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