the digestion of fibre in herbivorous anatidae - a review
TRANSCRIPT
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).
10 Digest ion of f ib re in herb ivo rous Anatidae
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
Bruinzeel et al. 1998
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
Bruinzeel et al. 1998
Mute Swan
Cygnus olor
10. 7 foliage marker: ADF 30. 0 winter-
autumn-
spring
Bruinzeel et al. 1998
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
Bruinzeel et al. 1998
Wigeon
Anas penelope
0. 6 seeds, tubers marker: ADF 35. 0 - - w inter-autum n-
spring
Bruinzeel et al. 1998
Barnacle Goose
Branta leucopsis
1. 8 seeds, tubers marker: ADF 0-29. 0 ■ ■ ■ w inter-autum n-
spring
Bruinzeel et al. 1998
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
Bruinzeel et al. 1998
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
Bruinzeel et al. 1998
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
Bruinzeel et al. 1998
? 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 &
18 Digest ion of f ib re in herb ivo rous Anatidae
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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