Nutritional composition of the diet of the gorilla (Gorilla beringei ): a comparison between two montane habitats
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Journal of Tropical Ecology (2007) 23:673–682. Copyright © 2007 Cambridge University Press
doi:10.1017/S0266467407004555 Printed in the United Kingdom
Nutritional composition of the diet of the gorilla (Gorilla beringei ):
a comparison between two montane habitats
Jessica M. Rothman∗,1 , Andrew J. Plumptre†, Ellen S. Dierenfeld∗, ‡, § and Alice N. Pell∗
∗ Department of Animal Science, Cornell University, Ithaca, New York, 14853, USA
† Albertine Rift Programme, Wildlife Conservation Society, PO Box 7487, Kampala, Uganda
‡ Nutrition Department, Wildlife Conservation Society, Bronx, New York, 10460, USA
§ Department of Animal Health and Nutrition, Saint Louis Zoo, St. Louis, Missouri, 63110, USA
(Accepted 6 September 2007)
Abstract: The mountain gorilla (Gorilla beringei beringei) lives in two geographically separated populations, Bwindi
Impenetrable National Park, Uganda and in three national parks spanning the Virunga mountain region in Rwanda,
Democratic Republic of Congo, and Uganda. The altitude, climate and plant composition of these habitats differ. Our
goal was to compare the diets of gorillas living in each of these habitats. The nutrients in staple foods and in the diets
of individuals in a group of gorillas in Bwindi (N = 12 individuals) and a group in the Virungas (N = 7 individuals)
were compared to determine if differences in dietary composition affected concentrations of nutrients in their diets.
At both sites gorilla diets consisted primarily of herbaceous leaves, but the diet of Bwindi gorillas contained more tree
leaves, fruit, pith and dry wood, and fewer stems. Despite differences in habitat and dietary composition, the nutrient
concentrations in both gorilla diets were remarkably similar. On a dry matter basis, the diets and staple foods of
Bwindi and Virunga gorillas contained similar concentrations of crude protein (CP), fibre (NDF) and non-structural
carbohydrates (TNC). Bwindi gorillas ate diets containing 18% CP, 43% NDF and 19% TNC on a dry-matter basis,
while the diets of the Virunga gorillas contained 17% CP, 41% NDF and 18% TNC. Our results demonstrate that gorillas
consume diets that differ by plant species and part, but contain similar concentrations of nutrients. This suggests that
classifying animals by broad dietary strategy (e.g. frugivory and folivory) does not provide a reliable indicator of the
nutritional quality of their diet, and that our previous assumptions about these categories should be re-evaluated.
Key Words: apes, dietary variability, food chemistry, nutritional ecology, primates, tropical forests
INTRODUCTION Congo and Uganda. The altitude of this 440-km2 area
varies from 2000 to 4507 m, and much of the vegetation
Although the remaining two populations of mountain occurs above 2500 m. As a result, a wide range of high-
gorilla (Gorilla beringei beringei) are geographically altitude vegetation zones occur, including Afroalpine
separated by just 30 km, their habitats differ markedly. vegetation, Hagenia–Hypericum forest and bamboo
At an elevation of 1160–2607 m, the 331-km2 Bwindi dominating the vegetation types (Fossey & Harcourt
Impenetrable National Park (BINP) in Uganda contains a 1977, Watts 1984). This difference in the altitude ranges
continuum of lowland and montane forest with fruiting of BINP and PNV means that the vegetation types found
trees (Butynski & Kalina 1993, Howard 1991). The Parc within each site differ greatly. Mountain gorillas therefore
National des Volcans (PNV) in Rwanda is within the subsist on different plants in the two forests.
Virunga mountain region, a chain of volcanoes which The variability in diet items chosen by Gorilla spp. in dif-
spans three countries, Rwanda, Democratic Republic of ferent habitats has been documented through a number
of studies (Doran & McNeilage 1998, Rogers et al. 2004,
Stanford & Nkurunungi 2003, Watts 1984, Yamagiwa
1Corresponding author, at McGill School of Environment, 3534
et al. 2003). Mountain gorillas in both PNV and BINP
University Avenue Room 20, McGill University, Montreal, Quebec, H3A consume parts of many different plant species, but concen-
2T7, Canada. Email: jessica.rothman@mcgill.ca trate on a few foods that are generally abundant in their674 JESSICA M. ROTHMAN ET AL.
habitat (Goldsmith 2003, Plumptre 1995, Stanford & Volcanoes (Figure 1). The plant material collected from
Nkurunungi 2003, Vedder 1984, Watts 1984). Gorillas the PNV for chemical analysis was obtained in the study
in PNV eat leaves, stems, pith and shoots of terrestrial area around the Karisoke Research Station, and details
herbaceous vegetation (THV), and some groups season- of the study site were outlined in other reports (Plumptre
ally consume bamboo (McNeilage 2001, Plumptre 1995, 1991, 1995). The Karisoke study area was south of the
Watts 1984). The Bwindi gorillas eat a more varied diet Volcano Visoke, but included its summit and southern
of THV, tree leaves, fruit, bark, peel and decaying wood, flanks, south to the flanks of the volcano Karisimbi to an
and consume a greater number of plant species than do altitude of 3500 m (Plumptre 1991, 1996). This region
the Virunga gorillas (Stanford & Nkurunungi 2003). ranges from 2900–3700 m and included habitat from
Although the variability of plant species and parts bamboo at the lowest altitude to afroalpine vegetation
consumed by gorillas across sites is well documented, at the highest altitude. Observational data on gorilla
to better understand their feeding ecology, it is not only food plant intake were collected by David Watts on
important to consider the types of dietary items consumed one habituated gorilla group, Group 4 (Watts 1984),
but also to evaluate the types and amounts of nutrients which ranged in part of the Karisoke study area and
these items provide. Using data on food intake (wet weight up to 2 km further west into the Democratic Republic of
basis) of the Virunga (Watts 1984) and Bwindi gorillas Congo. Another gorilla group (Group 5) used the eastern
(determined during this study), and a nutritional analysis portion of the Karisoke study area but had a similar plant
of the diet items of gorillas in PNV and BINP, the objective species intake in their diet compared with Group 4 (Watts
of our study was to determine whether dietary variability 1984).
affected the nutrient concentrations in gorilla diets.
Study animals and field methods
METHODS
The Kyagurilo research group of Bwindi gorillas has
Study sites been habituated to humans for research by the Uganda
Wildlife Authority and the Institute of Tropical Forest
Bwindi Impenetrable National Park, Uganda. Bwindi Impene- Conservation. At the beginning of the study, there were
trable National Park is a rugged, mountainous rain forest, 14 group members: two silverbacks (mature males), six
that was initially designated as a Forest Reserve in 1932 females, four juveniles and two infants. During the study,
but was upgraded to a national park in 1991 (Butynski & an infant was born, bringing group membership to 15.
Kalina 1993). It is located in the south-western Kigezi The Bwindi gorillas were observed for at least 4 h daily
region of Uganda, 0◦ 53 –1◦ 08 S, 29◦ 35 –29◦ 50 E, and by JMR and field assistants for 319 d. These 4-h periods
contains both medium-altitude and montane forest ranged from 8h00 to 18h00, but on most days, the
(Figure 1). As there is micro-scale variation in the animals were observed between 09h00 and 14h00 due
composition and density of the vegetation within the to the logistics of travelling in the field. We could not
forest at different elevations (Nkurunungi et al. 2004), follow the gorillas for longer time periods due to regula-
the food available to and chosen by the gorillas differ tions of the Uganda Wildlife Authority.
in different locations within BINP (Ganas et al. 2004, We used a similar method to that of Watts (1984)
Nkurunungi et al. 2004). to calculate food intake on a wet weight basis for each
The Bwindi study was conducted during August individual. Using focal animal sampling, the proportional
2002–July 2003 in Ruhija which is in a high-altitude wet-weight intake of each diet item was calculated
region of the park, between 2100–2500 m. Annually, for each independent individual animal (N = 12). Each
there are bimodal rains in Uganda; the dry months are individual was observed for as long as possible while
December to February and June to August, while the wet feeding until it was out of view. Similar to Watts (1984)
months are September to November and March to May. the time when the animal started and ended feeding
Annual rainfall at Bwindi typically ranges from 1130– represented a timed feeding bout; however, instead of
2390 mm (Howard 1991). The annual rainfall for the using feeding rates and times, we counted the actual
study period was 1436 mm. The daily mean minimum number of diet items and the amounts eaten during these
temperature at Ruhija was 13.6 ◦ C ± 0.41 ◦ C SD (range: bouts. Each animal was observed at least 6 days per month
12.8–14.1 ◦ C), and the mean maximum temperature was and observer biases were minimized by having JMR and
16.7 ◦ C ± 0.65 ◦ C (range: 15.5–17.7 ◦ C). field assistants observe the same animal on 3 days per
month. These focal observations were collected on 319
days by JMR and/or field assistants and totalled 1318 h
Parc National des Volcans, Rwanda. Located at 1◦ 50 S, (Rothman 2006). The gorillas spent approximately 55%
29◦ 30 E, PNV lies in the Rwandan portion of the Virunga of their time feeding. On a monthly basis, plant collectionsA comparison of mountain gorilla diets 675
Figure 1. Map of the study areas.
of each individual diet item (i.e. a single leaf) in the gorilla Plant collections
feeding area were weighed (N = 50) and an average was
calculated for each month (Watts 1984). To obtain an Approximately 0.5–1 kg of each plant part consumed
estimate of diet quality over the year, these monthly unit was collected over different seasons and from different
weights were averaged for the year. We used the unit environments in areas where the gorillas fed in both
weight to estimate the wet weight contribution of each BINP (by JMR and field assistants) and PNV (by AJP
ingredient to the total daily diet. For some food items, and Aimable Nsanzurwimo, Karisoke Research Center).
e.g. Momordica spp., it was impossible to tell which of the The samples were collected to ensure that they were
Momordica species was being eaten during observations. similar to what was consumed by the gorillas. For
However, the gorillas were either eating one of two most foods, we collected between 4 and 12 samples in
species, Momordica foetida or M. pterocarpa during the different seasons and environments at each study site.
study. Similarly, it was impossible to identify the species After collection, food items were dried in a cool, dark area
or genus of the pieces of wood eaten, so we grouped all (≤ 22 ◦ C), and were ground in a Wiley Mill R
through a
dry wood eaten into one category to estimate wet-weight 1-mm screen. Dry matter was calculated by a two-step
intake. process involving both field and oven-drying. In the field,
We used published estimates of food intake from samples were weighed shortly after collection and then
Group 4 for estimating the diets of gorillas in PNV (Watts were dried at ambient temperature in the dark. Initial
1984). moisture was calculated by subtracting the constant dry676 JESSICA M. ROTHMAN ET AL.
weight of the plant part from the weight obtained shortly 1998). Crude protein was estimated by multiplying N by
after collection. Immediately before chemical analysis, 6.25.
an accurately weighed small portion of the previously To calculate the DM contribution of each nutrient to
dried samples were dried again at 105 ◦ C to remove any each individual’s diet, we used a process that included
adsorbed atmospheric water to calculate the true dry three calculations:
matter of each sample.
First, we estimated the total dry matter content of the diet
using the following formula:
Nutritional and statistical analyses DMdiet = [(DMi )(Pi )]
where: i = the i th food item in the diet, P = proportion
Food samples were analysed either in the Animal
of wet weight intake, DM = dry matter.
Nutrition laboratory at Cornell University, New York,
Second, we estimated the weighted (w) dry matter
USA (BINP samples), or at the Wildlife Health Center
contribution of each food item to the diet:
at the Wildlife Conservation Society, New York, USA
(PNV samples). A subset of Bwindi plants from an earlier wDMi = Pi /DMdiet
study (Rothman et al. 2006a) was analysed in both
Lastly, we estimated the DM contribution of CP and ADF
laboratories to check the accuracy of chemical protocols
to each individual’s diet:
and all samples were found to be within 2% error. The
samples were first analysed for neutral detergent fibre Ndiet = (Ni × wDMi )
with residual ash (NDF), and then for acid detergent
where N = nutrient on a DM basis.
fibre with residual ash (ADF) (Van Soest et al. 1991)
using filter bags in an A200 fibre analyser (ANKOM, This process was used to calculate the nutritional
Macedon, NY, USA). Sodium sulphite was added to contributions of each diet item for each individual. Then
the neutral detergent solution of the Bwindi, but not the diets of individuals were pooled to provide ranked
the Virunga samples. Most of the staple Bwindi foods proportional intake values of each food item for the group
contain condensed tannins (Rothman et al. 2006a), (Watts 1984). Only foods that formed > 1% of the total
while Virunga foods do not (Waterman et al. 1983). diet were included in the pooled data set for nutritional
The addition of sodium sulphite reduces the amount analysis; these were considered ‘staple’ foods. There are
of insoluble proanthocyanidin complexes bound to fibre seasonal differences in dietary composition and nutrient
(Krueger et al. 1999). Analysis of the foods that do not intake of the Kyagurilo group (Rothman 2006), but we
contain condensed tannins (n = 5) with and without pooled the data on wet-weight proportional intake over
sodium sulphite added to the neutral detergent solution the year to permit uniform comparisons to the Virunga
did not result in a significant difference in fibre fractions data set (Watts 1984). Dr Peter Waterman and colleagues
(paired t-test, t = 1.59, P = 0.19). Since the Bwindi foods analysed plant species from the Virunga region in earlier
have tannins, we quantified them (%DM) by using the years but the analytical methods used were different
acid butanol assay (Porter et al. 1986) and internal from those used for the Bwindi sample set and were
standards were generated for each plant species. We not comparable. For example, Waterman et al. (1983)
determined the ether extract of the Bwindi foods by did not collect multiple samples from different seasons
standard methods. We did not determine ether extract and environments, plants were sun-dried and the fibre
on the Virunga food samples but since the ether extract analyses were not sequential.
of leaf and stems was low for the Bwindi samples (mean: While it would have been preferable to sample more
1.8 ± 0.55 %DM), and is generally low in tropical leaves than one group in each habitat, mountain gorillas are
and stems (Conklin-Brittain et al. 1998), we used this critically endangered and research access to study groups
Bwindi average to estimate the ether extract in leaves is limited. Because there is only one group of habituated
and stems of the Virunga samples. The amount of mountain gorillas where observations are permitted by
hemicellulose (HC) in the diet was assessed by subtracting the Uganda Wildlife Authority, our data collection was
ADF from NDF, and the amount of cellulose (CS) limited to one group of gorillas in Bwindi. Groups within
in the diet was estimated by subtracting lignin from Bwindi may have different diets (Ganas et al. 2004), and
ADF. For the Virunga samples, total nitrogen (N) was it is not yet known whether their diets are nutritionally
determined using the macro-Kjeldahl method with a comparable. Detailed information on food intake of the
copper catalyst (AOAC 1990). For the Bwindi samples, N Virunga population was limited to a single group (Watts
was determined by a Leco FP-528 Combustion analyser 1984). Individuals within each gorilla group cannot be
(AOAC 1990), which is faster and uses less-hazardous considered independent samples (i.e. a group member is
materials. The combustion procedure gives N values that influenced in what they eat by the rest of the group)
are comparable to the Kjeldahl procedure (Etheridge et al. therefore we provide descriptive statistics of the meanA comparison of mountain gorilla diets 677
( ± SD) intake of individuals in each of the groups for each Similarly, when we considered the weighted nutritional
nutrient. To statistically compare the differences between contribution of each food to the diet, the Bwindi and
the staple foods of the two gorilla groups, we used t-tests Virunga gorillas ate diets that were nearly identical
(all the assumptions of normality and variance were met). nutritionally (Table 3). The mean (± SD) individual
diets within each group for protein: Bwindi 18.2 ± 2.4;
Virunga 17.2 ± 0.5, NDF: Bwindi 42.9 ± 3.7; Virunga
41.1 ± 1.6, HC: Bwindi 10.8 ± 0.35; Virunga 12.5 ± 0.3,
RESULTS
CS: Bwindi 17.5 ± 1.9; Virunga 19.8 ± 1.2, TNC: Bwindi
18.8 ± 1.7; 18.2 ± 0.64 (Table 3).
On a wet-weight intake basis, the diet composition of
the Bwindi and Virunga gorillas varied with respect to
plant part (Table 1). Although both groups of gorillas ate
DISCUSSION
diets composed primarily of leaves from THV, the Bwindi
gorillas ate more fruit, tree leaves, pith and peel than
We found that mountain gorillas living in two
the Virunga gorillas, while the Virunga gorillas ate more
geographically separated habitats consumed different
herbaceous stems. The staple diet of the Bwindi gorillas
plant species and plant parts, yet their diets and staple
was more diverse than the diet of the Virunga gorillas
foods contained similar concentrations of nutrients.
and they ate different plant species and parts. The Bwindi
Virunga gorillas in PNV consumed fewer staple foods
gorillas ate 15 foods that each comprised > 1% of their
from different plant species than did gorillas in BINP.
diet, while the Virunga gorillas ate nine staple foods. In
Similarly, fewer foods and less fruit formed the staple diet of
both cases over 90% of the diet was comprised of these
cercopithicine monkeys (Cercopithicus mitis kandti) living
staple foods.
in the Virunga Region compared with those in Kibale
Despite differences in their habitats and availability
National Park, Uganda (Cercopithicus mitis stuhlmanni)
of diet items, the nutrients in both gorilla diets were
(a middle-elevation forest with a diverse community of
remarkably similar. The mean percentage of CP in the
fruiting trees), yet their diets were nutritionally similar
staple foods eaten by the Virunga gorillas (15.3 ± 9.0%
(Twinomugisha et al. 2006). That the diet of a single
DM) was not significantly different from the mean
species can vary between geographically separated areas,
amount of CP in the Bwindi staple foods (17.0 ± 9.2%
and on spatial and temporal scales within the same area
DM) (t = −0.43, df = 17, P = 0.67). The NDF in the
has been documented for many taxa, including primates
staple foods eaten by the Virunga gorillas (51.3 ± 12.3%
(Chapman et al. 2002a, b; Hill & Dunbar 2002, Russo et al.
DM) was similar to the NDF content of the Bwindi
2005), and gorillas specifically (Doran & McNeilage 1998,
staple foods (41.3 ± 14.3% DM) (t = 1.81, df = 19,
Ganas et al. 2004, McNeilage 2001, Rogers et al. 2004).
P = 0.11). Similarly, the HC contents of the gorilla
However, it is possible that groups or populations of the
staple foods were similar (Bwindi: 13.3 ± 3.8% DM;
same species living in different habitats that eat different
Virunga: 10.6 ± 2.8, t = 1.88, df = 12, P = 0.10), as
foods consume diets containing similar proportions of
were the CS contents (Bwindi: 25.8 ± 11.7; Virunga
nutrients. Therefore, while gorillas may consume diets
25.8 ± 10.4, t = 1.53, df = 15, P = 0.15) and the TNC
that differ by plant species and part, the nutritional
contents (Bwindi: 20.5 ± 9.2 %DM; Virunga: 20.7 ± 8.8,
quality of their diets may be quite similar (Conklin-Brittain
t = −0.06. P = 0.95) (Table 2).
et al. 1998, Dierenfeld & McCann 1999). Our study
provides further evidence that broad food classes and
dietary categories such as frugivory and folivory are not
Table 1. Proportion of different gorilla foods (wet-weight basis) eaten by
necessarily useful in predicting diet nutritional quality
Bwindi and Virunga gorillas.
(Barton et al. 1993, Oftedal 1991).
Category % Bwindi intake % Virunga intakea
Like many other primates, both of these gorilla groups
Herb/shrub leaves 61.1 67.7
ate a diverse diet. The Virunga gorilla group ate 75 foods
Fruit 15.3 0.2
Tree leaves 7.3 < 0.1 from 38 plant species (Watts 1984) and the Bwindi group
Inner stem cortex/pith 6.4 2.4 ate 158 parts from 107 plant species (Rothman 2006).
Peel 5.5 < 0.1 However, we found that in both groups the bulk of gorilla
Decaying wood 3.9 0.3 diets were comprised of only a few species, suggesting
Tree bark/twigs 0.5 0.9
that dietary diversity and composition tells us little about
Herbaceous stems 0.1 25.0
Root/ root epidermis < 0.1 1.7 nutritional quality. Bwindi gorillas are more frugivorous
Flowers < 0.1 1.1 than Virunga gorillas (Stanford & Nkurunungi 2003).
Fungus < 0.1 0.2 Our wet-weight estimates suggest that the annual diet
Dead leaves < 0.1 0.2 of the Bwindi gorillas contains 15.3% fruit. Myrianthus
a Data adapted from Group 4 in the Virungas (Watts 1984). holstii contains more sugar than other fruits in the Bwindi678 JESSICA M. ROTHMAN ET AL.
Table 2. Mean concentrations of nutrients (percentage of dry matter) in the staple foods eaten by Virunga and Bwindi mountain gorillas. Key:
CP = crude protein; NDF = neutral detergent fibre; HC = hemicellulose; CS = cellulose; TNC = total non-structural carbohydrates; HL = herbaceous
leaves; HS = herbaceous stems; F = fruit; TL = tree leaves; PL = peel; DW = decaying wood; P = pith.
Part % Intakea CP NDF HC CS TNC
Virunga gorillas
Galium ruwenzoriense (Cortesi) Chiov. HL 35.7 19.5 36.7 13.5 19.4 29.6
Carduus nyassanus (S.Moore) R.E.Fr. HL 22.1 30.0 49.1 18.8 15.4 6.4
Carduus nyassanus HS 9.4 6.6 62.6 13.5 38.5 15.5
Peucedanum linderi C.Norman HS 9.0 4.9 65.3 14.5 42.4 15.6
Laportea alatipes Hook.f. HL 4.2 27.9 38.2 14.1 10.3 17.6
Rubus kirungensis Engl. HL 3.4 8.6 62.4 5.8 35.5 21.2
Laportea alatipes Hook.f. HS 3.0 15.2 41.3 14.6 18.5 34.3
Urtica massaica Mildbr. HS 2.4 9.9 64.6 16.2 33.9 13.8
Helichrysum formosissimum Sch.Bip. HL 1.3 15.2 41.3 8.9 18.5 30.5
Total 90.5
Bwindi Gorillas
Urera hypselodendron (Hochst. ex A.Rich.) Wedd. HL 19.2 24.4 31.9 10.4 9.5 20.3
Ipomoea involucrata Beauv. HL 8.8 24.6 33.7 10.5 12.5 29.6
Myrianthus holstii Engl. F 8.6 8.9 55.8 12.3 25.3 10.7
Momordica foetida Schumach./Momordica pterocarpa A.Rich. HL 8.0 30.2 20.4 7.6 8.7 35.6
Basella alba L. HL 7.8 28.4 25.5 10.8 9.5 23.2
Mimulopsis solmsii Schweinf. HL 7.1 28.2 33.9 15.2 11.1 22.7
Myrianthus holstii Engl. TL 6.6 16.1 50.7 13.7 22.3 6.3
Urera hypselodendron PL 5.4 11.4 64.8 7.4 43.3 5.4
Triumfetta tomentosa Bojer HL 5.4 24.7 36.8 16.0 11.8 20.4
Carduus sp. HL 4.2 18.9 33.0 9.2 16.1 28.0
Mimulopsis arborescens C.B. Clarke P 4.1 8.4 43.6 10.0 28.1 23.9
Decaying wood pieces DW 3.9 4.7 69.4 10.4 30.0 23.5
Chrysophyllum albidum G.Don F 3.0 10.0 40.2 10.4 11.2 24.9
Cyathea manniana Hook. P 2.2 4.1 50.5 7.6 29.0 26.1
Maesa lanceolata Forssk. F 1.8 11.3 29.3 7.1 10.4 10.5
Total 96.1
a Intake data for the Virunga gorillas adapted from Group 4 in the Virungas (Watts 1984).
gorilla diet (Rothman et al. 2006a), and comprises over red colobus and red-tailed monkey consumed leaves that
half of wet-weight fruit intake. In an earlier study, M. had similar sugar contents to fruit (Danish et al. 2006).
holstii seeds were found in 13.9% of faecal samples These results suggest that categorizing gorilla non-fruit
(Nkurunungi 2005). Although fruits are usually less food items as ‘fibrous’ (Doran et al. 2002, Ganas et al.
fibrous than leaves, the three fruits included in the 2004, Remis 1997, Robbins et al. 2006) makes an implicit
staple diet of the gorillas were similar in fibre to staple assumption that non-fruit foods have more fibre than
herbaceous leaves. In the Bwindi gorilla diet, fruits also fruit, and that fruit-dominated diets vary nutritionally
contained the same amounts of protein as tree leaves from leaf-dominated diets, which was not the case here.
(Rothman et al. 2006a) and in a neighbouring forest Additionally, the considerable inter- and intraspecific
Table 3. Nutrient concentrations (percentage of dry matter intake) in the diets of mountain gorillas and other hindgut-fermenting primates. Key:
CP = crude protein; NDF = neutral detergent fibre; HC = hemicellulose; CS = cellulose; TNC = total non-structural carbohydrates.
CP NDF HC CS TNC
Bwindi gorilla (Gorilla beringei Matschie 1903)a 18.2 42.9 10.8 17.5 18.8
Virunga gorilla (Gorilla beringei Matschie 1903)a 17.2 41.2 12.5 19.8 18.2
Howler monkey (Alouatta palliata Gray 1849)b,c 12.4 27.5 – – –
Blue monkey (Cercopithecus mitis stuhlmanni Matschie 1893)d 17.6 32.3 11.8 12.3 35.3
Mangabey (Lophocebus albigena johnstoni Gray 1850)d 16.3 32.0 12.0 11.9 34.0
Bonobo (Pan paniscus Schwarz 1934)e,c 8.3 26.8 10.1 11.5 –
Red-tailed monkey (Cercopithecus ascanius schmidti Matschie 1892)d 17.6 31.3 11.4 11.6 36.5
Chimpanzee (Pan troglodytes schweinfurthii Giglioli 1872)d 9.5 33.6 13.7 11.8 38.8
a From this study.
b Milton (1979) (mean value of commonly eaten leaves that comprise 48% of the diet).
c Mean value of commonly eaten foods.
d Conklin-Brittain et al. (1998), values are room temperature DM (20 ◦ C).
e Hohmann et al. (2006).A comparison of mountain gorilla diets 679 variability in the nutritional content of primate foods that sodium (Rode et al. 2003). The Bwindi gorilla group we has been demonstrated at different spatial and temporal studied ate decaying wood, which provided 95% of their scales (Chapman et al. 2003, Worman & Chapman 2005) sodium intake, a micronutrient that was limited in their needs to be considered. Despite the fact that gorillas in diet (Rothman et al. 2006c). PNV are more folivorous than those in BINP, they did not The nutrient concentrations in the diets of other consume more fibre. hindgut-fermenting primates were compared with those Of the staple foods eaten by gorillas in both habitats, of gorillas (Table 3). Due to its high concentration of herbaceous leaves contributed the most wet weight mass hemicellulose (18.7% DM) and cellulose (28.1% DM), and CP to the diet. Milton (1979) proposed that the the consumption of pith probably provides energy to protein:fibre ratio was the single most important factor chimpanzees when fruits are not available (Wrangham for food selection of primates and building on this work, et al. 1991). Piths eaten by the Virunga gorillas were also several studies have emphasized the importance of protein high in hemicellulose and cellulose and may be a valuable and fibre in the diets and habitats of primates (Chapman energy source for this group of mountain gorillas. Pith, et al. 2004, Davies et al. 1988, Ganzhorn 1992, Oates et al. decaying wood and the frequently eaten outer peel of 1990). Across study sites there is evidence that gorillas eat the herb Urera had high concentrations of hemicellulose foods higher in CP than non-food plants, suggesting that (Table 3), similar to the piths in the Virunga gorilla diet high-protein foods, and herbs in particular, are important and chimpanzee diet (Wrangham et al. 1991). Our study for gorillas and other apes (Calvert 1985, Malenky & suggests that hemicellulose concentrations in the diets Stiles 1991, Rogers et al. 1990, Wrangham et al. 1991). of mountain gorillas are similar to that of chimpanzees In Cameroon, lowland gorillas selected foods that had and cercopithecines, but that cellulose concentrations in the most CP, were most digestible (determined from in the diets of gorillas are higher and TNC concentrations vitro digestibility analysis) and had less lignin than foods are lower than other primates. Based on captive studies, avoided (Calvert 1985). Similarly, gorilla foods in Lopé, chimpanzees can digest about 60% of the hemicellulose Gabon, contained more CP and less fibre than non-foods and 38% of the cellulose in their diets on a high-fibre diet (Rogers et al. 1990). (34% NDF) (Milton & Demment 1988), indicating that Foods frequently eaten by Bwindi gorillas have more hemicellulose and cellulose are important energy sources CP than other diet items (Rothman et al. 2006b) but in for chimpanzees. Like chimpanzees, gorillas have a large PNV, availability and digestibility (determined from in colon relative to other segments of their gastrointestinal vitro digestibility analysis of gorilla foods) are important tract (Milton 1985), harbour fibre-digesting bacteria selection criteria for gorillas (Plumptre 1995), and CP is (Frey et al. 2006) and have a relatively slow passage rate not as important when non-foods and foods are compared, (∼ 50 h) to facilitate fibre digestion (Remis 2000, Remis & likely because most of the available plants in PNV are also Dierenfeld 2004). In general, the fibre concentrations high in CP. It may be that the high protein concentrations of wild chimpanzee diets were lower than gorilla diets in ape diets is simply a consequence of the availability of (Table 3), and the diets of gorillas were lower in TNC high-protein foods in their habitats, while other nutrients than those of chimpanzees and other more frugivorous might be limiting and apes are eating high-protein foods to primates. Although the large body size of gorillas is likely meet other nutritional needs. Just because a high-protein important for fibre digestion, small-sized cercopithicines, diet is consumed does not necessarily mean that it is such as red-tailed and blue monkeys may also have an required; animals such as gorillas that have a long life span increased capacity for digesting fibrous foods based on and slow growth require a relatively low CP diet (Oftedal their long retention times (Lambert 2002), and howler 1991). Wild chimpanzees consumed diets containing monkeys have considerable fermentation returns (Milton 9.5% CP and the average leaf consumed by orang-utans 1983, Milton & McBee 1983, Milton et al. 1980). No is 11.9% CP. Further studies are needed to investigate generalizations can be made regarding digestive strategies protein quality and amino acid composition (Milton & and body size without more data on fibre digestibility Dintzis 1981). For example, in Kibale National Park forest across the Primate Order (Lambert 1998, Milton 1981, elephants ate a diet of 22% CP (Rode et al. 2006), which 1998). is quite high compared to their estimated requirements, Our study provides further evidence that understand- while another nearby population of elephants ate a diet ing the dietary diversity alone is insufficient to assess the of 13% CP (Jachmann 1989). It is likely that elephants in quality of food species and evaluate habitat suitability Kibale were ingesting high-protein foods because these (Twinomugisha et al. 2006). In both BINP and PNV, foods met other nutritional requirements, particularly gorilla diets contained similar concentrations of protein, minerals (Rode et al. 2006). Several other nutritional fibre and non-structural carbohydrates. While the diets factors need to be considered in assessing what might of gorillas and nutrients in dietary items differ across be limiting in gorilla diets, such as energy, as seen with study sites (Rothman et al. 2006b), we do not know if orang-utans (Knott 1998) and micronutrients such as the nutritional proportions of their diets vary as well, and
680 JESSICA M. ROTHMAN ET AL.
whether a variation might change seasonally or spatially CHAPMAN, C. A., CHAPMAN, L. J., CORDS, M., GAUTHUA, A.,
within habitats. Unfortunately, it will be increasingly GAUTIER-HION, A., LAMBERT, J. E., RODE, K. D., TUTIN, C. E. G. &
important to understand the adaptability of gorillas in WHITE, L. J. T. 2002a. Variation in the diets of Cercopithecus
a range of habitats, as tropical forests are progressively species: differences within forests, among forests, and across species.
being anthropogenically modified. Presently both the Pp. 325–350 in Glenn, M. & Cords, M. (eds.). The guenons: diversity
BINP and PNV are well protected, but the same cannot and adaptation in African monkeys. Academic/Plenum Publishers,
be said for other gorilla habitats; habitat loss, civil New York.
unrest, encroachment and disease have seriously affected CHAPMAN, C. A., CHAPMAN, L. J. & GILLESPIE, T. R. 2002b. Scale
mountain gorilla populations in the past (Plumptre & issues in the study of primate foraging: red colobus of Kibale National
Williamson 2001). The capacity for gorillas and other Park. American Journal of Physical Anthropology 117:349–363.
primates to survive in marginal habitats is likely CHAPMAN, C. A., CHAPMAN, L. J., RODE, K. D., HAUCK, E. M. &
dependent on their ability to avoid nutritional stress. MCDOWELL, L. R. 2003. Variation in the nutritional value of primate
foods: among trees, time periods, and areas. International Journal of
Primatology 24:317–333.
ACKNOWLEDGEMENTS CHAPMAN, C. A., CHAPMAN, L. J., NAUGHTON-TREVES, L., LAWES,
M. J. & MCDOWELL, L. R. 2004. Predicting folivorous primate
We appreciate the long term commitment of the abundance: validation of a nutrition model. American Journal of
Office Rwandais pour la Tourisme et Parcs Nationaux Primatology 62:55–69.
(ORTPN) for supporting the research activities at the CONKLIN-BRITTAIN, N. L., WRANGHAM, R. W. & HUNT, K. D. 1998.
Karisoke Research Center. We are especially grateful Dietary response of chimpanzees and cercopithecines to seasonal
to Dr Katie Fawcett and Aimable Nsanzurwimo of the variation in fruit abundance. II. Macronutrients. International Journal
Karisoke Research Center and Dian Fossey Gorilla Fund of Primatology 19:971–998.
International for organizing, collecting and storing the DANISH, L., CHAPMAN, C. A., HALL, M. B. & WORMAN, C. O. 2006.
plant samples and material transfer agreements and The role of sugar in diet selection in redtail and red colobus monkeys.
shipments. We thank the Uganda Wildlife Authority Pp. 473–488 in Hohmann, G., Robbins, M. M. & Boesch, C. (eds.).
and the Uganda Council of Science and Technology Feeding ecology in apes and other primates: ecological, physiological and
for permission to conduct research in BINP and the behavioural aspects. Academic/Plenum Publishers, New York.
Institute for Tropical Forest Conservation for logistical DAVIES, A. G., BENNETT, E. L. & WATERMAN, P. G. 1988. Food
support. Bristol University, Wildlife Conservation Society selection by two South-East Asian colobine monkeys (Presbytis
and the Dian Fossey Gorilla Fund provided funding for rubicunda and Presbytis melalophos) in relation to plant chemistry.
data collection, plant collection and nutritional analyses Biological Journal of the Linnean Society 34:33–56.
in PNV. In Bwindi Impenetrable National Park we thank DIERENFELD, E. S. & MCCANN, C. M. 1999. Nutrient composition
the field assistants of the Institute of Tropical Forest of selected plant species consumed by semi free-ranging lion-tailed
Conservation for their hard work in the field. Funding for macaques (Macaca silenus) and ring-tailed lemurs (Lemur catta) on St.
fieldwork and nutritional analyses of the samples in BINP Catherines Island, Georgia, USA. Zoo Biology 18:481–494.
was provided by a graduate assistantship to JMR through DORAN, D. M. & MCNEILAGE, A. 1998. Gorilla ecology and behavior.
the Animal Science Department at Cornell University, the Evolutionary Anthropology 6:120–131.
Robert G. Engel Family Foundation, the Mario Einaudi DORAN, D. M., MCNEILAGE, A., GREER, D., BOCIAN, C., MELHMAN,
Foundation, the Institute of African Development and P. & SHAH, N. 2002. Western lowland gorilla diet and resource
the Graduate School at Cornell University. Dr Katie availability: new evidence, cross-site comparisons, and reflections
Milton and two anonymous reviewers provided helpful on indirect sampling methods. American Journal of Primatology
comments that improved the quality of this manuscript. 58:91–116.
ETHERIDGE, R. D., PESTI, G. M. & FOSTER, E. H. 1998. A comparison of
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