the digestion of fibre in herbivorous anatidae - a review

The digestion of fibre in herbivorous Anatidae - a review

D. Durant

CNRS UPR 1934-, Centre d'Etudes Biologiques de Chizé, 79360 Beauvoir-sur-Niort, France.

New address: Institut National de la Recherche Agronomique, Domaine du Bois Mâché,

17450 Saint-Laurent-de-la-Prée, France. Email: durantBstlaurent. lusignan. inra. fr

N um erous s tud ies on the ab il i ty of herb ivorous Anatidae to digest f ibre

f rom a var iety of food types (foliage, seeds, tubers) have yie lded var iable

resu l ts . Herb ivorous ducks and geese have the capacity to digest some

com ponen ts of f ib re (between 0% and 85%, depending on the s tudy and

the f ib re c o m p o n e n ts analysed), in p a r t i c u la r h e m ic e l lu lo s e .

H em ice l lu lose may be part ia l ly d igested by acid hydro lysis ear ly in the

digestive tract, and the s m a l l part ic les of the flu id digesta obta ined may

undergo a l im i ted fe rm en ta t ion in the caecae (with the aid of symbio t ic

m icro f lo ra) . Two sources of var ia t ion in the d igest ib i l i ty of f ib re ident if ied

by the s tud ies are d iscussed: expe r im en ta l fac tors (in p a r t ic u la r the d i f

ferences in the method used) and b io logical factors . In the la t te r some of

the var iation in f ib re d iges t ib i l i ty reported by the s tud ies is probably due

to d ie t-based factors: d if ferences in s t ru c tu ra l and chem ica l propert ies

of the p lant species consumed. But o the r factors , unre la ted to diet, may

be taken into account. C onsum er-based factors , such as seasona l va r i

ation (in re la t ion to the re tent ion t im e of food in the gut) and d i f fe rences

in body mass o r caecal length of the bird species, m us t also be cons id

ered. The use of f ib re as a m a rk e r in s tud ies of food d iges t ib i l i ty in

herb ivorous Anatidae is discussed.

Key Words: herbivorous Anatidae , digestibil ity , f ibre , fe rm e n ta t io n , caecae

©Wildfowl & Wetlands Trust Wildfowl (2003) 54: 7-24

8 Digest ion of f ib re in herb ivo rous Anatidae

One of the main com ponen ts of

p lant tissues is fibre, which consti tu tes

the cell wal ls . As digestion of fibre

plays an im po r tan t role in the energy

balance of herb ivorous birds, it has

received pa r t icu la r attention (Gasaway

1976; Herd & Dawson 1984;

Buchsbaum et a i 1986; Sedinger et al.

1995; Bair le in 1999). Measures of fibre

digestion can have im por tan t im p l ica

t ions fo r u n d e rs ta n d in g fo rag ing

behaviour and habita t use of herbivores

(Boudewijn 1984) because [a) f ibre is a

non-neg l ig ib le source of energy since it

represents half of the b iomass of the

green parts of p lants (Van Soest 1982;

Sedinger & Raveling 1984], and (b) if

ce ll w a l ls can be digested, the cell con

ten t is more accessib le and digestion

more comple te (Rybicki & Lubanska

1959).

V e r teb ra tes are not capab le of

secret ing cellu lase, the enzyme which

digests cellu lose, but m any herbivores,

inc lud ing some birds, rely on symbiot ic

m ic ro -o rg a n is m s in th e i r gut. This

necess ita tes a su i tab le site fo r the

retention of p lant m a te r ia l and fe r

m enta t ion of fibre (ie the breakdown of

ce l lu lose into volat ile fa tty acids; see

below). B irds possess a la te ra l pair of

saccula te tubes called caecae between

the sm a l l and large intestines, where

c e l lu lo ly t ic fe r m e n ta t io n may occu r

(Mattocks 1971). The abil ity to digest

fibre varies among groups and taxa

(Bair le in 1999). It is s ign i f icant in some

bird species which have enlarged cae

cae as fe rm en ta t ion chambers, such as

spec ies in the fa m i ly Te traon idae

(grouse and ptarmigan), the rat i tes (the

Austra l ian Emu Dromaius novaehollan-

diae), and the Hoatzin Opisthocomus

hoazin (Moss 1977; Herd & Dawson

1984). The possession of an effective,

large, heavy fe rm e n ta t io n cham ber ,

however, im p a c ts on f l ig h t energy

costs, which increase d irectly w ith body

mass.

Anatidae often make long m ig ra to ry

f l ights. As th e i r caecae contain a p ro l i f

ic m ic ro b ia l fauna (M a ttocks 1971;

Vu link 1980; Prop & Vulink 1992), these

organs have long been assumed to be

cen tres of ce l lu lo ly t ic fe rm e n ta t io n ,

and func t iona l ly analogue to a rum en

(Lorenz 1952; M i l le r 1976). However,

m ic ro b ia l fe rm e n ta t io n is a lengthy

process (ie it takes several hours: about

12 hours in cows, sheep and goats, for

example), and the rapid rate of passage

of food in the gut of he rb ivo rous

Anat idae [two hours in the Greylag

Goose A nser anser on grass (Mattocks

1971); 70-75 m inu tes in Wigeon Anas

penelope on grass (Mayhew & Houston

1993); 3. 2 hours in Lesser Snow Goose

Chen caeru lescens caeru lescens on

Alfa lfa Medicago sativa and 7. 5 hours on

corn (Post et al. 1998)] is l ikely to l im i t

the opportun it ies fo r fibre breakdown.

A fte r a b r ie f in t roduct ion on the

na tu re of d ie ta ry fib re , th is paper

reviews w ha t is known about the abili ty

of he rb ivo rous ducks and geese to

digest the f ibre of a variety of food types

(foliage, seeds, tubers], and the u n d e r

lying digest ive m echan ism s. The review

w i l l then d iscuss the potent ia l sources

of variat ion in f ibre d igest ib i l i ty in her-

Digest ion of f ib re in herb ivo rous Anatidae 9

bivorous Anatidae and the po ten t ia l

reasons fo r these variations, as repo r t

ed in the studies. The use of fibre as an

in te rna l m a rk e r as a means to ca lcu

la te food d ige s t ib i l i ty w i l l a lso be

discussed.

The fibre content of plant

m a ter ia l

Fibre is made up of three main c o m

ponents: cellu lose, hem ice l lu lose and

lignin (Van Soest 1982). Cel lu lose is a

carbohydrate composed m ain ly of g lu

cose un i ts l inked together.

Hem ice l lu lose is made up of diverse

groups of polysaccharides, and has a

d if ferent and more complex con f igu ra

t ion than ce l lu lose . L ign in is a

polyphenol.

Many s tud ies have exp lo red the

c h e m ic a l com p o s i t io n of food c o n

sum ed by grazing Anatidae, ie mainly

the exposed parts of grasses and forbs

(Ebbinge et al. 1975; Sedinger 1989;

Am at et a l . 1991; Prop & Vul ink 1992),

but also seeds, tube rs and rh izomes

[B é la n g e r et al. 1990; M a th e rs &

M o n tg o m e ry 1997; van Eerden &

M uns te rm an 1998). For instance, the

f ib re con ten t of te m p e ra te g rasses

varies according to species, m a tu r i ty

and season (Van Soest 1982) and, in

general, ranges from 50% to 60% of dry

matter. C e l lu lose and hem ice l lu lose

are the main com ponents of ce ll w a l ls

(45-50% and 40-45%, respectively) (Van

Soest 1982). Lignin is less abundan t (5-

10%).

M easurem ents of the f ibre content

of p lants are made using the detergent

fibre method (Gauth ier et al. 1991; Van

Soest 1982). This method is based on

the division of food com ponents into

solub le m etabo li tes and cell w a l l con

s t i tu e n ts (m ain ly hem ice l lu lo se ,

ce l lu lose and lignin). The NDF fract ion

(neutra l detergent fibre) conta ins c e l lu

lose, hem ice l lu lose and lignin whereas

the ADF residue (acid detergent fibre)

conta ins only ce l lu lose and lignin. In

general, the NDF and ADF contents of

p lant m a te r ia l fo l low the re lat ionship :

N DF=[1 , 5 -2 . 5]xADF (van Eerden &

M uns te rm an 1998). Lignin (ADL: acid

detergent lignin) is de te rm ined as the

ash-f ree residue left a f te r treating ADF

w ith s u lp h u r ic acid. The d is t inc t ion

between NDF and ADF is often made,

since ADF is the fract ion of the cell w a l l

which is the least d igest ib le (ie in NDF,

hem ice l lu lose is the fract ion which is

quite w e l l digested by Anatidae, see

below). Moreover, th is d is t inc t ion is

usefu l in the part i t ion ing of the d i f fe r

ent ce l l w a l l c o m p o n e n ts ; the

dif ference between NDF and ADF va l

ues is often used to evaluate

hem ice l lu lose content, and ce llu lose

can be de te rm ined by removing l ignin

(and ash) f rom ADF (Sedinger et al.

1995).


The digestion of fibre in herbiv

orous Anatidae

Fibre d igest ib i l i ty is defined as the

f ract ion of d ie tary fibre tha t is digested

and converted into usable energy or

nu tr ien ts (several o the r te rm s are f re

quen t ly used in the l i te ra tu re :

ass im ila t ion effic iency, uti l isa t ion e ff i

c iency, d iges t ion e ff ic iency,

metabo l isab i l i ty coeff ic ient, etc. but a ll

are used as synonyms). To est imate the

d ig e s t ib i l i ty of fib re , two p r in c ip a l

m ethods are used: 1) the inpu t /ou tpu t

method and 2) the m a rk e r method

(Tables 1 & 2). The inpu t /ou tpu t method

is a d irect one and involves the use of

captive birds. The birds' food intake and

excreta are d irect ly measured over a

period of several days. The m easure of

the fibre compos it ion of the food and

droppings gives the quanti ty of fibre

eaten (intake) and excreted (output) by

the birds. Fibre digestibility (%) is then

calculated as: (intake-output)/(intake)*100

(Sedinger et al. 1989, 1995).

The o the r method uses a m arker ,

and is an ind irect method. A m a rk e r is

a substance tha t rem ains unchanged

dur ing the passage th rough the d iges

tive t rac t of an an im al. A m a rk e r may

be ' in terna l ' (produced f rom the plant]

o r 'external ' (admin istered to the an i

mal) (Mayes et al. 1995). The m a rke r

method is based on assessm ent of the

percent m a rk e r in the food and the

droppings. Percentage fibre d iges t ib i l i

ty is then est imated as:

1-[(%marker food/%markerdroppings)*(%

fibref00d/% fibredroppings)*100]

This method [Buchsbaum et a i 1986)

has the advantage of being applicable

e ither w ith captive or w ith free -rang ing

birds (ie in a fie ld si tuation). For Kotb &

Luckey (1972), " ine r tness and lack of

absorpt ion o r m etabo l ism occurr ing in

the d igest ive t r a c t " w ere the m os t

im por tan t cr i te r ia fo r a component to

be a rel iable marker. The choice of a

m a rk e r is im po r tan t because a m a rk e r

tha t is partly digested w i l l give an u n d e r

est imat ion of digestibi l i ty.

Eighteen papers were found that

reported stud ies on the digestion of

f ibre in herb ivorous Anatidae, w ith a

large n u m b e r of species covered (four

spec ies of ducks , e igh t spec ies of

geese and three species of swans; see

Tables 1 & 2). In the early twent ie th

cen tu ry , geese w ere cons ide red to

make li t t le use of d ie tary fibre. The f irst

w o rk on the digestion of fibre in geese

was carr ied out w ith domest ic geese

derived f ro m the genus Anser, and

showed tha t geese digested less than

1 % of fibre (Weiser & Zeitscheck 1902).

Subsequently , fibre d igest ib i l i t ies ra n g

ing from negative values fo r rice to

positive values fo r maize (33. 5%) were

ob ta ined in s tud ies w i th cereals,

legum es or roots and protein concen

t ra tes (Nehring & Nerge 1966). Later,

M arr io t t & Forbes (1970) showed that

Cape Barren Geese Cereopsis novaehol-

iandiae fed w ith lucerne pelle ts (Alfalfa,

w ith less than 35% of fibre) did not

digest s ign i f ican t am oun ts of ce llu lose

and l ignin (0. 8%). Recent investigations

Table 1: Review o f fo liage f ib re d igest ion in he rb ivo rous Anatidae. Values are given as % of DM l±S. D., o r S. E. )

Species Mass

(kg)

Food Method usedhemicellulose

Digestibility (%]

cellulose lignin NDF ADF

Period References

Wigeon

Anas penelope

0. 6 foliage m arker: ADF 17. 0 -33. 0 - - - w in te r-

au tum n-

spring

Bruinzeel et al. 1998

Wigeon

Anas penelope

0. 6 grass input/output - 30. 8±4 . 1 5. 0±3. 0 autum n This study

Australian Wood Duck

Chenonetta jubata

0. 9 grass, forbs m arker:

m anganese

74. 0 11. 0 4. 0 40. 0 9. 0 no

indication

Dawson et al. 1989

Brent Goose

Branta bernicla

1. 1 Alfalfa pellets input/output - 1. 3±1. 7 negative 15. 5± 1. 6 negativet*] w inter Sedinger et al. 1989

Brent Goose

Branta bernicla

1. 6 Spartina

patens

m arker: lignin 13. 0±10. 7(*) 30. 8±8. 9(*) 18. 0±10. 3(*1 20. 8±14. 5(*) May Buchsbaum et al.

1986

Brent Goose

Branta bernicla

1. 6 Spartina

alterniflora

m arker: lignin 38. 7±16. 8(*] 32. 9±13. 4(*) 29. 0±5. 6(*) 22. 3±6. 5(*] May Buchsbaum et al.

1986

Barnacle Goose

Branta leucopsis

no

indication

graminoids m arker: lignin 20. 4±5. 9

47. 3±11. 3(*)- - 0. 3±3. 2

26. 2±7. 7l*)

w in te r-

su m m er

Prop & Vulink 1992

Barnacle Goose

Branta leucopsis

1. 8 foliage m arker: ADF 50. 0±56. 0 - - - w in te r-

autum n-

spring

Bruinzeel et al.

1998

Magpie Goose

Anseranas semipalmata

1. 8 -2 . 0 grass input/output

method

32. 0±6. 0 - 27. 0±7. 0 19. 0±8. 0 no

indication

Dawson et al. 2000

White-fronted Goose

Anser albifrons

2. 0 foliage m arker: ADF 32. 0±55. 0 - - ■ w in te r-

autum n-

spring

Bruinzeel et al.

1998

Lesser Snow Goose

Chen c. caerulescens

>2. 0 Alfalfa pellets input/output

method

52. 6±2. 7 44. 6±6. 0 7. 8±6. 4 30. 9±2. 8 16. 3+2. 8 autum n Sedinger et al. 1995

Dig

es

tion

of

fibre in

he

rbiv

oro

us

A

na

tida

e

11

Table 1: Continued

Species Mass Food Method used Digestibility (%] Period References

(kg) hemi

cellulosecellulose lignin NDF ADF

Greylag Goose

Anser anser

2. 6 Phragmites

australis

m arker: ADF 21. 0 -3 4 . 0(*) no digestion' - - June

1998a

van Eerden et al.

Greylag Goose

Anser anser

3. 3 foliage m arker: ADF 12. 0 -6 7 . 0 - - - w inter-

autum n-

spring

Bruinzeel et al.

1998

Greylag Goose

Anser anser

3. 4 grass input/output - - 28. 4±10. 2 10. 7±9. 3 autumn This study

Cape Barren Goose

Cereopsis novaehollandiae

3 . 7 chaffed

lucerne

input/output - - - 0. 8 no

indication

Marriott & Forbes

1970

Canada Goose

Branta canadensis

4. 0 Spart ina

alterni flora

m arker: lignin 22. 6±6. 7(*) 29. 7±2. 4[*) 22. 0±3. 8(*) 21. 3±11. 7U) August Buchsbaum et al.

1986

Canada Goose

Branta canadensis

4. 0 Juncus

geradii

m arker: lignin 25. 5±6. 3(*) 18. 1 i6 . 3 l*) 17. 9±2. 5(*1 12. 4±10. 7(*) April Buchsbaum et al.

1986

Domestic Goose

Anser sp.

5. 3 pelleted grass no indication - - 7. 2 - no

indication

Koram & Greenhalgh

1982

Bewick's Swan

Cygnus c. bewickii

6. 0 foliage marker: ADF 30. 0-55. 0 - - - winter-

autumn-

spring


Bewick's Swan

Cygnus c. bewickii

5. 7-6. 4 grass marker: ADF 55. 9 - - - autumn van Eerden et al.

1998b

Whooper Swan

Cygnus Cygnus

8. 7 foliage marker: ADF 45. 0 -73. 0 ■ - winter-

autumn-spring


Mute Swan

Cygnus olor

10. 7 foliage marker: ADF 30. 0 winter-

autumn-

spring


12 D

ige

stio

n

of fibre

in h

erb

ivo

rou

s

An

atid

ae

Table 2: Review of seed and tu b e r f ib re d igest ion in herb ivorous Anatidae. Values are given as % of DM (±S. D., o r S . E. ).

S p e c i e s M a s s

(k g )

F o o d M e t h o d u s e d

h e m i

c e l l u l o s e

D i g e s t ib i l i t y (%

c e l l u l o s e l ig n in N D F A D F

P e r io d R e f e r e n c e s

Young domestic ducks

Anas sp.

no

indication

maize, barley

wheat, rye

input/output 27. 8±12. ¿ - 18. 1 ±8. 6 2. 8±10. 0 no indication Jamroz et al. 1996

Teal

Anas crecca

0. 3 seeds, tubers marker: ADF 45. 0 - - w inter-autum n-

spring


Wigeon

Anas penelope

0. 6 seeds, tubers marker: ADF 35. 0 - - w inter-autum n-

spring


Barnacle Goose

Branta leucopsis

1. 8 seeds, tubers marker: ADF 0-29. 0 ■ ■ ■ w inter-autum n-

spring


Magpie Goose

Anseranas semipalmata

1. 8 -2 . 0 rice grain input/output 21. 0±3. 0 ■ 19. 0±3. 0 18. 0±4. 0 no indication Dawson et al. 2000

Greylag Goose

Anser anser

3. 3 seeds, tubers marker: ADF 3. 0-71. 0 - - - winter-autum n-

spring


Greylag Goose

Anser anser

no

indication

Scirpus

littoralis

marker: lignin 56. 8 17. 1 - autumn-winter Amat et al. 1991

Greylag Goose

Anser anser

no

indication

Scirpus

maritimus

marker: lignin 65. 7 31. 0 - - autumn-winter Amat et al. 1991

Domestic Goose

Anser sp.

no

indication

maize, barley,

wheat, rye

input/output 34. 1 ±12. 9 - 23. 2±8. 6 5. 9±9. 4 no indication Jamroz et al. 1996

Domestic Goose

Anser sp.

? carrots ? - - 16. 1 - ? Pres et al. 1957

Domestic Goose

Anser sp.

? oats ? - - U . 1 ? Brüggemann 1931

Domestic Goose

Anser sp.

? maize ? " ■ 22. 6 ■ ? Brüggemann 1931

Bewick’s Swan

Cygnus c. bewickii

6. 0 seeds, tubers marker: ADF 47. 0 -77. 0

' ' '

winter-autumn-

spring


Bewick's Swan

Cygnus c. bewickii

5. 7-6. 4 sago tubers marker: ADF 85. 6 - - autumn van Eerden et al. 1998a

Bewick's Swan

Cygnus c. bewickii

5. 7-6. 4 sugarbeet marker: ADF 6. 5 - - - autumn van Eerden et al. 1998b

Whooper Swan

Cygnus Cygnus

8. 7 seeds, tubers marker: ADF 83. 0 - - - winter-autumn-

spring


? means that the results of the study were reported elsewhere, with no further information available.

Dig

es

tion

of

fibre in

he

rbiv

oro

us

A

na

tida

e

13

14 Digest ion of f ib re in herb ivo rou s Anatidae

confirm , however, that Anatidae can in

fact digest fibre to variable extents, and

the presence of bacter ia in the caecae

and the colon was dem onstra ted in

domest ic geese (Vulink 1980).

The resu lts of the studies on the

digestion of fibre from foliage, seeds

and tubers are given in Tables 1 and 2.

Fibre d igest ib i l i ty varies greatly [0-85%]

according to the study and the fibre

componen ts considered. The cellu lose

d igest ib i l i ty (44%) found by Sedinger et

at. (1995) in A lfa lfa pellets is one of the

h ighest values fo r birds reported in the

l i te ra ture (Hupp et a l. 1996). Fibre can

be an im po r tan t source of energy and

Buchsbaum et al . (1986) found tha t the

digestion of ce ll w a l ls provided up to

31% of the energy geese extract f rom

food plants. This is consis tent w ith a

study perfo rmed on Austra l ian Wood

Duck Chenonetta jubata (c. 870g) fo rag

ing on grasses and forbs, which is

among the few stud ies on herbivorous

ducks (Dawson et a l . 1989). The authors

showed tha t fibre digestion contr ibuted

30% of the ass im ila ted energy, w ith

most coming f rom hemice l lu lose (74%

of digestib il i ty). The compar ison of f ibre

digest ib i l i ty in herbage and seeds by

Bair le in (1999) showed tha t in herb ivo

rous birds the f ibre content of seeds is

be tte r digested than tha t of herbage

(55% vs. 19%).

The mechanics of fibre digestion

in herbivorous Anatidae

Herbivorous ducks and geese thus

have some capacity to digest com po

nen ts of f ibre, in p a r t ic u la r

hem ice l lu lose . However, the m e ch a n

ics and location of fibre degradat ion are

not w e l l known. Fermentat ion is the

process by which the s t ru c tu ra l poly

saccharides (cel lulose) are converted

by symbio t ic m ic ro f lo ra into m e tabo l is

able sho r t chain vola t ile fa t ty acids

(VFAs). D ucks and geese have few

gross m o rpho log ica l adapta t ions for

fibre fe rm en ta t ion w ith in the gut, and

the caecae are not w e l l developed c o m

pared to those of grouse of s im i la r size

(Owen 1980; Barnes & Thomas 1987;

Dawson et a l . 1989, 2000; Sed inger

1997).

One of the explanat ions fo r the s ig

n i f ican t level of d iges t ion of

hem ice l lu lose in Anatidae is tha t some

f ibre com ponents may be digested by

non -m ic rob ia l processes p r io r to fe r

m e n ta t io n (Herd & Dawson 1984·).

Dawson et al. (1989) found high levels of

hem ice l lu lose digestion in the prox imal

s m a l l intest ine of the Austra l ian Wood

Duck. Dawson et al. (1989, 2000) su g

gested, therefore, tha t hem ice l lu lose

may be p a r t ia l ly d igested by acid

hydro lys is w i th in the p rove n t r icu lu s

(g la n d u la r gizzard), the gizzard

(m echan ica l gizzard) and the proximate

part of the s m a l l intestine (duodenum).

This process wou ld a l low fibre to be

placed in solu t ion, and then t ra n s p o r t

ed to the caecae fo r rapid fe rm enta t ion

Digest ion of f ib re in he rb ivo rou s Anatidae 15

(<12 h o u rs , C le m e n s et at. 2000).

Fermenta t ion also occurs in the rectum

and c loaca (Dawson et at. 2000).

According to these authors, since it is a

complex of polysaccharides, it is possi

ble that hem ice l lu lose is digested by

both m echan ism s (ie acid hydrolysis

and fermentat ion) .

The part ic le size of the digesta is

clear ly an im po r tan t variable in fe r

m e n ta t io n (B jo rn d a l et at. 1990).

Indeed, the caecal ori fice (ie a kind of

i leo -caeca l sph inc te r) may separa te

the digesta, leaving the s m a l l intestine

with a fract ion conta in ing main ly fluid,

dissolved substances and s m a l l pa r t i

c les ( resu l t ing f ro m the hydrolysis)

(C lem ens et at. 1975; B jö rnhag &

S p e rb e r 1977; Dawson et at. 1989,

2000). This m echan ism fo r select ive

retention of f lu id digesta in the caecae

is w e l l known in o the r species of h e r

b ivorous b irds [p ta rm ig a n , grouse,

turkey) and m a m m a ls [rabbit , hare,

lem ming). It s lows the f low of w a te r

so lub le substances and f ine part ic les

(the more d igestib le parts of the food)

in o rder to effect a sa t is fac tory m ic ro

b ia l fe rm e n ta t io n . The la rg e r (less

digest ible) part ic les pass rapidly into

the large intestine. Herbivorous ducks

and geese probably show th is m echa

n ism of selective retention (see study of

M cW il l iam s (1999) on geese) but f u r

th e r stud ies are necessary to explore

this.

The a rgum en t fo r the existence of a

process of bacter ia l fe rm en ta t ion (in

the caecae, rec tum and cloaca) in h e r

bivorous Anatidae, even if l im ited, is

supported by:

1) bacter ia present in the caecae that

are capable of hem ice l lu lose and c e l lu

lose fe rm enta t ion (Vulink 1980; Prop &

Vul ink 1992); see also stud ies on d iges

tive enzyme activ ity on geese in N itsan

etat. [1973) and M cW il l iam s (1999);

2) the presence of volat ile fatty acids

(VFAs) produced in the gut by geese

during digestion, VFAs being the p r inc i

pal e n d -p ro d u c ts of fe rm e n ta t ive

digestion (the am oun ts of VFAs vary

among bird species, C lemens et at.

1975; Dawson et at. 1989; Jam roz et at.

1996). VFAs are then absorbed in the

caecae;

3) the homogeneous and viscous da rk -

green paste found among droppings of

ducks and geese (Dawson et at. 1989;

Mattocks 1971; pers. obs. ), which has a

pronounced sm e l l and a rich m ic ro f lo

ra s im i la r to tha t in the caecae

(indicating its caecal orig in ; Mattocks

1971).

Such a m echan ism fo r fibre d iges

t ion is p robab ly assoc ia ted w i th

re t rog rade m o v e m e n ts of the f lu id

digesta between the s m a l l intest ine

and the gizzard and p ro ve n t r icu lu s

a nd /o r f rom the cloaca to the colon,

caecum and d is ta l part of the sm a l l

in tes t in . This w as d e m o n s t ra te d by

Clemens et at. (1975) in domestic geese

(see also Dawson et at. 2000), but also in

turkeys (Duke et at. 1989). These move

ments probably enhance the digestion of

fibre by increasing its retention t ime in

the gut, but the existence of such a

mechanism in herbivorous birds needs

fu r ther investigation.

16 D igest ion of f ib re in he rb ivo rous Anatidae

Variation in the extent of fibre

digestion

Studies on f ibre digestion in herb iv

orous Anatidae show tha t the extent of

d igestion varies s trong ly (0-85%). There

are both expe r im en ta l and b iological

reasons fo r this.

From an expe r im en ta l point of view,

it may be prob lem atic to make c o m p a r

isons between these studies. First, the

method used to assess digestion of

fibre dif fers f rom one study to another:

data are genera l ly derived f rom the

in p u t /o u tp u t m e thod o r by using a

m a rk e r (see Tables 1 & 2). Second,

s tudies using m a rke rs were carr ied out

w ith both captive and w ild birds, and

the m a rke rs vary (ADF, l ignin or m a n

ganese).

The variat ions in fibre d igestib i l i ty

are also likely to be caused by b io log i

cal factors. First, the p lant species

concerned (Bru inzeel et at. 1998], the

part of the plant, s t ruc tu re of its t issues

and its degree of m a tu r i ty are likely to

play a role in how its fibre is digested by

birds (Buchsbaum et ai. 1986). This can

be a t t r ibu ted to var ia t ions in the fibre

content of the var ious foods and d i f fe r

ences in the s t ru c tu ra l and chem ica l

com pos i t ion of ce l l w a l ls (Mangold

1934). Second, the re are also con

sum er-based fac tors tha t are likely to

play a role in the var ia t ions in the ab i l i

ty of herbivorous birds to digest fibre.

The digest ive eff ic iency of a given diet

or quanti ty is a positive funct ion of

retention t im e [Prop & Vulink 1992).

However, increasing retention t im e has

costs fo r a bird: it increases the bird's

mass and thus its f l igh t costs; it also

reduces the mass of food tha t can be

ingested, and hence energy that can be

ass im i la ted . Moreover, b irds shou ld

mainta in the sm a l les t func t iona l gut

size because s m a l le r organs reduce

m etabo l ic energy expend itu re (Moss

1974) and because theore t ica l studies

predict that extra mass is associated

w ith h igher predation r isk (L ima 1986).

This is certa in ly why the re tention t ime

and the length of the digestive trac t are

both highly p last ic in birds (M il le r 1975;

Burton et al. 1979; Kehoe et a i 1988).

For instance, gut size varies w ith the

vo lum e /qua l i ty of the food consumed

(Ankney 1977; Karasov 1990). This sug

gests that there is a complex interp lay

[based on t ra d e -o f fs ) between the

nu tr i t iona l requ irem en ts of herb ivorous

birds, th e i r f l ig h t costs , food

quant i ty /qua l i ty and gut size or re ten

tion t im e tha t de te rm ines the op t im a l

digestion s tra tegy and leads to ad jus t

m en ts in th e i r digestive physiology. The

seasonal changes in ass im ila t ion e ff i

ciency reported in herb ivorous Anatidae

i l lustra te th is concept well . They are

probably due to a change in food use

(Bédard & Gauthier 1989; Boudewijn

1984) or variat ions in gut morphology

th roughout the annua l cycle. For exam

ple, in female Lesser Snow Geese the

intest ines decrease in Length during

laying and incubation (Ankney 1977). It

is then likely that geese compensate for

th is reduction in gut size by an increase

in food re ten t ion t im e, in o rd e r to

improve the d igestib i l i ty of fibre. Prop &

D igest ion of f ib re in herb ivo rous Ana tidae 17

Vu l ink (1992) d e m o n s t ra te d tha t

Barnacle Geese Branta leucopsis did

not digest ADF in w in te r but were able

to re ta in food (m ain ly g rasses and

bryophytes) in the digestive t rac t fo r

longer (ie up to fou r t im e s longer) in

su m m er , w hen food is rare and of poor

qua l i ty , in o rd e r to im prove the

d ig e s t ib i l i ty of ADF (up to 26%).

Evidence fo r the causal l ink between

ADF d iges t ib i l i ty and re ten t ion t im e

was also obtained in studies carr ied out

in spr ing in captive Brent Geese Branta

bernic la (Prins et at. 1981) and Barnacle

Geese (Van Marken L ich tenbe lt 1981).

Even if fu r th e r research is needed to

d e te rm in e the exact re la t io n sh ip

between changes in food intake and

quali ty, gut size, food retention t ime

and fibre d igest ib i l i ty th roughou t the

year, it seems certa in tha t the flexib i li ty

of the digest ive system of herb ivorous

Anatidae can be regarded as an adap

ta t ion to d i f fe rences in energy

requ irem en ts and env ironm en ta l con

dit ions.

At an interspeci f ic level, dif ferences

in fibre d igest ib i l i ty are likely to occur

because in vertebrate herbivores m e ta

bolic requ irements , gut vo lum e and the

abil ity to process and d igest food are

s t rong ly co rre la ted w i th body mass

(D em m ent & Van Soest 1985). W hether

body size in f luences the processes by

w hich the food is digested in herb ivo

rous b irds is, however, not c lea r

(McWil l iams 1999). This hypothesis has

been tested recently am ong Anatidae

species over a large range of body sizes

(f rom Teal Anas crecca, 300g, to Mute

Swan Cygnus olor, 11 kg) and a variety of

foods (seeds, tu b e rs and leaves)

(Bru inzeel et at. 1998). Digestib il ity of

hem ice l lu lose also corre la ted s ign i f i

can t ly w i th body m ass. However,

separate analyses fo r seeds and leaves

showed tha t body size had no effect.

The effect of retention t im e on fibre

d ig e s t ib i l i ty is c lear , however (see

above). Due to the i r longer re tention

time, la rger birds should be able to

digest fibre more eff ic iently than do

sm a l le r ones (Bru inzeel et at. 1998)

unless, in o rde r to reduce the predicted

a l lom e t r ic cons tra in ts and to com pen

sate fo r evident f l igh t constra in ts tha t

m igh t prevent them from having long

retention t imes, s m a l le r herb ivorous

Anatidae could: 1) increase retention of

the m os t d iges t ib le f ib re only (ie

th rough the fe rm en ta t ion in the caecae

of s m a l l part ic les f rom the select ive

retention of f lu id digesta) whi le m a in

ta in ing relatively fast passage rates,

and 2) have a h igher rate of m ic rob ia l

activity. These hypotheses are drawn

from the review by M cW il l iam s (1999)

on avian herbivores but more data are

needed to test them . Since body size is

though t to l im i t the qual i ty of food

ingested, B ru inzee l et at. (1998) sug

gested tha t it is possib le tha t s m a l le r

birds compensate fo r the i r apparent

re s t r ic te d ab i l i ty to d iges t f ib re by

select ing p lants of h igher qua l i ty (ie

conta in ing a h igher p roport ion of pro

te ins and solub le carbohydra tes and a

low er fibre content).

Anatidae species also vary in caecal

length (Bru inzeel et at. 1998; Kehoe &


Ankney 1985; Kehoe & Thomas 1987;

DeGolier et al. 1999). It is known that

gut and caecal lengths increase with

the am oun t of f ibre in the diet of g a l l i

naceous b irds (Moss 1972) and

Anat idae (Kehoe et al. 1988; M i l le r

1975; Whyte & Bolen 1985). In ga l l ina

ceous birds, the length of the caecae is

genera l ly indicative of the degree of

ce l lu lo ly t ic fe r m e n ta t io n (Gasaway

1976). However, the potent ia l re la t ion

ship between caecal length and fibre

digestion is unknown in herbivorous

Anatidae.

Practical implications

This review has im po r tan t im p l ica

t ions fo r the choice of a rel iable m a rke r

to quanti fy food passage and to assess

the digestive eff ic iency of food in h e r

b ivorous Ana t idae (Grajal & Parra

1995). The w orks of Marr io t t & Forbes

(1970) and Mattocks (1971) are often

ci ted to a f f i rm tha t fibre is not digested

by herbivorous Anatidae, and thus to

use fibre as an in te rna l marker. NDF

has been w ide ly used (Halse 1984;

Bédard & Gauth ier 1989; Mayes 1991;

B lack et al. 1992). However, h e m ice l lu

lose, which is a com ponent of NDF, is

digested in re latively large proport ions

(Sedinger et al. 1995), and can make a

large contr ibu t ion to energy acqu is i

tion, in pa r t icu la r in fo liage (ie 26% in

B ru inzee l et al. 1998; see also Dawson

et al. 1989). For these reasons, it seems

tha t NDF is not a rel iable marker.

Since ADF is in g ene ra l less

d igestib le than NDF, it is potent ia l ly a

m ore e ffect ive m a r k e r (Gadallah &

Jeffer ies 1995); it is also a m a jo r c o m

ponent of p lant tissue, which reduces

m easu rem en t error. For example, the

Austra l ian Wood Duck is able to digest

4-0% of NDF (because of the high h e m i

ce llu lose content of NDF), whereas the

digestion of ADF is only 9%, S um m ers

& Grieve (1982) showed tha t food

d igest ib i l i ty values obtained by the ir

inpu t /ou tpu t method or by the use of

ADF as a m a rk e r are s im i la r (25% vs

25%). They concluded tha t ADF is a re l i

able m arker , and it has been used in

m any s tud ies (Prop & Deerenberg

1991; M anseau & G au th ie r 1993;

Gadallah & Jeffer ies 1995; B ru inzee l et

al. 1998; van Eerden et al. 1998a). ADF

(and cellu lose) have the advantage of

being easy to use in field s ituations

(Prop & Deerenberg 1991; Gauth ie r

1996; ). However, ADF (and fibre in gen

eral) seem s to undergo variation in its

digest ib i l i ty th rough the annua l cycle

(Prop & Vulink 1992; van Eerden et al.

1998b). There is, therefore, a need for

more w o rk on th is aspect in o rder to

ascerta in the most rel iable m a rk e r to

use in ecological studies.

Since d iges t ion of ce l lu lose can

occur to som e extent, o ther w orke rs

have pre fe red to use l ign in

[Buchsbaum et al. 1986; Dawson et al.

1989; Am at et al. 1991; Prop & Vulink

1992). Indeed, l ignin is very res is tant to

degradat ion (Buchsbaum et al. 1986):

a lm os t a ll l ignin ingested by Barnacle

Geese was found in the faeces (97%)

(Prop & Vulink 1992). However, l ignin is

d i f f icu l t to m easure accura te ly (Van

Digest ion of f ib re in herb ivo rous Anatidae 19

Soest 1982], pa r t icu la r ly in the young

t issues of grasses and forbs consumed

by geese and grazing ducks, since it is

p resen t in low c o n c e n tra t io ns . For

som e authors, however, l ign in is a re l i

able m a rk e r provided tha t its m in im a l

concentra t ion in the forage is 6-7% of

dry m a t te r (Soest 1982: p. 131;

B uchsbaum et al. 1986; Van ). The su i t

ab i l i ty of l ign in as an ind iges t ib le

m a rk e r seems, however, to be in need

of re a s s e s s m e n t (Van Soest 1982;

S e d inge r et a l . 1989; Gada l lah &

Jeffer ies 1995).

Conclusion

Var ia t ions in the re s u l ts of the

n u m e ro u s s tu d ie s repo r ted in th is

review indicate the need fo r more m e a

surem ents , especia l ly on ducks and

swans. New stud ies on the d igest ib i l i ty

of fibre th roughou t a species's annua l

cycle are essentia l since ADF (and fibre

in general) undergoes var ia t ions in its

digest ib i l i ty according to the season.

This should increase the unders tanding

of the adaptive s igni f icance of such

variations. Moreover, the in terspec i f ic

fac tors of variat ion (ie body mass, cae

cal length) of fibre d igest ib i l i ty are not

clear. The p r io r i t ies fo r fu tu re research

should be exper im ents m ak ing s im u l

ta neous c o m p a r is o n s of f ib re

d igest ib i l i ty in var ious species tha t vary

in body size and gut m orpho logy under

s tanda rd cond it ions . Such s tud ies

wou ld pe rm i t a be tte r unders tanding of

the role of th is phenom enon in energy

budgets, fo rag ing behav iour and hab i

tat use in avian herbivores as w e l l as

resource part i t ion ing between species.

Acknowledgements

This review was supported by a doc

to ra l g rant to Daphné Durant f rom the

'C onse i l R ég iona l de Po itou -

Charentes'. I should like to thank the

INRA de Lusignan fo r the chem ica l

analyses. I should also like to thank

Glenn lason fo r his help in the l i te ra ture

search fo r papers on the subject, and

Patr ick Duncan, Hervé Fritz, Matth ieu

Gui l lemain and two anonym ous re fe r

ees fo r th e i r c o m m e n ts on the

m anuscr ip t .

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