close

Вход

Забыли?

вход по аккаунту

?

Distribution of terrestrial herbaceous vegetation and its consumption by Pan paniscus in the Lomako Forest Zaire.

код для вставкиСкачать
American Journal of Primatology 23:153-169 (1991)
Distribution of Terrestrial Herbaceous Vegetation
and its Consumption by Pan paniscus inthe
Lomako Forest, Zaire
RICHARD K. MALENKY' AND EDMUND W. STILES'
'Department of Anatomical Sciences, Health Sciences Center, State University of New York
at Stony Brook, Stony Brook, New York; 'Department of Biological Sciences, Rutgers
University, Piscataway, New Jersey
Data available on behavior and morphology of Pan paniscus (bonobos)
suggest that terrestrial herbaceous vegetation (THV) is an important component of their diet and that it may be preferred by bonobos to a greater
extent than by chimpanzees (Pan troglodytes). It has also been reported
that THV is ubiquitously distributed in the lowland rain forests inhabited
by bonobos. These data suggest that THV exploitation may be causally
related t o the evolution of the more cohesive social system found in bonobos compared to that of chimpanzees. Here, we present data that quantify
the spatial distribution of THV in the Lomako Forest, an analysis of the
nutrient content of the plant parts commonly consumed, and patterns of
THV consumption in relation to its distribution. The data clearly demonstrate that THV, and particularly Haumania liebrechtsiana (Marantaceae), is ubiquitously distributed as previously suggested. However, THV
feeding patches are rare because of distinct feeding preferences. Bonobos
preferentially choose H . liebrechtsiana over other species of THV, choose
patches with larger stems, and, within patches, choose larger stems over
smaller stems. The plant parts chosen are high in proteins and relatively
low in carbohydrates. Given the selectivity of the study population and the
patchy distribution of THV, it is unlikely that THV has been responsible
for the evolution of the unique social system reported for bonobos. Data
presented on party size are consistent with this conclusion.
Key words: Bonobo, THV, surveys, nutrition, social organization,folivory,
frugivory
INTRODUCTION
The quality and spatio-temporal distribution of critical food resources can
influence the social organization of foraging animals [e.g., Rubenstein, 1986; Sussman, 19771. Pan paniscus (bonobos) and Pan troglodytes (chimpanzees) are similar
in body size [Jungers & Susman, 19841, are primarily frugivorous, and have fis-
Received for publication May 16, 1990; revision accepted October 17, 1990.
Address reprint requests to Richard K. Malenky, c/o Dr. Randall Susman, Department of Anatomical
Sciences, Health Sciences Center, State University ofNew York a t Stony Brook, Stony Brook, NY 11794.
0 1991 Wiley-Liss, Inc.
154 I Malenky and Stiles
sion-fusion societies. However, consistent differences are reported in their grouping patterns and socio-sexual behavior. Bonobo temporary parties are generally
larger than those reported for chimpanzees and are more often mixed in composition (composed of animals of both sexes and all ages) [Badrian & Badrian, 1984;
Kano, 1980, 1982, 19871. Females are more cohesive. Regardless of reproductive
state, female bonobos frequently associate with one another and engage in a variety of affiliative behaviors (mutual grooming and genito-genital rubbing)
[Thompson-Handler et al., 1984; Kano, 1987,1980; White, 19881. In contrast, anestrous female chimpanzees are more solitary and less affiliative [Nishida, 1979;
Wrangham, 1979; Wrangham & Smuts, 19801. Male bonobos groom females more
often than they do other males [Kano, 1980; Badrian & Badrian, 19841, while
among chimpanzees, males are more affiliative toward each other [Nishida, 1979;
Wrangham, 1979; Wrangham & Smuts, 19801 and associate with unrelated females primarily during estrus [Goodall, 19861.
Wrangham [19861 proposes that lower levels of feeding competition, particularly among bonobo females, has been a causal factor in the evolution of the more
cohesive social system found in this species. He suggests that due to decreased
competition for food female bonobos were initially able to forage together and then
attracted males to their groups via increased sexuality. Two environmental factors
that might account for the presumed lower levels of competition in bonobos are
larger fruit patch sizes and abundant levels of terrestrial herbaceous vegetation
(hereafter referred to as THV) (see below).
In fruit trees, party size increased with patch size and is probably restricted at
smaller patches by feeding competition, in both species of Pan [Wrangham, 1977;
Ghiglieri, 1984; Isabirye-Basuta, 1988; White & Wrangham, 1988; Malenky,
19901. White and Wrangham [19881 report that mean fruit patch size in the Lomako Forest, Zaire, is larger than at the Gombe Stream Reserve in Tanzania,
suggesting that bonobo feeding parties may be less constrained by fruit patch size.
However, both species of Pan also consume animals (i.e., insects and/or vertebrates) and nonreproductive plant parts (i.e., leaves, pith, stems), including those
of THV. Unlike most reports on the feeding ecology of chimpanzees, those for
bonobos suggest that THV is densely and evenly distributed in their habitat and
constitutes a major dietary component throughout the year (see below).
Free-ranging populations of bonobos have been studied primarily at two sites,
the Lomako Forest and at Wamba (Fig. l),but studies have also been conducted at
Yalosidi [Kano, 19831 and Lac Tumba [Horn, 19791. At both major sites, bonobos
regularly consume the pith and new leaves of a variety of herbaceous plant species
[Kuroda 1979; Badrian and Malenky 1984; Kano & Mulavwa 19841.
Badrian and Malenky [19841 report that, if judged by the frequency of consumption, THV is the second most important dietary component exploited in
the Lomako Forest after fruit pulp. Kano [1983:12] reports that at Yalosidi,
during a 3 month period in 1974-75, nonreproductive plant parts “occupied as
important a place in the diet as did tree fruits.” He suggests that THV is consumed
as an alternative resource when fruit is in short supply [also see Badrian et al.,
19811.
In the Lomako Forest, one species in particular, Haumania Ziebrechtsiana
(Marantaceae), is consumed during every month of the year, and if direct observation, fecal analysis, and frequency of feeding remains are combined, H . liebrechtsiana is the food most frequently utilized by bonobos [Badrian & Malenky, 19841.
These authors also report that H . liebrechtsiana is prevalent throughout the study
area in all forest zones. Kano [1983:29] describes THV as “characterized by yearround production and lack of notable seasonality.” These reports have led t o the
Bonobo Feeding Ecology: Patch and Party Size / 155
WAMBA
v LOMAKO
FOREST
Fig. 1. The locations of the two principal sites for field studies of Pan paniscus in Zaire.
generally accepted characterization of THV as spatially and temporally ubiquitous
in the bonobos’ habitat.
While THV is consumed by chimpanzees, it seems to be eaten less frequently
and less regularly. Hladik [1977al reports that Pan troglodytes troglodytes in the
lowland forests of Gabon consume the stems of only one Marantaceous herb
(Hypselodelphis uiolacea) and it is not ingested in large quantities throughout the
year. Since the stems of this species contain relatively high levels of protein,
Hladik [1977a:4941suggests that, along with leaves, these plants “may be eaten to
complement fruit when invertebrates or other animal prey cannot be obtained in
sufficient quantity.” At the Gombe Stream Reserve in Tanzania, Wrangham [1977]
reports the consumption of nonreproductive plant parts from 15 species of THV.
However, THV consumption at Gombe comprises approximately 7% of the monthly
food intake, whereas at Wamba, THV accounts for 33% [Wrangham, 19861.
Data on dental morphology also suggest that THV is more important to bonobos [Kinzey, 19841. There is relatively more wear on bonobo incisors, which,
Kinzey suggests, may result from using the front teeth to open the fibrous outer
covering of terrestrial plant stems. He also notes that the structure of the upper
and lower molars may provide greater shearing efficiency. In other primates, a
similar molar structure is associated with a more folivorous diet [e.g., Kay, 19891.
Thus, bonobos may have evolved to depend on nonreproductive plant parts more
extensively than have chimpanzees.
If THV is continuously available to bonobos in space and time, is a major food
source, and is exploited regularly, then it seems plausible that THV (in conjunction
with or instead of large fruit patches) has promoted the evolution of larger party
size and a more cohesive social organization [e.g., Wrangham, 19861. Yet, quantitative data have not been reported on the spatial distribution, temporal availability, or patterns of exploitation of THV for any site where either species has been
156 I Malenky and Stiles
studied. Also, observations of party sizes during ground feeding are scarce [White
& Wrangham, 1988; Kuroda, 19791.In this paper, we present quantitative data on
the spatial distribution and nutrient content of THV in the Lomako Forest, as well
as data on selectivity in the feeding behavior of the bonobo population. We then use
these data to evaluate some of the qualitative impressions reported in the literature on THV distribution and use. Specifically, we address the following points:
1. Are the species of THV consumed by bonobos ubiquitously distributed in
the Lomako Forest?
2. Are the study animals selective as to the feeding sites chosen?
3. Within feeding sites, do bonobos select particular species and individual
plants?
4. Within plants, do they select some plant parts over others?
5. Do the species and plant parts consumed by bonobos have protein levels as
high as those reported by Hladik [1977al?
6. How does 'THV compare nutritionally to fruit?
The Study Site
The Lomako Forest study site is located in the Cuvette Centrale, province of
Equateur in Central Zaire at 0" 51' north, 21" 05' east (Fig. 1)between the Lomako
and Yekokora rivers. The study site covers approximately 35 square kilometers
and is composed of three forest types: primary forest, secondary forest, and swamp
forest (Fig. 2). Primary forest is by far the most common and has the greatest
concentration of fruit trees exploited by the study population. Thus, most direct
observations of bonobos were made in primary forest.
The data presented here were collected during two field seasons that ran from
October 1984 through July 1985 and from October 1985 through July 1986. During
the 1984-1985 field season, R.K.M. directly observed bonobos for 188 hours and 19
minutes, and during the same 10 months of the following year, for 237 hours and
30 minutes.
METHODS
In part, this study was designed to examine food choice in THV consumption.
However, in most cases, only selectivity, not preferences, could be measured. Measures of selectivity are site- and time-specific; i.e., they are the proportion of an
item in the diet relative to its availability during the time the study was conducted
[Johnson, 19801. Preference is independent of availability and is the likelihood
that an item will be chosen if offered on an equal basis with all others. While it is
possible to infer preference mathematically from field data [e.g., Johnson, 1980;
Chesson, 19831, direct observation of focal animals is required. Since bonobos in
the Lomako Forest, are not fully habituated t o human observers, it was impossible
to collect such data and conclusions regarding preference must remain, in most
cases, conjectural. However, in one case (see Results), the bonobos consistently
encountered two herbaceous food species simultaneously. In such cases, preference
can be assessed with respect to those species.
Transect Surveys: Spatial Distribution of THV in the Forest
Surveys were conducted along existing trails throughout the central core of the
study site (Fig. 2). Plots of 25 m2 were laid out every 100 paces along the trails, and
the presence and abundance of seven species of herbs known to be exploited by
-s.$sasuBzq 30 sJa?auropy 11 dIa??.?uI!xoJdde 8upaao3 ‘padaa
-ms aJaM sloid ZTI 30 ~ e i o qv -sJade1 ddoum afpppu pue ddoue3 Jaddn pue s p 3
a a q 30 amasqe .IO aauasazd aqq papiosai am ‘ails q m a qv .quasqB (p pue fal8ueq ou
q ? ! ~?old ay33o qmd p a p g s a i e u! d1uo TuasaJd aiaM sways-asmds (E faupq.ra)uT
JOU p ~ qnq
p loid aqq qnoqSnoxqy quasaid aiaM suraqs-uoururo3 (z fpeaqJaao a I8 u q
xalduros e pau1.103 put? qold a q u a aqi Jaao paqnq!qsyp aJaM suraqs uaqM-JuBp
-unqe (1:sa!Lo8aqm q8noJ m03 uo palom SBM asuepunqv .papioaai aJaM soqouoq
158 / Malenky and Stiles
Exploited vs. Unexploited Sites: Selectivity for Sites of THV Consumption
and Among Different Species of THV Within Sites
Bonobos consume THV on the ground and leave easily identifiable feeding
remains. It is therefore possible to identify sites confidently where they have exploited THV.
Eight sites were surveyed where animals were observed feeding on ground
herbs or where feeding remains indicated recent THV consumption. To compare
these sites with the forest as a whole, a series of nine randomly chosen plots were
surveyed in the primary forest. Survey plots were 100 m2 (10 m x 10 m). All H .
liebrechtsiana plants present were counted, and for every tenth plant, the basal
diameter, number of segments, and height of plant were measured. Similar measurements were made on plants of Palisota sp. (Commelinaceae) since it commonly
appears in association with H . liebrechtsiana and, therefore, was assumed to be of
comparable availability. For each site, the forest type, terrain, and the presence of
gaps i n the canopy and/or the presence of tree falls were recorded i n order to
explore the effect of gross environmental differences on the growth of herbaceous
plants.
Collections of Feeding Remains: Selectivity Among Species, Within
Species, and Within Plants
To obtain a n independent measure of plants chosen for consumption, feeding
remains of all herbaceous plants exploited by the bonobos were noted daily as to
location, species, and plant parts consumed. Different trails were covered by different researchers each day, and all instances of herbaceous feeding remains were
noted. We collected and measured 146 sets of plants. Each set represents a unique
instance of feeding on THV and was composed of one or more plants of a varying
number of species. For H . liebrechtsiana, we recorded the number of segments per
plant and the diameter and length of all segments. For those segments in which
pith was consumed, we measured the amount (length) of pith eaten (i.e., missing).
All segments were opened, and the presence of available pith not eaten was recorded. Terminal segments contained either new leaves or new stem material (i.e.,
new shoots) or both. If parts of these segments were consumed, this too was measured. The number of new (unfurled) leaves consumed was recorded when part of
a n expanding leaf was consumed or when the mature petiole surrounding a new
leaf was left split open and newer leaf material inside was missing. The diameter
of the basal segment was recorded only when the association of eaten parts and
uneaten parts still in the ground was clear.
Segments closer to the top of the plant are younger than those at the base.
However, within each segment, pith differentiates basipetally; i.e., from the top
down, so that the lower portion of pith within each segment is younger and less
fibrous than is the upper portion. A comparison of feeding remains, and untouched
plants revealed that within each stem segment the animals are selecting the
younger (lower) portion of the pith. There is a n abrupt transition between young
and old tissue within segments, and i t is, therefore, possible to snap off the younger
portion of the pith easily after cracking open the outer cortical layers of the stem.
The two types of tissue are also of different color. Using these characteristics as a
guide, it was possible to examine unexploited sections of plants collected with
feeding remains and to assess the extent to which available pith within a plant is
ignored.
Bonobo Feeding Ecology: Patch and Party Size I 159
Party Size
Observations of bonobos feeding on THV are scarce because the density of the
vegetation results in poor viewing conditions and because the animals are shy
when on the ground [personal observation; Kuroda, 19791. Thus, counts are only
reported for instances in which the number of animals present could be confirmed
by an independent measure. This was possible if the animals left the area by
climbing above the ground vegetation andlor if the number of feeding sites found
after they left equaled the number of animals observed during the sighting.
Statistical Analysis: Measures of Selectivity
Individual plants of species chosen for consumption were measured using the
diameter of the basal segment since this measure is positively correlated with the
overall size of the plants and, therefore, with the biomass of available food material. Data from the eight exploited and nine randomly chosen survey plots were
analyzed for differences in the average basal diameter using a nested analysis of
variance design [SAS, 19851 to determine whether or not bonobos are selective in
their choice of site for the consumption of THV.
Selectivity among sites was also measured as the ratio of the frequency of
exploitation relative to the availability in the forest. Values greater than one are
taken to demonstrate positive selection, and less than one, avoidance. A one-way
analysis of variance was used to analyze differences in stem densities between
randomly chosen and exploited sites. Selectivity among species was assessed as the
frequency with which each appeared in samples of feeding remains compared to its
frequency in transect surveys.
To determine if the eaten plants of a species were a subset of those available
in exploited sites, ranked basal diameters of plants found in feeding remains were
compared to those in exploited sites using a Kruskal-Wallis test. Simple frequencies were calculated for tree fall occurrence and distribution of all herbaceous
plants in the forest as a whole. The frequency of consumption of different plant
parts was calculated from feeding remains.
Biochemical Analysis
All plant parts consumed from the two most common food species in the forest
(H. lzebrechtsialza and Palisota sp.) were dried to constant weight in the field, using
a drying oven following Hladik [1977b]. However, the specimens of Palisota sp.
were destroyed by a fungal infestation and only those of H . liebrechtsiana remained. These were assayed for carbohydrate content, protein content, and lipid
content. In the laboratory, plant samples were again dried to constant weight at
60°C and ground to a fine powder with a glass mortar and pestle.
Soluble carbohydrate content was assessed against a glucose standard using
Anthrone reagent [Allen, 19741 after a 2 hour extraction in hot water. Proteins
were assayed using a micro-Kjeldahl extraction to ascertain percent dry weight
nitrogen, which was then multiplied by 6.25 to obtain an estimate of protein
content [Association of Agricultural Chemists, 19651. The lipid content was determined gravimetrically as the percent of mass lost after a 16-18 hour extraction
with petroleum ether. Reproted values are means of replicate samples.
RESULTS
Distribution of Herbaceous Species
Transect surveys indicate that two species, H . liebrechtsiana and Palisota sp.,
are found far more commonly in the primary forest than is any other. Of the 112
160 / Malenky and Stiles
TABLE I. Frequency and Distribution of THV in 25 m2Plots (Transect Surveys)
Genus
Species
Family ( )”
Haumania liebrechtsiana
Marantaceae (F)
Palisota spp.
Commelinaceae (F)
Trachyphryium braunianum
Marantaceae (F)
Sarcophrynium schweinfurthii
Marantaceae (F)
Renealmia africana
Zingerberaceae (F)
Megaphrynium macrostachum
Marantaceae (F)
Afromomum spp.
Zingerberaceae (F)
Costus afer
Zingerberaceae (FIL)
Pb
(96)
Abs
(%I
Abu
(96)
C
S
N
(%)
(%I
(%)
108
96.4
4
3.6
39
34.8
49
43.7
20
17.9
0
0
94
83.9
18
16.1
23
20.5
39
34.8
30
26.8
2
1.8
29
25.9
83
74.1
27
24.1
5
4.5
85
75.9
107
95.5
0
0
-
6
5.4
-
18
16.1
-
5
4.5
-
0
0
-
-
-
-
0
0
-
-
-
-
-
a(F)-Known as a food from both Wamba and Lomako. (F/L)-Known a s a food in the Lomako only. Sources:
Badrian and Malenky [19841; Kana and Mulavwa 119841.
bNumber of sites in which the species is: P-present; Abs-absent; Abu-abundant; C-common; %sparse;
N-no data. %-is the 4s of the total number of survey sites.
sites surveyed (Table I), 96% contained H . liebrechtsiana and 83% contained Palisota sp. The next most common herbaceous plant, Trachyphrynium braunianum
was found in only 26% of all the surveyed sites. Thus, two species of THV are
encountered throughout the primary forest and are virtually ubiquitous in their
distributions.
Selectivity Among Herbaceous Species
Selectivity among species, as assessed from feeding remains, shows that bonobos favor H . liebrechtsiana over Palisota sp. (Table 11). Of 146 samples (“sets”) of
feeding remains, 100% included H . liebrechtsiana while only 2.05% included Palisota sp. H . liebrechtsiana is consumed far more often than is any other species of
herbaceous plant.
Selectivity Among Sites Within the Forest and Among Plants Within Sites
Exploited sites are composed of plants with significantly larger stem diameters
than are randomly chosen sites (Table IIIa; Fig. 3). The mean basal diameter in
exploited sites is 10.45 mm and only 7.45 mm in randomly chosen sites. Comparisons of plants within exploited or unexploited plots show no significant difference
with respect to size (stem diameter). Clearly, bonobos choose feeding sites for H .
liebrechtsiana that are a specific subset of those encountered in the forest as a
whole.
Plants collected from feeding remains (Table IIIb; Fig. 3) are an independent
measure of plant size found at preferred feeding sites, as well as the size preference
for plants within these sites. On average, bonobos choose larger plants than are
Bonobo Feeding Ecology: Patch and Party Size / 161
TABLE 11. Collections of Feeding Remains
A. Species of THV found in samples
(total number of samules = 146)
Frequency
Percent
of occurrence of samples
Species
Haumania liebrechtsiana
Palisota sp.
Trachyphrynium braunianum
Sarcophrynium schweinfurthii
Afromomum sp.
Unidentified (common name = Weye)
146
3
2
3
1
1
100
2.05
1.37
2.05
0.68
0.68
B. Parts of Huumania liebrechtsiana consumed
(total number of plants collected = 259)
Plant part eaten
Immature pith
New leaves
New shoots
Number of
plants (%)
230 (89)
90 (35)
229 (88)
found in exploited sites. The mean basal diameter of plants consumed (11.68 mm)
is significantly larger (P < 0.005) than for plants found at exploited sites.
Characteristics of Exploited Plots and the Selectivity Index
Of the eight exploited sites surveyed, five were located within clearings created by tree falls. These sites have openings in the canopy, and sunlight reaches
the forest floor, stimulating THV growth. When all tree fall sites encountered are
combined (whether exploited or unexploited), the average stem density of H. liebrechtsiana plants (mean = 1.43 stems/m2, n = 6; s.d. = 0.71) is significantly
greater (P < .001) than at sites in the primary forest which have a closed canopy
(mean = 1.04, n = 10, s.d. = 0.25). The average basal diameter ofH. liebrechtsiana
plants is also greater at tree falls. The mean diameter at tree falls is 10.13 mm (n
= six sites), while in closed canopy sites, it is only 7.72 mm (n = ten sites).
During transect surveys, tree falls were encountered at 13 sites along the 11
km of trails surveyed (approximately 1.2 tree fallslkm of trail covered). Thus, not
only are such sites relatively rare in the forest, but the bonobos also exploit them
selectively.
The selectivity index for tree fall sites can be calculated in two ways, both of
which yield identical results. The frequency with which tree fall sites are exploited
is 518 or 0.63. This can be divided by two different estimates of tree fall frequency
in the forest as a whole. The first is derived from the transect surveys. Of the 112
sites surveyed, 13 were tree falls or 0.11. This yields a selectivity index of 5.73. The
second tree fall frequency estimate comes from the surveys of randomly chosen
plots, or 119 which also equals 0.11 and a selectivity index of 5.73. Clearly, the
bonobos are selective in their choice of plots for THV consumption.
Selectivity Within Plants
Bonobos consume three classes of plant parts of H. liebrechtsiana: young pith,
new shoots, and new or parts of new, unfurled leaves. Table IIb shows that the pith
162 / Malenky and Stiles
TABLE 111. Statistical Analysis of Stem Diameters
A. Nested ANOVA of exploited vs. random (unexploited) plots
Source of
variance
Exploited vs.
unexploited plots
Within plot type
Error
D.F.
Sumof
squares
Mean
square
1
15
178
401.10
215.31
1559.92
401.10
14.35
9.33
Percent
of
variance
F
(sign.)
27.95***
1.54n.s.
28.93
3.24
67.83
~~~
***P < 0.001
Descriptive statistics for plants within plot categories
No. of
plants
Exploited
Unexaloited
Mean basal
diameter (mm)
104
91
10.45
7.45
S.D.
range
3.29
2.95
2.9-16.7
2.4-15.2
B. Average basal diameter of feeding remains vs. exploited plots
Level
Exploited plots"
Feedine remains
N
Mean
104
294
10.45
11.68
Kruskal-Wallis test: x2 := 7.99; DF = 1; Prob > x2 = 0.0047.
"Some plants in exploited sites may have been removed completely by pygmy chimpanzees and, therefore, not
recorded. Thus, the mean basal diameter may be slightly larger or smaller than that reported here.
RANDOM S U R V E Y P L O T S
E A T E N PLANTS
1 3 5 7
S T E M DIAMETER ( m m )
P L O T S E X P L O I T E D F O R FOOD
s nnisvwa
S T E M DIAMETER (mm)
S T E M DIAMETER ( m m )
Fig. 3. Comparison of the frequency distributions of plant size (measured by basal diameter) for Haumania
liebrechtsiana plants found among feeding remains, a t sites where pygmy chimpanzees are known to consume
THV and a t randomly chosen plots in the primary forest.
and new shoots are eaten with the greatest frequency. New leaves are eaten with
less than half the frequency as other plant parts.
It was possible to assess the extent of the young pith consumption in 159
plants. In only 15% of cases was edible pith material not exploited. Often the
ignored pith was contained i n the younger, thinner segments which contain very
little edible material compared to the larger segments near the base of the plants.
Bonobo Feeding Ecology: Patch and Party Size I 163
TABLE IV. Nutrient content of Haumania liebrechtsiana
(% drv wt.)
Plant part
Protein
Carbohydrates
Lipids
New leaves
New shoots
New pith
40.35
44.60
30.62
2.35
2.65
1.65
1.59
1.98
1.26
Party Size
During 19 months of field work, R.K.M. witnessed seven instances of bonobos
feeding on ground vegetation. The average group size observed feeding on THV
was 2.1 (range 1-5). The average group size observed feeding on fruit was 5.6 (n =
128).
Biochemical Analysis
Table IV shows that all parts of H . liebrechtsiana consumed by bonobos are
high in protein. The average ripe fruit consumed by bonobos in the Lomako Forest
contains 4.5% dry weight protein [Malenky, 19901, while, on average, the nonreproductive parts of H . liebrechtsiana consumed have a protein content of 38.52%
dry weight. The highest level of protein found in any ripe fruit analyzed was 9.2%
dry weight, or less than 113 the amount in the pith of H . liebrechtsiana which had
the lowest levels of any part analyzed.
On the other hand, the carbohydrate content is significantly lower than that of
ripe fruits. The average carbohydrate content of ripe fruit eaten by bonobos is
31.96% dry weight, while that of H. liebrechtsiana is 2.22%. The average lipid
content in H . Ziebrechtsiana (1.61% dry weight) is also lower than that of ripe fruit
(5.48% dry weight).
DISCUSSION
The results reported here demonstrate that preferred stems of THV are distributed in discrete patches, much like fruit. Furthermore, this resource does not
appear to support larger party sizes. If lowered levels of feeding competition have
played an important role in the evolution of bonobo society, large fruit patch size
is more likely to have been the causal factor. In addition, nutritional analysis and
behavioral observations summarized below imply that the THV consumed by bonobos in the Lomako Forest is more important as a protein source than as an alternative to fruit.
Selectivity Among Species
One species of THV, H . liebrechtsiana, is selected for consumption over other
commonly encountered herbaceous species in the forest (i.e., Palisota sp.). Kano
and Mulavwa [1984] also find that at Wamba H. liebrechtsiana is consumed regularly while Palisota sp. is rarely eaten even though it is abundant in the primary
forest. The fact that H . liebrechtsiana and Palisota sp. are encountered simultaneously suggests that bonobos not only select H . liebrechtsiana, but also that they
prefer it. This result echoes similar findings reported in many studies of primate
feeding ecology (e.g., mountain gorillas: [Watts, 1984; Vedder, 19841);that is, some
food species (such as H . liebrechtsiana) are preferred over others in a similar
category and are, therefore, more likely to have a significant impact on the behavioral ecology of the consumer population.
164 / Malenky and Stiles
Is Haumania Ziebrechtsianu Ubiquitously Distributed?
Transect surveys (Table I) clearly show that H . Ziebrechtsiana is found nearly
everywhere in the study site. Similarly, Rogers and Williamson [1987:2781 report
that in Gabon herbaceous plants in the Marantaceae (which includes H . liebrechtsiana) are “essentially continuous.”
This does not seem t o be the case from the bonobos’ viewpoint, however. They
exhibit strong selectivity both for sites where THV is exploited and for plants
within those sites when plant size is taken into account. Bonobos show a strong
preference for tree fall sites (selectivity index = 5.68). Also, evidence of previous
exploitation (i.e., old feeding remains found next to broken stems with lateral
regeneration) is often found at these sites. Future studies, with increased sample
size, are therefore expected to corroborate this finding.
At tree fall sites, where the upper and middle canopy layers are missing, there
is a more luxuriant growth of H . liebrechtsiana than in the forest as a whole and
stem density is higher and stems are larger. As such, these sites represent discrete
patches of preferred food. Since tree falls occur in low frequency’ (approximately
1.2/km of transect), they might be expected to promote feeding competition and to
restrict party size.
Does THV Promote Larger Group Sizes in Pygmy Chimpanzees?
Reports of party sizes while feeding on THV are few, but suggest that they are
smaller than average. In the Lomako Forest, White [in White and Wrangham,
19881 reports a mean group size of 1.32 individuals feeding on H. liebrechtsiana
and that groups feeding on the ground tended to disperse rather than to remain
cohesive. Our data corroborate this finding. Mean party size while feeding on THV
is 2.1 (n = 7) and on fruit is 5.6 (n = 128). Kuroda [I9791 notes that at Wamba
bonobos feeding on THV split up into smaller groups. In spite of the small sample,
these data are consistent and its seems likely that bonobos feed on THV in small,
dispersed parties. Therefore, if lower levels of feeding competition among bonobos
have led to larger party size and the evolution of a more cohesive social system, a
food resource other than THV has been the selective factor. Data presented by
White and Wrangham [1988] suggest that fruit patch size is larger for bonobos in
the Lomako Forest than for chimpanzees at Gombe and may have selected for the
bonobo’s cohesive social system. While their hypothesis is consistent with the
available data, studies a t a greater variety of sites are needed to confirm the
generality of this pattern. Other factors affecting food choice and feeding behavior
must also be examined to understand why THV patches are effectively smaller
than those of fruit. H . liebrechtsiana is very different biochemically than is fruit
consumed by bonobos in the Lomako Forest, suggesting that nutrient content
might be important.
‘To evaluate the rarity of tree fall sites as a “food resource,” R.K.M. compared the density (average
abundance) of tree falls encountered during transect surveys to the densities of exploited fruit tree
species recorded in twelve 50 m x 50 m quadrats [Malenky, 19901. The total length of transects surveyed
(11km) was converted t o a measure of area by conservatively assuming that the transects were 1meter
wide. Thus, the total area covered by transects was 11,000 m2,and the average density of tree fall sites
(n = 13) is 11.8ihectare. The densities of exploited fruit tree species ranged from 0.33 to 41.00 trees per
hectare. The range of fruit tree densities was divided into nine equally sized classes. On this scale, the
density calculated above for tree fall sites falls into the third rarest class.
Bonobo Feeding Ecology: Patch and Party Size / 165
The Role of THV in the Bonobo Diet
Studies of primate feeding ecology have shown that nutrient content can play
an important positive role in food choice [e.g., Casimir, 1975; Oates et al., 1977;
Glander, 1978; Milton, 1979; Watts, 1984; Calvert, 1985; Gautier-Hion, 1986;
Marks et al., 1987; Ganzhorn, 19881, and that secondary compounds (e.g., tannins)
can play a negative role [e.g., Oates et al., 1977; Glander, 1981, 1982; Wrangham
and Waterman, 1983; Ganzhorn, 19881. It is also clear that while a minimum of all
essential nutrients is necessary, most resources provide only a limited array of
these components [Altmann and Wagner, 19781.
It is unclear whether THV is eaten as a substitute for fruit (i.e., carbohydrates)
by bonobos but is less preferred [Badrian et al., 1981; Kano, 19831or whether it is
eaten as a protein source and is, therefore, a substitute for animals [Hladik,
1977al. Lower levels of carbohydrates (relative to fruits) and higher protein levels
suggest that THV is consumed as a protein source and not as a source of carbohydrates.
Furthermore, if THV is eaten as a fruit substitute, it should be ignored when
fruit is more abundant since fruit is a far more profitable source of carbohydrates.
However, THV (and especially H . Ziebrechtsiana) is consumed throughout the year
in the Lomako Forest [Badrian & Malenky, 19841,regardless of fruit abundance or
scarcity. Similarly, Kano and Mulavwa [1984] show that consumption of H . Ziebrechtsiana during the driest months (January-February), when fruit is most
likely to be scarce [e.g., Augspurger, 1982; Garwood,' 19831, was not noticeably
greater than during wetter months.
Studies in the Lomako Forest indicate that fruit does not markedly decrease
during the drier periods of the year [Badrian and Malenky, 1984; Malenky 19901,
suggesting that bonobos may not experience a seasonal shortage of soluble carbohydrates as many primates, including chimpanzees, do elsewhere [e.g., Wrangham, 1977; Gautier- Hion, 1980; Foster, 1982; Terborgh, 1983, 1986; Ghiglieri,
19841. Thus, the consumption of THV in all seasons corroborates the suggestion
that it contains an essential nutrient (i.e., proteins) lacking in fruit. Also, the pith,
young leaves, and shoots of H . Ziebrechtsiana are neither bitter nor astringent
[R.K.M., personal observation], suggesting that they lack significant levels of secondary compounds which would further enhance their profitability.
Nutrient Content and Group Size
Mammalian daily carbohydrate requirements are much greater than are protein requirements [e.g., Kerr, 19721, and we estimate that bonobos need at least
ten times the amount of carbohydrates as proteins.2 If bonobos consume THV as
a source of protein, they would, therefore, require much less plant material to
'Daily adult nutrient requirements were estimated assuming a body weight of a n adult male as 45 kg
following Jungers and Susman [19841. Kerr [1972:4311reports that the daily carbohydrate requirement
of an adult chimpanzee is approximately 55 kcalikg of body weight. One gram of carbohydrates contains
approximately 4.1 kcal of energy [Johnson, 19832581. Thus, the daily caloric need of a n adult male
pygmy chimpanzees is approximately 2,475 kcal(55 kcalikg x 45 kg), which is equivalent t o 603.65, or
604 g of Carbohydrates. Estimates of daily protein requirements for adult chimpanzees are not available.
Hodson et al. 119671,as cited in Kerr [19721,report that young chimpanzees require approximately 4 g/kg
per day, but Kerr [19721notes that daily requirements decrease markedly with age. For a 70 kg human
male, estimates of the daily adult protein requirement range from 0.5 to 1.0 gikglday [Hegsted, 19641.A
45 kg adult chimpanzee would require somewhat more than this since metabolic rates decrease with
increasing body size [Kleiber, 19611. Using a n estimated daily protein requirement of 1.2 gikgiday, a n
adult male bonobo would need approximately 54 glday. The carbohydrate requirement for the same
animal is, therefore, 11.2 times the protein requirement.
166 I Malenky and Stiles
satisfy nutritional needs, which might be expected to decrease the intensity of
feeding competition.
Nonetheless, THV patches might restrict party size if time constraints were
influencing bonobo feeding behavior. The need to satisfy other nutritional requirements, as well as social needs, might necessitate the maximization of intake rates,
effectively decreasing the size of available patches [Stephens & Krebs, 19861.
THV Relative to Other Protein Sources
Kano and Mulavwa [1984:267]suggest that “it is doubtful whether the animal
foods in the diet reach the level observed in common chimpanzees. For pygmy
chimpanzees, plant foods appear to be more important than for common chimpanzees.” The regular consumption of THV and the bonobo’s apparent molar specialization suggest that, this may be the case. If so, and if THV is consumed as a source
of protein, then bonobos might be expected to consume more THV and less animal
material relative to their availability than do chimpanzees, which might help to
decrease the effective size of available patches and limit party size.
However, at Bossou, Guinea, Pan troglodytes uerus consumes the pith andtor
young leaves of 12 herbaceous species, taxonomically similar to those eaten by
bonobos, year-round [Sugiyama & Koman, 19871. Thus, at least one population of
chimpanzees in moist lowland forest may be as dependent on THV as are bonobos,
although comparative data on resource distribution and consumption at this site
are not available.
Finally, the quality of available protein must also be considered. Like other
non-ruminant vertebrates, bonobos probably cannot synthesize essential amino
acids often missing in plant material [Hegsted, 19641. While bonobos do capture
and eat other vertebrates [Badrian & Malenky, 19841,they may not do so with the
same regularity as reported for some chimpanzee sites. For example, in the Tai
Forest of Ivory Coast, chimpanzees engaged in 135 hunts in 7 years (Boesch &
Boesch, 19891. In contrast, from 1983 to 1986, no instances of carnivory were
recorded in the Lomako Forest [F. White, personal communication; R.K.M., personal observation]. Circumstantial evidence suggests that bonobos in the Lomako
Forest may be able to supplement the amino acids of H . liebrechtsiana with the
leaves of Scorodophleus zenkeri. This leguminous tree is the most common tree
species in the upland forest (47.7 treesthectare of upland forest [Malenky, 19901).
Its leaf phenology is asynchronous; young leaves are available throughout the year
and are regularly consumed by bonobos [personal observation]. The possibility,
therefore, exists that bonobos are able to procure a greater proportion of their
protein requirement from plants available throughout the year and to reduce
their dependence on animal resources, whose availability may be less predictable
and whose exploitation may require greater energy expenditure. More quantitative data are needed on resource distribution, quality, and food choice in freeranging populations of both species of Pan, if the dietary role of THV and its
influence on party size is to be understood.
CONCLUSIONS
1. Terrestrial herbaceous vegetation (THV), and especially one species, Haumania liebrechtsiana, is ubiquitously distributed in the Lomako Forest.
2. H . liebrechtsiana feeding sites are not ubiquitously distributed.
3. Bonobos select patches of H . liebrechtsiana which
Bonobo Feeding Ecology: Patch and Party Size / 167
(a) have a higher density and are found primarily in clearings created by
tree falls; and
(b) have stems with a larger basal diameter.
4. Within patches, the bonobos select
(a) H . Ziebrechtsiana over other plant species of THV;
(b) plants with larger basal diameters; and
(c) young plant parts high in proteins and relatively low in carbohydrates.
5. The patchy, discontinuous distribution of preferred THV sites is not likely
to be responsible for the evolution of larger party size in Pan paniscus compared to
Pan troglodytes.
ACKNOWLEDGMENTS
We thank the government of the Republic of Zaire, the Institute for Scientific
Research, and Dr. Nkanza Dolomingu for their facilitation of research efforts in
Zaire. Dr. Randall L. Susman provided generous support during all phases of this
project. We are also grateful to my colleagues Noel Badrian, Allison Badrian,
Annette Lanjouw, Diane Doran, Nancy Thompson-Handler, and Frances White for
their collaboration in the field. Ikwa Nyamaolo, Bofaso Bozenza, Lofinda Bongenge, and Lokuli Isekofaso gave generously of their enviable expertise and knowledge of the Lomako Forest ecosystem. We also thank John Fleagle, Charles Janson, Lawrence Slobodkin, Sue Boinski, Randall L. Susman, Warren Kinzey, Alison
Richard, Barbara Ruth, and Nancy Thompson-Handler and four reviewers for
their helpful criticism during the preparation of this manuscript. Finally, we
thank Steven Nash and Luci Betti for the time they gave and materials they
provided for the preparation of the illustrations. Funding for this work was furnished by NSF grant BNS 831120601 and Wildlife Conservation International.
REFERENCES
Allen, S.E. CHEMICAL ANALYSIS OF
ECOLOGICAL MATERIALS. New York,
Wiley, 1974.
Altmann, S.A.; Wagner, S.S. A general
model of optimal diet. RECENT ADVANCES IN PRIMATOLOGY 4:407-414,
1978.
Association of Agricultural Chemists. OFFICIAL METHODS OF ANALYSIS, 10th ed.
Washington, DC, Association of Agricultural Chemists, 1969.
Augspurger, C.K. A cue for synchronous
flowering. Pp. 133-150 in THE ECOLOGY OF A TROPICAL FOREST: SEASONAL RHYTHMS AND LONG-TERM
CHANGES. E.G. Leigh, Jr.; A S . Rand;
D.M. Windsor, eds. Washington, DC,
Smithsonian Institution Press, 1982.
Badrian, A.; Badrian, N. Social organization
of Pan paniscus in the Lomako Forest,
Zaire. Pp. 325-346 in THE PYGMY
CHIMPANZEE: EVOLUTIONARY BIOLOGY AND BEHAVIOR. R.L. Susman, ed.
New York, Plenum Press, 1984.
Badrian, N.I.; Malenky, R.K. Feeding ecology of Pan paniscus in the Lomako Forest,
Zaire. Pp. 275-299 in THE PYGMY
CHIMPANZEE: EVOLUTIONARY BIOL-
OGY AND BEHAVIOR. R.L. Susman, ed.
New York, Plenum Press, 1984.
Badrian, N.; Badrian, A,; Susman, R.W.
Preliminary observations on the feeding
behavior of Pan paniscus in the Lomako
forest of central Ziare. PRIMATES 22(2):
173-181, 1981.
Boesch, C.; Boesch, H. Hunting behavior of
wild chimpanzees in the Tai National
Park. AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 78547-573,
1989.
Calvert, J.J. Food selection by western gorillas (G. g. gorilla) in relation to food
chemistry. OECOLOGIA 65236-246,
1985.
Casimir, M.J. Feeding ecology and nutrition
of a n eastern gorilla group in the Mt.
Kahuzi Region (Republ. du Zaire). FOLIA
PRIMATOLOGICA 24%-136,1975.
Chesson, J. The estimation and analysis of
preference and its relationship to foraging
models. ECOLOGY 641297-1304, 1983.
Foster, R.B. Famine on Barro Colorado
Island. Pp. 201-212 in THE ECOLOGY
OF A TROPICAL FOREST: SEASONAL RHYTHMS AND LONG-TERM
CHANGES. E.G. Leigh, Jr.; A.S. Rand;
168 / Malenky and Stiles
D.M. Windsor, eds. Washington, DC,
Smithsonian Institution Press, 1982.
Ganzhorn, J.U. Food partitioning among
Malagasy primates. OECOLOGIA 75436450, 1988.
Garwood, N.C. Seed germination in a seasonal tropical forest in Panama: A community study. ECOLOGICAL MONOGRAPHS 53(2):159-181, 1983.
Gautier-Hion, A. Seasonal variations of diet
related to species and sex in a community
of Cercopithecus monkeys. JOURNAL OF
ANIMAL ECOLOGY 49:237-269,1980.
Ghialiere, M.P. THE CHIMPANZEES OF
KfBALE FOREST: A FIELD STUDY OF
ECOLOGY AND SOCIAL STRUCTURE.
New York, Columbia University Press,
1984.
Glander, K. Howling monkey feeding behavior and plant secondary compounds: A
study of strategies. Pp. 561-573 in THE
ECOLOGY OF ARBORIAL FOLIVORES.
G.G. Montgomery, ed. New York, Garland
STPM Press, 1978.
Glander, K. Feeding patterns in mantled
howling monkeys. Pp. 231-259 in FORAGING BEHAVIOR ECOLOGICAL, ETHOLOGICAL AND PSYCHOLOGICAL APPROACHES. A Kamil; T.D. Sargent, eds.
Washington, D.C., Smithsonian Institution
Press, 1981.
Glander, K. The impact of plant secondary
compounds on primate feeding behavior.
YEARBOOK OF PHYSICAL ANTHROPOLOGY 25:l-18,1982.
Goodall, J . THE CHIMPANZEES OF
GOMBE: PATTERNS OF BEHAVIOR.
Cambridge, MA, The Belknap Press of
Harvard University, 1986.
Hegsted, D.M. Proteins. Pp. 115-179 in
NUTRITION: A COMPREHENSIVE
TREATISE. VOLUME I, MACRONUTRIENTS AND NUTRIENT ELEMENTS.
G.H. Beaton; E.W. McHenry, eds. New
York, Academic Press, 1964.
Hladik, C.M. Chimpanzees of Gabon and
chimpanzees of Gombe: Some comparative
data on the diet. F’D. 481-501 in PRIMATE
ECOLOGY: STUDIES OF FEEDING AND
RANGING BEHAVIOR IN LEMURS.
MONKEYS, AND APES. T.H. Glutton:
Brock, ed. New York, Academic Press,
1977a.
Hladik, C.M. Field methods for processing
food samples. Pp. 595-601 in PRIMATE
ECOLOGY: STUDIES OF FEEDING AND
RANGING BEHAVIOR IN LEMURS,
MONKEYS, AND APES. T.H. CluttonBrock, ed. New York, Academic Press,
1977b.
Hodson, H.H., Jr.; Mesa, V.L., Van Riper,
D.C. Protein requirement of the young,
growing chimpanzee. LABORATORY ANIMAL CARE 17:551-562, 1967.
Horn, A.D. A preliminary report on the ecology of the bonobo chimpanzee (Panpaniscus, Schwartz, 1929). AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY
51:273-281, 1979.
Isabirye-Basuta, G. Food competition among
individuals in a free-ranging chimpanzee
community in Kibale forest, Uganda. BEHAVIOUR 105135-147,1988.
Johnson, D.H. The comparison of usage and
availability measurements for evaluating
resource preference. ECOLOGY 61(1):6571, 1980.
Jungers, W.L.; Susman, R.L. Body size and
skeletal allometrv in African apes. Pp.
131-177 in THE PYGMY CHIMPANZEE:
EVOLUTIONARY BIOLOGY AND BEHAVIOR. R.L. Susman, ed. New York,
Plenum Press, 1984.
Kano, T. Social behavior of wild pygmy
chimpanzees, Pan paniscus of Wamba: A
preliminary report. JOURNAL OF HUMAN EVOLUTION 9:243-260,1980,
Kano, T. The social group of pygmy chimpanzees (Pan paniscus) of Wamba. PRIMATES 23(2):171-188, 1982.
Kano, T. An ecological study of the pygmy
chimpanzees (Pan paniscus) of Yalosidi,
Republic of Zaire. INTERNATIONAL
JOURNAL OF PRIMATOLOGY 4(1):
1-31,1983.
Kano, T. Social organization of pygmy chimpanzees and the common chimpanzee: Similarities and differences. Pp. 53-64 in EVOLUTION AND COADAPTATION IN
BIOTIC COMMUNITIES. S. Kawano; J.H.
Connell; T. Hidaka, eds. University of Tokyo Press, 1987.
Kano, T.; Mulavwa, M. Feeding ecology of
the pygmy chimpanzees (Pan paniscus) of
Wamba. Pp. 233-274 in THE PYGMY
CHIMPANZEE: EVOLUTIONARY BIOLOGY AND BEHAVIOR. R.L. Susman, ed.
New York, Plenum Press, 1984.
Kay, R.F. On the use of anatomical features
to infer foraging behavior in extinct primates. Pp. -21153 in ADAPTATIONS
FOR FORAGING IN NONHUMAN PRIMATES: CONTRIBUTIONS TO AN
ORGANISMAL BIOLOGY OF PROSIMIANS, MONKEYS, AND APES. P.S. Rodman; J.H.G. Cant, eds. New York, Columbia University Press, 1984.
Kerr, G.R. Nutritional requirements of subhuman primates. PHYSIOLOGICAL REVIEWS 52(2):415-467, 1972.
Kinzen, W.G. The dentition of the pygmy
chimpanzee, Pan paniscus. Pp. 65-88 in
THE PYGMY CHIMPANZEE: EVOLUTIONARY BIOLOGY AND BEHAVIOR.
Bonobo Feeding Ecology: Patch and Party Size / 169
MATES: A STUDY IN COMPARATIVE
R.L. Susman ed. New York, Plenum Press,
ECOLOGY. Princeton, NJ, Princeton Uni1984.
versity Press, 1983.
Kleiber, M. THE FIRE OF LIFE. New York,
Terborah J. Keystone plant resources in the
Wiley, 1961.
tropical forest. Pp. 330-344 in CONSERKuroda, S. Grouping of the pygmy chimpanzees. PRIMATES 20(2):161-183, 1979.
VATION BIOLOGY: THE SCIENCE OF
Malenky, R.K. Ecological Factors Affecting
SCARCITY AND DIVERSITY. E.S. Soule,
ed. Sunderland, MA, Sinauer Associates,
Food Choice and Social Organization in
1986.
Pan paniscus. Ph.D. Thesis, SUNY a t
Thompson-Handler, N.; Malenky, R.K.,
Stony Brook, Stony Brook, NY, 1990.
Badrian, N. Sexual behavior of Pan panisMarks, D.L.; Swain, T.; Goldstein, S.; Richard, A,; Leighton, M. Chemical correlates
cus under natural conditions in the Loof rhesus monkey food choice: The influmako Forest, Equateur, Zaire. Pp. 347-368
in THE PYGMY CHIMPANZEE: EVOLUence of hydrolyzable tannins. JOURNAL
TIONARY BIOLOGY AND BEHAVIOR.
OF CHEMICAL ECOLOGY 14:213-235,
R.L. Susman, ed. New York, Plenum Press,
1987.
1984.
Milton, K. Factors influencing leaf choice by
howler monkeys: A test of some hypotheses Vedder, A.L. Movement patterns of freeof food selection by generalist herbivores.
ranging mountain gorillas (Gorilla gorilla
beringei) and their relation to food availAMERICAN NATURALIST 114(3):362ability. AMERICAN JOURNAL OF PRI378, 1979.
MATOLOGY. 7:73-88,1984.
Nishida. T. The social structure of chimDanzees ofthe Mahale Mountains. Pp. 73-122
Watts, D.P. Composition and variability of
in THE GREAT APES. D.A. Hamburg;
mountain gorilla diets in the central VirE.R. McCown, eds. Menlo Park, CA, Benungas. AMERICAN JOURNAL OF PRIjaminicummings, 1979.
MATOLOGY 7:323-356, 1984.
Oates, J.F. The guereza and its food. Pp. White, F. Party composition and dynamics
276-321 in PRIMATE ECOLOGY: STUDin Pan paniscus. INTERNATIONAL
IES OF FEEDING AND RANGING BEJOURNAL OF PRIMATOLOGY 9:179HAVIOR IN LEMURS, MONKEYS, AND
193, 1988.
APES. T.H. Clutton-Brock, ed. New York, White, F.; Wrangham, R.W. Feeding compeAcademic Press, 1977.
tition and patch size in the chimpanzee
Rogers, M.E.; Williamson, E.A. Density of
species Pan paniscus and Pan troglodytes.
herbaceous plants eaten by gorillas in GaBEHAVIOUR 105(1/2):148-163, 1988.
bon: Some preliminary data. BIOTRO- Wrangham, R.W. Feeding behaviour of
PICA 19(3):278-281, 1987.
chimpanzees in Gombe National Park,
Rubenstein, D.I. Ecology and sociality in
Tanzania. Pp. 504-538 in PRIMATE
horses and zebras. Pp. 282-302 in ECOECOLOGY: STUDIES OF FEEDING AND
LOGICAL ASPECTS OF SOCIAL EVORANGING BEHAVIOR IN LEMURS,
LUTION. D.I. Rubenstein; R.W. WrangMONKEYS, AND APES. T.H. Cluttonham, eds. Princeton, NJ, Princeton
Brock, ed. New York, Academic Press,
University Press, 1986.
1977.
SAS Institute. SAS USERS GUIDE: STA- Wrangham, R.W. Sex differences in chimTISTICS, Version 5 Edition. Cary, NC,
panzee dispersion. Pp. 481-489 in THE
SAS Institute, Inc., 1985.
GREAT APES. D.A. Hamburg; E.R. McSourd, C.; Gautier-Hion, A. Fruit selection
Cown, eds. Menlo Park, CA, Benjamin/
by a forest guenon. JOURNAL OF ANICummings, 1979.
MAL ECOLOGY 55:235-244,1986.
Wrangham, R.W. Ecology and social relaStephens, D.W.; Krebs, J.R. FORAGING
tionships in two species of chimpanzee. Pp.
THEORY. Princeton, NJ, Princeton Uni352-378 in ECOLOGICAL ASPECTS OF
versity Press, 1986.
SOCIAL EVOLUTION. D.L. Rubenstein;
R.W. Wrangham, eds. Princeton, NJ,
Sugiyama, Y.; Koman, J . A preliminary list
Princeton University Press, 1986.
of chimpanzees’ alimentation at Bossou,
Guinea. PRIMATES 28(1):133-147, 1987. Wrangham, R.W.; Smuts, B.B. Sex differences in the behavioural ecology of chimSussman, R.W. Feeding behaviour of Lemur
panzees in the Gombe Stream National
catta and Lemur fuluus. Pp. 1-36 in PRIMATE ECOLOGY: STUDIES OF FEEDPark, Tanzania. JOURNAL OF REPRODUCTION AND FERTILITY [Suppl] 28:
ING AND RANGING BEHAVIOR IN LE13-31, 1980.
MURS, MONKEYS, AND APES. T.H.
Clutton-Brock, ed. New York, Academic Wrangham, R.W.; Waterman, P.G. ConPress, 1977.
densed tannins in fruits eaten by chimpanzees. BIOTROPICA 15(3):217-222, 1983.
Terborgh, J . FIVE NEW WORLD PRI-
Документ
Категория
Без категории
Просмотров
1
Размер файла
1 256 Кб
Теги
distributions, pan, zaire, herbaceous, consumption, lomako, vegetation, paniscus, terrestrial, forest
1/--страниц
Пожаловаться на содержимое документа