CELLULOSE DIGESTION AND METABOLISM

BY C A P T I V E R O C K P T A R M I G A N
WILLIAM C. GASA\VAY*
Institute of Arctic Biology. University of Alaska, Fairbanks. AK 99701, U.S.A.

(Received 14 A.ugt*.st 1975)

Abstract--l, Carbon-14 labeled cellulose was fed to rock ptarmigan to provide evidence of cellulose
digestion and metabolism. Digestibility of cellulose and energy metabolized by ptarmigan fed a diet
of 6 and 30';0 cellulose were determined by a feeding trial.
2. Recovery of t'~CO2 in expired gases from ptarmigan fed t*C labeled cellulose demonstrates the
digestion and metabolism of cellulose by gut microbes and the ptarmigan.
3, Rapid recovery of 14CO2 in expired gases suggested preeccat digestion of cellulose,
4. Cellulose digestibility averaged 34~; and was not signiticantly different between groups of birds,
however, total cellulose digestion was significantly different in birds fed 6 and 309~, cellulose diets,
0-4 and 3.7 g/day, respectively.
5. Indirect evidence is presented which suggests cellulose digestion in the cecum is relatively eol~aplete.
6, Caged existence energy averaged 63 kcal/day and was not significantly different between birds
fed low and high cellulose diets.
INTRODUCTION
VUR"nZBRAa~animals are not capable of producing cellulases which are capable of hydrolyzing the 1-4 [~
linkage of cellulose a n d some other structural carbohydrates. Therefore, herbivorous birds rely on the
symbiotic bacteria of the gut to digest cellulose and
other complex carbohydrates (Halnan, 1949; Henning, 1929: Radefl: I928; Ziswitcr & Farner, 1972;
T h o r n b u r n & Willcox, 1965a,h). Evidence of microbial hydrolysis of cellulose was presented by Suomalainen & Arhimo (1945) who found cellulase activity in cultures from ceca of various tetraonids. The
metabolism of carbohydrates by microbes of the gut
is through fermentation yielding principally volatile
fatty acids (VFA) and ethanol (Beattie & Shrimpton,
t958; Shrimpton, 1963; Annison et at., 1968; McBee
& W e s t , 1969; Gasaway, 1975a,b), The c o n t r i b u t i o n
of VFA to free living energy requirements of willow
and rock ptarmigan has been estimated at 4 a n d 7 ~ ,
respectively (Gasaway, 1975a,b).
Estimates of cellulose a n d crude fiber digestibility
vary widely with diets a n d avian species, r a n g i n g from
0 to 50~'o (.Kaupp & lvey, 1922; Radeff, 1928; Maas,
1934; Mangold, 1934; Dymsza er aL, 1955; Halnan,
1949; T h o r n b u r n & Wiltcox, 1965a), Most cellulose
digestibility studies have been conducted using
domestic species with relatively small ceca; some
exceptions are studies of rock ptarmigan (Laoopus
mutus) (Moss & Parkinson, 1975), red grouse
(Laaopus lagopus scoticus) (Moss & Parkinson, 1972),
ruffed grouse (Bonasa umbeilus) and chukars (Alectoris
oracea) (Inman, 1973).
Disappearance of cellulose from the digestive tract
does not conclusively prove that the bird derived
energy from the cellulose. Therefore, the present experiment was designed to determine if carbon-14 ~aC
labeled cellulose was digested, metabolized a n d oxi* Present address: Alaska Department of Fish and
Game, 1300 College Road, Fairbanks, AK 99701, U.S.A.
179

dized to CO2 by rock ptarmigan. Since wild ptarmigan have adapted to a relatively high cellulose and
fiber diet, compared to grain or fruit eating species,
it is of interest to compare their ability to utilize cellulose as a n energy source. In the present study digestibility trials were used to estimate total cellulose digestion or dis~tppearance and energy metabolized by
rock ptarmigan fed high and low cellulose diets.
MATERIALS AND METHODS
Birds

Five 2-year-old captive rock ptarmigan were used in

cellulose digestion trials. Three of the above five birds were
used in the cellulose metabolism trial. These birds were
raised from chicks captured in the summer of 1970 at Eagle
Summit, Alaska (65~30' N, 145025' W). They were maintained indoors at 18C on a daily photoperiod of 18 hr.

Cellulose metabolism trial

Each ptarmigan was orally dosed with 0"5 ml solution
of I ~ methylcellulose suspending 7 ,ttCi of ground, purified
cellulose uniformly labeled with 14C (International Chemical and Nuclear Corp., lrvine, Calif.). All birds were fed
ad lib. until the time the dose was administered. The suspension had been acidified with HCI to release the volatile
CO2 then neutralized with KOH. The dose was administered by syringe through a polyethylene tube extended into
the esophagus. Immediately following dosing, the bird was
placed in a 10 gal airtiEht, plexiglass chamber. Carbon
dioxide free air was drawn through the chamber by a
pump, Carbon dioxide produced by the ptarmigan was
periodically collected as a Ba(CO3)2 precipitate by bubbling chamber air through a solution or 0-5 N NaOH and
9 ~ BaCI2. Samples were collected for approx 5 min in
duration at 15-45 min intervals during the 10--11 hr period
following administration of the labeled cellulose. Most fiequent CO2 sampling was carried out during the first 3
hr, the period of peak I'LC recovery. The Ba(COa)2 precipitate was filtered under suction, and rinsed with distilled
water, ethanol and ether. A 35--50 mg sample of the dried
Ba(COa): was weighed and suspended in 5 ml scintillation
cocktail (5 g PPO and (~1 g POPOP/L toluene with 2~,~

18()

W I I , I . I A M C . ('IAS,k!.',,'AY

El

Table 2. Me~ll daily energy consumed, excreted and rectabellied by captive rock ptarmigan

,4oot

Cellul0~e
content of
diet
(~)

"t
,oooIoot

rlO.
of

hlrds

30

Intake
(keallday)

[~creta (w{al/~v)
................
Intestin~I
Cecal

81.q(21.&)'" 28.)(S.7)t
147.7{1q.6)

6q.9(6.C)

Hetabolized
enemy
{kca|/d~v)

q.9(4.4) 48.~{11.3)
13.8(1,6%

73.0(11.S)

*:~ean (~tanaard deviation),

6O0

{,oo)- V /
f}~I

5(1 ~

"Yalues are s(qnWf~cantlv

"-o-k_o"-...
tSQk:l~;'5~30~:i~,~(~O
Time

A f t e r IngeNion

~r:,~:O'~3
/l-~in)

Fig. t. Speeilic activity of I'~C in expired CO, from O~ree

rock ptarmigan fed uniformly labeled [~'~C]eellulose and
maintained o n Purina flight conditioner (6",, celluloseL
Ce~d defecations occurred during the period indicated by
C.
C'ab-O-Sil). Sanlples were nidioassayed it| a Nuclear Chicago. Mark ! liquid scintillation systenl.
Celluh~xe dlqestihility trial

Apparent digestibility of food ~tnd cellulose was cstimatetl in two ptarmigan fed Purina flight conditioner (6",;
cellulose) and three birds fed Purina llight conditioner supplemented with powdered cellu|ose (3t)');, cellulose). All
birds had been previously maintained on Purina flight condilioner, however. 90 days prior to tile digestion trial the
three birds were changed to the 30",; cellulose diet. Two
wcek.~ prior to the experiment ztll birds were placed in
individt,al wire mesh cages.
|'ood intake and excreta o u l p t l t Were nleaStll-ed during
a 3-day period. Excreta was separated into droppings of
intestinal and cecal origin, o,,'en dried and weighed. Apparent digestibility of the diets was estimated by food intake
minus excreln output divided by intake. Ceilulose content
of food. intestinal and cecal excreta was determined
(Cr~,mpton & Maynard, 19381 and lotal cellulose digestion
was estimated by the difference between cellulose intake
and cellulose excretion. Metabolized energy was obtained
by subtracting the caloric energy of excreta from that of
food consumption.
RESULTS
Digestion and oxidation of the t'~C labeled celhlI o ~ occurred within 15-25 rain based on the recovery
of 14C in the expired C O , (Fig. 1). Peak concentration of ~ C in exhaled gases occurred 100--150 rain
after ingestion and were followed by a rapid decline

d i f f e r e n t (~,0.051 between nrouD$ OF birds,

in conoJntration, reaching low levels tO-I I hr after

ingestion ( Fig. 1).
Peak tdC specific activity varied considerably.
Defecation of labeled cellulose from the cecum during
a period when rapid digestion was occurring may
have resulted in the variability of peak i'~C specific
activity (Fig. 1t.
Apparent digestibility of the 6", cellulose diet (60";3
was significantly greater (P < 0-05) than tile digestibility of the 30",, cellulose diet lSt)"~,) (Table 11. This
difference in apparent digestibility of food was due
to the relatively low and similar cellulose digestibility
t31 and 36",,) determined for each group of ptarmigan
{Table I). However, tile total digestion of cellulose
was significantly different for ptarmigan fed the 6 nrtd
30"i, cctlulose diets. Birds fed the 30".,, cellulose diet
digested an a~'erage of 3.7 g cellulose/day or 9 times
more cellulose than birds fed the 6".o diet (Table I).
Tile ditierence in total digestion of cellulose was
clearly a result of cellulose intake being 8 times
greater by birds fed the 30",, cellulose diet. Energy
consumed and excreted was significantly greater
(P < 0-05) for birds fed the 30", cellulose diet, however. the energy metabolized was not significantly different (Table 2).

DISCUSSION

The recovery of ~4C in expired gases implies that

cellulose was digested and oxidized to COz. However,
microbial fermentation processes convert hexose to
VFA as tile principal end products and yield as a .
by product COz (Beattie & Shrimpton, I958; H u n gate. 1966; Annison e t aL, 1968) and likewise, CO2
is produced from the oxidation of these VFA by the
avian tissues (Annison e t al.. 19691. Therefore two
sources of l'~CO2 exist, namely gut microbes and
ptarmigan tissue, and t h e s e s o u r c e s cannot be distinguished. Since bacteria are capable of metabolizing
hexose (cellulose) to VFA and sincc VFA is oxidized

Table 1. Mean apparent digestibility of dry matter (DM) and cellulose by captive
rock ptarmigan
Cellulose

content
of diet
(%)

No.
of
birds

Food
consumed
(g/day)

21(5) +*

30

36(s)

Excreta (g/day)
Intestinal
/,lit.6)*

Is.o(/.9)

Cecal

Apparent ~
digestibility
(%)

Apparent

Cellulose

Cellulose
digestibility
(%)

cellulose
dlgestlon
(g/day)

in cecal
dro~)nqs
k*
4.5{1.8)*

1.6(0.6)

~(0.7)*

31(3)

O.a(O.l)*

2.2(0.2)

SO(Z.7)

3e(e)

3.7(0.4) Iz.4(2.6)

+Mean (standard deviation).

~alues a ~ significantly different (P~O.O5) between groups of birds.

Cellulose digestion and metabolism

by avian species, it follows that birds derive energy
from cellulose.
Recovery of t4CO, in respiratory gases commences
within 15-20 rain of ingestin of labeled cellulose. The
transit time for liquid and D M markers through the
intestine of rock ptarmigan was 54 a n d 84 rain, respectively (Gasaway et al., 1975). Hence 14C appears
in the respiratory gases prior to the labeled cellulose
reaching the cecum suggesting that partial degradalion and metabolism of cel|ulose by microbes occurs
anterior to the cecum. Evidence does exist for fermentation anterior to the cecum and the most likely, sites
would be the crop and ilium. Cecetomized fowl have
been reported to digest cellulose at levels approaching
lhat for normal fowl (Thornburn & Willcox, 1965,).
Annison et aL (1968) have reported VFA in the proventriculus, gizzard and small intestine of the fowl,
however Ille concentration of VFA was 0.05-0.1 of
t h a t , . ~ u n d in tim cecum. Also Moss & Parkinson
(1972~'report that concentrations of VFA in the posterior small intestine of wild red grouse were equal
to that found in the cecum. Although in one wild
rock ptarmigan, VFA cot~centralions in the small arid
large intestine were approx 0.05 the concentration
found in the cecal contents (Gasaway, unpubl, data).
In the domestic fowl. microbes were numerous in the
crop, declined in numbers in the gizzard and anterior
small intestine and again increased in the posterior
small intestine, however, these microbial concentrations were small compared to those found in the
cecum (Jayne-Williams & Fuller, 1971). Lactobacilli
predominate in the crop of domestic lbwl and lactic
acid concentration in crop contents is positively correlated with their numbers (Jayne-Williams & Fuller,
1971). Contrary to these reports, McBce & West
(1969) found no evidence for significant bacterial
action in any section of the digestive tract of willow
ptarmigan except the cecum, in spite of evidence indicating microbial digestion of carbohydrates in the
anterior gut, the cectun is considered the principal
site of digestion and fermentation by microbes (Annison et al., 1968) a n d the major site for cellulose digestion in rock ptarmigan (Moss & Parkinson, 1975).
Significant proportions of dietary cellulose are
digested in avian species with well developed ceca.
Rock ptarmigan digested 31-36~[, of dietary cellulose
in the present study and up to 41% in studies by
Moss & Parkinson (1975) which was greater than that
reported i n red grouse (14,%) (Moss & Parkinson,
1972), ruffed grouse, chukar and bobwhite quail (Colh~is virginianus) (I0--22~0/0) (lnman, 1973).
Digestion a n d catabolism of cellulose occurs
rapidly following ingestion by ptarmigan rather than
at a uniform rate over the duration that the labeled
cellulose remained in the intestine and cecum (Fig.
i). Entry of labeled cellulose into the cecum begins
a b o u t 45 rain after ingestion and is nearly complete
130 rain later (Gasaway et al., 1975). From the specific
activity curves (Fig. 1), it is suggested that either most
labeled cellulose entering the cecum was rapidly
digested or that only a portion of the cellulose was
rapidly catabolized with the undigested portion eventually excreted.
The concept that cellulose digestion is rapid and
nearly complete in the ptarmigan cecum is substantiated by low concentrations of cellulose in cecal

ISl

droppings, e.g. less than 2!'i; in captive red grouse

(Moss & Parkinson, 1972), approx 6", ill spruce
grouse (Canachitis camMensis) (Pendergast & Boag,
I9711, l l",i, in captive rock ptarmigan (Moss & Parkinson, 1975), l"g in wild rock ptarmigan (Gasaway,
unpubt, data) and 4.5 and 12-4'~'/,in the present study.
Low concentrations of cellulose in ce,~d droppings
could imply that very little cellulose enters the cecum,
however if only small quantities of cellulose entered
the cecum then the cellulose digested by birds in the
present study and in those by Moss & Parkinson
41972. 1975) and Inman (1973) would have had to
occur iu the crop or intestine. This seems unlikely considering the magnitude of lhc cellulose digested, the
rapid flow through the intestine and the low n u m b e r
of microbes in the crop and intestines as compared to
the cectnn. In addition, Moss & , Parkinson (1972,
1975) found significant a m o u n t s of lignin in cecal
droppings of red grouse and rock ptarmigan. Since
lignin and cellulose are bonded in cell walls of plants,
significant a m o u n t s of cellulose likely entered the
cecum with the lignin. Hence, a high digeslibility of
cellulose in the cecum is likely to be the reason for
the observed low cellulose concentration and low
cellulose to lignin ratios in cecal droppings (Moss &
Parkinson. 1972, 1975).
M E intake by rock ptarmigan averaged 63 kcal/day
which was lower than the 67 kcal/day (80 kcal/day
when corrected for weight loss) found by Moss &
Parkinson (1975)and the 71 kcal/day lbr the resting
metabolic rate reported by West (1972).
Acknowledgemems--The author lhanks Drs. G. C. West,
R. G. White and D. F. Holleman fo," guidance during the
study and review of the manuscript, Drs. R. Moss and
D. A. Boag for criticism of the manuscript and Mr. A.
M. Gau and Mrs. Marilyn Ailes for tcchnicad and analytical assistance. The research was supported (in part) by
NIH research grant number GM 10402. awarded by the
Institt,le of General Medical Sciences. PHS/DHEW, and
Atomic Energy Commission Comract AT i45-1-22291.

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182

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