Bio/o&icdJournal ofthe Linncan Society (19811, 16: 115-146. With 6 figures
Food selection by black colobus monkeys
(Colobus satanas) in relation to
plant chemistry*
DOYLE B. MXKEY, J. STEPHEN GARTLAN
Primate Ecology Unit, WisconsinRegional Primate Research Center,
1223 Capitol Court, Madison, WI 53706, U.S.A.
PETER G. WATERMAN, F.L.S.? ANDGILLIANM. C H O O
Phytochemistry Research Laboratory, Department of Pharmaceutical Chemistry,
University of Strathclyde, Glasgow GI I X W , Scotland, U.K.
Accepled fmpublication April 1981
Black colobus monkeys (CO~U/JU\
wlnruir) in the Douala-Edea Reserve, a rain-forest on the coast of
Cameroon, have been shown to avoid young and mature leaves of most of the common plants in
their habitat and to feed disproportionately heavily on leaves of rare plants. The proportion of
leaves in the diet was low compared to most colobines studied, and the monkeys spent over half their
feeding time eating seeds. Patterns of food selection were analysed in relation to distribution of
nutrients, digestion-inhibitors and toxins in the vegetation. Colobw ~ a t r m select
c~
food items that are
rich in mineral nutrients and nitrogen and low in content of the general digestion-inhibitors,lignin
and tannin. They achieve this in the following ways: (i) by feeding preferentially on young leaves,
which have higher nutrient content and lower contents of digestion-inhibitors than mature leaves;
(ii) by eating those mature leaves with highest nument content relative to content of digestioninhibitors; and (iii) by eating seeds, which are sources of readily available energy and which, as an
item class, are less rich in digestion-inhibitors.Seeds at Douala-Edea appear to contain Ins nitrogen
than leaves and C.J&UUU selects those seeds with highest nitrogen content. It is suggested that seedfeeding may be facilitated by the ability of the forestomach flora of these ruminant-likemonkeys to
detoxify some of the secondary compounds contained in seeds. Avoidance of most unused young
and mature leaf items is correlated with a low nutrienudigestion-inhibitorratio; avoidance of most
unused seeds could be accounted for by their low nitrogen contents. Most items whose avoidance
could not be explained in terms of these major constraints on food selection possess secondary
compounds likely to be toxic. It is proposed that relative importance of digestion-inhibitors,low
nutrient content and toxins as constraints on food selectionby generalist herbivoreswill vary greatly
among forests with different nutrient and secondary chemistry profiles.
KEY WORDS:- Community ecology - tropical rainforest - plant-animal interactions - generalist
herbivores - plant chemical defences food selection - ruminant-likedigestion- C o l h sutmw.
-
'Publication 20-02 1 of the Wisconsin Regional Primate Research Center.
tTo whom reprint requests should be directed.
115
0024-4066/8 1/060115 + 32S02.00/0
Q 198 1 The Linnean Society of London
. .
D B McKEY ET AL .
116
CONTENTS
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Chemicalcompositionofvegctation . . . . .
CompositionofC.sataMsdiet . . . . . . .
Feedingselectivity . . . . . . . . . .
Results
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Availability of potential foods
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Introduction
Approachandobjectives
Colobinemonkeysasherbivores
Ruminant-likedigestionand food selection
Materialsandmethods
Studysite . . . . . . . . . . . .
Estimation ofplant density and relative biomass
Treephenology
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Vegetationcomposition
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Treephenology
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FeedingbehaviourofC.sdaMs
Compositionofthediet
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Plant chemistry in relation to food selection
Sekctivityinleaffeeding . . . . . . . . .
Preferenceforyoungleaves . . . . . . . .
Preference among young leaves . . . . . . .
Prefnenceamongmatureleaves
Preferenceforseeds
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Preferenceamongseeds . . . . . . . . .
Discussion . . . . . . . . . . . . . . . .
Whicharethecriticalnutrients?
PatternsoffoodselectionbyC.sdaMs . . . . . .
Major constraintson food selection . . . . . .
0therconstraintsonC.sataMsfoodselection . . .
Rurninant-likedigestionandseedfeedingbyC.s&aMs
Furtherquestions . . . . . . . . . . .
Between community variation in vegetation chemistry and
general hypothesesaboutherbivorefoodselection
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Acknowledgements
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References . . . . . . . . . . . . . . . .
Appendix
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INTRODUCTION
All herbivorous primates that have been studied in the field are selective in
their food choices. The behaviours associated with food selection form the
interface between the animal. with a particular set of metabolic requirements and
digestive capacities. and the vegetation confronting it Food selection is the link
between the structure of the plant community and the foraging movements.
activity patterns. social systems and population densities of the animals which
exploit it as generalist herbivores Because of its central role in the ecology of
generalist herbivores. food selection has been the focus of several recent studies
of herbivorous primates (Oates. Swain & Zantovska. 1977; Glander. 1978;
Milton. 1979; Oates. Waterman & Choo. 1980)
This study presents an analysis of food selection by the black colobus monkey.
Colobus satam Waterhouse. in a rain-forest in Cameroon I t is based upon
extensive studies of forest composition (McKey. 1978a; Gartlan et al., in prep.)
and upon the most comprehensive set of data yet available on chemical features
of forest vegetation likely to be important in food selection by generalist
mammalian herbivores
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FOOD SELECTION BY COLOBUS SATANAS
117
Approach and objectives
Food selection can be approached as a cost-benefit problem. Optimal
foraging theory is based on the premise that natural selection will favour those
animals that maximize their rate of net intake of energy (or other critical
nutrients) and that food selection patterns observed today are thus adaptive, or
even optimal (Pyke, Pulliam 8c Charnov, 1977). Optimal foraging theory has
been applied with relative success to carnivorous animals but not to herbivores,
whose potential food species display more complex chemical variation, not only
in nutrient content, but also in their diverse array of substances inhibiting
digestion, or which are actually toxic (Rhoades 8c Cates, 1976; Rosenthal 8c
Janzen, 1979). Some workers have sought to accommodate generalist herbivores
within the framework of a general theory of foraging strategies by constructing
models with more elaborate constraints, introduced to account for effects of
large-scale qualitative chemical variation among plant species (Westoby, 1974;
Alunann 8c Wagner, 197 7 1.
In principle, using such models one should be able to predict many features of
the optimal diet of an herbivore: which potential foods will be included in the
diet and to what extent, relative preferences for various combinations of foods,
and the diversity of the diet. In practice, however, such predictions require that
much more be known than at present about the chemical composition of plants,
the requirements and susceptibilities of the particular herbivore, and the
interaction of ingested toxins and nutrients in the animal. This is especially true
for herbivores attempting to exploit taxonomically and chemically diverse
tropical rain-forest.
Colobine monkeys as herbivores
Colobine monkeys are clearly analogous to ruminants in fundamental aspects
of their digestion (Bauchop, 197 7). As in ruminants, the stomach is divided into a
proximal portion in which pH is near neutrality, and in which are found a large
population of cellulolytic bacteria, and an acid distal region. Bacteria found in
the stomach of langurs (Asiatic colobines) are similar to the major cellulolytic
bacteria found in the bovine rumen (Baucho , 1978). Fermentation rates in the
colobine stomach are similar to those in s m a 1 ruminants (Kuhn, 1964) as is the
composition of fatty acids produced (Drawert, Kuhn 8c Rapp, 1962; Bauchop 8c
Martucci, 1968). Protozoa appear to be absent from colobine stomachs (Kuhn,
1964; Ohwaki et al., 1974), a feature they appear to share with small ruminants
(Giesecke, 1970).
The capacious but comparatively non-specialized digestive tract of howler
monkeys has recently been shown to be capable of considerable fermentation of
plant structural carbohydrates (Milton, van Soest 8c Robertson, 1980). The extent
of cellulose digestion in the colobine stomach has yet to be measured but is
almost certainly appreciably greater. Also unknown is whether colobines can
recycle urea via the stomach, resulting in increased nitrogen economy and
decreased urine formation (Bauchop, 1978). The stomach flora of colobines may
exhibit some taxonomic peculiarities, such as diversity of Staphylococcus spp.,
possibly the result of constant inoculation with externally-living Staphylococcus
during allogrooming (Ohwakiet d.,1974).
Colobines are smaller than the best-studied ruminant species, cattle and
sheep. Among the ruminant artiodactyls, small species have smaller and less
P
D. 8. McKEY ET AL.
118
complex stomachs (Hoffmann & Stewart, 19721, select higher quality food lower
in fibre (Hungate et al., 19591, pass food more rapidly through the gut and digest
cellulose less thoroughly (Giesecke, 1970). It would not be su rising if colobines
were more similar in their digestive physiology to small ante opes than to cattle
or sheep.
rp
Ruminant-lih digestion andfood selection
The presence of high1 evolved ruminant-like digestion should have several
important consequences or food selection by colobine monkeys.
(i) Because of the diverse synthetic capacities of its foregut flora,the ruminantlike herbivore may require a smaller number of essential nutrients. Rumen
bacteria can synthesize B-vitamins (Zahorik& Houpt, 197 7) and stomach bacteria
of colobines can probably do likewise (Oxnard, 1969). Rumen bacteria also
possess the ability, given an adequate nitrogen supply, to synthesize the amino
acids required by the host (Moir, 1968).
(ii) The stomach flora of ruminants has the capaci’y to detoxify various kinds
of toxic compounds (Watermanet al., 19801, and it IS likely that the stomach flora
of colobines also possess such capacities. A generalist ruminant-like herbivore
with a diverse stomach flora may actually be a “community of specialists”, able
to detoxify a greater varie of secondary compounds and to change its diet more
rapidly in response to c anges in food availability, than if it were wholly
dependent on its own enzyme systems.
(iii) The animal may be constrained from eating plants or plant parts that
contain large amounts of substances that exert toxic or bacteriostatic effects on
its stomach flora, such as tannins, volatile oils and coumarins (Waterman et al.,
1980). While all of these may exert toxic activity in mammalian systems as well,
the dependence of ruminant-like animals on their stomach flora may lead to
shifts from plants containing com ounds especially toxic to bacteria.
(iv) Owing to the presence o materials such as lignin, cellulose, silicates,
tannins and waxes that b physical or chemical means decrease the rate at which
plant material is digested: nutrient ca ture by mammalian herbivores is limited
primarily by the rate and efficiency of ood processing. Only thorough1 digested
foods are allowed to pass from the stomach to the rest of the gut Hungate,
1975). This feature has an advantage additional to that of maximizing use of
slowly digestible nutrients in that it reduces the chance that undigested toxins will
be allowed to pass to the rest of the gut.
However, while slowly digestible food can be retained in the rumen and used
efficiently, this results in a decreased rate of food intake. Thus, if food intake is to
be maximized, the diet must consist of foods that are relatively highly digestible.
The range of digestibilities that an animal can tolerate in its food items should
be met by some form of compromise between the following: (a) Metabolic
requirements relative to gut capacity. Small herbivores, with high metabolic
requirements relative to gut capacity, should emphasize high intake and rapid
passage of relatively digestible food. Large herbivores can more likely satisfytheir
needs by longer retention of less digestible foods (Janis, 1976; Parra, 1978).
(b)Nutrient content of the food. The lower the digestibility of a food item the
smaller the amount that can be processed in unit time and the higher the
minimum concmtration of a nutrient r uired to supply the animal’s needs.
Also, if the rest of its food is highly digestib e, the herbivore may be able to ingest
F
x
F
F
7
7
FOOD SELECTION BY COLOEUS SATANAS
119
some low-digestibility foods that are still its best net suppliers of some critical
nutrient.
These features of ruminant-like digestion suggest that food selection by
C. satanar might be sub’ect to the following constraints: (i) The quali
arts as potential food items might be largely determined by the
getween their content of nutrients and content of digestion-inhibitors, such as
lignin and tannins, which lower assirhilation rates of- ingested nutrients.
(ii)Potential food quality might also depend on the presence or absence of toxins
which the monkeys’ stomach flora, or the monkey itself, cannot tolerate, or
which impose a cost in terms of drains on specific nutrients.
If C.satanar possess the behavioural mechanisms many other animals have
enabling them to avoid, or learn to avoid, diets that are unsuitable (Barker, Best
& Domjan, 19771, their choice of food should reflect chemical constraints on
food quality. In order to identify the constraints and examine how they may
interact to determine C. satanas feeding strategy, we have examined food choice
by this monkey and its correlation with distribution of nutrients, general
digestion-inhibitors and toxins in the vegetation of their home range.
MATERIALS AND METHODS
Study site
The study was performed at the Lombe study site in the Douala-Edea Forest
Reserve, a rain-forest reserve of over 100000 ha, on the Cameroon coast
(Gartlan, McKey & Waterman, 1978; Gartlan et al., 1980, for information).
Letouzey ( 1975) has published observations on the composition of vegetation in
the reserve. The forest is of a type restricted to the coastal region of Cameroon
and Gabon, characterized by the occurrence and local abundance of emergent
species such as Lophira alata, Sacoglottis gabonensis Urb. (Humiriaceae), and
Cynometra hankei Harms. (Caesalpiniaceae). It has never been logged and
disturbance has been mostly limited to hunting and trapping.
Estimation ofplant demity and relative b i o m s
Strip enumerations of trees were carried out within the C. satanus study area. In
these enumerations, all trees exceeding 50 cm circumference at breast height (or
above buttresses) were counted and identified in strips 5 m wide and totalling
2900 m in length (1.45 ha) in the main study group’s home range (Strip I).
Analogous information was gathered from a strip totalling 0.20 ha in an area
occupied by an adjacent group of C. satanas (Strip 11).These enumerations were
performed along trails previously cut along compass lines in the study area (Fig.
1). Smaller understorey trees were not enumerated as they were rarely entered by
C. satanas.
N o attempt was made to estimate average crown volumes for different tree
species. In an effort to account for size differences between species in arriving at
an estimate of relative biomass, the proportional contribution of each species to
total basal area was determined. Oates et al. (1980: 46) found basal area to be
highly correlated with crown volume.
Tree phenology
Fluctuations in abundance of different plant parts were assessed by means of
120
D. B. McKEY ET AI..
Strip I1
YN
rJrI
i
I
J
1
I
I
J
U
100 m
Strip I
Figure I . Locations ot' enumerated strips and quadrats used by the major group of Colobur
Lotiibe study area, Douala-Edea Forest Reserve, Cameroon.
saw,
monthly observations on selected species. In these observations, the abundance
of young leaves, floral buds, flowers, immature fruits, mature h i t s and mature
leaves on individual trees was scored on a scale of zero to four. Two groups of
trees were included in the study. Five species heavily used by C . s a t a m were
observed in order to assess the relation between fluctuations in abundance of
plant parts and extent of use by the monkeys. The five species were Protmgaban'a
stafifiana, Strombosia pustulata, Lophira data, Trichilia renheti and Berlinia bracteosa.
Five marked individuals (seven for P. stapfian) of each species were observed in
each month. In addition, 93 individual trees, belonging to 64 species, were
observed each month to assess fluctuations in overall abundance of seeds and
young leaves in the habitat. This sample included several individuals of many
common species not represented in the first set, and one or two individuals of a
large number of species.
Chenrical composition of vegetation
Assay methods for total phenolics (TP)and condensed tannins (CT)
have been
reported (Gartlan et d., 1980). Nutrient analyses for nitrogen (N),phosphorus
(PI, ash, total nonstructural carbohydrate (TNC) and gross energy were
performed using standard methods (Waterman et al., 1980). Estimates of dry
matter digestibility were obtained using rumen-liquor (RDIG)(Waterman et al.,
1980) and pcpsitdcellulase enzymes (CDIG)(Oates el nl., 1980; Choo el nl., 198 1).
FOOD SELECTION
BY COLOBUS SATANAS
121
Not all plant parts could be examined for all measures. The sets of species
represented in each comparison discussed are given in the Appendix 1.
Composition of C. satanas diet
Methods of gathering quantified information on feeding behaviour closely
followed those of Struhsaker (1975) and Oates (197 7 ) in studies on C. badius (red
colobus) and C.guereza (black-and-whitecolobus), respectively, in Kibale Forest,
Uganda. Most of the information on C.satanas was gathered from a single wellhabituated group. A system of trails cut along compass lines divided most of the
home range of this group into 50 x 50 m quadrats. The trails allowed the
observer to move rapidly and silently through the forest and permitted mapping
of the study group’s movements.
Most information on the feeding behaviour of this group was gathered during
systematic monthly samples on five consecutive full days, as in the Ugandan
studies. In these samples, the group was followed from about 06.45 to 18.15
hours. This period usually encompassed the first and last feeding and moving
bouts each day. On almost all mornings the group was inactive when first
encountered. Samples were usually conducted in the second or third week of
each month. Systematic samples were begun in October 1973; the monkeys were
well habituated to the presence of an observer by April 1974. Even prior to full
habituation it was possible to remain in fairly close visual contact with the group
throughout the day without their being much disturbed. Analysis is here
restricted to the final 12 systematic samples, March 1974 to March 1975 (no
systematic sampling in February or April 1974).
I t proved impossible to follow individual monkeys continuously, to estimate
the amount of food eaten during a feeding bout, or to record the time spent
feeding by an individual monkey on a specific item. Therefore, quantitative
estimation of diet composition was based on a frequency criterion: when a
monkey was first seen feeding on an item, this was scored as one record. If the
same monkey fed on the same item at least 1 h after the previous item it was
scored again. Thus, the feeding records are estimates of the amount of time spent
feeding on different items. This method of quantibing feeding records is the
same as that used in the Ugandan studies (Struhsaker, 1975; Oates, 1974, 1977).
Oates ( 197 7 ) compared this method with a frequency method similar to that used
by Waser (1974) and by Clutton-Brock (1972) and found little difference in their
estimation of time spent feeding on different items by C. guereza.
Relative amount of time spent feeding on different items can vary strikingly
from relative food intake, when items differ in characteristics affecting handling
time (Hladik, 1977a). However, the differences examined here in extent of use
are so gross that they will not be greatly affected by this source of bias. Most plant
parts were never seen to be used, and some were used extremely frequently.
Furthermore, the comparisons subjected to statistical analysis in this study are
restricted to items within a single item class.
Feeding selectivity
An indication of the degree to which the monkeys feed selectively on different
tree species can be derived by comparing the relative number of feeding
observations on a plant species with its relative abundance or biomass as
122
D. B. McKEY ET AL.
estimated from tree enumerations. Such selection ratios were computed
separately for each plant art using basal area as the estimator of relative
biomass (see footnote, Tab e 1). Selection ratios can only be rough estimates of
relative selectivity, since it is difficult to compare the quantity of young leaves,
h i t s , etc. actually available across a variety of tree species. Factors such as the
size of fmit crops and intervals at which they are produced, and the time young
leaves remain vulnerable to herbivores, are highly variable and difficult to
estimate accurately. Even when selectivity is accurately measured, it may not
reflect 'preference'. Many factors determine whether feeding selectively on rare
or scattered items involves an incremental cost in terms of food search, and thus
whether the relative abundance of an item, as well as its quality as food, will affect
the animal's preference for it.
P
RESULTS
Availability ofpotentidfoods
Vegetation composition
Results of the Strip I enumeration are given in Table 1. Some trees not
encountered in the enumeration, but known to be present in the home range of
the main C. satam group and used by them, are also listed. Protomegabaria
Table 1. Relative abundance, basal area and use of tree species by Colobw satanus
in the Lombe study site
Species
Deciduous
or
evergreen
Species encountered in Strip 1 enumeration
E
D
E
E
Prolomegabaria stafiJiana
Lophira &a
Libreuillea hlaim'
Coula edulis
Klainedoxa g a b m u
Anlhonolha macrophylla
L'apacastaudlii
Tnchosqpha p e n s
Anthocleisla vogebi
An'oa sp. 48
Slrombosiopsis letrandra
Uiscoglypremna caheura
Garcinia mannii
Lcptaulus daphm'des
Pachypodanthium sp. nov.
Anthostemma aubrcyanum
Pausinyslaliajohimbe
Indet. 7B
Ctenolophon englerianw
S l r e p h o m pseudocola
Maminea qfncaM
Maprounea mcmbranaceac
Erylhrophleumivorense
Diospyros dendo
U i c h o s t m glauccscens
Brrlinia braclcosa
Xylopia quintasii
E
E
E
E
E
E
E
D
E
E
E
E
E
E
E
E
E
D
D
E
E
D
E
Feeding records
%
Number of Basal Mature leaves Young leaves
Seeds
individuals area No. S.R. No. S.R. No. S.R.
161
10
7
11
2
14
12
19
8
6
3
1
13
11
7
2
7
3
1
1
6
4
2
9
8
3
3
22.4
15.4
10.5
7.0
5.4
3.6
2.6
2.5
2.0
1.7
1.7
1.7
1.5
1.4
1.3
1.2
1.1
1.1
1.1
1.1
1.0
1.0
1.0
0.9
0.9
0.9
0.8
0
1
1
0
0.02
0.03
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1.54
9
0
0
1
0.21
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0.90
2 0.64
0
0
121 39.20
0
0
0
7
1
0
0
I1
0
0
0
0
0
38
0
3
0
0
0
0
0
0
0
0
12
0
0
64
0
0
0.11
0.02
181
200
6
0
0
0.76
0
0
0
0
0
5.57
0
0.53
0
0
0
0
0
0
0
0
2.99
0
0
17.73
0
0
0
0
0
83
0
10
40
178
0
0
0
0
0
0
0
0
0
0
137
0
0
0
0
0.77'
1.24
0.06
0
0
0
0
3.18
0
0.87
2.25
10.02.
0
0
0
0
0
0
0
0
0
0
13.11
0
0
0
0
FOOD SELECTION BY COLOBUS SATANAS
123
Table 1--continued
Feeding records
Deciduous
%
or
Number of- Basal Mature leaves Young leaves
Seeds
cvergrwn individuals
area No.
S.R. No. S.R. No. S.R.
Xylopia aethiopica
Berlinia auriculala
lndet Flacourtiaceae
Slrombosiapwlulala
Symphonia globulgera
Diospyros pcilesccns
Baihiaea insibmis
Indet. 4C
Coelocaryonpreusii
Anlhonolha pacillipora
Ouralea afjSnis
Slrephonema mannii
Beilschmedia sp.
Antidesma vogelianum
Indet. No. 13
lndet. No. 20
Diospyros hoyleana
Toubaouate brevipaniculala
Barleria.jslulosa
Garcinia conrauana
Rubiaceae 1481
Millelia sp.
Garcinia oval~olia
Indet. sp. 5
1
E
D
E
4
E
5
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
1
3
2
2
1
4
3
2
2
2
1
1
I
1
?
E
E
1
1
1
I
1
1
1
0.8
0. I
0.7
0.5
0.5
0.4
0.4
0.4
0.4
0.3
0.3
0.3
0.2
0.2
0.2
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0
5
0
0
2.09
0
2.34
0
0
4
0
0
0
0
0
0
34 24.18
0
0
0
0
0
0
0
0
1
1.45
0
0
0
0
0
0
0
0
2 5.80
0
0
0
0
0
0
1
2.90
0
0
1
0
0
89 31.71
0
0
43 21.45
0
0
0
0
3
1.87
0
0
51 31.80
8
6.65
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
4
9.98
1 2.49
0
0
71
0.12
0
0
13.59
0
0
0
0
0
0
0
13
0
0
0
0
0
3.11
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
Species not encountered in enumeration but present in the home range and known to be used
Trichilia renheri
Macaranp barleri
Hauvolfra vomiloria
Mareyopsis lonbviolia
Panda oleosa
Cola sp.
E
E
0
0
D
0
0
E
E
E
Number 0 1 teeding records accounted for
Total number otrecords trom tree species
0
0
0.1
0.1
0.1
0.1
0.1
0.1
4
11.10
0
82 239.00
0
0
13 37.90
11 32.01
0
283
343
15
11 21.43
0
0
7 11.46
1
2.49
3
7.48
0
0
351
401
11.77
15 14.35
0
0
21 25.84.
0
0
0
0
1037
1045
Data obtained from systematic sampling ofmain study group,March 1914-March 1975.
* These three used species are dioecious and actual selection ratios will depend upon sex ratios.
% of tree feeding records for the item class concerned accounted for by sp. A
S.R.=selection ratio =
%of total basal area accounted for by sp. A in Strip 1 enumeration
Enumeration 01'Strip 1 based on all trees with a girth at breast height of)dOcm.
stuffiunu is by far the most abundant tree, whether abundance is measured by
frequency or by basal area. This species is the most frequent tree in all size classes
up to 175 an circumference (McKey, 1978a)and occurs in high density in many
parts of the study group's range. It was, however, virtually absent from the
extreme north and north-west of the range, and was uncommon in some
adjacent areas, such as Strip 11. Lophiru alutu, the most common large emergent,
accounted for only 2.6% of individual trees but 15.4% of basal area and was
common throughout most of the study group's range. The enumerations
indicated strongly clumped distributions, usually associated with obvious
physical-environmental variables such as drainage and soil texture, for several
D. B. McKEY ET AL.
124
frequent species, including Trichoscypha patens, Anthonothu mucrophyllu, Diospyros
dendo and Dichostemmaglaucescens. Vine density and biomass were not studied.
Tree phenology
Monthly observations of the large series of marked trees showed a distinct
peak in fruit production from June to August (early/middlerainy season).Young
leaf production showed no strong seasonal pattern (McKey, 1978a)at this study
site. Observation of five Colobus food species showed that seed and young leaf
items heavily used by the monkeys were always used whenever th were present
in appreciable uantities. Our impression is that this is true of a 1 heavily used
seed and young eaf items.
7
3
Feeding behuviour of C . satanas
The main study group used a total of at least 84 plant species during the last 12
systematic samples. Identification of food plants, especially vines and epiphytes,
proved a major problem, Of the 84 food species, only 39 were identified to the
species level. However, these accounted for 78% of the records. Of the
remainder, 16 species have been identified to genus and 23 more to family. A
further six species were never identified to family level but each was always
recognizable as a distinct food species. In all, 2474 records (94.6%)were from
plants that could always be distinguished. Most cases in which the food species
was unidentified involved feeding on vine leaves. When feeding on these items,
the monkeys were often poorly visible, and feeding often consisted of a rapid
series of bouts on different species. Also, it was difficult to mark vines for later
identification.
When observations of the main study group outside the last 12 systematic
samples are included, 15 food species (seven identified) are added. Observations
of other groups added only one food species to the total. Thus, C. satam was
recorded feeding on a minimum of 100 plant species.
The following plant parts were distinguished in recording feeding behaviour :
mature leaf blades, young leaf blades, leaves of undetermined age, leaf buds,
shoot tips, flowers, floral buds, petal-like bracts, seeds, seeds plus fleshy parts of
fruits, and arils. Detailed composition of feeding records by species and item has
been recorded (McKey, 1978a).All of the 20 most important food species, and 18
of the 20 most important food items (Lophira data floral buds and very young
floral and/or leaf buds, accounted for 45 and 35 records, respectively),are given
in Table I (tree species)and in Table 2 (vinespecies).
Compositionofthe diet
Leaves accounted for less than half of C. s a t a m feeding records (Fig. 2A).
Young leaf blades comprised on average 19.7%of each month’s records during
the last 12 systematic s a m les, mature leaf blades averaged 18.1%, flowers and
floral buds 3.3% and lea buds 0.8%. On average, over half (53.2%) of each
month’s records were contributed by feeding on seeds (and seeds plus
accompanying fruit flesh). The ingested seeds are virtually without exception
destroyed and digested. That these monkeys feed on many seeds not
accompanied by a fleshy fruit and that they sometimes discard fruit flesh eating
only the seeds, indicates that seeds, and not fruit flesh, are the principal items
being selected (McKey, 1978a,b).
P
FOOD SELECTION BY COLOBUS SATAMAS
125
Table 2. Vine species frequently used by Colobus satanas at the Lombe study site
Species
Hhnphiosfylis ?beninensis
Cissus poductn
Iiippocmfen sp.
Agnnope sp.
Sfrychnos sp. 2
Deidarnin clemafoides
Hyrnenodiclyon sp.
Sfrychnos sp. 1
Connaraceae Indet. sp. 2
Slrychnos fricnlysioides
Sfrychnos sp. ‘sinall leat’
Morindn ?morindoides
Connaraceae Indet. sp. 1
Sfrychnos sp. ‘small seed’
?Mezoneuron sp.
Feeding records
Mature Young
Fruit/
leaves
leaves
seeds
41
O
0
6
0
0
0
0
5
7
0
29
10
15
4
1
43
0
0
13
0
0
0
1
0
0
0
6
12
9
38
31
2
19
0
0
0
0
0
0
10
10
10
4
0
Remarks o n frequency and
habitat
C,MFC
T
U,MFC
only o n Librevillea hlainei,
areas of extremely sandy soil
U,MFC
T
U,MFC
U,MFC
C,MFC
C,MFC
C,MFC
T
U,MFC
U,MFC
U,MFC
C = coininon; U = uncommon; MFC =mature forest canopy; T = secondary growth around treefall only.
Seeds of a large number of species from many plant families are eaten,
including seeds inside woody capsules, seeds of legumes, winged seeds, arillate
seeds, and seeds enclosed in drupes. When a highly favoured seed item is
available, C. satanas feed heavily upon it. As much as 60% of a month’s feeding
records may be contributed by the seeds of a single tree species. Because the
relatively brief fruiting periods of each species occur at different times in the year,
the pattern of seed use is one of a fairly rapid procession from one major food
species to another (McKey, 1978a). However, acceptable seeds are not always
abundant (Fig. 2A).
Leaves observed to be eaten were also from a large number of species and
plant families. Young leaves seem to be strongly preferred. However, used young
leaves were not always available despite the absence of seasonality in their
production. For example, most heavily used young leaf items are supplied by
deciduous trees, all of which replace their leaves sometime during the dry season
or early rainy season (November/June). The diversity of acceptable young leaf
items thus shows strong seasonal variation (Fig. 2B). In the period March to
October 1974, young leaves of, at most, one species contributed ten or more
feeding records to the monthly diet. In every month during the period November
1974 to March 1975, two or three s ecies contributed ten or more records.
Mature leaves, though not pre erred, account for over half the leaf feeding
records. Though mature leaves of the species used by C. satanas are present in
constant quantity throughout virtually the whole year, great inter-monthly
variation in intensity of use was observed for each species. The pattern of
variation suggests that the extent to which mature leaves are used depends on the
abundance of more favoured food items (McKey, 1978a).
Different plant life forms contribute differentially to the leaf portion of the diet
(Table 3). Epiphytes (ferns and orchids are most common) are very seldom used
while vines, on the other hand, are extensively used. Many of the vine leaves were
obtained during bouts of foraging in very low vegetation in treefalls. Deciduous
trees also contribute heavily to the leaf records. Although they account for only
P
D. 8. McKEY ET AL.
M
A
M
J
J
A
S
O
N
D
Month
1974
J
F
M
I975
B
M
M
J
J
A
S
O
N
D
Month
1974
J
M
F
1975
Figure 2. A. Intermonthly variation in the proportions of seeds (O),mature leaves R),
young leaves
(V),floral buds (a)observed to be eaten by black colobus during systematic samples (no data for
April 1974). B. Intermonthly variation in the availability of preferred seed (0)
and young leaf
lbod items.
'l'iil)Ic
m)
3. Composition o f leaf portion of' Colobus snlnnns diet, systematic sariiplcs,
March 1973-March 1974
E\,l*rgrl*Cll
trws i i i i c l
sllrlll~s
I19
%of %ol'
Deciduous
total leal
trcw
Vines Epiphytes Mistletoes Indct. Total dirt diet
0
224
225
0
0
23
297
472
289
11.3
18.0
41.8
11.0
I76
2
0
26.3
141
127
15
5
1
25.6
19
0
0
0
0
3
0
19
0
0
I1
0
0
517
535
49
5
24
19
0.7
1.7
22
0.8
1.9
31
1130
1.2
2.1
43.0
7
13
19.7
20.4
1.9
0.2
0.9
45.8
47.4
4.3
0.4
2.1
127
FOOD SELECTION BY COLOBUS SATANAS
7.2% of individual trees in the Strip I enumeration and 20.7% of basal area,
deciduous trees contributed 65% of tree mature leaf and 55% of tree young leaf
records. Vine density was not assessed, so we cannot determine whether vine
leaves were also disproportionately heavily used. However, those vine species
whose leaves were used certainly accounted for much lower biomass than the
most common trees.
Floral buds, flowers, young stems and other items are irregularly eaten by
C. satanus and account for about 5% of the records only. Floral buds of Lophira
d a t a were the only item among these that were heavily used when present,
accounting for 10.5% of records in December 1974. No activity resembling
foraging for animals was ever recorded. The monkeys were never observed to eat
fig fruits. Few of the seed types eaten suffer substantial predispersal predation by
insects. Lophira is the only striking exception, the young seeds being attacked by
microlepidoptera. The attacked seeds are aborted when about half-size. The
monkeys ate mostly larger, intact Lophira seeds.
Diet diversity, seasonal changes in diet composition, and C. satanas use of its
home range will be analysed elsewhere (D.B. McKey, in prep.).
Plant chemistry in relation tofood selection
Results of the chemical analyses, whose relationship to food selection is
examined in this study, have been published elsewhere. By far the largest set of
assay results is available for TP, CT and alkaloids (Gartlan et al., 1980). In this
study, analysis is mostly restricted to plant parts for which there is also
information on nutrient content, fibre content and digestibility (Waterman et ul.,
1980; Choo et d.,1981). The pattern and degree of relationship between food
selection and contents of phenolics, tannins and alkaloids in this restricted data
set is similar to that observed in the h l l set of data for these assays.
Analysis of food preference is also restricted to plant species known to occur in
the home range of the main study group of C. satanas. Five sets of data form the
core upon which the analysis is based: (i) information com aring young and
mature leaves of the same species; (ii) comparing young eaves of different
species ; (iii) comparing mature leaves of different species; (iv)comparing seeds
and mature leaves of the same species; and (v)comparing seeds of different
species. Sample sizes vary for the different analyses; the species available for each
are listed in Appendix 1. Sample sizes are largest for the comparison among
mature leaves, for which there is information on all criteria studied for 20 items.
The same information (exceptingADF and CDIG) is available for the analysis of
preference among seeds of 16 species.
P
Selectivity in leaffeeding
Table 1 illustrates the extreme selectivity of C. sutunai when feeding on leaves.
Mature leaves of all common trees are avoided; the most frequent tree with a
mature leaf selection ratio above 1.00 is Berlinia auriculutu, which accounts for
1.8% of individual trees and 0.7% of basal area. Although a few young leaves from
more abundant trees are eaten, B . auriculuta is again the most frequent tree with a
young leaf selection ratio greater than 1.00. Also, no tree which accounts for
more than 1.7% of basal area has a young leaf or mature leaf selection ratio
above 1.00.
128
D. B. McKEY ET AL.
For both young and mature leaves, selection ratios as calculated in this study
are highly correlated with the number of feeding records obtained. For example,
rank correlation of the mature leaf selection ratio with number of records among
the 17 species encountered in the enumeration with selection ratios above zero
was r, = 0.72, P < 0.01. Young leaves present a similar pattern, r, = 0.78, n = 14,
P < 0.0 1. This is the result of the fact that most of the heavily used species are rare
and about equally so, so that by far the greater contribution in variation in
selection ratio is variation in number of records, rather than variation in tree
relative abundance. A consequence is that in the examination of correlates of
preference among young leaves, and among mature leaves, it should not make
much difference whether the number of feeding records or selection ratios are
used. We chose to use the former, since its computation is less subject to error
and its use involves fewer assumptions. Also,the total number of feeding records
obtained for an item is highly correlated with the maximum percentage of
monthly records it contributes, for both mature (rs= 0.92, n = 17, P < 0.001) and
young (rs= 0.97, n = 18, P < 0.001) leaves. The items giving the largest number of
feeding records are thus also those used most heavily when available and results
presented here are consistent whether total number of records or maximum
contribution to monthly diet are used to estimate preference.
young leaves
An indication of the relative preference for young and mature leaves of the
same plant species can be obtained by comparing the extent to which young
leaves are used when present with the extent to which the species' mature leaves
were used. We compared the highest percentage contribution to monthly records
by young and mature leaves of the 18 plant species whose leaves accounted for
ten or more feeding records (Table 4). In 13 cases, young leaves, when present,
were used more heavily than mature leaves of the same species ever were in any
month of the study. Of the ten species which provided the largest numbers of
Preferencef
i
Table 4. Comparison of the maximum contribution to monthly diet records of
young and mature leaves of the same species
Maximum contribution to the monthly diet (%I
Species
Anlhonotha macrophylla
Discoglyprmma caimura
Erylhrophlrum iuorensc
Berlinia bracleosa
Berlinia auriculala
Slrornbosia pwlulara
Coelocaryonprewsii
Tnchilia mkm'
Rnuuoljia u o m h i a
Panda oleosa
Cola sp.
Cissw poducta
Deidamh clemdoidrs
Iiyrnendiclyon sp.
Connaraceae Indet. 2
Slrychms tricaiysioides
Strychnos sp. 'sinall leaf
?Meronruron sp.
Mature leaves
Young leaves
0
3.63
1.02
9.63
1.80
1.14
7.53
4.44
13.67
3.63
27.50
18.07
10.70
19.98
4.18
1.90
1.21
0
0.34
1.61
5.40
4.64
3.80
3.38
1.61
0.93
8.63
2.14
2.47
4.45
1.07
1.63
0
0
0.46
2.67
FOOD SELECTION BY COLOBUS SATANAS
129
leaf-feeding records, in eight species young leaves were clearly preferred to
mature. Cis5u5 producta mature leaves seem to have been preferred to young
leaves ; Rauvoffia vomitoria young leaves were produced during very brief periods
and young leaf feeding could have been missed in our samples.
Matched-pair comparisons (Table 5 ) show that young leaves contain
consistently higher dry-weight concentrations of N, P and TNC, contain lower
concentrations of ADF, and are more digestible than mature leaves of the same
species. Their apparent higher concentrations of TP and CT may be an artefact of
higher extractibilityof these compounds from young leaves (Gartlan et al., 1980).
The higher nutrient content, lower fibre and greater digestibility of young leaves
result from their being rapidly growing, metabolically highly active tissues. These
features probably combine to make them more suitable and more highly
preferred sources of food for C. satam than are mature leaves.
Five species are exceptional in that their young leaves have fibre contents
similar to (within 6% dry-weight) that of their mature leaves (Table 6). The young
leaves of these species look very different from those of species whose young
leaves are deficient in fibre relative to their mature leaves. Whereas young leaves
of the latter group are limp, soft and exceedingly fragile up to the time of full
expansion, those of the former are turgid, erect and relatively tough even when
quite small. There are also five species with young leaves no more digestible than
their mature leaves. Three of these are ones in which young leaves are highly
fibrous. Thus, some lants in the study site do ap ear to construct young leaves
which contain much bre or other digestibility-re ucers.
Young leaves of six of the 14 species in this comparison are eaten by C. satanas.
Five of these are species in which young leaves are appreciably lower in fibre, or
appreciably higher in digestibility than mature leaves, or both. These include the
.two highly preferred trees, Berlinia auriculuta and E . bracteosa. The young leaves of
one species, Eythrophleum ivorense, appear both slightly higher in fibre and
slightly lower in digestibility than mature leaves but are eaten more heavily by
C. satanas ( 12 records) than are mature leaves (one record).
B
R
Table 5. Pairwise comparisons of digestibility and of nutrient and
digestion-inhibitor contents for young and mature leaves of the
same species
Measure
n
Ash (%)
N (%I
5
TNC (%I
GE (kcal mole-')
5
5
5
5
RDlG (%)
5
CDIG (%)
14
14
38
P (%)
ADF (%I
T P (%)
CT (961
6.25N/(ADF+ CTI
38
5
Mature leaves
2 (range)
Young leaves
2 (range)
5.74 (3.37-8.82)
1.93 (1.61-2.523
0.104 (0.076-0.193)
4.28 (1.90-5.71)
4.62 (4.22-4.90)
9.21 (5.22-17.08)
22.38 (10.5-41.0)
60.76 (36.8-77.2)
6.87 (1.07-19.51)
7.86 (0.00-36.94)
0.164 (0.135-O.208)
5.16 (2.85-7.39)
2.75 (1.79-3.69)
0.269 (0.140-0.450)
9.74 (5.35-16.05)
4.47 (4.23-4.64)
14.16 (6.82-24.26)
33.99 (15.3-59.4)
48.60 ( 2 5 . 6 7 1.7)
9.52 (0.74-96.01)
9.41 (0.00-90.74)
0.284 (0.187-0.991)
4
0.45
-3.77.
-3.05.
-9.33*
2.24
-1.25
-3.29**
3.54..
-2.89'.
-1.16
-4.32..
* P < 0 . 0 5 ; " ' P < O . O I ; ***P<0.001.
N=nitrogen; P=phosphorus; TNC= total non-structural carbohydrate; CE=gross energy;
RDIG=rurnen-liquor digestibility; CDIC=pepsin/cellulase digestibility; ADF=acid
detergent fibre; TP= total phenolics; CTocondensed tannins.
D. B. MrKEY ET AI.
130
Reference a m g young leaves
Data on TP and CT content of young leaves are available for a large number of
species. Information on other chemical variables is restricted to smaller sets of
species. Of the 14 tree species included in Table 6 for which there are data on
ADF and CDIG, 12 were present in the home range of the main study group and
were considered in analysis of relative preference. For six of these species there
are also data on nutrient content and RDIG. These data indicate that there are
negative relationships between extent of use and ADF and CT content, and
positive relationships between extent of use and N content, and use and
digestibility (Table 7). Correlation coefficients are not high and sample sizes
small. The ratio N/(ADF+ CT)is more strongly related to use than is any of its
component variabTes. This result is also seen for C. satanas food choice among
mature leaves, where sample sizes are much larger (seebelow).
Preferences among mature leaves
Table 8 presents the relationships among different chemical variables and the
relationship of each variable with extent of use, for the mature leaves of 20
species for which a full set of data was available. The results show significant
positive correlations of use with ash content and digestibility (both assays), and
significant negative correlations with ADF and with GE, which is itself correlated
with ADF and seems largely to reflect content of cell wall polymers (Choo et al.,
198 1). Weak positive correlation with N content, and weak negative correlation
with content of TP and CT,are also apparent. No single variable correlates very
strongly with extent of use among this set of mature leaves. RDIG, which among
these variables is the closest approach to a com osite measure of potential food
quality, is correlated most strongly with extent o use.
F
Table 6. Differences in pepsidcellulase digestibility and acid detergent fibre
between young and mature leaves ofthe same species in relation to use by Colobw
satanac
Species
Prolovnegabaria slafljiana
laphira dala
Anlhonolha macroplrylla
L'apaca staudtii
rrichosvpha p a l m
Etylhrophlcum ivorense
Dichoslemma glaucescm
Berlinia bracteosa
Xylopta quinlarii
Berlinia auriculata
Anlhonolha gracillifora
Cleistopholis slaud6ii
Diospyros lon@/lora
Englerophytum stelechanfha'
*Speciesnot in enumeration.
Pepsidcellulase
digestibility
Young Mature
leaves leaves
34.5
26.5
45.8
17.1
18.8
15.3
50.3
36.4
24.2
59.4
20.3
38.9
37.0
29.1
55.4
13.7
18.9
14.7
19.2
22.0
36.9
22.2
14.5
25.5
12.9
41.0
25.9
10.5
4.9
12.6
26.9
2.4
4.4
-6.7
13.4
14.2
9.7
33.9
7.4
-2.1
11.1
18.6
Acid detergent
Maximum monthly
contribution to feeding
Young
Mature
leaves
leaves
fibre
Young Mature
leaves leaves
27.2
62.5
42.8
63.4
51.1
71.7
25.6
33.4
63.2
36.7
57.5
38.2
51.1
55.6
60.3
76.3
69.4
64.4
70.8
66.2
36.8
57.4
61.8
58.7
77.2
37.5
44.8
69.1
-33.1
-13.8
-26.6
-1.0
-19.7
5.5
-11.2
-24.0
1.9
-22.0
-19.5
0.7
6.3
-13.5
0
2.94
4.44
0
0
3.63
0
27.45
0
18.07
3.36
0
0
0
0
0.46
0
0
0
1.02
0
9.63
0
1.80
0
0
0
0
FOOD SELECTION BY COLOEUS SATANAS
131
Table 7. Relationships between extent of use by Colobw sutunar (number of
feeding records) and chemical content and digestibility for young leaves
n
r
Ash
N
P
TNC
CE
RDlG
CDIC
ADF
CT
6
6
0.68
6
0.87'
6
-0.30
6
0.15
6
0.35
12
0.54
12
-0.30
12
-0.19
0.94**
6.25N
(ADF+ CT)
6
0.89.
Key: see Table 5.
Table 8. Relationships among chemical content, digestibility and use by Colobus satanas
(number of feeding records) for mature leaves (n= 20)
Ash
N
P
TNC
CE
RDlC
CDIG
ADF
TP
CT
Feeding
records
N
P
TNC
CE
-0.01
0.21
0.46.
-0.61..
-0.61..
-0.56.
RDIG
CDIC
ADF
TP
CT
0.52*
0.44*
-0.12
-0.72"'
0. 73"'
-0.30
-0.38
0.57"
0.40
-0.36
-0.35
-0.36
0.42
0.23
0.51'
-0.35
-0.17
-0.41
-0.30
0.25
0.01
0.03
-0.41
-0.07
0.33
0.36
-0.22
-0.47.
-0.06
-0.11
0.52.
0.33
0.38
-0.55'
0.89***
-0.86".
-0.25
-0.93***
-0.11
-0.07
-0.55.
-0.48.
0.42
0.15
0.48.
-0.51.
-0.34
0.68***
-0.32
Key: see Table 5.
Current hypotheses contend that quality of an item as food to ruminant-like
herbivores is greatest when its content of critical nutrients is high relative to its
content of substances that reduce digestibility and assimilation rates. These
hypotheses emphasize N and energy as nutrients particularly likely to be limiting
(Janis, 1976; Milton, 1979). In order to test whether the ratio between content of
these nutrients and content of digestion-inhibitors can account for food choice
in C.satanas among mature leaves, we examined the correlations between extent
of use and a series of nutrienddigestion-inhibitor ratios (Table 9). The results
show that the ratio N/(ADF + CT) can account for food choice to a substantial
degree. The lack of correlation of use with ratios employing TNC as the nutrient
may indicate that this assay is not a good measure of energy available to a
ruminant-like herbivore, rather than that energy is not a critical nutrient in this
case.
While N content relative to content of ADF and CT can account for much of
C.satanas mature leaf food choice, we cannot, using our data, assign N any
greater likelihood of being causally related to food selection than the other
nutrients measured, ash and P. Table 9 illustrates that the ratio of each of these
nutrient measures to digestion-inhibitor content is as strongly correlated with
use as is the ratio using N. One reason for this, as examination of Table 8 shows,
is that N, P and ash contents are all positively correlated with one another. While
C.satanas select mature leaves with high contents of N and mineral nutrients
relative to digestion-inhibitors, which of these nutrients is most critical is difficult
to assess.
D. B. McKEY ET Al..
132
Table 9. Relationships among nutrienddigestion-inhibitorratios and use by Culo0u.s
salnnas (number offeeding records) (n= 20)
r=
N
-
N
-
N
P
Ash
N + 10P+Ash
CT
ADF
(ADF+CT)
(ADF+CT)
(ADF+CT)
(ADF+CT)
(N+lOP+Ash)RDIC
(ADF+ CT)
0.67**
0.70*'*
0.72***
0.81***
0.82***
0.89***
0.80*'*
Key: see Table 5 .
Preferencefor seeds
Colobus sutanar clearly prefer seeds to most leaf items, as indicated by the
following facts. (i) Seeds always accounted for at least 27% of monthly feeding
records, even during periods when availability of suitable seeds was very low.
Seeds comprised up to 90% of monthly feeding records when they were
abundant. (ii)Mature leaf food items, which were present in virtually constant
quantity throughout the year, were fed upon less extensively when highly
favoured seed items were present. (iii) Individual seed items comprised much
higher proportions of monthly diets than did individual mature leaf or young
leaf items, indicating that voluntary intake of food is greatest from seed items. In
11 of the last 12 systematic samples, the most heavily used food item was a seed
and accounted for up to 60% of records in a month. Individual young leaf items
never accounted for more than 27.5% of any month's records, and usually the
most heavily used young leaf item accounted for 13-18% of the monthly records.
N o mature leaf item ever accounted for more than 9.6% of the diet records for
any month.
Our data show that seeds contain lower concentrations of TP and CT, and are
more digestible than either young or mature leaves (Gartlan et d.,1980;
Waterman et al., 1980). They also show that seeds are richer in fats, but lower in
ash and N than are leaves. Differences between seeds and leaves will be discussed
separately for each chemical content variable studied.
Fat and energy content. Fat content (petroleum ether soluble fraction) has been
measured in seeds of 21 species from the study site and found to range between
3.7 and 57.2% ( G .M. Choo, unpubl.) with a mean of 18.5%. Fat content of leaves
has not been measured but the mean is certainly much lower than for seeds. GE
yield of seeds is not significantly higher than that of mature leaves of the same
species (Table 10) but the energy contained in seeds is likely to be more available
to the animal. GE yield in seeds is significantly positively correlated with fat
content ( r = 0.62, n = 11, P < 0.051, suggesting that fats account for a substantial
part of GE yield. A large proportion of the energy contained in leaves is bound
up in cell wall olymers, rather than in soluble carbohydrates and fats, and the
cell wall carbo ydrates are likely to be more highly lignified in leaves than in
seeds.
Fibre. Measurement of ADF has not been made for seeds from the site. ADF
values available to us for seeds of eight species from Malaysian rainforest trees
ranged from 2.53 to 8.89% for six species, but in two species were 45.5 and 47.2%.
We have no further information on these two high fibre seeds but these data
clearly show that some seeds have less fibre than is ever encountered in leaves. If
most of the lignified fibre in seeds is found in the seed coat, it should not hinder
digestion of seed contents once the seed has been cracked and chewed.
g
FOOD SELECTION BY COLOEUS SATANAS
133
Table 1.O. Pairwise comparison of digestibility and of
nutrient and digestion-inhibitor contents for mature leaves
and seeds of the same species
Measure
n
Mature leaves
2 (range)
Seeds
Z (range)
4
~
Ash
N
P
TNC
GE
RDIG
TP
CT
8 3.92 (1.53-7.07)
2.43 (1.19-5.32)
8 1.93 (1.38-3.58)
1.33 (0.61-2.32)
8 0.104(0.035-0.193) 0.152 (0.063-0.348)
8 6.42 (2.81-13.78)
7.17 (1.66-14.83)
8 4.88 (4.38-5.25)
5.18 (3.99-7.21)
8 15.81 (3.30-48.31) 34.10 ( 10.60-62.91)
39 7.49 (0.79-17.95)
4.35 (0.13-32.26)
39 7.84 (0.27-36.94)
3.91 (0.00-17.25)
~~
2.79'
2.63'
-1.11
-0.46
4.12
-1.83
3.66***
3.03***
~~~~
Key: see Table 5.
Dry-matter digestibility. Seeds are, on average, about twice as digestible in
rumen-liquor as are mature leaves of the same species (Table 10). In the two
species for which there is information on seeds and young leaves of the same
species, seeds are in both cases at least twice as digestible. The CDIG assay has
not been applied to a large number of seed items. Because it does not assess fat
digestibility, it is likely to greatly underestimate the true digestibility of seeds.
This is reflected by the low correlation between the two digestibility assays for
seeds (rs= 0.33, n = 12) (Choo, unpubl.), contrasting to their high correlation in
leaves (Choo et al., 1981). Even though the CDIG values we have obtained for
seeds are likely to be underestimates, with few exceptions they are still higher
than values given by young leaves (44.4% v. 22.6%, n=6, one exception)or mature
leaves (37.7% u. 23.9%, n= 12, two exceptions) of the same species.
PhenoVtannin content. Seeds are significantly lower in content of TP and CT than
mature leaves (Table 101, young leaves (paired-t-test, ts= 5.79 for TP, 4.33 for
CT, n = 23, P < 0.011, or indeed other vegetative parts such as barks (Gartlan el
d.,1980). Examination of our data (Gartlan et d., 1980) shows, however, some
variation among species in this respect. In 30 species for which there is
information on seeds, mature leaves and bark, seeds have decidedly lower tannin
content than vegetative parts in 14 cases. Differences in some cases are 10-15fold. Although seeds in no case contained much greater tannin concentrations
than vegetative parts, in 12 species seeds and vegetative parts were about equally
tannin-rich. Four species more or less completely lacked tannins in all parts.
Thus seeds contain about as much tannin as vegetative parts, or they contain substantially less.
Nitrogen content. The seeds examined contain significantly lower amounts of N
than do mature leaves of the same species (Table 10). For only two species is there
information comparing N content of seeds and young leaves; in both cases
values for young leaves are at least twice as great. Since N contents of young
leaves are significantly greater than those of mature leaves, they are probably also
greater than those of seeds.
Other nutrients. Seeds contain significantly lower quantities of ash than do
mature leaves of the same species (Table 10). The significanceof this is unknown
in the absence of data on specific cations. There are no apparent differences in
content of P and TNC between seeds and mature leaves (Table 10).
I34
D. B. MrKEY ET AI..
The preference of C. satanas for seeds probably results from the fact that seeds
of many species are a source of readily available energy and N accompanied by
only low amounts of digestion-inhibitory compounds. This combination of
features is possessed by only a few leaf items in the site, most of them rare or only
seasonally available.
Preference among seeds
Table 1 shows that C. satanus exploited the seeds of common trees to a much
greater extent than their leaves. The 20 tree species that make up the greatest
contribution to basal area (86% of basal area in total) supplied only 3.5% of all
mature leaf feeding records for trees, and 15.0% of young leaf feeding records,
but 66.8% of all records for feeding on tree seeds. Seeds of the two species with
greatest contribution to basal area, Protmgdaria stupjam and Lophira data, were
both heavily used. The monkeys are nevertheless very selective among species.
Seeds of only five ofthe 20 most abundant tree species are heavily used, and seeds
of43 ofthe 57 tree species listed in Table 1 were never observed to be eaten.
In contrast to the situation for young and mature leaves, seed selection ratios
are not highly correlated with number of records obtained (rs=0.42, n = 11
species encountered in enumeration with selection ratios above zero). This is
because seeds of both common and rare trees are used, in contrast to leaves,
most of which are obtained from rare trees. This raises the problem of which of
these measures to use as an estimate of relative preference in examining chemical
correlates of food choice. The aim must be to choose the estimate which would
more closely parallel the animal's response in a choice experiment. Selection
ratios would be suitable when feeding on rare plant species imposes a cost in
terms of greater energy expenditure required to find or move to the feeding tree,
and to move from one feeding tree to the next. This cost would lower the net
benetit gained from the food item and would be expected to affect relative
preferences. Colobew s a t a m ranging patterns, however, do not suggest that
feeding on seeds of rare trees imposes a substantially greater energy expenditure
than feeding on seeds of common trees. This is because a single tree with a large
seed crop can supply most of the grou 's diet for a period of several days.
Movement is only required to find supp ementary food items, and to locate a
new major feeding tree when one seed crop has been depleted (McKey, in prep.).
We feel that number of feeding records is a fairer indication of relative
preferences of C. s a t m among seeds than are seed selection ratios, and employ
this measure in our analyses. Total number of feeding records is also highly
correlated with maximum contribution to monthly diet (rs= 0.89, n = I3 tree
species from Table 1, P < 0.01).
Table 11 presents the relationships among different chemical variables and
correlations with extent of use, for the seeds of 16 species for which there are a
complete data set. Two variables, N and GE, are significantly positively
correlated with extent of use. Weak negative correlations are apparent between
use and all other variables measured. The negative correlation between RDIG
and use is due to the low digestibility of the two heavily used items, seeds of
Lophira data and Discoglypremnu caloneura. Both these items have relatively low
phenolic content and their low digestibility may be due not to general digestioninhibitors but to other substances, whose digestibility may differ greatly to the
rumen-liquor used in the assay (from a fistulated steer) and to a C. satanas
P
135
FOOD SELECTION BY COLOBUS SATANAS
Table 1 1. Relationships among chemical content, digestibility and use by
Colobus satanas (number of feeding records) for seeds (n= 16)
Ash
N
P
TNC
CE
RDIG
TP
CT
Feeding
records
0.18
0.32
0.21
-0.02
0
-0.12
0.05
-0.10
N
P
TNC
0.48
-0.26
0.31
0.18
-0.52.
-0.48*
0.65**
-0.06
0.39
0.41
-0.37
-0.28
0.32
CE
RDIC
TP
cr
-0.41
0.11
-0.15
0.61*
-0.50*
-0.40
-0.24
0.32
-0.21
-0.22
-0.05
0.06
0.60.
0.26
-0.17
Key: see Table 5.
stomach Hora that is presumably adapted to high intake of the items concerned
(Watermanet al., 1980).
Both N and GE are related to extent of use. Graphical examination of the
relationships showed that they were of different kinds. All the used seeds are distinguished from almost all the unused seeds by their high N content. Within this
set of high N seeds, those with the greatest number of feeding records are the
ones with highest GE. The correlation with GE depends almost entirely on
relative extent of use among five used items. However, these seeds varied greatly
in the number of months they were available, and when maximum contribution
to monthly diet rather than total number of records is used as an estimate of
relative preferences no strong relationship with GE is evident (Fig. 3). The
relationship of use with N content persists whatever estimate of preference is
used, because it almost cleanly divides used from unused items.
DISCUSSION
Which are the critical nutrients?
Colobus satanas select mature leaves with high content of N and mineral
nutrients relative to content of digestion-inhibitors. However, we are unable to
assess which of the nutrients measured might be the most critical, because high
levels of ash, P and N tend to occur together in the same leaves. Furthermore,
high contents of these nutrients tend to be associated with low contents of CT
and ADF (Table 8). To a large extent, there seem to be ‘good’ leaves rich in
mineral nutrients and N and low in digestion-inhibitors, and ‘bad’ leaves, with
the opposite characteristics. Thus, a ratio incorporating N, P and ash in the
numerator and ADF and CT in the denominator, is quite a good predictor of
C. satanas food choice among young and mature leaves (Fig. 4). At this gross level
of analysis, leaves seem to exhibit a rather uni-dimensional pattern of variation
among species in nutrient supplying capacity. Monkeys which select leaves
because of their high N content, for example, will automatically obtain a diet
rich in P (Table 81, without having to seek out other leaves.
The leaves among those examined which have the highest contents of N, P and
ash, and the lowest contents of digestion-inhibitors, are of light-demanding,
early successional species : Rauvolfia vomitoria, Discoglypremna caloneura (both
deciduous trees), Deidamia clematoides and Cissw producta (both fast growing semiherbaceous vines). Strategies of such plants favour low investment in defence of
D. 8 . McKEY ET AL.
136
t
111
0
40
30
Y
.
5'
I-
I
Figure 3. Relation between: I grow energy content (kcal g9;I1 nitrogen content (%I; and 111
riiaxiiiiuin monthly contribution ofa seed item (%I to the diet of Colobw ~ c l l ~ n aEach
c.
cross represents
a dilferent available seed item (n= 16).
0
A
0
A
0
A
0
0
0
0
Y
0
I
0.I
0.2
0.3
I
(x4
I
0.5
0.6
N+llOxPI+Ash
ADF +CT
Figure 4. Relation between the ratio of nutrient to digestion-inhibitor and number of feeding
records (log scale)by Colobur salanac for 26 young (A)or mature (0)leaf items.
FOOD SELECTION BY COLOBUS SATANAS
IS7
leaves, and metabolically highly active leaves rich in N and other nutrients.
Simply as a result of the plant’s own requirements, leaves of any one species of such
plants might supply to an herbivore adequate amounts of most minerals, in highly
digestible packets. The picture will certainly become more complex, however,
when more is known about content of specificminerals, especially those needed by
animals but not by plants (e.g. sodium, Oates, 1978).
In seeds, the picture is clearer because contents of mineral nutrients and N are
not so strongly intercorrelated ; evidently there are more different feasible ways
to put together a seed nutrient package than there are to construct a
metabolically active leaf. In seeds, use is strongly related to N content but not to
ash or P. Because N is unequivocally related to food choice among seeds, and
because N content of many of the leaf items may be lower than the critical
requirement of’ a small ruminant-like herbivore (especially considering the low
digestibility of these leaves), we consider it plausible that N, rather than other
nutrients measured, is also important in leaf food choice by these monkeys.
Patterns
offood selection 6y C . satanas
Major constraints onfood selection
The pattern of preferences shown by C. satanar suggests that selection of food is
shaped mainly by the requirement to obtain adequate amounts of N and readily
available energy, while avoiding digestion-inhibitory compounds, from
vegetation poor in these nutrients and rich in digestion-inhibitors such as
tannins and lignin. The monkeys achieve this in the following manner.
(i) They preferentially feed upon young leaves, which are richer in N and
TNC and more digestible than mature leaves. However, not all species produce
highly digestible young leaves. Our data indicate that there is variation between
species in the strategy of young leaf development, as suggested by McKey (1979).
Features such as the time course of leaf expansion relative to cell differentiation
and cell wall lignification, and the pattern of leaf expansion (e.g.
acropetal v. basipetal growth), vary between species and result in varying quality
of‘ young leaves as food for herbivores. Also young leaf production is seasonal
and suitable young leaves are not always present in quantity.
(ii) For mature leaves, as for young leaves, C. satanar feeds preferentially on
those with high concentration of N and low concentrations of digestioninhibitors (Figs 4, 5 ) . Such plants are rarer at Douala-Edea than in some other
rain-forest sites (Gartlan et al., 1980; Choo et al., 1981).Inmonths when C. satanar
are forced to rely to a large extent on mature leaves, the distance they move each
day increases dramatically (McKey, 1978a).Increased energy expenditure in food
search at these times, when quality of food ingested is already low, suggests
stringent limits to the degree to which these monkeys can depend on mature
leaves.
(iii) Col06us satanas preferentially feed on seeds, which are more digestible than
leaves. The chemical composition of seeds is subject to selective pressures very
ditt’erent from those affecting leaves and other vegetative parts. The function of a
seed is to serve as a highly concentrated nutrient package. Substances such as
lignin and tannin, which must be present in large amounts to provide effective
defence and which cannot be utilized by the growing seedling, conflict with this
function. In the chemical defences of seeds, compounds are emphasized which
D. 8 . MrKEY E 7 A /..
198
15
1
60
Figure 5. Relation between: I ADF+CT (%I; 11 crude protein (%); and 111 maximum monthly
contribution(%I to the diet of C d h solanas. Mature leaves (circles)and young leaves (triangles).
are effective toxins in low concentration, or which, like non-protein amino acids
and toxic lipids, double as toxins and nutrients (Janzen, 1978; McKey, 1979).
Thus, in a site like the Douala-Edea Reserve where most common tree species
produce tannin-rich, fibrous leaves, their seeds often largely lack such general
digestion-inhibitors.
Many seeds, however, appear low in N content relative to leaves and C. satanas
select those seeds that are richest in N.
Other constraints on C . satanasfood selection
How much of C. satanas food choice can the major constraints outlined above
account for, and how do they interact with the other variables that might be
expected to affect food selection in particular cases? One approach to this
question is to define the range of values along a major dimension of food quality
within which all accepted items fall, and determine which unaccepted items also
tall within this range and whose avoidance thus cannot be explained by the major
constraint. Two examples will be considered here.
(i)In the 26 young and mature leaf items for which there is information on all
the component variables, the ratio 6.25N/(ADF + CT)ranges from 0.118 to 0.647
(Table 12). All of the eight items which are significantly used (five or more
records) fall within the range 0.202-0.647. This means that no critical nutrient in
short supply, for example, has ever induced the monkeys to accept leaves with a
lower ratio. Of the 18 items not used, 13 fall into the ‘unacceptable’ range
0.118-0.202. Thus, the monkeys’ avoidance of five items cannot be adequately
139
FOOD SELECTION BY COLOBUS SATANAS
Table 12. Calculated nutrienddigestion-inhibitor
ratios for mature leaves and young leaves and
nitrogen values for seeds
6.25N/(ADF+ CT)
Mature
Young
leaves
leaves
Species
Protomegabaria slapfirma
Lophira alata
Librevillea hlainei
C o d a edulis
Anthonotha macrophylla
L'apaca staudtii
Trichoscyphapatens
Strombosiopsis letrandra
Uiscoglypremna caloneura
Garcinia mannii
Leptaulus daphnoides
Pachypodanthium sp. nov.
S t r e p h o r n pseudocola
Uiosjyros dendo
Dichostrmma ghucescens
Berlinia bracteosa
Xylopia quintasii
Berlinia auriculata
St rombosia pustulata
Anthonotha pcilliflora
Uiospyros hoyleana
Barteria,fistulosa
Gorcinia conrauana
Garcinia ovalgolia
Rauvolja vomitoria
Cissus produda
Hippocratea sp.
Ueidamia clematoides
Strychnos tricalysioides
0.165
0.135
0.146
0.145
0.209
0.192
0.133
-
0.515+
0.313
0.296
-
0.146
0317
-
0.202+
-
0.170
0.184
0.198
-
0.118
0.647*
0.280+
-
0.339+
-
N
seeds
0.292
-
-
2.26+
-
1.41
1.01
1.13
0.392+
0.201
0.187
-
-
0.547+
-
1.89+
2.32+
0.61
-
1.48
0.60
1.16
-
-
1.65
0.350+
-
2.16+
-
-
-
-
-
0.43
0.77
-
1.60+
-
2.32
~~
Key: see Table 5.
+ I terns utilized by Colobuc satanar.
explained, since their protein/digestion-inhibitorratio falls within the acceptable
range. One item, mature leaves of Anthonotha mucrophylla, is barely within (0.209).
Only one lightly used item has a lower ratio. Four items fall well within the
acceptable range and their avoidance must be due to other factors. Leptaulus
leaves contain alkaloids (Gartlan et d.,1980),Garcinia munnii leaves contain about
15% biflavanoids (Crichton 8c Waterman, 1979), and Dichostemm leaves possess
abundant milky latex. Protomegabaria young leaves, although lower in fibre than
the mature leaves, are less digestible in both RDIG (Waterman et al., 1980) and
CDIG (Choo et al., 1981) assays. We have no evidence to relate any of these
teatures to monkey avoidance. The point is that the procedure described
identifies those items whose avoidance is unexplained by major patterns and
suggests further work.
Relative preferences among the used items might be due to variation along the
major food-quality dimension in question, or in content of other essential
nutrients, or of secondary compounds, or might depend on the composition of
other foods available at the time. The sources of variation may be very difficult to
establish. In the case examined here, extent of use among the eight items which
140
D. B. McKEY ET AL.
are used is positively correlated with the protein/digestion-inhibitorratio
(rs = 0.74, P < 0.05).
(ii) In seeds of' the 16 species for which there is information, N content varies
from 0.43 to 2.32% (Table 12). The five of these which are used fall within the
range 1.60-2.32%. Two unused seeds, those of Strychnos triculysioides and Xylopia
quintasii also fall within this range. The family to which Xylopia belongs, the
Annonaceae, are uniformly avoided by C. satanas. They contain a variety of
secondary compounds including volatile oils, alkaloids and diterpene acids,
some of which might be especially deleterious to ruminant-like herbivores.
Strychnos tricalysioides seeds contain alkaloids (Zhong& Waterman, unpubl. ). Some
workers have drawn attention to lack of correlation between alkaloid presence/absence and food selection by primates (Hladik, 1977a, b). However, one
alkaloid may have very different properties from another (Levin& York, 1978).
We believe that procedures such as those outlined above are a useful first step
towards unravelling the role in food selection of the great variety of secondary
compounds whose highly restricted distributions in vegetation make correlation
analyses unsuitable.
Ruminant-like digestion and seedfeeding by C . satanas
Seeds represent the only item class which C. sutanas exploit heavily from any of
the common trees in the study site. The carrying capacity of this forest for
C.satanas would be greatly reduced if their feeding were restricted to young and
mature leaves, Ruminant-like digestion has probably facilitated the evolution of
the C.satanas feeding strategy. First, seeds probably contain higher concentrations of many types of toxins than do leaves. Second, each particular kind
of seed is available for only a short period once a year (or at longer intervals), so
that diet is constantly changing. Rapid adaptation to new diets containing high
concentrations of toxins would tax the capacity of a mammalian detoxification
system (Freeland & Janzen, 1974).The maintenance of a highly diverse gut flora,
consisting of billions of cells, with capacity for rapid evolution (Parra, 19781,with
much more diverse enzymatic potential than the animal itself, and with the
ability to rapidly induce specific detoxification enzymes when a new secondary
compound is added to the diet (Russell 8c Smith, 19681, may be an essential prerequisite ofthe C. satanas feeding strategy.
Further questiom
Some information is available on the chemistry of most C. satanas food items;
for only four of the top 20 is chemical data completely lacking. Among the
chemically characterized food items, there are two apparent exceptions to the
major patterns of food selection discussed above. Mature leaves of Berlinia
bructeosa were eaten heavily in several months, although they were relatively high
in fibre (57.4%)and low in digestibility (22.2%by CDIG). Nothing is known of
their nutrient content. Young leaves of Erythrophleum ivorense were lightly fed
upon in two months, contributing a total of 12 records. This item is extremely
tibre-rich ( 7 1.7%) and indigestible (15.3%by CDIG).
Another area of uncertainty concerns vine leaves. These account for about 1 1%
of all feeding records but owing to difficulties in identifying, marking and
collecting vine leaves, chemical data are available for leaves of only two heavily
used species (Cissus producta and Deidamia clemutoides),which account for 23% of
vine feeding records.
FOOD SELECTION BY COLOBUS SATANAS
141
More information is also required on toxin chemistry in plants available to the
monkeys. Unlike tannins and lignin, other classes of anti-herbivore compounds
are comprised of a diversity of structures varying greatly in their chemical and
biological properties, and each of restricted distribution. Many such compounds
have been identified in Douala-Edea vegetation (Table 131, but this is only a
small fraction of those present and likely to influence food selection in particular
cases.
Between community variation in vegetation chemistry and general hypotheses about herbivore
food selection
Our comparative studies of the chemistry of vegetation in the Douala-Edea
Reserve and Kibale Forest, Uganda have shown the former to have vegetation
richer in tannin and fibre, poorer in content of N and mineral nutrients, and less
digestible than that of Kibale Forest (Gartlan et al., 1980; Waterman et al., 1980;
Choo et al., 1981). Kibale Forest tree species more frequently contain alkaloids
(Gartlan et al., 1980). Studies in progress on the vegetation of other rain-forest
sites indicate that differences among tropical forests in nutrient and secondary
chemisy are not idios ncratic but rather form a pattern corresponding to
variation in ecological actors such as soil quality, altitude and plant species
diversity. Such a pattern would be expected if the extent and nature of plant
investment in chemical defence is partly determined by productivity of individual
plants and species diversity of the community (Janzen, 1974). Betweencommunity variation in vegetation chemistry must be appreciated if general
hypotheses about food selection by mammalian herbivores are to be related to
studies of diet composition by herbivores in the real world.
r
Table 13. Known distribution of toxins among plants of the Lombe study site
Species
Plant
part
Compoundsfound
~
Anihocleista vogelii
Garcinia mannii
Leplaulus daphnoides
Pachypodanthium sp. nov.
Pausinyslaliajohimbe
Mamma africana
Baikiaea inrigpis
Diospyros dendo
Xylopia quiaasii
Xylopia aethiopica
Symphonia globulqera
Diospyros gracilescenr
Diospyros hoyleana
Barleria,bstulosa
Carcinia conrauana
Garcinia ovalqolia
Rauvolba vom'loria
Shychnos tricalysioides
~
~~
Iridoids
BiHavanone (yield 15%)(Crichton & Waterman, 1979)
Arnyrin, alkaloids
Styrenes and alkaloids(Pootakahrn, 1978)
known source ofalkaloids (Hegnauer, 1975)
NeoHavonoids (Crichton & Waterman, 1978)
hetidine-2-carboxylicacid (E.A. Bell, p a . comm.)and
alkaloids
Napthoquinones (Waterman& Mbi, 1979)
Diterpene acids
Diterpene acids
Xanthones
Naphthoquinones (Waterman & Mbi, 1979)
Naphthoquinones (Waterman & Mbi, 1979)
Cyanogenic glycosides
Lactone (Waterman& Crichton, 1980a)
Benzophenone (Waterman& Crichton, 1980b)
Alkaloids
Alkaloids
B=bark; S=seed; L=leat.
Where no reterence quoted then unpublished data from the Phytochemisay Research Laboratory, University
o t Strathclyde.
142
D. 8. McKEY ET AI..
A
B
Douob-Eh
Kibole
Figure 6. Comparisonof digestion-inhibitor (1) and crude protein (11) levels ofmature leaves (circles)
and young leaves (triangles).A, From Douala-Edea; B, From Kibale (for data see Waterman cf al.
(1980)).
FOOD SELECXION BY COLOBUS SATANAS
143
For example, current theory predicts that the ratio of protein (and other
nutrients) to fibre (and other digestion-inhibitors) will be an important variable
atfecting food quality and hence food choice. This prediction seems to be borne
out by C. satanas food selection patterns. However, the ratio of protein to
digestion-inhibitors in C. satanas food items, representing leaves of rare trees and
highly seasonal seed items, could be supplied by young or mature leaves of the
most common trees in a site such as Kibale Forest (13.
Figs 5, 6). Other things
being equal, protein/digestion-inhibitorratios might in these circumstances not
greatly constrain diet choice, and other variables may assume paramount
importance.
ACKNOWLEDGEMENTS
Aspects of this study formed part of a PhD dissertation, University of Michigan
(D.B.M.). D.B.M. wishes to thank D. H. Janzen, his doctoral advisor, for his
sustained interest in this study, and the other members of his doctoral committee,
M. M. Martin, B. Hazlett and J. Vandermeer, for their critical readings of the
dissertation. Field work was financed by an N.S.F. Pre-doctoral Fellowship, The
New York Zoological Society and a Field Assistantship from J. S. Gartlan (N.I.H.
Grants No. RR 01055-02 and RR 00167-17) (to D.B.M.). Chemical studies were
financed by The Natural Environment Research Council Grant No. GR3/3455 (to
P.G.W.). The study was performed while D.B.M. was an investigator with
O.N.A.R.E.S.T. (Institut de Recherches Agricoles et Foriestieres). Ferdinand
Namata and Stephen Ekondo are thanked for their valuable assistance in the field.
The award o f a N.A.T.O. ScientificAffairs Division Travel Grant (No. 1748)to
P.G.W. and D.B.M. greatly facilitated collaboration.
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APPENDIX
Nomenclature of plant species cited in this study and their articipation in the
various comparisons used (A= mature leaf/young lea{ B =young leaf;
C =mature leaf; D =mature leaf/seed; E = seed)
Species
Acioa sp.
Aganope sp.
Anrhocleisln uogelii Planch.
Anlhonolha pcillipora Harms.
Anlhonolha macrophylla P. Beauv.
Anlhoslemma aubryanum Bail].
Anlidesma uogelianum Mull. Arg.
Bnihiaea insipis Benth.
Barlen'a,fislulosa Mast.
Beilschmiedia sp.
Berlinia auriculala Benth.
Berlinia hracleosa Benth.
Cissus producta Atiel.
Coelocaryon peussii Warb.
Cola sp.
Coula edulis Baill.
Clenolophon englerianus Mildbr.
Deidamia clemafoides Harms.
Dichoslemma glaucescens Pierre
DioJpyros dendo Welw. & Hiern
Diospyros bvacilescens Gurke
Diospyros hoyleana F. White
Disco&remna caloneura Prain
Erylhrophleum iuorense A. Chev.
Gnrcinia conrauana Engl.
Family
Rosaceae
Papilionaceae
Loganiaceae
Caesalpiniaceae
Caesalpiniaceae
Euphorbiaceae
Euphorbiaceae
Caesalpiniaceae
Passitloraceae
Lauraceae
Caesalpiniaceae
Caesalpiniaceae
Vitaceae
Myristicaceae
Sterculiaceae
Olacaceae
Ctenolophonaceae
Passitloraceae
Euphorbiaceae
Ebenaceae
Ebenaceae
Ebenaceae
Euphorbiaceae
Caesalpiniaceae
Guttiferae
A
Comparison
B C D
-
-
+
-
E
-
146
FOOD SELECTlON BY COLOBCS SATANAS
Species
Family
A
Garcinia mannii Oliv.
Garcinia ovalfolia Oliv.
Hipjiocralea sp.
Hyrnenodiclyon sp.
Hainedoxa gabonensis Pierre ex Engl.
I~plaulurdaphnoides Benth.
Librevillea Maim' Hoyle
Iaphira alala Banks ex Gaertn.f.
Macaranga barleri Mull. Arg.
Mammea a f i c a m Sabine
Majirounea rnembranacea Pax & K. Hotfm.
Mareyopsis longttolia Pax & K. Hotfm.
?Meroneuron sp.
Millelia sp.
Morinda morindoidcs Milne-Redh.
Ouralea afbnis Engl.
Pachypodanfhium sp.
Panda oleoia Pierre
Pauausinyslalia johimbe Pierre ex Beille
Prolomegabaria slakjana Hutch.
HauvolJia vamilm'a Afiel.
Hhaphioilylis ?bminnuisPlanch. ex Benth.
Strephonema mannii Ho0k.f.
Slrephonema pseudocola A. Chev.
Strombosia purlulata Oliv.
Slrombosiopsis tctrandra Engl.
Shychnos lricalysioides Hutch. & Moss
Slrychnos sp. 1
Slrychnos sp. 2
Strychnoi sp. 'small leaf
strychnos sp. 'small seed'
Symjihonia globul@ra Linn.f.
Toubaouale brevipaninclala Aubrev. & Pellegr.
Trichilin Ututm' Harms.
Trichoscyphapatcr Engl.
1:apaca slaudtii Pax
Xylopia aethiopica A. Rich.
Xylopia quinlasii Engl.
sp. 1
sp. 2
Sp. 1481
Guttiferae
Guttiferae
Hippocrataceae
Rubiaceae
lrvingiaceae
lcacinaceae
Caesalpiniaceae
Ochnaceae
Euphorbiaceae
Guttiferae
Euphorbiaceae
Euphorbiaceae
Cacsalpiniaceae
Papilionaceae
Rubiaceac
Ochnaceae
AMOMceae
Pandaceae
Rubiaceae
Euphorbiaceae
Apocynaceae
Icacinaceae
Combretaceae
Combretaceae
Olacaceae
Olacaceae
Loganiaceae
Loganiaceae
Logvliaceae
Loganiaceae
Loganiaceae
Guttiferae
Caesalpiniaceae
Meliaceac
Anacardiaceae
Euphorbiaceae
Annonaceae
AMOMCeae
Connaraceac
Connaraceae
Rubiaceae
Flacourtiaceae
sp. 4c
Sp. 78
sp. 5
?
?
?
Sp. 13
?
-
sp. 20
Comparison
B C D
E
?
~
~~~
~~
~~
~
~
+Denotes an item, or pair of items, subjected to all assay procedures. Many other items have been subjected
some assay procedures and these are denoted by (0);in column B (for young leaves), in column C (for
mature leaves),and in column E (for seeds). These data will be found in Gartlan ct al. (19801,Waterman el al.
(1980)andG.M.Chooctd.(1981).
to