective of body size , and t hus t here is a
wash2back system.
At t he same time , in bot h
direct relationship between passage time or mean
systems t he more int ractable component s of t he
retention time ( MR T) of digesta and body size of t he
digesta entering t he hindgut are cleared f rom t he
carnivore.
This has t he important
In omnivores t here is usually greater complexity
consequence of alleviating t he gut2filling effect s of
of t he stomach and/ or t he hindgut . Consequently
plant cell walls , and allowing much higher intakes of
t here is no simple relationship between digesta MR T
forage diet s by t hese small mammals t han would be
and body size. However , MR Ts are generally longer
predicted purely on t he basis of body mass. The
in omnivores t han in carnivores of similar body size.
efficiency of
Such a digestive st rategy correlates wit h t he inclusion
colon relatively rapidly.
enhanced
t he caecal fermentation system is
and ,
caecot rop hic
at
species ,
least
in
cellular
coprop hagic
product s
of
and
of plant as well as animal material in t he diet , and
t he
wit h t he lower rate of digestion of plant material.
fermentation ( microbial protein and B2vitamins) are
Each of
t he
t hree
groups of
mammalian
recycled to t he stomach and small intestine. All
herbivores (foregut fermenters , colon fermenters and
caecum fermenters benefit by t he direct absorption of
caecum fermenters) has a different digestive st rategy ,
t he SCFA produced in t he hindgut .
The main
and consequently each fills a specific nut ritional niche
subst rates utilised in t he fermentation are not plant
( Fig. 10 ) . Many of t he foregut fermenters and t he
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)
1期
Ian D. Hume : Digestive strategies of mammals
17
colon fermenters specialise on digestion of plant fibre ,
cell content s t hat are resistant to catalytic digestion in
and fit most closely Stevens and Hume ’s ( 1995 )
an enlarged
definition of herbivores. On t he ot her hand , t he
fermenters have a colonic separation mechanism in t he
caecum fermenters specialise on fermentation of non2
proximal colon t hat leads to t he selective retention of
caecum.
However ,
many
caecum
fibre component s of t he digesta leaving t he small
bacteria , and in some species solutes and small food
intestine. Their capacity to retain plant cell walls for
particles as well , in t he caecum. At t he same time t he
t he extended periods
substantial
elimination of large food particles is facilitated , which
breakdown of t he fibre is limited by t heir small body
alleviates t he gut filling effect of plant cell walls ,
size and t hus small absolute gut capacity. Therefore
allowing t hese small mammals to utilise forages of
t hey feed on plant species and plant part s of lower cell
much higher cell wall content t han would be predicted
wall content , digest most of t he cell content s in a
on t he basis of t heir small body size.
necessary for
simple stomach and small intestine , and ferment any
References ( 参考文献)
Belovsky , G. E. 1978 Diet optimization in a generalist herbivore : t he moose. Theor. Popul . Biol . 14 : 105～124.
Bjgrnhag , G. 1981 The retrograde transport of fluid in t he proximal colon of rabbits. S wed. J . A gric. Res. 11 : 63～69.
Bjgrnhag , G. 1987 Comparative aspects of digestion in t he hindgut of mammals. The colonic separation mechanism ( CSM) (a review) . Dtsch.
Tierg
rz l . Wshr. 94 : 33 ～36.
Bjgrnhag , G. 1994 Adaptations in t he large intestine allowing small animals to eat fibrous foods. I n : Chivers , D. J . and P. Langer ed. The
Digestive System of Mammals : Food , Form and Function. Cambridge : Cambridge University Press , 287～309.
Caton , J . M. 1997 Digestive Strategies of Non2Human Primates. Ph. D. Thesis , Australian National University , Canberra.
Caton , J . M. and I. D. Hume 2000 Chemical reactors of t he mammalian gastro2intestinal tract . Z. S g
ugetierk unde 65 : 33 ～50.
Cochran , P. A. 1987 Optimal digestion in a batch2reactor gut : t he analogy to partial prey consumption. Oikos 50 : 268～270.
Comport , S. S. and I. D. Hume 1998 Gut morphology and rate of passage of fungal spores t hrough t he gut of a tropical rodent , t he giant white2
tailed rat ( U romys caudi m aculat us) . A ust . J . Zool . 46 : 461～471.
Cork , S. J . , I. D. Hume and G. J . Faichney 1999 Digestive Strategies of Nonruminant herbivores : t he role of t he hindgut . I n : J ung , H. 2J .
G. and G. C. Fahey , J r. ed. Nutritional Ecology of Herbivores. Savoy , Illinois : Amer. Soc. Anim. Sci. , 210～260.
Darlington , J . M. and T. V. Hershberger 1968 Effect of forage maturity on digestibility , intake and nutritive value of alfalfa , timot hy and
orchardgrass by equine. J . A ni m . Sci . 27 : 1 572～1 576.
Dellow , D. W. , J . V. Nolan and I. D. Hume 1983 Studies on t he nutrition of macropodine marsupial. Ⅴ. Microbial fermentation in t he
forestomach of Thylogale t hetis and M acropus eugenii . A ust . J . Zool . 31 : 433～4431
Demment , M. W. and P. J . Van Soest 1985 A nutritional explanation for body size patterns of ruminant and non2ruminant herbivores. A m .
N at . 125 : 641～672.
Engelhardt , W. V. , M. Lechner2Doll , R. Heller , H. J . Schwartz , T. Rutagwenda and W. Schult ka 1987 Physiology of t he forestomach in
camelids wit h particular reference to adaptation to extreme dietary conditions —a comparative approach. Zoo. Beit r. 30 : 1～15.
Flannery , T. F. 1995 Mammals of New Guinea. Chatswood , New Sout h Wales : Reed.
Foose , T. J . 1982 Trophic Strategies of Ruminant Versus Nonruminant Ungulates. Ph. D. Thesis , University of Chicago.
Foot , J . Z. and B. Romberg 1965 The utilisation of roughage by sheep and t he red kangaroo , M acropus ruf us (Desmarest) . A ust . J . A gric.
Res. 16 : 429～435.
Frakes , L . A. , B. Mc Gowran and J . M. Bowler 1987 Evolution of Australian environments. I n : Dyne , G. R. ed. Fauna of Australia. Vol.
1A. Canberra : Australian Government Publications , 1～16.
Freudenberger , D. O. and I. D. Hume 1992 Ingestive and digestive responses to dietary fibre and nitrogen by two macropodid marsupials
( M acropus robust us erubescens and M . r. robust us) and a ruminant ( Capra hi rcus) . A ust . J . Zool . 40 : 181～194.
Freudenberger , D. O. , I. R. Wallis and I. D. Hume 1989 Digestive adaptations of kangaroos , wallabies and rat2kangaroos. I n : Grigg , G. ,
P. Jarman and I. Hume ed. Kangaroos , Wallabies and Rat2kangaroos. Sydney : Surrey Beatty , 179～187.
Gibson , L . A. and I. D. Hume 2000 Digestive performance and digesta passage in t he omnivorous greater bilby , M acrotis lagotis ( Marsupialia :
Peramelidae) . J . Com p . Physiol . B170 : 457～467.
Hayes , K. C , R. E. Carey and S. Y. Schmidt 1975 Retinal degeneration associated wit h taurine deficiency in t he cat . Science 188 : 949～951.
Hof mann , R. R. 1973 The Ruminant Stomach. Nairobi : East Africa Literature Bureau.
Hof mann , R. R. 1988 Morphophysiological evolutionary adaptations of t he ruminant digestive system. I n : Dobson , A. and M. J . Dobson ed.
18
动 物 学 报
48 卷
Aspects of Digestive Physiology in Ruminants. It haca : Comstock , 1～20.
Hollis , C. J . 1984 The Ability of Two Macropods ( M acropus eugenii and M . robust us robust us) of Different Body Size to Utilize Diets of
Different Fibre Content Compared Wit h Sheep . Unpublished t hesis , University of New England , Armidale , Australia.
Hoppe , P. P. 1977 Rumen fermentation and body weight in African ruminants. I n : Peterle , T. J . ed. Proc. 13 th Int . Congr. Game Biologists.
Washington , D , C. : Wildlife Society , 141～150.
Horn , M. H. and K. S. Messer 1992 Fish guts as chemical reactors : a model of t he alimentary canals of marine herbivorous fishes. M ar. Biol .
113 : 527～535.
Hume , I. D. 1989 Optimal digestive strategies in mammalian herbivores. Physiol . Zool . 62 : 1 145～1 163.
Hume , I. D. 1999 Marsupial Nutrition. Cambridge : Cambridge University Press.
Hume , I. D. , C. Smit h and P. A. Woolley 2000 Anatomy and physiology of t he gastrointestinal tract of t he J ulia Creek dunnart , S mi nt hopsis
douglasi ( Marsupialia : Dasyuridae) . A ust . J . Zool . 48 : 475～485.
Hume , I. D. , A. C. I. Warner 1980 Evolution of microbial digestion in mammals. I n : Ruckebusch , Y. and P. Thivend ed. Digestive
Physiology and Metabolism in Ruminants. Lancaster : M TP Press , 665～684.
Janis , C. 1976 The evolutionary strategy of t he Equidae and t he origins of rumen and cecal digestion. Evol ution 30 : 757～774.
Janzen, D. H. 1981 Evolutionary physiology of personal defence. I n : Townsend , C. R. and P. Calow ed. Physiological Ecology : An
Evolutionary Approach to Resource Use. Sunderland , Mass. : Sinauer , 145 ～164.
J umars , P. A. 2000 Animal guts as nonideal chemical reactors : partial mixing and axial variation in absorption kinetics. A m . N at . 155 : 544～
555.
Karasov , W. H. , D. Phan , J . M. Diamond and F. L . Carpenter 1986 Food passage and intestinal nutrient absorption in hummingbirds. A uk
103 : 453～464.
Langer , P. 1988 The Mammalian Herbivore Stomach. Stuttgart : Fischer.
Lentle , R. G. , M. A. Potter , K. J . Stafford , B. P. Springett and S. Haslett 1998 The temporal characteristics of feeding activity in
free2ranging tammar wallabies ( M acropus eugenii Desmarest) . A ust . J . Zool . 46 : 601～615.
Lentle , R. G. , K. J . Stafford and M. A. Potter , B. P. Springett and S. Haslett 1999 Ingesta particle size , food handling and ingestion in t he
tammar wallaby ( M acropus eugenii Desmarest) . A ust . J . Zool . 47 : 75～85.
Macdonald , D. ed. 1984 The Encyclopedia of Mammals. New York : Facts on File Publications.
Mackie , R. I. 1997 Gut environment and evolution of mutualistic fermentative digestion. In : Mackie , R. I. and B. A. White ed. Gastrointestinal
Microbiology , Vol. 1. Gastrointestinal Ecosystems and Fermentations. New York : Chapman and Hall , 13～35.
Martinez , del Rio , C. , S. J . Cork and W. H. Karasov 1994 Modelling gut function : an introduction. I n : Chivers , D. J . and P. Langer ed.
The Digestive System in Mammals : Food , Form and Function. Cambridge : Cambridge University Press , 25 ～53.
Martinez , del Rio and C. and W. H. Karasov 1990 Digestion strategies in nectar2 and fruit2eating birds and t he composition of plant rewards. A m .
N at . 136 : 618～637.
McClelland , K. L . , I. D. Hume and N. Soran 1999 Responses of t he digestive tract of t he omnivorous nort hern brown bandicoot , Isoodon
m acrourus ( Marsupialia : Peramelidae) , to plant2 and insect2containing diets. J . Com p . Physiol . B169 : 411～4181
McNab , B. K. 1986 Food habits , energetics and t he reproduction of marsupials. J . Zool . L ond . ( A ) 208 : 595～614.
Mertens , D. R. and L . O. Ely 1979 A dynamic model of fiber digestion and passage in t he ruminant for evaluating forage quality. J . A ni m . Sci .
49 : 1 085～1 095.
Morris , J . G. 1994 Metabolic adaptations of carnivores in relation to diet . I n : Wahlqvist , M. et al . ed. Nutrition in a Sustainable Environment .
U . K. : Smit h2 Gordon , 502～505.
Moyle , D. I. , I. D. Hume and D. M. Hill 1995 Digestive performance and selective digesta retention in t he long2nosed bandicoot , Perameles
nasuta , a small omnivorous marsupial. J . Com p. Physiol . B164 : 552～560.
Parra , R. 1978 Comparison of foregut and hindgut fermentation in herbivores. I n : Montgomery , G. G. ed. The Ecology of Arboreal Folivores.
Washington , D. C. : Smit hsonian Institution Press , 205～229.
Penry , D. L . 1993 Digestive constraints on diet selection. I n : Hughes , R. N. ed. Diet Selection : An Interdisciplinary Approach to Foraging
Behaviour. Oxford : Blackwell Scientific Publications , 32～55.
Penry , D. L . and P. A. J umars 1986 Chemical reactor analysis and optimal digestion t heory. BioScience 36 : 310～315.
Penry , D. L . and P. A. J umars 1987 Modeling animal guts as chemical reactors. A m . N at . 129 : 69～96.
Pernetta , J . C. 1976 Diets of t he shrews Sorex araneus L . and Sorex mi nut us L . in Wyt ham grassland. J . A ni m . Ecol . 45 : 899～912.
Read , D. G. 1987 Rate of food passage in Plani gale spp . ( Marsupialia : Dasyuridae) . A ust . M am m al . 10 : 27～28.
Rhoades, D. F. 1985 Offensive2defensive interactions between herbivores and plants : t heir relevance in herbivore population dynamics and
ecological t heory. A m . N at . 125 : 205～238.
Richardson , K. C. , M. K. Vidyadaran , N. H. Fuzina and T. I. Azmi 1988 Topographic anatomy of t he abdomen of t he lesser mousedeer
1期
Ian D. Hume : Digestive strategies of mammals
19
( T ragul us javanicus) . Pertanika 11 : 419～426.
Rogers , Q. R. , J . G. Morris and R. A. Freedland 1977 Lack of hepatic enzymatic adaptation of low and high levels of dietary protein in t he adult
cat . Enz y me 22 : 348～356.
Sauer , W. S. , T. J . Devlin , R. J . Parker , N. E. Stanger , S. C. Strot hers and K. Wittenberg 1979 Effect of cecectomy on digestibility
coefficients and nitrogen balance in ponies. Can J . A ni m . Sci . 59 : 145～151.
Sibly , R. M. 1981 Strategies of digestion and defecation. I n : Townsend , C. R. and P. Calow ed. Physiological Ecology : An Evolutionary
Approach to Resource Use. Sunderland , Mass. : Sinauer , 109 ～139.
Spalinger , D. E. and C. T. Robbins 1992 The dynamics of particle flow in t he rumen of mule deer ( O docileus hemionus hemionus) and elk
( Cerv us elaphus nelsoni) . Physiol . Zool . 65 : 379～402.
Sperber , I. , G. Bjgrnhag and Y. Ridderstrale 1983 Function of proximal colon in lemming and rat . S wed. J . A gric. Res. 13 : 243～256.
Stevens , C. E. and I. D. Hume 1995 Comparative Physiology of t he Vertebrate Digestive System , 2 nd. ed. Cambridge : Cambridge University
Press.
Stevens , C. E. and I. D. Hume 1998 Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients.
Physiol . Rev . 78 : 393～427.
Strahan , R. 1995 The Mammals of Australia. Chatswood , New Sout h Wales : Reed.
Takahashi , T. and E. Sakaguchi 2000 Role of t he furrow of t he proximal colon in t he production of soft and hard feces in nutrias , M yocastor
coypus . J . Com p . Physiol . B 170 : 531～535.
Tedman , R. A. and L . S. Hall 1985 The morphology of t he gastrointestinal tract and food transit time in t he fruit bats Pteropus alecto and P.
poliocephal us ( Megachirptera) . A ust . J . Zool . 33 : 625～640.
Townsend , C. R. and R. N. Hughes 1981 Maximizing net energy returns from foraging. I n : Townsend , C. R. and P. Calow ed. Physiological
Ecology : An Evolutionary Approach to Resource Use. Sunderland , Mass. : Sinauer , 86～108.
Waldo , D. R. , L . W. Smit h and E. L . Cox 1972 Model of cellulose disappearance from t he rumen. J . Dai ry Sci . 55 : 125～129.
Van Soest , P. J . 1965 Symposium on factors influencing t he voluntary intake of herbage by ruminants : voluntary intake in relation to chemical
composition and digestibility. J . A ni m . Sci . 24 : 834～843.
Van Soest , P. J . 1982 Nutritional Ecology of t he Ruminant . Corvallis , Oregon : O & B Books.
Warner , A. C. I. 1981 Rate of passage of digesta t hrough t he gut in mammals and birds. N ut r. A bst r. Rev . Ser. B 51 : 789～820.
Weems , W. A. 1987 Intestinal fluid flow : its production and control. I n : Robinson , L . R. ed. Physiology of t he Gastrointestinal Tract . New
York : Raven Press , 571～593.
Wellard , G. A. and I. D. Hume 1981 Digestion and digesta passage in t he brushtail possum T richosurus v ul pecula ( Kerr) . A ust . J . Zool . 29 :
157～166.
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 , MR Ts) 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