In Vitro Fermentation of Dietary Carbohydrates Consumed by African Apes and Monkeys: Preliminary Results for Interpreting Microbial and Digestive Strategy

Primates derive significant nutritional benefits from hosting symbiotic, fermenting microbes in their gut, including the provision of energy from short-chain fatty acids (SCFAs). We measured fermentation parameters in fecal samples of 4 hindgut fermenting species (Gorilla gorilla, Pan troglodytes, Papio hamadryas, Cercopithecus neglectus) and 1 foregut fermenting species (Colobus guereza) to determine whether differences in SCFA profiles exist between the 2 digestive systems. We analyzed SCFA profiles, culture pH, and methane from fecal samples collected at the North Carolina Zoological Park. Results indicate that the captive individuals exhibit high total SCFA concentrations, with a particularly high acetate-to-propionate ratio. Methane levels were highest in the 2 ape species, and lowest in Colobus guereza and Cercopithecus neglectus. Total SCFA concentrations were similar between wild and captive-born Gorilla gorilla, although concentrations of acetate were significantly greater —and butyrate concentration and methane production significantly lower— in wild-caught gorillas relative to captive-born. These results are consistent with data on diet and digestive retention times among Catarrhini and have implications for our understanding of the interactions among diet, body mass, digestion, and how monogastric cercopithecines can consume either similar or greater levels of fiber than larger-bodied apes.     

Influence of Chimpanzee Predation on Associations Between Red Colobus and Red-tailed Monkeys at Ngogo,Kibale National Park,Uganda

Colobines often associate with cercopithecines at various African sites. Such polyspecific associations presumably have an antipredation function. At Ngogo, Kibale National Park, Uganda, red colobus (Procolobus rufomitratus) spend considerable time in association with red-tailed monkeys (Cercopithecus ascanius), and they are also heavily hunted by chimpanzees (Pan troglodytes). I conducted behavioral observations and playback experiments to test the hypothesis that red colobus and red-tailed monkeys obtain mutual protection and predator-related benefits by associating. Despite high chimpanzee hunting pressure on red colobus and much lower hunting pressure on red-tailed monkeys, red-tailed monkeys initiate, maintain, and terminate the associations. The results suggest that rather than providing red colobus with protection against chimpanzees, the associations occur mostly because they protect red-tailed monkeys against predation by eagles.     

Blue monkey (Cercopithecus mitis stuhlmanni) predation on galagos

Two cases of predation on galagos by free-ranging blue monkeys (Cercopithecus mitis stuhlmanni) are described.C. mitis is only the second species of the genusCercopithecus known to prey on mammals. “Wadging,” the intermixing and chewing of leaves with meat, is reported for the first time in a primate other than the chimpanzee (Pan troglodytes). Meat-sharing was not observed inC. mitis.     

Digesta Passage Time,Digestibility, and Total Gut Fill in Captive Japanese Macaques (<Emphasis Type="BoldItalic">Macaca fuscata</Emphasis>): Effects Food Type and Food Intake Level

Digestion is an important process in understanding the feeding ecology of animals. We examined digesta passage time, digestibility, and total gut fill in Japanese macaques (Macaca fuscata; n = 4) under 4 dietary conditions representing the seasonal and regional variations in the diets of wild populations to determine the effects of food type and food intake on these digestive features. Food type is associated with mean retention time (MRT), digestibility, and total gut fill. Dry matter intake (DMI) of food correlates positively with total gut fill but not with MRT or digestibility. Conversely, indigestible DMI affected MRT negatively. Thus, when Japanese macaques consume high-fiber foods, MRT becomes shorter and digestibility is lower than when eating low-fiber foods. Moreover, macaques experience increases in total gut fill when they consume high-fiber diets or a large amount of food. Japanese macaques may excrete difficult-to-digest food components quickly; they nevertheless buffer an increase in food intake by an increase in gut fill. Our study offers new insights into the relationship between feeding ecology and nutritional physiology in primates by simultaneously examining the effects of food type and intake level on MRT and digestibility.     

Effect of different primate species on germination of Ficus (Urostigma) seeds

We examined the germination of Ficus seeds (subgenus Urostigma) after defecation by six primate species (New World monkeys, Old World monkeys, and apes). Seeds from figs (control) and primate feces were placed in a thermostatically controlled chamber for 30 days. Seeds defecated by Alouatta palliata, A. pigra, and Cercopithecus aethiops showed significantly higher germination rates than control seeds. In addition, seeds from A. palliata feces germinated significantly faster than control seeds and seeds from C. aethiops and Pan troglodytes. These differences may be due to the different digestive characteristics of the six primate species. Zoo Biol 23:273–278, 2004. © 2004 Wiley‐Liss, Inc.     

Feed intake,digestion and passage of the proboscis monkey (Nasalis larvatus) in captivity

Feeding trials were conducted with a troop of six proboscis monkeys (Nasalis larvatus) at the New York Zoological Park to quantify aspects of digestive physiology. Diets consumed comprised, on an as-fed basis, 55% browse and green produce, 11% fruit, 9% commercial primate diets, 9% root vegetables, and 16% miscellaneous items. Total feed intake averaged 12% of body mass; dry matter intake was 3%. Dry matter and plant cell wall disappearance exceeded 80%. Passage marker studies (three 6-day trials) revealed: transit time=14 hr; mean passage time=49 hr; and 5–80% retention time=52 hr. Digestion coefficients and retention times were greater than expected based on body size. These results might reflect the low fiber content of the diets fed, or alternatively, provide evidence that proboscis monkeys are efficient digesters of cell wall constituents.     

A note on the present situation of the primate fauna found from south-eastern Cameroon to northern Congo

Brief results of a survey are reported for the primate fauna in south-eastern Cameroon and northern Congo. The survey was carried over the period from October 1988 to January 1989. I confirmed the occurrence ofMandrillus sphinx in the south-eastern part of Cameroon, viz. the south bank of the Dja river, the occurrence ofCercocebus albigena in almost all the survey areas, the occurrence ofCercopithecus cephus, C. nictitans, C. pogonias, andGorilla g. gorilla throughout the areas, and the occurrence ofCercopithecus neglectus andColobus badius near Bomassa, 70 km north of Ouesso, in Congo. I also confirmedColobus polykomos satanas in some parts of Cameroon, but this species is declining. Local people provided information onCercocebus galeritus agilis, Colobus guereza, andPan troglodytes in almost all the areas, in some of which I confirmed the animals directly. They also provided information aboutCercocebus torquatus on the north bank of the Dja river in Cameroon andMiopithecus talapoin in Sembe in Congo, although I could not confirm these species myself. Human activities had begun reducing the populations of the above primates, particularly those ofMandrillus sphinx, Colobus polykomos satanas, andGorilla g. gorilla, in south-eastern Cameroon and in northern Congo despite the low density of the human populations.     

Modelling the nutritional ecology of ungulate herbivores: evolution of body size and competitive interactions

Summary A simulation model is used to quantify relationships between diet quality, digestive processes and body weight in ungulate herbivores. Retention time of food in the digestive tract is shown by regression to scale with W^0.27, and to be longer in ruminants than in hindgut fermenters. Allometric relationships between whole gut mean retention time (MRT, h) and weight (W) were: MRT=9.4 W^0.255 (r ²=0.80) for hindgut fermenters and MRT=15.3 W^0.251 (r ²=0.76) in ruminants. Longer retention of ingesta by large-bodied ruminants and hindgut fermenters increases digestive efficiency relative to small animals and permits them to survive on lower-quality foods. Compared with ruminants, hindgut fermenters' faster throughput is an advantage which outweighs their lower digestive efficiency, particularly on poor quality foods, provided that food resources are not limiting. This suggests that the predominance of ruminants in the middle range of body weights results from their more efficient use of scarce resources under conditions of resource depletion. Considering only physical limitations on intake, the model shows that the allometric coefficient which scales energy intake to body mass is 0.88 in ruminants and 0.82 in hindgut fermenters. The advantages of large body size are countered by disadvantages where food quantity is limited, and we suggest that the upper limit to ungulate body size is determined by the ability to extract nutrients from feeding niches during the nadir of the seasonal cycle of resource quality and abundance.     

Body size and proportions in chimpanzees,with special reference toPan troglodytes schweinfurthii from Gombe National Park,Tanzania

Body weight, cranial capacity, linear and joint area data from ten free-ranging adult chimpanzees from Gombe National Park, Tanzania with known life histories allow study of variation in a local population and comparison to other populations ofPan troglodytes and toPan paniscus. Because individuals in the Gombe population are small compared to other common chimpanzees, they provide a useful comparison toPan paniscus. Body weight and some linear dimensions overlap withPan paniscus. However, cranial capacity, tooth size, and body proportions of Gombe individuals lie within the range of otherPan troglodytes and are distinct fromPan paniscus.     

Digesta retention in the gastro-intestinal tract of the orang utan (Pongo pygmaeus)

The diet of the orang utanPongo pygmaeus consists of fruit, leaves, communal insects, and bark, and contains appreciable amounts of non-starch polysaccharides. These complex carbohydrates require microbial fermentation before they can be used as an energy source by the orang utans. The gastrointestinal tract ofP. pygmaeus consists of a simple or unipartite stomach, a relatively long small intestine, and a complex haustrated caecum and colon. This morphology suggests that the capacious proximal colon is the principal site of digesta retention and fermentation of non-starch polysaccharides. We measured several parameters of digesta retention by giving three captive adultP. pygmaeus a pulse dose of inert markers specific for the solute and particulate phases of the digesta and collected their faeces at regular intervals over 192–338 hours. Transit times (times of first appearance of the markers in the faeces) and mean retention times (MRT) were long, consistent with a large complex gastro-intestinal tract. MRTs for the particulate marker were longer (p=0.032) than for the solute marker, indicative of selective retention of large particulate digesta. These results are consistent with the patterns of marker excretion in other mammals that use the digestive strategy of colon fermentation.     

A quantitative comparison of terrestrial herbaceous food consumption by Pan paniscus in the Lomako Forest,Zaire, and Pan troglodytes in the Kibale Forest,Uganda

Differences in the social organization and dental morphology of Pan paniscus (bonobos) and Pan troglodytes (chimpanzees) have been related to differences in the spatiotemporal availability of food and its exploitation. The presence of abundant terrestrial herbaceous vegetation (THV) in the bonobo's habitat and the apparent greater reliance on herbs for food has been used to explain differences in party size and, by extension, social organization. Using fecal analysis, we assess quantitatively the amount of herbaceous foods consumed by Pan paniscus in the Lomako Forest, Zaire, compared to similar data for Pan troglodytes in the Kibale Forest, Uganda. We examine this data in the context of spatiotemporal patterns of availability of herbaceous foods and fruit, as well as their nutritional content. The results support the suggestion that bonobos consume more herbaceous food than do the Kibale chimpanzees and that these foods are more prevalent in the bonobo's habitat than in the Kibale Forest. However, temporal changes in fruit availability and herb consumption, along with nutritional analyses, suggest that chimpanzees consume herbs as a fallback source of carbohydrates, whereas bonobos consume herbs as a source of protein regardless of season or fruit abundance. Available data suggest that party size while feeding on terrestrial herbs is restricted at both sites, but a determination of the relative strength of this constraint is not possible at this time. Difficulties in methods used for data collection are discussed and areas where more information is needed are highlighted. © 1994 Wiley-Liss, Inc.     

Binturong (Arctictis binturong) and Kinkajou (Potos flavus) Digestive Strategy: Implications for Interpreting Frugivory in Carnivora and Primates

Exclusive frugivory is rare. As a food resource, fruit is temporally and spatially patchy, low in protein, and variable in terms of energy yield from different carbohydrate types. Here, we evaluate the digestive physiology of two frugivorous Carnivora species (Potos flavus, Arctictis binturong) that converge with primates in a diversity of ecological and anatomical traits related to fruit consumption. We conducted feeding trials to determine mean digestive retention times (MRT) on captive animals at the Carnivore Preservation Trust (now Carolina Tiger Rescue), Pittsboro, NC. Fecal samples were collected on study subjects for in vitro analysis to determine methane, pH, and short chain fatty acid profiles; fiber was assayed using standard neutral detergent (NDF) and acid detergent (ADF) fiber methods. Results indicate that both carnivoran species have rapid digestive passage for mammals that consume a predominantly plant-based diet: A. binturong MRT = 6.5 hrs (0.3); P. flavus MRT = 2.5 hrs (1.6). In vitro experiments revealed no fermentation of structural polysaccharides – methane levels did not shift from 0 h to either 24 or 48 hours and no short chain fatty acids were detected. In both species, however, pH declined from one incubation period to another suggesting acidification and bacterial activity of microbes using soluble carbohydrates. A comparison with primates indicates that the study species are most similar in digestive retention times to Ateles – the most frugivorous anthropoid primate taxon.     

Behavior of bonobos (Pan paniscus) following their capture of monkeys in Zaire

For the first time, three cases of capture and forced interaction were observed between bonobos (Pan paniscus)and two other species of primates (Colobus angolensisand Cercopithecus ascanius)in the Lilungu (Ikela) region, Republic of Zaire. The bonobos interacted with the captured primates as if they were dealing with individuals of their own species. They sought cooperation in their interactions with the captured young primates without scccess. There is no evidence that they ate the captives.     

External body dimensions ofPan paniscus andPan troglodytes chimpanzees

Postcranial skeletal studies have demonstrated thatPan paniscus is a more gracile animal thanPan troglodytes, with different arm to leg proportions. Published data on external body dimensions are extremely rare forPan paniscus, however. We present here a series of such measures for a sample ofpaniscus, and we compare these to similar measures forPan troglodytes. This comparison further clarifies the morphological distinctions between the two chimpanzee species, and indicates that bonobos have longer legs and smaller chest girths relative to overall body height than doPan troglodytes chimpanzees.     

Fluid and particle retention in the digestive tract of the addax antelope (Addax nasomaculatus)--adaptations of a grazing desert ruminant

Retention time of food in the digestive tract is a major aspect describing the digestive physiology of herbivores. Differences in feed retention times have been described for different ruminant feeding types. In this study, a dominantly grazing desert ruminant, the addax (Addax nasomaculatus), was investigated in this respect. Eight animals with a body weight (BW) of 87+/-5.3 kg on an ad libitum grass hay (Chloris gayana) diet were available. Co-EDTA and Cr-mordanted fibers (<2 mm) were used as pulse-dose markers. Mean retention time (MRT) in the digestive tract was calculated from faecal marker excretion. Average daily intake of the addax was found to be 1.7 kg dry matter (DM) or 60+/-8.3 g DM/kg BW(0.75). The MRT of fluid and particles in the reticulo-rumen (MRT(fluid)RR and MRT(particle)RR) were quantified to be 20+/-5.8 and 42+/-7.0 h respectively. When compared to literature data, MRT(fluid)RR was significantly longer than in cattle species, and MRT(particle)RR was significantly longer than in 11 taxa of all feeding types. The ratio of MRT(particle)RR/MRT(fluid)RR (2.3+/-0.5) was found to be within the range described for grazing ruminants. The long retention times found in the addax can be interpreted as an adaptation to a diet including a high proportion of slow fermenting grasses, while the long retention time of the fluid phase can be interpreted as a consequence of water saving mechanisms of the desert-adapted addax with a potentially low water turnover and capacious water storing rumen.     

Fluid and particle retention in the digestive tract of the addax antelope (Addax nasomaculatus)--adaptations of a grazing desert ruminant.

Retention time of food in the digestive tract is a major aspect describing the digestive physiology of herbivores. Differences in feed retention times have been described for different ruminant feeding types. In this study, a dominantly grazing desert ruminant, the addax (Addax nasomaculatus), was investigated in this respect. Eight animals with a body weight (BW) of 87+/-5.3 kg on an ad libitum grass hay (Chloris gayana) diet were available. Co-EDTA and Cr-mordanted fibers (<2 mm) were used as pulse-dose markers. Mean retention time (MRT) in the digestive tract was calculated from faecal marker excretion. Average daily intake of the addax was found to be 1.7 kg dry matter (DM) or 60+/-8.3 g DM/kg BW(0.75). The MRT of fluid and particles in the reticulo-rumen (MRT(fluid)RR and MRT(particle)RR) were quantified to be 20+/-5.8 and 42+/-7.0 h respectively. When compared to literature data, MRT(fluid)RR was significantly longer than in cattle species, and MRT(particle)RR was significantly longer than in 11 taxa of all feeding types. The ratio of MRT(particle)RR/MRT(fluid)RR (2.3+/-0.5) was found to be within the range described for grazing ruminants. The long retention times found in the addax can be interpreted as an adaptation to a diet including a high proportion of slow fermenting grasses, while the long retention time of the fluid phase can be interpreted as a consequence of water saving mechanisms of the desert-adapted addax with a potentially low water turnover and capacious water storing rumen.     

Inter-menstrual intervals in captive bonobosPan paniscus

In this study we provide new data on the duration of the inter-menstrual intervals of six captive female bonobos (Pan paniscus). We found that the mean duration of the inter-menstrual interval was about 34 days. This lies close to the average value of 37 days that has been reported for common chimpanzees (Pan troglodytes).     

Coping with Forest Fragmentation: The Primates of Kibale National Park,Uganda

A goal of conservation biology is to determine which types of species are most susceptible to habitat disturbance and which types of disturbed habitats can support particular species. We studied 20 forest fragments outside of Kibale National Park, Uganda, to address this question. At each patch, we determined the presence of primate species, tree species composition, patch size, and distance to nearest patch. We collected demographic, behavioral, and dietary data for Abyssinian black-and-white colobus (Colobus guereza). Black-and-white colobus and red-tailed guenons (Cercopithecus ascanius) were in almost all fragments; Pennant's red colobus (Procolobus pennantii) and chimpanzees (Pan troglodytes) were in some fragments; and blue monkeys (Cercopithecus mitis) and gray-cheeked mangabeys (Lophocebus albigena) were absent from all fragments. No species characteristics—home range, body size, group size, or degree of frugivory—predicted the ability of species to live in patches. No characteristics of patches—area, distance to the nearest patch, distance to Kibale, or number of food trees present—predicted the presence of a particular species in a patch, but distance to Kibale may have influenced presence of red colobus. Black-and-white colobus group size was significantly smaller in the forest patches than in the continuous forest of Kibale. For a group of black-and-white colobus in one patch, food plant species and home range size were very different from those of a group within Kibale. However, their activity budget and plant parts eaten were quite similar to those of the Kibale group. The lack of strong predictive variables as well as differences between other studies of fragmentation and ours caution against making generalizations about primate responses to fragmentation.     

Fluid and particle retention in captive okapi (Okapia johnstoni)

Retention time of food in the digestive tract is among the key variables that describe the digestive strategy of a herbivore. Mean retention time (MRT) was measured on 4 captive specimens of the okapi, a strictly browsing ruminant. Retention time was quantified on different diets, using Co-EDTA (fluid phase) and Cr-mordanted fibres (1–2 mm) (particle phase) as pulse-fed markers. Average food intake was 55–65 g DM/(kg BW^0.75*d). Fecal excretion of the markers was quantified over 10 days. Different models to calculate retention time and passage rate in the gastrointestinal tract (GIT) and the reticulorumen (RR) were applied. Average MRT_particleGIT was quantified to be 47 ± 8 h and MRT_fluidGIT 36 ± 5 h. Concerning estimation of retention times in the reticulorumen, MRT_particleRR was quantified to be 27 ± 7 h, while MRT_fluidRR was 17 ± 4 h. The quotients MRT_particle/MRT_fluid were quantified to be 1.3 ± 0.1 for the GIT and 1.6 ± 0.2 for the RR. Compared to data established with comparable markers, the okapi has low coefficients of MRT_particle/MRT_fluid. A less well developed retention mechanism for fibres compared to species like cattle or sheep can be explained by a comparatively high fermentation rate and low digestibility of the natural food of the okapi—browse—in comparison to grass.     

Is the chimpanzee, Pan troglodytes, an endangered species? It depends on what “endangered” means

I review information on the status in the wild of the robust chimpanzee, Pan troglodytes, and consider whether this evidence is consistent with the designation of P. troglodytes as Endangered in the International Union for the Conservation of Nature and Natural Resources (IUCN) Red List, and with public statements to the effect that great apes as a whole will be extinct within a few decades. Chimpanzees remain widespread in tropical Africa, occurring in a variety of forested habitats. Estimates of total surviving numbers have increased from about 200,000 in the 1980s to a maximum of almost 300,000 in 2003. However, this apparent increase comes about from new survey data, rather than representing a measured increase in actual population numbers. Infectious disease decimated several chimpanzee populations during the 1990s, and data from parts of Gabon, extrapolated to that country as a whole, suggest a major decline in great ape populations caused by disease and hunting. However, accurate data on population numbers are absent for the majority of wild chimpanzee populations. I found reports of the presence of Pan troglodytes in at least 51 national parks in at least 19 countries; some of these parks have been established very recently. Chimpanzees also occur in many non-park conservation areas. A set of large, well-protected parks could safeguard chimpanzees for the foreseeable future. Although many African parks do not function well at present, mechanisms to improve their function are understood and available. By a strict application of IUCN threat criteria, P. troglodytes can be considered Endangered, based on estimated rates of past decline and on the species long generation time. Relatively speaking, however, P. troglodytes is less endangered than are orangutans or gorillas, and the species is unlikely to go extinct by the year 2100, especially if existing conservation measures improve. The IUCN threat-rating system has become overly complex; the system can produce results that do not accord with common sense and these results must therefore be interpreted with care.