frugivorous bat
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BiologíaTRANSCRIPT
-
~) Pergamon Biochemical Systematics and Ecology, Vol. 22, No. 2, pp. 137-151, 1994 Copyright 1994 Elsevier Science Ltd Printed in Great Britain. All rights reserved 0305-1978/94 $6.00 + 0.00
The Value of Figs to a Hind-gut Fermenting Frugivore: a Nutritional Analysis
NANCY LOU CONKLIN* and RICHARD W. WRANGHAM Department of Anthropology, Peabody Museum, Harvard University, Cambridge MA 02138, U.S.A.
Key Word Index--Ficus; figs; nutritional value; carbohydrates; fermentable fibers; frugivory. Abstract--The fleshy wall of figs is an important food item for a wide range of frugivore animals. However, the nutritional significance of figs as a genus is poorly understood and somewhat puzzling, since there is considerable variation among species in chemical content. This study examined nutritional features of nine species of Ugandan figs, from Kibale Forest, eaten by chimpanzees (Pan troglodytes) and many other frugivores. Fig samples were chemically analyzed for their percentages of lipid, crude protein (CP), available protein, water-soluble carbohydrates (WSC), pectin, total cell wall, hemicellulose, cellulose, lignin, cutin, tannins, dry matter and total ash. Complex carbohydrates (cxCHO) were calculated by difference. The pulp or flesh of the figs was analyzed separately from the seed fraction. None of the assayed nutrients alone explain why figs are eaten by so many of the frugivores in Kibale Forest. Furthermore, standard calculations suggested that figs have rather low values of metabolizable energy (ME). However ME may be misunderstood when calculated by the orthodox method, because it does not acknowledge nutritional components available to frugivores capable of fore- or hind-gut fermentation. As a result of including pectin, hemicellulose and cellulose as potential energy sources through fermentation, we suggest that total ME for a chimpanzee is some 50% higher (2.78 kcal g-~ compared to 1.91 kcal g ~) than estimated purely on the basis of cxCHO, WSC, CP and lipid. When calculated in this way, the digestibility/fermentability of soluble and insoluble fiber components may explain the attractiveness of figs to many frugivores.
Introduction The genus Ficus contains some 750 species and occurs in all tropical regions. All Ficus species produce edible figs ("fruits", or synconia; Janzen, 1979). Diverse mammals and birds eat figs, and some species rely heavily on them when non-fig fruits are scarce [e.g. Sumatran orangutans, Pongo pygmaeus (Sugardjito eta/., 1987); Ugandan chimpanzees, Pan troglodytes (Wrangham et al., 1991)]. The aim of this study is to understand the nutritional basis for fig-eating by frugivores such as chimpanzees and determine whether there are shared chemical features responsible for making figs of different species attractive to a wide variety of generalist frugivores.
Despite the importance of figs as food sources for a wide variety of generalist and specialist frugivores, relatively little is known about their nutritional value. There are at least two kinds of problem. First, generalizations appear inconsistent. Many studies refer to figs as low quality foods, principally because they are not high in protein (Jordano, 1983; Herbst, 1986; Bronstein and Hoffmann, 1987; Lambert, 1989). In contrast, in her study of African hornbill foods, Kalina (1988) found that F. exasperata figs were excellent sources of protein (Table 1). There is clear evidence that some of the reported nutrient differences between fig species are real, and influence frugivore feeding behavior. Thus Leighton (1993) found that selectivity among figs by orangutans varied positively with the concentration of water-soluble carbohydrates (WSC) and negatively with total phenolics and condensed tannin. What is unclear from such comparisons is what makes figs generally attractive, especially since WSC concentrations are normally low (Table 1).
Second, few of the available data are comparable. Previous studies have rarely
*Author to whom all correspondence should be addressed.
(Received 16 June 1993)
137
-
TA
BLE
1 C
HEM
ICA
L CO
MPO
SIT
ION
OF
FIG
S R
EPO
RTE
D IN
TH
E L
ITER
ATU
RE
Speci
es
Non-f
iber
carb
ohydra
tes
Fiber f
ract
ions
DM
ash
EE
C
P PD
C
TP
CT
energ
y
TN
C
WSC
N
FE
ND
F A
DF
C
HC
L cu
t.
pe
c.
Item
p/s
%
%
%
%
%
%
%
kc
al g
%
%
%
%
%
%
%
%
%
%
S
ou
rce
t
E a
cam
pto
ph
ylla
F. b
enja
min
a
F, b
Jnne
ndiy
kfi v
. lati
fofia
E b
ract
ea
ta
F~ ca
rica
*
Ecar
ica
F ca
nca
* E
con
soci
ata
fi
co
nti
nif
olia
F.
cra
ssir
amea
E d
elo
syce
v. o
btu
sa
E d
ep
ress
a
E d
ub
ia
E e
xasp
era
ta
E e
xa
spe
[ata
E g
na
ph
alo
carp
a
E g
na
ph
a/o
carp
a
#
Tsip
lda
msi
pJda
E
insi
pid
a
E in
st~
oida
E
insp
ida
/h
sfp
ida
E
ma
cro
spe
rma
E m
acr
osp
erm
a
rp
4.1
rp
6.6
rp
4.6
d
37.7
3.1
2.4
5.6
ff
22.0
tr
ace
4.1
df
77,0
tr
ace
4.8
ff
14.8
1.4
5.4
rp
4.4
rp
2.0
33.6
8.8
2.7
5.3
rp
5.0
rp
5.0
rp
5.6
rf
27.6
5.6
5.8
6.4
f f
21.1
f 21.5
5,4
7
1
f rf
38
.0
2,8
4
5
rf
25.0
2.2
6.1
rf
23.0
3.5
-->
4.5
rf
6.4
8.8
rf
7.0
6
4.3
rf
p
16.4
4.9
4.3
sk
19,1
5.9
1.8
3.5
6.8
0.4
0.0
1.1
0,7
8.5
4.6
3.8
4.8
0.8
1.
1
2.5
9.0
1.4
1.8
2.2
0
.0
2.2
0
.0
1.0
21
.8
17
.8
11,0
8.5
8.9
3.6
91.8
2.8
71.4
3,4
35.3
53.8
18.5
75.0
56.4
49.2
48.9
26.7
80.4
39.3
51.0
59.5
23.7
42.0
51.9
34.7
49.9
33.8
58.8
57.2
33.0
77.7
23.2
37.8
22.4
30.1
12.2
341
26
.7 1
6.1
7.4
6.0
4.6
27
3
27.4
37.4
21.8
Leig
hto
n, 1
993
Leig
hto
n, 1
993
Leig
hto
n, 1
993
Subra
mania
m, 1
981
AR
S, 1964
AR
S,
1964
Leung, 1
968
Leig
hto
n, 1
993
Jord
ano, 1
983
Leig
hto
n, 1
993
Leig
hto
n, 1
993
Leig
hto
n, 1
993
Subra
mania
m, 1981
Gart
lan e
t al.,
1980
Kalio
a, 1
988
Hla
dik
et a
L, 1
971
Wra
ngham
and W
ate
rma
n
1983
Hla
dik
et a
L, 1
971
Hla
dik
eta
L, 1
971
Hla
dik
et a
L, 1
971
Milt
on a
nd D
intz
is, 1
981
Milt
on e
taL,
1980
121
Milt
on, 1
991
Rogers
et a
L, 1
990
Rogers
et a
l., 1
990
-
E m
ucu
so
f 15.0
7.1
8.4
2.3
5.4
10.7
39.1
R
ogers
et a
L, 1
990
F.. o
btus
ifol
ia
rf
3.9
M
ilton, 1
991
F, o
valis
p
1.4
21.5
5.2
3.8
35.4
H
erb
st, 1
986 poole
d 1
30 fr
uit
s
F. p
aya
rf
26.9
4.2
11.9
6.9
1.4
0.6
6.8
39.5
23,8
Subra
mania
rn, 1981
F. p
isoc
arpa
rp
5.2
2.3
7.5
39.1
48.2
Le
ighto
n, 1
993
F. p
lafy
phyl
la
ff
17.0
0.6
1
1.2
3,5
59.4
Le
ung, 1
968
F.. p
ertu
sa
0,1
8.0
W
heelw
right e
t al.,
198
4 F.
rec
urva
ta
p
19.4
1.9
2.7
2.7
8.0
37,5
27.3
R
ogers
eta/
., 1
990
F. r
ecur
vata
sk
17.8
2.3
4.1
2.6
8.1
24.0
33.5
R
ogers
etaL
, 1990
F. s
chw
arlz
ii
rp
8.7
2.1
1.8
34.5
54.7
Le
ighto
n, 1
993
F, s
tup
end
a v. m
ino
r rp
3.9
0.4
0.8
50.7
44.6
Le
ighto
n, 1
993
F. s
ubte
cta v
. nov
. rp
4.5
3.0
7.4
37.4
50.9
Le
ighto
n, 1
993
F. s
umat
rana
v. s
um
atra
na
rp
5.5
3.1
5.4
33.0
56,1
Le
ighto
n, 1
993
F. s
um
atra
nav
, mic
rosy
ce
rp
5.1
3.1
1
0.0
28.2
56.1
Le
ighto
n, 1
993
F. s
unda
ica v
. bec
cari
ana
rp
4.1
3.1
11.3
34.5
50.1
Le
ighto
n, 1
993
F to
nduz
ii f
22.0
4.8
>5
.9
12.5
-3
1.4
12.2
H
ladik
eta/
., 1
971
F. tr
Jcho
carp
a v.
bom
een
sis
rp
4.8
1,5
0,7
52.9
40.8
Le
igh
ton
, 1993
F. t
rich
ocar
pa v.
ob
tusa
? rp
7.7
0.8
0.0
45.1
43.B
Le
ighto
n, 1
993
F. t
rigo
nata
rf
5.0
M
ilton, 1
991
F. t
uerc
khei
mii
0.1
6.0
W
heelw
right e
t al.,
198
4
F. u
rceo
lari
s f
0.3
W
rangharn
and W
ate
rman,
1983
F. v
a//ia
-cho
udae
f
0.8
W
rangharn
and W
ate
rmark
, 1983
t~ vi
llosa
v, a
ppre
ssa
rp
6.2
3.1
3,8
50.1
38.8
Le
ighto
n, 1
993
xan
thop
hyl
la
rp
4.9
3.8
4.6
42.3
48.2
Le
ighto
n, 1
993
F, y
opon
ensi
s f
7.5
56.5
38.9
31.3
1
5,0
7.6
9.6
6.7
M
ilton e
ta/.
, 1980
*Dry
matt
er v
alu
es g
iven w
ere
calc
ula
ted fro
m th
e fr
esh
fru
it valu
es p
ublis
hed.
tSe
e th
e re
fere
nce
liste
d fo
r th
e a
uth
ori
ties u
sed w
he
n n
am
ing th
e Fic
us sp
eci
es.
A
s desi
gnate
d by a
uth
ors
: rf=
ripe fr
uit
(whole
); if
= fr
esh
fru
it; d
f = d
ry fr
uit
; rp =
ripe p
u(p
; fi =
flesh
putp
(pu
lp-s
kin
); f=
fru
it (p
resu
med whole
); p
= p
ulp
; sk =
skin
. p/s
= p
ulp
to s
eed ra
tio; D
M =
dry
m
att
er;
EE =
eth
er e
xtr
act
(fat)
; CP
= cru
de p
rote
in; P
DC
= cru
de p
rote
in dig
est
ion co
eff
icie
nt;
TP =
tota
l phenolic
s; C
T=
condense
d ta
nnin
s; TN
C =
tota
l non-s
truct
ura
l carb
ohydra
tes;
WS
C=
wate
r-so
tub)e
ca
rbohydra
tes;
NFE
= n
itro
gen fr
ee e
xtr
act
; ND
F =
neu
tral
-det
erg
ent fi
ber;
AD
F=
aci
d-d
ete
rgent fi
ber;
C =
cellu
lose
; HC
= h
erni
cellu
lose
; L =
}ig
nin
, cu
t= cu
tin;
pec =
pect
in. S
om
e v
alu
es
have b
een
convert
ed from
the fo
rm th
ey w
ere
ori
gin
ally
expre
ssed in
so
th
at a
ll valu
es a
re re
port
ed in
the
sam
e fo
rma
t.
-
140 N.L. CONKLIN AND R. W. WRANGHAM
presented complete chemical analyses (Table 1), and where data are available from different studies, methodological problems make them difficult to compare. Analytical procedures, and even nutrient nomenclature, differ widely. For example, considering whole fruit, species in Table 1 show large standard deviations for total non-structural carbohydrates (TNC) (mean 44.7%, S.D. 43.4) and nitrogen-free extract (NFE) (mean 72.5, S.D. 11.4). Theoretically these two categories represent the same chemical fraction, measured by different methods. Given the inherent problems in the standard method of analysis (the Proximate Analysis Method) it is difficult to know whether these differences are real (van Soest, 1982). For example the lower values reported as TNC or NFE might, in some studies, have been better labelled water-soluble carbo- hydrates (WSC). The essential problem is that these components are calculated indirectly (by subtraction), and there is variation in what is subtracted. By contrast, the large standard deviations for reported values of WSC and lignin (Ls) are likely to be real, because these analyses use newer methods designed to measure these fractions directly rather than by subtraction (van Soest, 1982).
A further source of confusion is that studies vary in which part of the fig is analyzed, between pulp (the only fraction digestible by most frugivores), seeds [digested only by seed predators such as Treron pigeons (Lambert, 1989)] and whole figs (Janzen, 1979). Previously we have shown that in comparison to pulp-only assays, whole fig assays tend to exaggerate the concentrations of fiber, tannins and lipid. Calculated calories and protein are affected less (Wrangham et al., 1993).
In this paper we present relatively complete analyses of the chemical characteris- tics of nine species of Ugandan figs. Each of these species is eaten intensively by a variety of generalist frugivores (Wrangham et aL, 1993). Our aim is to find out whether the different fig species have chemical characteristics in common that can explain their significance as a food source. We focus on chimpanzees, a hind-gut fermenter, because in vivo feeding trials have been performed on chimps to determine their ability to digest/ferment fiber (Milton and Demment, 1988). Alternatively, small ruminants, the duikers (genus Cephalophus), could be considered because in vivo feeding trials have been performed on them also (Hart, 1986). The necessary digestibility information is not available for other African frugivore species.
Materials and Methods Study site and samples. Fig samples of nine Ficus species were collected in Kibale Forest, Uganda, a 560 sq km reserve at Kanyawara (034"N, 3021"E, altitude 1500 m). Annual rainfall is 1500-1800 mm, and supports a multi-canopy forest to 50 m. Ripe figs were collected from the ground, avoiding those damaged by insects or vertebrates, and ideally collecting those that had just been knocked down by socially active animals. The samples were collected from October 1987 to November 1989 and air-dried in the field. Where replicate samples are reported they represent collections from more than one tree.
In reference to previously published literature from Kibale forest, Ficus brachylepis has been re-named as E sansibaricaWarb, subsp, macrosperma (Milbr. & Burrer) C. C. Berg, F. urceolaris as F. asperifolia Miq.; E dawei as/ : saussureana DC; and F. stipulifera as F. conrauiWarb. The other figs analyzed are: ~" exasperata Vahl., /: mucuso Ficalho, F. cyathistipula Warb.,/: natalensis Hochst. and /: thoningii BI. (Berg and Hijman, 1989).
Analytical techniques, Analysis was carried out in the nutritional biochemistry laboratory in the Anthro- pology Department of Harvard University. The pulp and seeds were separated and analyzed separately, except for Ficus thoningii because it was a very small sample. The pulp fraction included the wall and outer skin of the synconium. The seed fraction included seeds and the "true" fruit chaff immediately surrounding the seed. Standard chemical analyses were performed to estimate nutritional value. Protein. Crude protein (CP) was determined using the Kjeldahl procedure for total nitrogens and multiplying by 6.25 (Pierce and Haenisch, 1947). The digestion mix contained Na2SO 4 and CuSO~. The distillate was collected in 4% boric acid and titrated with 0.1 N HCI. This method very accurately measures total nitrogen, but preliminary work questions the 6.25 conversion factor (Milton and Dintzis, 1981).
To correct for some of the shortcomings of the Kjeldahl method, insoluble nitrogen fractions were deter- mined by performing the neutral-detergent or acid-detergent extraction and then the Kjeldahl procedure on that residue (Pichard, 1977a; Krishnamorthy, 1982), These values were multiplied by 6.25 to give neutral- or acid-detergent fiber crude protein (NDF-CP or ADF-CP). The ADF-CP fraction is totally unavailable protein
-
VALUE OF FIGS TO A HIND-GUT FERMENTING FRUGIVORE 141
and is subtracted from CP to give an estimate of available crude protein. The NDF-CP fraction in insoluble but not totally unavailable crude protein. Soluble protein is obtained by subtracting NDF--CP from CP.
The necessary in vivo protein digestibility information is not available for frugivore species. Consequently we draw only limited conclusions regarding protein availability. Other protein measuring methods also would be limited by this lack of in vivo digestibility information for vertebrates. Direct measurement of fibers, carbohydrates and h'pids. The detergent system of fiber analysis (Goering and van Soest, 1970) as modified by Robertson and van Soest (1980) was used to determine the neutral-detergent, or total cell wall fraction (NDF), hemicellulose (HC), cellulose (Cs), sulfuric acid lignin (Ls) and cutin. Lipid (LP) content was measured using petroleum ether extraction for 4 days at room temp., a modification of the method of an Association of Official Analytical Chemists (AOAC, 1984). Water-soluble carbohydrates (WSC) were estimated using a phenol/sulfuric acid colorimetric assay of Dubois et al. (1956), as modified by Strickland and Parsons (1972) and using sucrose as a standard. Total pectin content was determined directly on untreated samples and on samples that had been ND extracted first, following the colorimetric m- hydroxydiphenyl method of Blumenkrantz and Asboe-Hansen (1973) as modified by Bucher (1984). In this method total pectin is extracted from plant material using 72% sulfuric acid. Polyphenolics. Condensed tannin or proanthocyanidin (C'I') content was measured using the proanthocyanidin test of Bate-Smith (1975) and modified by Porter et al. (1986). Total tannin or protein binding ability was determined using the radial diffusion (RD) method of Hagerman (1987). Quebracho was the standard used for both assays. Water, ash and organic matter. Dry matter (DM) was determined by drying a subsample at 100C for 8 h and hot weighing. Total ash was measured by ashing the above subsample at 520=C for 8 h and then hot weighing at 100C. Organic matter (OM) was calculated as: (1--ash)*DM. Indirectly measured carbohydrates and energy. The remaining complex carbohydrate (cxCHO) fraction was estimated by subtraction. This fraction, in keeping with historical nomenclature, could also be referred to as the nitrogen-free extract (NFE). The calculation is 100 minus (sum of all the directly measured nutrient fractions, plus ash and fiber).
Total calories were calculated based on the energetic value of the above nutrient fractions assuming the values of 9 kcal, g-~ lipid, 4 kcal g-* protein and 4 kcal g-~ digestible carbohydrate taken from literature on humans, therefore giving an estimate of metabolizable energy (ME) [National Research Council (NRC), 1989]. For the fermentable fractions (pectins and cell wall constituents) 3.3 kcal g-1 was used because out of 36 moles of ATP per glucose unit, about 6 are lost to anaerobic microbes. The digestion coefficient used for the NDF was 54.3% from Milton and Demment (1988). This coefficient may be generous because the NDF levels in most of the figs were higher than the 34% used in their feeding trials, but it is the only value available.
Results Standard chemical analyses were relatively consistent within species, as shown by the small standard deviations (Table 2).
There were marked differences in the composit ion of the pulp and seed fractions. For example, NDF values were significantly higher in seeds than pulp in all species (seeds: 74.0%+5.1; pulp: 43.3%+11.9; t=--6.195; P
-
TA
BLE
2. S
UM
MA
RY O
F A
VER
AG
ED
VA
LUES O
BTA
INED
FO
R T
HE P
RIN
CIP
AL
NU
TR
IEN
T F
RA
CTIO
NS, O
N A
N O
RG
AN
IC M
ATTER
(O
M)
BA
SIS
p/s
ash
D
M
LP
CP
CT
WSC
N
DF
n
%
S.D
. %
S.D
. %
S.D
. %
S.D
, %
S.D
. %
S.D
. %
S.D
. %
S.D
.
cxC
HO
C
alc
ula
ted
calc
ula
ted
ME k
cal g
Genus
Ficu
s se
ct. S
ycid
ium
Fi
cus a
sper
ifolia
2
pulp
53.5
3.5
8.4
0.2
seed
46.5
3.5
7.7
2.8
w
hole
8.0
1.4
25.6
10.4
rati
o
1,2
Ficu
s exa
sper
ata
9
pulp
53.5
10.2
10.4
3.1
seed
46.5
10,2
5.8
2.8
w
hole
8.2
2.7
19.4
7.2
rati
o
1.2
subgenus S
ycom
orus
Ficu
s mucu
so
1
pulp
65.7
8.8
seed
34.3
5.3
whole
7.6
ra
tio
1
.9
Subgenus U
rost
igm
a se
ct. G
alog
lych
ia
Gro
up 1
Ficu
s san
sibar
lca
pulp
seed
whole
ra
tio
56.2
15.7
6.4
1.6
13.3
3.0
43.8
9.2
2
9
0.9
41.2
4.8
0.7
16.7
2.7
1.3
7.9
0
.4
16.1
3.0
0.2
0.1
23.0
1.3
23.5
3.8
9.4
1.6
16.4
1.2
0.4
0.1
13.3
0
.7
~.4
1.8
8.6
0
.6
16.3
2,2
0.3
0
.0
18.5
0.7
4
2.6
11,5
6.2
2.1
20.7
6.6
0.4
0.8
13.5
3.5
44.7
7.8
5.5
4
.5
13.9
4
.7
1.3
2.8
4
.6
t.0
75.6
5.2
5.9
2,9
17.4
5.4
0
7
1.4
9
,6
3.2
59,3
3.3
4.5
4
,4
0.4
23.2
34.9
7.5
9.1
4
.3
12.3
6
6.5
5.5
6
.0
17
19.5
45.7
3.5
1.2
9
.4
1,3
0.5
0.2
14.2
4
.8
35.7
5.0
90
2.3
8.2
1.2
1.1
0.4
4.9
3.4
7
3.9
4.9
5,7
1.2
9
.0
09
0
7
0.3
9
.2
3.3
52,2
6,2
29.4
3.4
4.0
2.0
13.7
2.7
14.4
2.5
0.8
1.2
7.2
1 9
32.6
2,8
0.4
1.5
21.5
2.4
36.6
2.7
2.9
1.4
23.2
2.2
-
Gro
up 2
Ficu
s cya
sthis
tipula
pulp
se
ed
whole
Ficu
s nata
lensi
s pulp
seed
whole
Ficu
s th
on
ing
ii w
ho
le
Gro
up 3
Ficu
s con
raul
pulp
se
ed
wh
ole
rati
o
rati
o
49.3
6.6
0.0
~
.7
2.9
0.3
5.3
0.8
1
.0
~.6
4.0
5.7
1.6
16.7
31.4
4.0
5.7
1.7
29.5
5.8
1.5
17.0
1.8
2
.2
5.1
0.1
4.3
0.1
0.2
0.2
12.8
0.8
50.4
0.6
27.2
2.2
11.3
0.6
6.6
0.1
1.7
0.3
4.1
0.4
78.4
0.1
--
2.2
1.4
7.6
1.3
5.2
0.4
0.7
0.6
10.3
2.9
61.6
3.9
14.6
1.9
1.7
0.2
6.5
0.3
0.9
1.0
8.2
2.4
65.4
5.4
17.3
1.4
1.5
0.6
6.1
0.2
2.9
1.2
7.6
4.9
75.7
10.0
6.2
0.9
2.4
0.8
6.7
0.4
1.5
0.7
8.0
3.1
~
.3
6.3
13.1
1.3
4.6
1,0
8.4
0.2
2.9
70.8
16.7
1.2
~.1
7.0
2.7
7.8
0.8
20.0
~
.6
25.1
2.4
~
.9
3.3
10.9
7.4
3.9
6.8
76.3
--
5.4
1.6
5.4
12.1
6.3
7.6
2.2
14.2
~
.0
11.7
1.9
ra
tio
1
.3
Gro
up 3
Ficu
s sau
ssur
eana
2
pulp
49.7
2.3
8.8
1.8
se
ed
50.4
2.3
4.2
0.1
w
ho
le
6.5
0.8
ra
tio
1
.0
4.6
0.2
8.6
1.3
1.3
0.2
6.6
1.1
~
.9
9.8
27.9
2.1
8.4
2.3
9.2
1.0
1.9
0.2
2.4
0,3
79.0
2.4
--
1.0
1.2
6.6
1.1
8.9
1.1
1.6
0.2
4.5
0.8
65.2
5.4
13.2
1.7
E -n
C3
(/3
-1-
w
Z
G} 5 -n
z z C
p/s
= %
pulp
or se
ed, w
hen li
sted fo
r wh
ole
fruit
s it i
s th
e ra
tio; %
= p
erc
enta
ge org
anic
matt
er;
DM
= d
ry m
att
er;
bla
nk s
pace
s are
unavaila
ble
data
poin
ts; L
P =
lipid
; CP
= cru
de p
rote
in; C
T =
condense
d
tannin
s; W
SC
=w
ate
r so
luble
carb
ohydra
tes;
ND
F=neutr
al-
dete
rgent fi
ber,
als
o c
alle
d t
ota
l ce
ll w
all;
cx
CH
O=
co
mp
lex
ca
rbo
hyd
rate
s=n
itro
ge
n
free e
xtr
act=
10
0-(
LP
+N
DF+
CP
+W
SC
+C
T);
M
E =
meta
boliz
able
energ
y, c
alc
ula
ted as:
9 k
cal g
~
(LP)+
4 kc
al g
I
(CP+
WSD
C+
cxC
HO
), fo
rmula
base
d o
n h
um
an lit
era
ture
.
-
144 N. L, CONKLIN AND R. W. WRANGHAM
To test this, we calculated metabolizable energy (ME) by summing the energy in WSC+cxCHO+CP, and in lipid (NRC, 1989); Table 2. Pulp ME mean was 2.4 kcal g 1-+0.6, but there was substantial variation among species. For example, ME pulp values varied between 1.4 kcal g-1 (F. natalensis) and 3.4 kcal g-1 (F. asperifolia). Again, therefore, this analysis does not suggest that figs present a consistent nutritional opportunity to frugivores. Comparison of our ME values (Table 2) with previous data (Table 1) indicate that our figures are significantly lower (for whole fruit: Table 1 mean ME is 3.3 kcal g-1-+0.4; Table 2 mean ME is 1.9 kcal g 1-+0.5; t = 5.195; P
-
TA
BLE
3. S
UM
MA
RY O
F A
VER
AG
ED
VA
LUES O
BTA
INED
FOR
TH
E A
DD
ITIO
NA
L N
UTR
IEN
T F
RA
CTIO
NS A
ND
A M
OR
E C
OM
PLE
TE B
REA
KD
OW
N O
F TH
E F
IBER
FR
AC
TIO
N
Pro
tein
fract
ions
Solu
ble
fiber
ND
F-C
P
AD
F-C
P
AC
P TPc
ND
Pc
%
%
%
n
%
S.D
. %
Inso
luble
fiber f
ract
ions
ND
F A
DF
HC
C
s LS
cu
tin
cor-
LS
S.D
. %
S.D
. %
S.D
. %
S.D
. %
S.D
. %
S.D
. %
S.D
. %
S.D
. m
E
Ficu
s asp
erifo
lia
pulp
1.5
1.5
seed
wh
ole
Ficu
s con
raul
pulp
4.5
3.4
seed
whole
Ficu
s cya
this
dpula
pulp
2.2
2.8
seed
wh
ole
Ficu
s exa
sper
ata
pulp
5.0
2.0
seed
wh
ole
Ficu
s mucu
so
pulp
2.6
2.0
seed
whole
Ficu
s nat
alen
sis
pulp
3.2
1.9
seed
wh
ole
Ficu
s san
sibar
ica
pulp
3.3
2.9
seed
wh
ole
Ficu
s seu
ssur
ena
pulp
5.6
4.0
seed
whole
12.4
1
8.7
1
2.9
1
5.9
1.5
1
21.1
16.5
4.7
11.8
4.6
4.4
1
10.5
1
2.3
1
6.9
1.3
1
43.6
~
.7
6.9
19.4
17.2
1.5
2
11,3
2.3
0.9
2
46.5
2.1
41.9
2.1
4.6
. 0.0
18.6
4.2
23.3
2.0
10.6
11.2
2
2.3
1.4
1
74.8
~
.1
10.6
25.7
3
.4
26.0
12.5
2
2.7
3.9
1
61.6
~
.9
7.6
23.7
30.2
18.4
11.9
23.4
4
5.9
3.2
2.1
3
2.8
0.4
3
4.4
1.8
2.4
1
11.1
1
3.3
1
8.4
-11
Gb
O
Z
c?
c z Gb
C
6b
<
3
29.4
4.3
21.5
3.5
8.0
1.5
15.0
2.0
6.4
1.7
3.5
1.9
2.9
1.6
m
3
75.0
1.8
62.2
2.4
12.9
0.7
18.8
7.0
43.3
5.0
~
,6
9,8
6,7
4.8
3
49.6
7.0
39.6
5.3
10.1
1.6
16.1
2.3
23.5
6.5
19.1
8.6
4.3
2.2
1.4
1
~.9
29,9
5.0
19.0
10.9
63.9
4.3
~
.7
4.0
9.1
2.1
27.2
2.2
27.5
1.B
15.3
6.6
12.2
1.9
79.4
8.3
73.5
0.5
5.8
7.7
26.5
1.6
47.1
0.9
33.1
3.6
14.0
2.7
70.6
1.4
62.1
2.8
8.5
4.1
27.4
1.2
~
.7
1.6
21.2
2.0
13.5
0.4
4,2
3
7.2
1.5
2.2
3
2
5.2
1.1
2
2
6.5
1.7
2
6.5
4
3.9
0.9
1.5
4
4
3.2
0.4
4
4
3.6
0.6
4
36.1
7.0
28.7
6,8
7.4
1.0
19.3
2.9
9.4
4,0
4.1
2.4
5.4
1.6
72.3
5.9
59.7
6.6
12.6
3.2
28.2
3.2
31.5
3.4
21.6
3.1
10.0
0.4
52.4
6.0
42.6
6.1
9.7
2.0
23.3
2.8
19.3
3.6
11.9
2.6
7.5
1.1
5.5
1
6.2
1.4
1
55.1
44.5
10.6
21.7
23.0
13.9
9.0
1
2.3
1
79.7
75.8
3.8
22.8
53.0
36.3
16.8
1
4.3
1
67.1
59.8
7.3
22.2
37.6
24.8
12.8
ND
F-C
P =
Cru
de p
rote
in (C
P) in
th
e n
eutr
al-
dete
rgent fiber;
AD
F-C
P =
CP
in th
e a
cid-d
ete
rgent fiber;
AC
P =
availa
ble
CP
= C
P fr
om
Table
3 m
inus A
DF-
CP;
TPc
= to
tal p
ect
in; N
Dpc =
pect
in co
nta
min
ati
ng
the n
eutr
al-
dete
rgent fiber;
ND
F =
neutr
al-
dete
rgent fiber;
AD
F =
aci
d-d
ete
rgent fiber;
HC
= h
em
icellu
lose
; Cs
= cellu
lose
; Ls =
lignin
dete
rmin
ed by th
e s
ulfuri
c aci
d m
eth
od; c
or-
Ls =
corr
ect
ed lig
nin
= L
s
min
us c
uti
n. B
lank s
pace
s are
due to
insu
ffic
ient sam
ple
.
-
146 N.L. CONKLIN AND R. W. WRANGHAM
values, we performed further assays for cutins, because in the detergent method of cell wall analysis, cutin is a contaminant of the lignin fraction unless a second procedure is sequentially performed [the potassium permanganate procedure (Goering and van Soest, 1970), followed by ashing]. The sequential procedure isolates what has been shown in other plants, particularly in seeds, to be a cutin fraction. This assay suggested that high cutin levels occurred in the fig species with high lignin levels (Table 3). However, since high cutin levels have not been reported before in a fruit pulp, we remain uncertain about the identity of the fraction. It may represent some derivation of the latex commonly found in Ficus, which is probably a triterpenoid, and therefore insoluble in petroleum ether. However, it would have to resist first the ND extraction, followed by the AD extraction, followed by 72% sulfuric acid digestion and potassium permanganate oxidation, as does cutin (a wax). The cause of these high "cutin" values merits further study. Cutin is usually considered indigestible by terrestrial mammals (van Soest, 1982) and nothing is known about the digestibility of latex.
Adjusted ME values Using the chimpanzee as a model animal, we can make adjustments to the ME
value (Table 4). The Table 4 values come from Tables 2 and 3, corrected for the diluting effect of
inert seeds. Consequently, the values listed in Table 4 are lower, by whatever percentage the pulp represents of the whole fig, than the values in Tables 2 and 3. Column "a" in Table 4 gives the ME values adjusted for this dilution but assuming neither pectin nor NDF are fermented. Column "b" includes the added energy a chimpanzee derives from fermenting the NDF and pectin in the hind gut. The chimpanzee appears to improve its energy extraction by fermenting these fibers (t-test, P
-
VALUE OF FIGS TO A HIND-GUT FERMENTING FRUGIVORE 147
Discussion The variation in nutritional composition among species indicates that none of the
assayed nutrients alone can account for the significance of figs as a food source. Water-soluble carbohydrates were not at high concentration, protein varied widely among species, and lipid levels were consistently low. Accordingly we considered how nutrient levels may complement each other by attempting to calculate total metabolizable energy (ME). Our consideration of total energy availability emphasizes that standard nutrient assays do not do justice to the complexity of frugivore strategies and/or components, as has previously been emphasized for birds (Martinez de Rio, in press).
When comparing our metabolizable energy (ME) values to the energy values in Table 1, our figures are low. However, it is important to note that the Table 1 energy values come from only three samples of one species and one sample of a second species. In addition, the energy values in Table 1 come from old (1960s) tables of human food, where they were reported simply as "energy" without differentiating between gross energy and ME. As a further problem, the Table 1 values come from the old Proximate Analysis system (or Weede system), which underestimates fiber and therefore would overestimate a calculated ME (van Soest, 1982). For these reasons any conclusions about ME of figs based on past data are premature. We therefore take the Ugandan data at face value.
The calculation of ME assumes that the NDF (neutral-detergent fiber) fraction is not available for digestion. But in chimpanzees, as in many medium to large sized frugivores, as much as 70% of the fiber fraction can be digested, usually by hindgut fermentation (Milton and Demment, 1988). How much fiber is digestible depends on several variables, including the species of frugivore, the quantity of fiber, and the nature of the fiber. Soluble fibers (gums and pectins) are more digestible (Siragusa et aL, 1988) than insoluble fibers (Bryant, 1978; Heller et al., 1980), but no study of figs has distinguished between soluble and insoluble fiber or even estimated the total amounts of both. The NDF includes all insoluble fibers and a variable portion of the soluble fiber, depending on the type of soluble fiber and its concentration in the sample (J. Robertson, pers. comm.).
Pectin is a soluble fiber matrixed into the cell wall but, being soluble, is usually lost during the NDF procedure and by default would end up in the complex carbohydrate (or NFE) fraction. It is somewhat fermentable by humans (Siragusa et al., 1988) and therefore is probably fermented rather effectively by chimpanzees. Other nonstarch polysaccharides, which in this study have been simply put in the "complex carbo- hydrate" category without further examination, may also be important nutrients for animals whose digestive physiology allows them to retain these components for digestion or fermentation. We suggest that in future considerations of fig nutritional value, an attempt be made to estimate the concentration of the different, and potentially available, carbohydrate fractions.
Our results, consequently, suggest that total available energy for a chimpanzee (that is, for a frugivore capable of fermenting pectins, hemicellulose, and cellulose) is some 50% higher (2.78 compared to 1.91) than estimated purely on the basis of cxCHO, WSC, CP, and lipid.
The justification for using the whole fruit NDF in calculations for an animal that ingests the seeds, but does not derive much nutrition from the seed fraction, is that the seeds occupy space in the gut. In the case of chimpanzees, seeds appear intact in the feces. The non-nutritional ballast eaten in the form of seeds has effects on the digestive process, and we therefore propose that it should be taken into account as we have done.
An additional source of error is that the ME calculations also assume that all protein is digested, but this is inaccurate because not all protein is available for digestion
-
148 N.L. CONKLIN AND R. W. WRANGHAM
(Pichard, 1977a,b; Krishnamorthy, 1982; Milton and Dintzis, 1981; Marks et al., 1985, 1987). In our estimate of available protein, we do not know whether alkaloid nitrogen or tannin-bound nitrogen is included in the ADP-CP fraction, so our available protein value may still be an overestimate of digestible protein. Nor have we investigated whether 6.25 is the best conversion factor. Milton and Dintzis (1981) suggested that 5.3 was a better figure, based on one fruit (Ficus insipida) and 10 leaf and flower species. More samples need to be analyzed using the same approach.
Speculation regarding protein digestibility can only be answered by performing in vivo digestibility trials of protein in figs. In Table 1, Milton et al. (1980) gave in vitro pepsin digestion coefficients for two neotropical fig species, but these have not been verified with in vivo work. Performing digestibility trials was beyond the scope of this study but these are urgently needed to definitively answer questions regarding protein and choice of protein analysis methods. Nevertheless, we recommend the ADF-CP correction as a simple procedure to obtain available protein where tannin levels are low. The Bradford assay (Bradford, 1976) and the Lowry method (Lowry et al., 1951) have been well tested on invertebrates but not on animals capable of some fermentation and therefore capable of digesting varying amounts of insoluble-but- available protein.
The protein issue becomes additionally complicated by the question of how much fig wasps contribute to the total value. Fig wasps are reared inside figs, and typically leave the fig before it ripens. The figs eaten by chimpanzees are almost invariably ripe and our analysis considers only ripe fruit. Therefore we consider that the only fig wasps likely to contribute to chimpanzee nutrition in the figs analyzed here are the corpses of developmental failures or males killed in reproductive combat. We doubt that these contribute enough nitrogen to significantly increase the Kjeldahl crude protein values. The question would be more important in the analysis of unripe figs.
Most Ficus species in Kibate are monoecious, but two are gyno-dioecious, F. exasperata and F. asperifolia, tn our samples, the sex is known for only two of the trees of F. exasperata that we analyzed (both female). Thus we currently have no information on the influence of sex on nutritional value. Female trees might be expected to be more nutritious, but our field observations indicate no obvious preference by frugivores for females in Kibale Forest. It is clearly desirable that sex differences be recognized in future nutritional assays.
TABLE 5. STAPLE FOOD VALUES ON A 100% DRY MATTER BASIS, COMPARED TO FIG VALUES
Food % CP % Lipid % CHO cal 100 g
Cassava, bitter 2.3 0.7 91.8 383 FAO, 1968
Potatoes, baked w/skin 103 0.4 83.3 378 Leveille et aL, 1983
Rice, brown, hulled 9.2 1.8 86.4 399 FAO, 1968
Sorgum, whole grain 12.4 3.1 61.5 324 NRC, 1982
Food % CP % Lipid % CHO ca1100 9
Ficus asperifolia 139 7.6 57.4 353.6
FJcus conraul -;'.6 2.7 45.9 239.1
Ficus cyathistipula 4.4 5 2 42.4 234.0
Ficus exasperata 25.4 6.6 42.6 331.4
Ficus mucuso 4.4 45 56.2 282.9
Ficus natalensss 6.1 1.6 27.2 147.6
Ficus sansibarica 10.2 2.8 58.8 301.2
Ficus saussureana 9.5 48 30.6 203.6
Mean 10.2 4 5 45.1 261.7
SD. 6.9 20 12.0 68.6
CP = crude protein; CHO = calculated total available carbohydrates ~: 100 (Lipid+ CP NDF); cal 100 g ~ == metabolizable
energy = 9 kcal g %
-
VALUE OF FIGS TO A HIND-GUT FERMENTING FRUGIVORE 149
Further investigations also are needed to determine whether the "cutin" fraction is in reality the Ficus latex. If it is, then we can easily evaluate the digestibil ity of this latex and evaluate whether or not it is a negative factor in selectivity.
In summary, figs provide an acceptable baseline level of ME and protein to which other food items can be added (e.g. Terborgh, 1983). It may not be useful to think of them as high or low quality. Instead, in habitats where figs are plentiful, they should probably be considered like the potato for humans, a food that wil l sustain life at maintenance. Table 5 shows that fig pulps appear to have a potential nutritional value that one would expect to find in a staple human food item.
In contrast to ME, our data show that individual nutrient concentrations differ importantly among fig species. Similarly we showed previously for five different frugivores that rates of nutrient and energy intake vary significantly among fig species [as a function of fig size (Wrangham et al., 1993)]. Assuming that figs are generally attractive to large-bodied frugivores, the implication of these observations is that neither the concentration of individual nutrients, nor the rate at which they are ingested, accounts for the frugivore interest in figs. Data on variation in frugivore selectivity for different fig species are needed to test further the relative importance of ME, other nutrients, and food intake rate. Meanwhi le the specific hypothesis that arises from our data is that because of its relatively high and consistent level, the ME value explains the strong tendency of large-bodied frugivores to be attracted to figs.
Acknowledgements--We thank the Government of Uganda, especially the National Research Council and Forestry Department, for permission to work in the Kibale Forest Reserve. Facilities were provided by Makerere University Biological Field Station. The Department of Zoology, Makerere University, assisted at all times. Acknowledgement for funding is due to the National Science Foundation (BNS-8704458), National Geographic Society (3603-87) and Leakey Foundation. Assistance in the field was provided by J. Basigara, J. Byaruhanga, C. Chapman, L. Chapman, A. Clark, K. Clement, the late G. Etot, B. Gault, M. Hauser, K. Hunt, G. Isabirye-Basuta, the late G. Kagaba, R. Marumba, C. Muruuli, P. Novelli, J. Obua, C. Opio, E. Tinkasimire, P. Tuhairwe, A. B. Katende and J. Kasenene kindly identified plants. D. McKey made valuable comments on the manuscript.
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