The welfare of nonhuman primates in captivity depends heavily on meeting their nutrient needs in a manner that considers normal foraging and feeding behavior, structure and functions of the digestive system, and the options and constraints of captive dietary husbandry.

In developing a system for the nourishment of captive nonhuman primates, it is helpful to examine the literature on the feeding ecology of primates in the wild. Several observational methods have been used to record foraging and feeding behavior in natural ecologic systems (Altmann, 1974; Lehner, 1996), and data derived with these methods are summarized in Tables 1-1 through 1-6. To interpret the findings properly, the reader should have a background in the methods used, and a brief discussion of them follows.

Data collected during visual observations of behavior typically include length of feeding bout, plant species eaten, plant parts eaten (for example, fruit and leaf), percentage of part eaten, feeding rate (for example, number of fruits consumed per minute), diameter and height of food plant, and food-plant location.

Choosing a data-collection method requires, as a first step, selection of one of two animal-observation options.

Focal-Animal Observation One individual is observed during a given session of data collection (it can also be a pair or a small subgroup). Sessions can vary from 5 min to a whole day. This method is used to identify multiple behaviors in selected individuals. When sessions are only 5-10 min long, it is common to switch observations to another animal in the group for the next session.

All-Animal Observation Primates that are naturally grouped are observed simultaneously. This method is feasible only when observing a few easy-to-see behaviors. It is not recommended for detailed feeding behaviors.

After selection of an animal-observation option, the second step is to select a method of sampling foraging and feeding behavior.

Ad Libitum (or Periodic) Sampling This is the classic, pre-1970s field method, used before modern statistical techniques and advanced technologies were commonly applied. Today, it is recommended only for preliminary reconnaissance or the study of rare behaviors. This method is biased toward spectacular behaviors, like hunting, thus overestimating faunivory compared with herbivory.

Continuous-Recording Sampling Method These sampling methods result in the most complete and accurate data. They are recommended for studying feeding ecology but are difficult to use with arboreal animals, such as primates.

• All-Occurrences Sampling. All occurrences of one or a few behaviors are recorded over an extended period,

often 1 day. Usually combined with focal-animal sampling, this is an excellent but difficult method for recording foraging and feeding behavior. Start-and-stop rules, independent of the behavior being studied, are required.

• Sequence Sampling. A sampling period starts with the beginning of a sequence of a chain of behaviors, such as foraging for insects and feeding. The sampling period ends when the observed sequence ends. This method is of lim-

ited use for quantifying a diet, because the time required for food acquisition varies.

Time Sampling Methods Less complete but more manageable methods for recording feeding behavior, these are probably the most commonly used today. These methods also require independent start-and-stop rules, and dawn and dusk are often used.

• One-Zero Sampling. A behavior is scored only once per observation period, regardless of the number of times it occurs. This method is adequate for preliminary reconnaissance. It is not recommended for detailed feeding-ecology studies, because it generally yields poor ‘‘time-spent’’ estimates.

• Instantaneous Sampling. The observer records a focal-animal’s behavior at predetermined times. This method works well with ongoing behavior that can be timed with a stopwatch, such as feeding behavior. For example, during a feeding bout, what the animal is eating every 30 or 60 seconds is recorded. Another approach is to observe the focal animal every 15 min and record all behaviors for 5 min. A limitation of this approach is that rare events often are not recorded. However, when continuous observations prove impossible, this generally is considered the next-best method.

• Scan Sampling. Instantaneous observations are made of several animals simultaneously. This is useful for studying less-detailed behavior.

In some circumstances, particularly if terrestrial primates are being studied in dense rainforest, visual observations of feeding behavior are impractical. It can be impossible to see the animals well enough to determine what they are eating or how much time they spend eating it, and alternative methods might be needed. Some researchers studying nocturnal animals use both visual observations and alternative methods (Nash 1983). Alternative methods for studying feeding ecology are outlined below.

Measurement of stomach contents, now rare, can be used to estimate the mass of different food categories consumed (for example, fruit, leaves, or insects); with care and skill, one can identify the species eaten (Booth, 1956; Fooden, 1964; Charles-Dominique, 1974; Gautier-Hion et al., 1980). However, because the animal must be killed, only a single measure per animal is obtained. An additional

limitation is the bias introduced by persistence of fibrous items compared with more easily digested foods.

Recognizing cell structures of different plants in feces and identifying them, even to the genus level, requires considerable microscope training. Most researchers send fecal samples to specialized laboratories for plant identification (Moreno-Black 1978). Fecal analysis has been used effectively in studying the feeding ecology of the nocturnal galagos (Nash, 1983; Harcourt 1984) and some cercopithecines (Moreno-Black and Maples, 1977). Tutin et al. (1991), and Tutin and Fernandez (1993), studying lowland gorillas, used a macroscopic method to evaluate feces, looking for seeds and fibrous material. However, fecal analysis has the same limitation as does analysis of stomach contents: that is, the items that persist tend to be fibrous, whereas the more easily digested foods leave no trace.

This method often is used in combination with fecal analysis or visual observation. It is useful when the animal

is not directly visible but the researcher is close enough to identify the species on which it is feeding. When the animal has moved on, the feeding location can be investigated and food remnants characterized (Tutin et al., 1991, Tutin and Fernandez, 1993; Rogers et al., 1996).

Once collected, feeding-behavior data may be reported in various ways. The following are some examples.

Feeding time may be reported as a percentage of all daily activities or as a percentage of feeding time. For example, 35% of the day might be spent in foraging for insects, 19% feeding on plants, 25% in traveling, and the remainder in other activities. Within the time spent on plants, 60% of it may have been on fruit, 40% on leaves.

The contribution that each food category makes to the total diet in mass terms may be expressed as a percentage of dry weight or of wet weight. The estimated grams consumed of each type of food may also be reported.

The feeding ecology of all extant primates that have been studied is summarized in Tables 1-1 through 1-6. The data in these tables were derived from studies that used nearly all the above methods. Although the methods varied, grand averages (with ranges in parentheses) were calculated because no correction factors have been developed to make data gathered with different methods comparable. We assumed that the predominant food items (such as fruits, leaves, and insects) would remain predominant regardless of the method used and that the variability in diets due to habitat and seasonal differences would overwhelm most differences due to methods. Studies of some

primate species did not report percentages of different foods in the diet but provided only a food list and general food preferences. A few studies lasted 3-6 months, but most lasted a year or more.

The feeding-ecology data provide only general guidelines for captive-diet formulation, and the proportions of foods in wild diets, as measured, should not be taken literally. Some seasonal extremes in food choices represent selections based on necessity, not on preference. Most primates can survive for a few weeks or months on an extreme diet; otherwise, they could not survive seasonal changes in food supply. However, primates are more likely to flourish on diets that are matched to their gastrointestinal systems and thus are typical for their species.

Classification of primates on the basis of feeding strategies, such as folivory or frugivory, seems straightforward and rational. However, it is clear from the tabular data that young leaves, mature leaves, petioles, shoots, and other plant parts are eaten with various degrees of preference. Fruit-eaters sometimes consume only the pulp and spit out the seed, or they might consume the whole fruit and digest the pulp and seeds or pass the seeds intact in the feces. Some fruit is consumed only for the seeds, and the pulp and pod or husk are discarded. Gummivores (gumeaters and sap-eaters) tend to feed heavily on one or a few species of trees. Reproduction of gummivore diets is facilitated by information on the chemistry of the preferred exudates.

Some primates specialize on immature insect forms (grubs, caterpillars, and larvae) rather than adult insects. Many primates, however, do not specialize. The nutritional value of insects and the issue of foraging time versus capture rate are elements of feeding ecology in need of much more study. There is little information on the chemical composition of insects, although larval forms are commonly assumed to be high in fat and adults high in protein. Many adult insects have a chitinous exoskeleton, and chitin contains nitrogen, but the effect on estimates of concentration of usable protein is often ignored (Oyarzun et al., 1996). In addition, most chemical-composition data have been generated in studies of temperate, rather than tropical, insects (Redford and Dorea, 1984; Studier and Sevick, 1992).

In the contribution of invertebrates to the total diet of a primate, foraging time versus capture rate is critical. Janson and Boinski (1992) reported that insect capture by Saimiri spp. was successful in 61% of total insect-foraging time; Cebus spp. had a capture rate of 38-42% of total insect-foraging time. Wright (1985, 1989) concluded that the insect-capture rate for Callicebus brunneus must be low inasmuch as the animals spent 15% of their foraging time searching for insects, but only 15% of their feces contained insect parts. Indigestible insect parts in the feces tend to overrepresent insects as a dietary item, so it appeared that the proportion of insect foraging time resulting in successful capture was limited.

Egler (1992) found that 59.1% of total food-foraging and feeding time of tamarins (Saguinus bicolor) was spent foraging for insects (14.3% of total daily activities), but only 5.4% of insect-foraging time resulted in successful capture and consumption of prey; thus, the fraction of total food-foraging and feeding time spent in eating insects was 3.2% (5.4% of 59.1%). Foraging for and feeding on plants are basically identical, considering how most plant-foraging and feeding data are collected. Assuming that the time spent in foraging for plants was identical with the time spent in feeding on plants (reported by Egler as 9.9% of total daily activities), then 24.2% (14.3% + 9.9%) would be the fraction of total daily activities devoted to foraging and feeding. However, if only 3.2% of total food-foraging and feeding time was spent in eating insects, then only 0.8% (3.2 % of 24.2%) of the total day was devoted to this activity. Adding the percentages of the day devoted to eating plants (9.9%) and to eating insects (0.8%) and dividing the latter by the total (10.7%) yields a fraction of 7.5% of total feeding time spent in eating insects (instead of 59.1%), leaving 92.5% of feeding time spent in eating plants (instead of 40.9%). However, the insects that the tamarins hunted were very large, perhaps a whole meal by themselves. This situation creates an interesting question: How does the size of the insect meal relate to the mass of plant material consumed? It is clear that the mass of each food item consumed would provide a more accurate measure of the composition of the natural diet than would timed records of foraging and feeding activity. The data in Tables 1-1 through 1-6 have not been adjusted for insect-capture rate, because for the vast majority of primates these rates are not known.

As previously stated, the percentage of time spent in feeding is probably the most common factor used in describing a primate diet, but if foraging time is included as eating time, it can be inflated (Kurland and Gaulin, 1987). In addition, a measure based on grams consumed would be sometimes more accurate than time spent in feeding. To estimate grams consumed, one needs to determine, for example, how many fruits are eaten in an hour (or a feeding bout), what portion of the fruit is consumed, and how much the consumed portion weighs. The weight of seeds may or may not be included, depending on whether they are digested.

Because foods vary greatly in their water content, dry weights are more useful indicators of nutrient intake than wet weights and allow more accurate comparisons among studies. Daily dry-matter intakes can be calculated by multiplying the grams of dry matter consumed per hour or per feeding bout by the hours or feeding bouts per day. That yields a good estimate of total dry matter consumed. If the time spent in eating is clearly separated from foraging time, the total time spent in feeding on a given food and the total dry matter taken in from eating that food tend to lead to the same answer (Knott, 1999).

Total dry matter consumed, however, is still not the best method for evaluating usable energy and nutrient intake, because losses during digestion are not considered. Ideally, the diet should be analyzed for fiber components, partly or mostly indigestible fractions of dry matter, depending on the consuming species (see Chapter 3, “Carbohydrates and Fiber”). If laboratory support is available, data on gross energy and nutrient concentrations in natural foods are additional useful measures. However, gathering such data is extremely time-consuming, expensive, and in some field situations almost impossible. For many small, fast-moving, and unhabituated arboreal primates, it is extremely difficult to collect all the needed bits of information. The percentage of time spent in feeding on particluar items is often as good a measure as is realistically possible to determine.

The designation of the different feeding strategies (folivory, frugivory, insectivory, and gummivory) is based on the food category with the highest percentage of use (Chapman, 1987). Seasonal differences can make a normally frugivorous species appear folivorous and vice versa (Chapman and Chapman, 1990). Many primates exploit a small number of plant species heavily but sample small amounts of many species (Hladik et al., 1971; Glander, 1975; Smith, 1977; Chapman, 1988). Insectivory and gummivory are two feeding strategies predominantly of very small primates. Tarsius are small and can survive by eating only insects. Saimiri (the second commonest experimental primate but not well studied in the wild) is the smallest cebid and the most insectivorous. Some prosimians and most Callithrix, are small and can survive by eating mostly gums. The cercopithecines have been separated into two groups, colobine (Table 1-4) and noncolobine (Table 1-5). All colobines are foregut fermenters and are folivorous or granivorous (seed-eating). The noncolobine cercopithicines are hindgut fermenters and are generally more omnivorous.

Considering the different methods and circumstances under which feeding-ecology data are collected, the information gathered will be variable in quality and subject to potential errors. The various data collection systems are described in this chapter, and the reader is urged to identify the system used in gathering the data of interest and to use personal judgement in interpretation of their applicability. Feeding-ecology data can be used to evaluate the appropriateness of a captive diet but do not provide a basis for setting quantitative nutrient requirements. They are used to classify primate species as primarily granivorous, folivorous, omnivorous, gummivorous, or insectivorous and provide guidance to food preferences and to probable qualitative and roughly quantitative nutrient needs. For example, leaves are generally higher in protein (dry basis) than are fruit, although wild fruits are much higher in protein than are fruits cultivated for human use (Conklin-Brittain et al., 1998, 1999, 2002). Consequently, folivores generally consume a diet higher in protein than do frugivores. An even more important consideration might be the presence of physical factors, such as fiber, in the natural foods of folivores and the effects these factors have on digestive function and health. Thus, evidence from feeding ecology studies and controlled research with captive primates has been used to develop the proposed dietary fiber concentrations shown in Chapter 3.

Many primate species consume diversified, omnivorous diets. Most of the primates that are routinely used in research fall into this category, in part because their diverse and omnivorous diet seems to make them more adaptable, and they are easier to keep in captivity than are more specialized species. For species that are rarely kept successfully in captivity, a close examination of their feeding ecology may be helpful in formulating a diet that is most appropriate for them. The folivorous monkeys pose a particular problem, and only recently have research trials begun to identify those combinations of formulated complete diets and cultivated foods that can substitute for their normal wild diet.

The primary function of the digestive system is to extract energy and essential nutrients from an animal’s environment in support of metabolic processes. Performing that function requires a series of physical and chemical steps that are related to the anatomy of the digestive system. The primary significance of gut structure is related to its effect on food selection and processing (Clemens and Phillips, 1980). Specialized structures are involved in food acquisition, ingestion, maceration, deglutition, and digestion. Secretions from the salivary glands, stomach, pancreas, liver, and intestinal tract provide lubrication and enzymes in a watery medium with a pH that is optimal for digestion. Symbiotic microorganisms in the foregut or hindgut of some animals provide energy and nutrients by degrading structural carbohydrates that are unaffected by endogenous enzymes and by synthesizing amino acids and

vitamins that are essential to their host. It is common for different orders of mammals to have different gastrointestinal tract specializations, but primates are unique among mammals in having diverse digestive tract arrangements within their own order (Chivers and Hladik, 1980).

The digestive systems of primates that consume animal material are typically simpler and shorter than those of plant-eating species. The basic gastrointestinal tract of faunivores includes a simple globular stomach, a tortuous small intestine, a short conical cecum, and a simple smooth-walled colon (Chivers and Hladik, 1980).

Primate faunivores, which tend to be small and nocturnal, feed primarily on invertebrates but can supplement their diet with plant materials. The diet of the angwantibo (Arctocebus calabarenis) consists of animal prey (85%) and fruits (15%). Similarly, Galago senegalensis, Microcebus spp., and Loris tardigradus are highly insectivorous, although Galago and Microcebus supplement their diet with gums and other plant exudates. The tarsiers (Tarsius spp.) are principally insectivorous, but they also eat such small vertebrates as geckos and other lizards (Napier and Napier, 1985).

Galago has a balloon-like stomach, a relatively short small intestine, a moderate-size cecum, and a smooth, non-complex colon (Clemens, 1980). The gastrointestinal tract of Tarsius includes a colon that is about one-fifth as long as the small intestine and a spiral cecum that is half as long as the colon (Figure 1-1).

Most primates are frugivorous, but none consume diets entirely of fruit. Fruit intake is augmented with variable proportions of invertebrates, vertebrates, and other plant parts, including leaves, flowers, and exudates. The gastrointestinal tracts of primates in this broad group exhibit little structural specialization, but variations among species have been described (Chivers and Hladik, 1980).

The basic frugivorous stomach is simple and globular (Hill, 1958). The marmoset stomach has a more elongated fundus than that of cebids, which is more specialized, with a globular fundus, conical body, and cylindrical pylorus (Chivers and Hladik, 1980).

Squirrel monkeys (Saimiri), douroucoulis (Aotus), woolly monkeys (Lagothrix), and spider monkeys (Ateles) have gastrointestinal tracts comparable with those of other frugivores (Figures 1-2 through 1-4), but in most of these species, the proximal portion of the colon is expanded and haustrated along its entire length (Hill, 1960; Hill and Rewell, 1948; Stevens and Hume, 1995). The cecum itself is not haustrated (Stevens and Hume, 1995).

Marmosets (Callithrix spp.) and tamarins (Saguinus spp., Leontopithecus spp.), as well as Saimiri and Aotus, have similar diets in the wild; fruits make up the majority of foods consumed, with invertebrate prey about 20%. The larger-bodied Lagothrix and Ateles consume diets composed mainly of fruit, with various proportions of leaves and seeds. Both Cebuella and Callithrix have a “short-tusked” tooth pattern in which the lower canines are incisiform and barely longer than the adjacent incisors; such dentition enables these species to create holes in bark to extract plant exudates (sap and gums) (Izawa, 1975).

Cercopithecine primates, except colobines, have cheek pouches that permit short-term storage of harvested ingesta. The stomach of these species (Cercopithecus, Macaca, and Papio) is relatively simple and smooth-walled, followed by a short small intestine (Figures 1-5 through 1-7). The cecum is typically haustrated by three taeniae, and can support some microbial breakdown of plant material. The galago (Galago crassicaudatus) (Figure 1-8) and the ruffed lemur (Varecia variegata) are prosimians that have a prominent cecum, but the cecum of the ruffed lemur is longer and more complex than that of the galago. The cecum of the vervet monkey (Cercopithecus pygerythrus) is sacculated (Clemens, 1980).

The enlargement of the colon or cecum in gibbons (Hylobates spp.), rhesus macaques (Macaca mulatta), Syke’s monkeys (Cercopithecus mitis), and vervet monkeys (Cercopithecus aethiops) is consistent with bacterial fermentation of leaf material in the diet (Sakaguchi et al., 1991; Bruorton et al., 1991). When they are fed identical diets, the production of volatile fatty acids (VFAs, end products of microbial fermentation) in the hindgut of the more omnivorous (Morris and Goodall, 1977) baboon (Papio cynocephalus) (Clemens and Phillips, 1980) is similar to that in the hindgut of the largely herbivorous Syke’s monkey (Cercopithecus mitis) (Hill, 1966).

The rates of digesta passage among frugivorous primates depend on proportions of fruit, leaf, and animal prey in the diet. Three groups of frugivorous lemurs—Varecia variegata variegata, Varecia v. rubra, and Lemur catta— fed a similar, mixed-ingredient diet exhibited median gut passage times of 1.71, 1.69, and 4.75 hours, respectively (Cabre-Vent and Feistner, 1995). Slightly longer mean transit times (2.7 hours) were reported for Varecia v. variegata and V. v. rubra fed experimental diets containing 15% and 30% acid detergent fiber (Edwards and Ullrey, 1999a).

Fiber type, not concentration, reduced passage time from 10 to 6 hours in Callithrix jachus and Saguinus fuscicollis (Krombach et al., 1984). Fiber concentration in diets consumed by macaques had no effect on the mean transit time of either particulate or liquid markers (Sakaguchi et al., 1991).

Baboons (Papio cynocephalus) had shorter mean transit times than Syke’s monkeys (Cercopithecus mitis), when

fed the same diet, for both fluid markers (35.0 vs. 39.9 hours) and 10-mm particulate markers (39.6 vs. 48.0 hours) (Clemens and Phillips, 1980). The mean transit times for the same diet fed to vervet monkeys (Cercopithecus aethiops) and the more insectivorous bushbaby (Otolemur crassicaudatus) were about 30 and 12 hours, respectively (Clemens, 1980).

Primate folivores have a variety of physical adaptations that promote, through symbiotic microbial fermentation and mechanical action, the degradation of the structural and chemical defenses of plants. The two principal adaptations involve enlargements of the stomach or the hindgut to accommodate microbial fermentation (Parra, 1978; Langer, 1988). The extent of gastrointestinal tract modification is related to the proportions of plant parts (leaves, seeds, and fruits) consumed.

Members of the subfamily Colobinae have capacious and morphologically complex adaptations of the foregut, providing a primary site of microbial activity (Bauchop and Martucci, 1968; Caton, 1998; Kuhn, 1964). Colobines can be further divided into two large groups on the basis of the presence (quadripartite) or absence (tripartite) of a presaccus that can act as a preliminary storage compartment proximal to the principal region of fermentation (saccus) (Table 1-7). The tubus gastricus and pars pylorica are distal to the saccus. This arrangement allows the separation of ingesta between more neutral or alkaline (proximal) and acidic (distal) environments, supporting microbial fermentation in advance of gastric and enzymatic digestion. Anaerobic cellulolytic bacteria and other microbial symbionts in the saccus produce enzymes that degrade plant cell walls and promote access to the cellular contents. Thus, these

species exhibit evolutionary convergence with ruminants in their adaptations of foregut structure for herbivory (Moir, 1968). As previously noted, in contrast with more-omnivorous cercopithecine primates, the colobines lack cheek pouches (Stevens and Hume, 1995).

The large sacculated forestomach of Asian colobines (such as Trachypithecus, Presbytis, and Pygathrix) includes a gastric canal in the presaccus, which might be analogous to the reticular groove in ruminants that shunts highly digestible milk, consumed during suckling, past the sites of fermentation to the distal portion of the stomach (Figure 1-9).

The small and large intestines of Asian colobines are about eight and two times body length, respectively. The cecum, serving as a secondary site of microbial fermentation, is one-fourth body length (Stevens and Hume, 1995).

Although the gastrointestinal tract of African colobines such as Colobus and Procolobus (Figure 1-10) is generally similar to that of Asian colobines, the small and large intestines are shorter, and the cecum is less well developed (Stevens and Hume, 1995). There is no evidence of rumination (regurgitation and chewing of a food bolus) in any colobine primate (Owen, 1835).

Several primate species exhibit hindgut fermentation, again reflecting the contribution of less-digestible plant materials in the natural diet. In these species, the symbiotic microorganisms occupy enlarged areas distal to the gastric and enzymatic sites of digestion. Quantitative recovery of nutrients produced by fermentation is not as high as in foregut fermenters (Edwards and Ullrey, 1999b).

The large intestine is enlarged in prosimians that feed on leaves or gums, both of which require microbial fermentation for digestion, and the cecum is elongated in Lepilemur, Phaner, Euoticus, and Indri (Chivers and Hladik, 1980).

The diet of the nocturnal sportive lemur (Lepilemur mustelinus) consists of flowers and leaves. This species practices coprophagy (ingestion of fecal material), which increases the recovery of nutrients from the relatively indigestible diet (Napier and Napier, 1985).

All great apes exhibit hindgut modification. The chimpanzee colon is haustrated by three taeniae over its length; the taeniae continue along the cecum and terminate in a vermiform appendix (Figure 1-11) (Stevens and Hume, 1995). The gastrointestinal tract of the gorilla is similar to that of the chimpanzee, although the small intestine is relatively long and the hindgut is more voluminous, indicative of its highly herbivorous diet. The small intestine and colon of the orangutan are longer than those of the chimpanzee, with an expanded proximal segment (Figure 1-12). The gastrointestinal tract of the gibbon is similar to that of other apes, although the colon is shorter. For purposes of comparison, the gastrointestinal tract of the adult human is shown in Figure 1-14.

Primate Gastrointestinal Tracts

FIGURE 1-13 Howler Monkey

Edwards, 1995

FIGURE 1-10 Adult Human

Stevens and Hume, 1995

Reprinted with the permission of Cambridge University Press

Adaptations for hindgut fermentation are most pronounced in the highly folivorous howler monkeys (Alouatta spp.) and Indrids (Avahi, Indri, and Propithecus). In these species, the complex nature of the hindgut is demonstrated by the presence of sacculations (haustra), longitudinal bands (taeniae), and flexures that presumably trap or slow the movement of digesta (Clemens and Phillips, 1980). Increased retention of food particles in this region facilitates microbial degradation by symbiotic organisms.

Some hindgut fermenters have adaptations in the foregut. For example, the stomach of Alouatta, which consumes a diet of at least 40% leaf material by weight (Hladik and Hladik, 1972; Edwards, 1995), is the most complex among the hindgut fermenters (Figure 1-13). It is a capacious globular sac, narrowing toward the bent tubular pylorus, guarded by strong pillars running longitudinally with the body (Chivers and Hladik, 1980).

Median gut passage time for a mixed-ingredient diet, including browse plants, fed to the highly folivorous Hapalemur griseus alaotrensis was 18.21 hours (Cabre-Vent and Feistner, 1995). Three species of howler monkeys fed two manufactured diets with different fiber concentrations (15% and 30% acid-detergent fiber [ADF]) exhibited no significant difference between diets in mean transit time of solids (28.0 vs. 21.5 hours) or liquids (14.6 vs 16.1 hours) (Edwards, 1995).

When fed a manufactured diet containing 15% ADF, silvered leaf monkeys (Semnopithecus cristatus) exhibited a mean transit time of 13.6 hours for both solid and liquid phases of digesta (Sakaguchi et al., 1991). Francois’ leaf monkeys (Trachypithecus f. francoisi) fed a comparable (15% ADF) diet had a comparable transit time for liquid digesta (13.5 hours), but the mean transit time for solid digesta was 27 hours (Edwards, 1995). When the same animals were fed a diet with twice the fiber concentration (30% ADF), there was no significant effect of the dietary change on the transit time of either liquids (15.5 hours) or solids (28.5 hours) (Edwards, 1995).

Digestibility studies with the Yunan snub-nosed monkey (Rhinopithecus bieti), a foregut fermenter that feeds primarily on lichens, revealed apparent dietary dry matter digestibilities of 71 to 80%. Mean (± SD) retention time of plastic digesta markers was 47 ± 17 hr (Kirkpatrick et al., 2001).

Development of scientifically sound feeding programs for captive primates requires a balance of information on the species of concern. Gastrointestinal tract structure, natural feeding behavior, and nutrient composition of foods consumed by free-ranging individual animals are some of the items required to address dietary husbandry requirements. Identifying readily available foods to meet physio-

logic and behavioral needs of the species in captivity might be a greater challenge.

Diets for strict faunivores in a captive setting—including Arctocebus, Galago, Loris, Microcebus, and Tarsius—are limited by the availability of suitable vertebrate and invertebrate prey. Although crickets (Acheta domestica) and meal-worm larvae (Tenebrio molitor and Zophobas morio) are readily available, they are not adequate to support the estimated nutritional requirements of these nonhuman primates (Oftedal and Allen, 1997). Guidelines on the handling and care of invertebrate prey to improve their nutrient quality as foods, specifically their calcium content, are provided by Allen and Oftedal (1989).

Food consumption by Tarsius appears to be influenced by movement of the prey offered as food. Thus, dietary prey must not only be living when presented, but must also be maintained in an environment (for example, with proper temperature, humidity, and photoperiod) that supports their needs and encourages natural movement.

As one reviews the literature on natural feeding habits of primates, it should be noted that biologists identify wild plant foods with botanic terms (such as fruit, flower, and petiole). However, these plant parts and their compositions are substantially different from commercially available produce that has been selectively cultivated for human consumption (Table 1-8). Thus, if commercial produce is to be offered to captive primates, that selection should be based on suitable nutrient composition and not solely on the basis of botanic classification.

Free-ranging primates devote a large percentage of their daily activity to acquisition and processing of food, and foraging not only satisfies a physiologic need, but plays a behavioral and social role in the life of primates. Provisioning captive populations of primates removes the need to forage in order to survive. However, if the diet is presented as a meal or on a predictable schedule, the behavioral needs of the animal might not be satisfied. Caretakers are encouraged to offer the diet in small portions distributed irregularly throughout the species-typical feeding period. The manner of diet preparation and presentation can also influence feeding behavior and the opportunity for equitable acquisition of food by individual animals in groups (Smith et al., 1989).

Leaf-eating primates—including Propithecus, Indri, Alouatta, Nasalis, and Pygathrix—have long been recognized as specialist feeders that are difficult to adapt to a “captive” diet. The impression that plant fiber is a negative dietary component and that a diet low in fiber is “preferred” by these captive primates has produced many of the health problems commonly seen (Edwards and Ullrey, 1999b). That conclusion is supported by a number of reports of a high incidence of gastrointestinal disorders among leaf-eating primates, many of which might be a result of consuming rapidly fermentable foods such as commercial fruits and vegetables (Hill, 1964; Bauchop and Martucci, 1968; Hick, 1972; Höllihn, 1973; Benton, 1976; Benirschke and Bogart, 1978; Heldstab, 1988; Taff and Dolhinow, 1989; Janssen, 1994). The beneficial role of plant fiber in promoting satiety, normal fecal consistency, and gastrointestinal health is well documented (Cummings, 1978).

Adiputra, I.M.W. 1994. Feeding behavior of Javan leaf monkey (Presbytis comata comata). 15th Congress International Primatology Society Handbook and Abstracts. #82. Kuta, Bali, Indonesia.

Agetsuma, N. 1995a. Foraging synchrony in a group of Yakushima macaques (Macaca fuscata yakui). Folia Primatol. 64:167-179.

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