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Nutrient Requirements of Nonhuman Primates: Second Revised Edition (2003)

Chapter: 1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity

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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
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1
Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity

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.

FEEDING ECOLOGY

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.

Feeding-Ecology Methods Involving Visual Observations of Behavior

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.

OBSERVATION OPTIONS

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.

SAMPLING METHODS

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,

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

TABLE 1-1 Prosimian Feeding Ecology

Scientific Name

Common Name

Dieta

Behavior

Body Weightb

References

100% insectivorous

Tarsius

T. bancanus

T. dianae

T. pumilus

T. spectrum

T. syrichta

Western tarsier

Dian’s tarsier

Pygmy tarsier

Spectral tarsier

Philippine tarsier

Animal prey 100%; T. bancanus example: beetles 35%, ants 21%, locusts 16%, cicadas 10%, cockroaches 8%, vertebrates 11% of feeding time (not seen eaten by all Tarsius); also eaten: crickets, mantids, moths

Nocturnal, arboreal, solitary or pairs or multimale/ multifemale, group size 2-6 individuals

77.6-117 g females, 27.5-134 g males

Crompton & Andah, 1986; Fogden, 1974; Gursky, 1996; Kappeler, 1991; MacKinnon & Mackinnon, 1980a; Niemitz, 1984; Nietsch & Niemitz, 1991; Tremble et al., 1993

Mostly insectivorous

Allocebus

A. trichotis

Hairy-eared dwarf lemur

In wild, unknown; in captivity, insects 70%, sweetened rice broth, fruit

Nocturnal, arboreal, forage solitary or male/female pair, sleep 2-6

78-90 g females, 75-98 g males

Albignac et al., 1991; Kappeler, 1991; Meier & Albignac, 1991; Mittermeier et al., 1994

Arctocebus

A. aureus

A. calabarensis

Golden angwantibo

Angwantibo

Animal prey 79% (73-85%), fruit 13% (12-18%), other vegetation 8%; prey: caterpillars 77% (65-90%) crickets, beetles, ants

Nocturnal, arboreal, forage solitary, sleep 1-2

A. aureus 150-270 g; A. calabarensis 200-465 g

Bearder, 1987; Charles-Dominique, 1974; Charles-Dominique & Bearder, 1979; Gonzalez-Kirchner, 1995; Silva & Downing, 1995; Wolfheim, 1983

Galagoides

G. demidoff

G. thomasic

G. zanzibaricus

Demidoff’s bush baby

Thomas’s bush baby

Zanzibar bush baby

Animal prey 75% (70-81%), fruit 17% (4-30%), gums/ resins 5% (0-18%), leaves, buds; prey:moths, beetles, grasshoppers, ants, some birds

Nocturnal, arboreal (mostly), forage solitary, sleep (females) 1-10

G.demidoff 46-69 g females, 78-85 g males; G. thomasi 55-149 g; G. zanzibaricus 118-155 g females, 130-183 g males

Charles-Dominique, 1974; Gonzalez-Kirchner, 1995; Harcourt & Bearder, 1989; Harcourt & Nash, 1986; Hladik, 1979; Kappeler, 1991; Nash et al., 1989; Nash & Harcourt, 1986; Silva & Downing, 1995

Loris

L. tardigradus

Slender loris

Almost exclusively insects, small amount of young leaves, shoots, hard-rind fruits, flowers, eggs, small vertebrates; often insects strong smelling

Nocturnal, arboreal, forage solitary, sleep 2-4

102-322 g

Butynski, 1982; Petter & Hladik, 1970; Silva & Downing, 1995; Wolfheim, 1983

Omnivorous, gums dominate

Euoticus

E. elegantulus (Galago elegantulus)

E. pallidusc

Southern needle-clawed bush baby

Northern needle-clawed bush baby

Gums 55% (35-75%), animal prey 32% (20-44%), fruit 12% (5-20%), birds

Nocturnal, arboreal, forage solitary, sleep 1-7

271 g female, 270-360 g males

Butynski, 1982; Charles-Dominique, 1974, 1977; Charles-Dominique & Bearder, 1979; Gonzalez-Kirchner, 1995; Hladik, 1979; Kappeler 1991

Galago

G. senegalensis

G. moholi

Northern lesser bush baby

Southern lesser bush baby

Gums (Acacia) 48%, animal prey 52% (butterflies, moths, beetles), gums from 2 tree species, no vertebrate prey

Nocturnal, arboreal, forage solitary, sleep 1-3

G. senegalensis 126-193 g females, 125-212 g males; G. moholi 140-229 g females, 160-255 g males

Bearder, 1987; Bearder & Doyle, 1974; Bearder & Martin, 1979; Doyle, 1979; Doyle & Bearder, 1977; Harcourt & Bearder, 1989; Nash & Whitten, 1989; Silva & Downing, 1995

Otolemur

O. crassicaudatus (Galago crassicaudatus)

Thick-tailed greater bush baby

Gums 44% (18-62%), fruit 27% (21-33%), animal prey 14% (1-27%) (invertbrates and vertebrates), nectar 4% (0-8%), seeds 3% (0-7%), misc. vegetable matter 8% (0-16%)

Nocturnal, arboreal, male solitary, female and offspring forage together, sleep 1-6

1122-1497 g females, 1126-1750 g males

Bearder & Doyle, 1974; Butynski, 1982; Doyle & Bearder, 1977; Kappeler, 1991; Masters et al., 1988

Phaner

P. furcifer

Fork-marked lemur

Tree gum (resins) bulk of diet, some fruit, sap, animal matter 10%, flowers, buds, nectar, secretions of Homoptera insects

Nocturnal, arboreal, solitary or male/ female pairs, sleep 1-4

350-600 g

Charles-Dominique & Petter, 1980; Hladik, 1979; Hladik et al., 1980; Kappeler, 1991; Pariente, 1979; Petter et al., 1971, 1975

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

Omnivorous, plants (especially fruits) dominate

Cheirogaleus

C. major

C. medius

Greater dwarf lemur

Fat-tailed dwarf lemur

Fruit, young leaves, flowers, nectar, leaf buds, gums, animal prey (mostly insects, some chameleons); C. major lethargic in cool, dry season; C. medius increase in body weight 120-250 g during rainy season (6 months), hibernate 7-9 months

Nocturnal, arboreal, forage solitary, sleep 1-5

C. major 235-470 g; C. medius when feeding (rainy season) 142-217 g, especially tail, hibernate loses 100 g

Hladik, 1979; Hladik et al., 1980; Mittermeier et al., 1994; Petter et al., 1977; Wright & Martin, 1995

Eulemur (Petterus)

E. coronatus

E. fulvus

E. macaco

E. mongoz

E. rubriventer

Crowned lemur

Brown lemur

Black lemur

Mongoose lemur

Red-bellied lemur

Fruit 45% (7-79%), leaves 45% (20-89%), flowers 10% (1-52%), few insects; dry season diet of E. mongoz, E. rubriventer, E.fulvus in some habitats nectar 82% (81-84), fruit 17%, leaf 1%; E. fulvus tolerates high levels of toxic plant compounds

Cathemeral, mostly arboreal, multimale/ multifemale groups, group size 5-18 or just family groups

1.4-2.4 kg

Andriatsarafara, 1988; Colquhoum, 1993; Dague & Petter, 1988; Hladik, 1979; Kappeler, 1991; Overdorff, 1993; Richard & Dewar, 1991; Silva & Downing, 1995; Sussman, 1974, 1977; Sussman & Tattersall, 1976; Tattersall, 1977, 1979; Wilson et al., 1989; Yamashita 1996

Galago

G. alleni

G. gallarum

G. matschiei

Allen’s bush baby

Somali bush baby

Matschie’s bush baby (was Euoticus inustus)

Fruit 74% (73-76%), animal prey 24% (23-25%) (invertebrates and frogs), 2% other vegetation (fallen fruit, seeds, gums)

Nocturnal, arboreal, forage solitary 86%, sleep (females) 1-4

G. alleni 200-445 g; G. gallarum 196-225 g

Butynski, 1982; Charles-Dominique, 1977; Gonzalez-Kirchner, 1995; Nash et al., 1989

Lemur

L. catta

Ring-tailed lemur

Fruit 54% (34-70%), leaves 33% (24-50%), flowers 3% (0-8%), herbs 8% (6-15%), bark, sap, cactus, misc 2% (0-7%); Tamarindus indicus is 25% of diet: 12% leaf, 12% pods

Diurnal, arboreal, terrestrial, multimale/ multifemale, with 1 alpha female, group size 5-30

1.96-2.705 kg

Jolly, 1966; Kappeler, 1991; Rasamimanana & Rafidinarivo, 1993; Sauther & Sussman, 1993; Silva & Downing, 1995; Sussman, 1974; Yamashita, 1996

Microcebus

M. (Mirza) coquereli

M. murinus

M. myoxinusc

M. rufus

Coquerel’s dwarf lemur

Gray mouse lemur

Pygmy mouse lemur

Brown mouse lemur

Fruit, animal matter (insects, frogs, bird eggs, chameleons), young leaves, flowers, gums, sap/resins, nectar, buds, seeds; spends up to 50%of time in dry season licking larval secretions of Homoptera off branches

Nocturnal, arboreal mostly, forage solitary, some pairs, sleep 1-4; M. murinus store fat in tail and less active in dry season, do not hibernate, sleep 1-15

M. coquereli, M. myoxinus 302 g female, 308 g male; M. rufus 41-63 g females, 35-70 g males; M. murinus 40-109 g varies 50-60 g when “hibernates”

Corbin & Schmid, 1995; Hladik, 1979; Kappeler, 1991; Pages, 1980; Petter et al., 1971, 1977; Wright & Martin, 1995

Nycticebus

N. coucang

N. pygmaeusc

Slow loris

Pygmy loris

Fruit 50%, animal prey 30%, gums 15% (10-19%), shoots, bird eggs, insects that have repugnant taste and smell

Nocturnal, arboreal, forage solitary

N. coucang 375-900 g female, 850-1207 g male: N. pygmaeus 372 g female, 462 g male

Bearder, 1987; Duckworth, 1994; Kappeler, 1991; Silva & Downing, 1995; Tan, 1994; Van Horn & Eaton, 1979

Otolemur

O.garnettii

Garnett’s greater bush baby

Fruit 27% (4-50%), animal prey 61% (44-78%) (beetles, ants, termites, snails, birds), seeds 3% (0-7%), other vegetation 9% (0-18%) (resins, bark, pollen)

Nocturnal, arboreal, male solitary, related females overlap

740-1460 g female, 822-1640 g male

Bearder, 1987; Harcourt & Nash, 1986; Masters et al., 1988; Nash & Harcourt, 1986; Nash et al., 1989; Silva & Downing, 1995

Perodicticus

P. potto

Potto

Fruit 74% (65-82%), gums 40% (21-60%), animal prey 20% (10-30%) (ants make up 65%of insect prey), some leaf and fungus; when fruit is scarce (dry season)

Nocturnal, arboreal, forage solitary 96%, pairs 4%, sleep 1-2

850-1600 g

Charles-Dominique, 1974; Gonzalez-Kirchner, 1995; Hladik, 1979; Oates, 1984

Varecia

V. variegata

Ruffed lemur

Ripe fruit 74%, 21% leaves (2% shoots, 1% young leaves, 18% mature leaf), flowers 5% (1-40%), seeds, nectar; 74% nectarivorous in 1 month of year

Diurnal, arboreal mostly, family or larger groups, 5-32 individuals

3.512 kg female, 3.471 kg male

Dew & Wright, 1994; Kappeler & Ganzhorn, 1993; Morland, 1993; Richard & Dewar, 1991; Rigamonti, 1993; White, 1989

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

Leavesdominate other plant parts

Avahi

A. laniger

Woolly lemur

Seasonally exclusively folivorous: 91% leaves (40% mature leaves, 51% mixed mature and young), 9% flowers, rarely fruit and bark

Nocturnal, arboreal, monogamous pairs, groups 2-5 individuals

1.3 kg female, 1.0 kg male

Albignac, 1981; Ganzhorn, 1988; Ganzhorn et al., 1985; Harcourt, 1991; Kappeler, 1991; Richard & Dewar, 1991

Indri

I. indri

Indri (babakoto)

Young leaves, buds, and petioles 45% (1-75%), fruit 38% (5-75%), unripe seeds 12% (10-15%), flowers and buds 3% (1-6%), mature leaves 2% (0-3%), occasionally soil

Diurnal, arboreal, monogamous family groups 2-6 individuals

7.1 kg female, 5.8 kg male

Hladik, 1979; Mittermeier et al., 1994; Pollock, 1975, 1977

Lepilemur

L. dorsalis

L. edwardsi

L. leucopus

L. microdonc

L. mustelinus

L. ruficaudatus

L. septentrionalis

Gray-backed sportive lemur

Milne-Edwards’ sportive lemur

White-footed sportive lemur

Small-toothed sportive lemur

Weasel sportive lemur

Red-tailed sportive lemur

Northern sportive lemur

Leaves primarily, some fruit, bark, seeds, flowers; L. mustelinus can tolerate high alkaloid levels; L. ruficaudatus may practice caecotrophy and have high tolerance for toxins; L. leucopus 100% leaves

Nocturnal, arboreal, solitary or male/ female pairs, sleep 1-3; do not hibernate

544-915 g, L. edwardsi 1000g

Albignac, 1981; Charles-Dominique & Hladik, 1971; Ganzhorn, 1988; Hladik, 1979; Hladik & Charles-Dominique, 1974; Hladik et al., 1980; Kappeler, 1990, 1991; Kappeler & Ganzhorn, 1993; Nash, 1994; Silva & Downing, 1995

Propithecus

P. diadema

P. tattersalli

P. verreauxi

Diademed sifaka

Golden-crowned sifaka

Verreaux’s sifaka

P. diadema and P. tattersalli: young leaves 25% (5-44%), mature leaves 25% (0-46%), fruit, ripe or unripe 43% (0-72%), flowers 7% (0-23%); P. verreauxi: mature leaves 38% (2-70%), young leaves 40% (0-70%), fruit 7% (5-8%), flowers 10% (0-40%), bark 5% (4-9%)

Diurnal, mostly arboreal, pairs to multimale/ multifemale groups, 2-12 individuals

P. diadema: 5.6-7.2 kg, P. tattersalli: 2.1-3.8 kg, P. verreauxi: 3.5-3.6 kg

Hemingway, 1998; Hladik, 1979; Jolly, 1966; Kappeler, 1991; Meyers & Wright, 1993; Richard, 1974, 1977, 1978; Yamashita, 1996

Mostly bamboo

Hapalemur

H. aureus

H. griseus

H. simus

Golden bamboo lemur

Lesser bamboo lemur

Greater bamboo lemur

Bamboo 95% (85-98%) (shoots 89%, mature leaves 6%, young leaves 1%, petioles 1%), flowers 1%, fruit 2%, fungus 2%; H. griseus also eats phragmites leaves and shoots, Papyrus pith; H. aureus eats a bamboo containing 12 × lethal dose (for humans) of cyanide

Diurnal or cathemeral, arboreal, family 2-6 individuals; H. simus 1 male + multifemale or multimale/ multifemale groups 4-30 individuals

H. aureus 1.5 kg female, 1.7 kg male; H. griseus 800-939 g; H. simus 1.3-2.4 kg

Glander et al., 1989; Kappeler, 1990; Meier & Rumpler, 1987; Overdorff et al., 1997; Petter & Peyrieras, 1970a; Petter et al., 1975, 1977; Silva & Downing, 1995; Wright, 1986; Wright & Randrimanantena, 1989; Wright et al., 1987

Wasthought of asinsectivorousbut isomnivorous-frugivorous

Daubentonia

D. madagascariensis

Aye-aye

Seeds/nuts 47% (12-84%), nectar 8% (1-20%), larvae 20% (2-45%), canker 20% (5-42%), other (soft fruit, fungus, galls, bamboo) 5% (0-12%); larvae extracted with long thin finger; eat coconuts (0-58% where available) same way.

Nocturnal, arboreal, forage solitary, sleep 1-2

2.6 kg female, 2.8 kg male

Ancrenaz et al., 1994; Andriamasimanana, 1994; Erickson, 1995; Iwano & Iwakawa, 1985; Kappeler, 1991; Petter & Peyrieras, 1970b; Pollock et al.,1985; Sterling, 1994; Sterling et al., 1993

aDiet format: mean (range).

bBody weights in ranges whenever possible; single numbers are not averages but indicate that only one individual of the species has been weighed in the wild.

cNo data available from the wild but assumed to be similar to congenerics.

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-

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

TABLE 1-2 Callitrhix Feeding Ecology

Scientific Name

 

Dieta

Behavior

Body Weightb

References

Fruit and insect foraging dominate diet, gums seasonally important

Callithrix

C. argentata

C. aurita

C. geoffroyi

C. humeralifer

C. kuhlii

C. mauesic

C. nigriceps

Bare-ear marmoset

Buffy tufted-eared marmoset

Geoffroy’s tufted-eared marmoset

Tassel-eared marmoset

Wied’s tufted-eared marmoset

Maues marmoset

Black-headed marmoset

27% (24-30%) of total daily activity foraging for insects; therefore, total feeding time spent on insect foraging 56% (50-63%), fruit 33% (28-37%), exudates (gums) 11% (5-16%); when fruit scarce, exudate intake increased

Diurnal, arboreal mostly, multimale/ multifemale group size 3-20 individuals

190-320 g females, 357-450 g males; C. nigriceps 370 g male, 390 g female

Ferrari, 1993; Ferrari & Ferrari, 1989; Ferrari & Rylands,1994; Ford & Davis, 1992; Harrison & Tardif, 1994; Koenig, 1995; Muskin, 1984; Rylands, 1993; Rylands & de Faria, 1993; Stevenson & Rylands, 1988

Fruit dominates, insects important, gums or nectar seasonal

Leontopithecus

L. caissarac

L. chrysomelas

L. chrysopygus

L. rosalia

Black-faced lion tamarin

Golden-headed lion tamarin

Black lion tamarin

Golden lion tamarin

Ripe fruit 53% (32-78%), insect foraging 25% (14-50%) of feeding time, unripe fruit 6-7%, exudates (gums) 9% (1-20%), nectar 7% (0-43%)

Diurnal, arboreal mostly, pairs or multimale/ multifemale 2-3 adults/group, 2-16 total

361-794 g females, 437-710 g males

Albernaz, 1997; Butynski, 1982; Dietz et al., 1997; Ferrari, 1993; Ferrari & Ferrari, 1989; Ford & Davis, 1992; Rylands, 1993; Tardif et al., 1993

Gumsdominate, insectsimportant, fruit can depend on location

Callithrix

C. jacchus

C. flaviceps

C. penicillata

C. pygmaea (was genus Cebuella)

Common marmoset

Buffy-headed marmoset

Black tufted-eared marmoset

Pygmy marmoset

Exudates (gums) 45% (24-70%), fruit 16% (14-30%), insect foraging 39% (30-70%), nectar in dry season; C.pygmaea exudates (gums) 60% (30-77%), fruit 8% (0-10%), insects 30% (20-33%)

Diurnal, arboreal mostly, multimale/ multifemale, groups 1-15; C. pygmaea monogamous families, up to 4 litters living together

182-354 g females, 225-406 g males; C. pygmaea 112-140 g females, 99-160 g males

Coimbra-Filho & Mittermeir, 1978; Ferrari & Ferrari, 1989; Ferrari & Rylands, 1994; Ford & Davis, 1992; Ramirez, 1985a; Rylands & de Faria, 1993; Silva & Downing, 1995; Soini, 1982, 1988, 1993

Insects and fruit dominate, gums and nectar seasonally important

Callimico

C. goeldii

Goeldi’s monkey

Preferred food insects; also soft, sweet fruit in wet season, sticky coating of gum on pods in dry season; rarely buds or young leaves; diet similar to Saguinus spp, sometimes live with mixed Saguinus troops

Diurnal, arboreal mostly, monogamous pairs, some within group, 2-8 individuals

400-535 g

Ford & Davis, 1992; Heltne et al., 1981; Mittermeier & Coimbra-Filho, 1977; Pook & Pook, 1981, 1982

Saguinus

S. bicolor

S. fuscicollis

S. geoffroyi

S. imperator

S. inustusc

S. labiatus

S. leucopus

S. midas

S. mystax

S. nigricollis

S. cedipus

S. tripartitusc

Bare-faced tamarin

Saddleback tamarin

Red-crested tamarin

Emperor tamarin

Mottled-faced tamarin

Red-bellied tamarin

Silvery-brown bare-faced tamarin

Golden-handed tamarin

Mustached tamarin

Spix’s black-mantled tamarin

Golden-mantled

Cotton-top tamarin saddleback tamarin

Insects 45% (30-77%), fruit 35% (13-74%), exudate 10% (0-37%), nectar 7% (0-35%), young leaves 3%, seeds; 34.8% of total activities foraging for insects, 17% plant foods; insect capture rate might be only 5.4% of prey-foraging time

Diurnal, arboreal, multimale/ multifemale groups, 2-16 individuals; S. imperator, S. labiatus, and S. midas multimale/ multifemale, but only 1 reproducing female

272-600 g females, 242-633 g males

Crandlemire-Sacco, 1988; Egler, 1992; Ferrari & Ferrari, 1989; Ford & Davis, 1992; Garber, 1984, 1988, 1993a,b; Harrison & Tardif, 1994; Lopes & Ferrari, 1994; Pack et al., 1999; Peres, 1993a; Ramirez, 1985a,b; Skinner, 1985; Silva & Downing, 1995; Soini, 1987; Terborgh, 1983

aDiet format: mean (range).

bBody weights in ranges whenever possible; single numbers are not averages but indicate that only one individual of the species has been weighed in the wild.

cNo data available from the wild but assumed to be similar to congenerics.

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

TABLE 1-3 Cebid Feeding Ecology

Scientific Name

Common Name

Dieta

Behavior

Body Weightb

References

More insectivorous than frugivorous

Saimiri

S. boliviensis

S. oerstedii

S. sciureus

S. ustusc

S. vanzoliniic

Bolivian squirrel monkey

Red-backed squirrel monkey

Common squirrel monkey

Golden-backed squirrel monkey

Black squirrel monkey

Animal prey, particularly insects 60% (47-100%), vertebrates 1%, fruit 25% (15-39%), flowers 5% (2-13%), leaves 13% (11-18%), seeds/ nuts, successful in 61% of insect foraging; during dry season, rely on figs

S. boliviensis, S. oerstedii: diurnal, arboreal, multimale/ multifemale, groups, up to 23 individuals; S. sciureus, S. vanzolinii: groups, 22-50 individuals

0.54-1.25 kg females, 0.48-1.2 kg males

Costello et al., 1993; Ford & Davis, 1992; Janson & Boinski, 1992; Mittermeier & vanRoosmalen, 1981; Rosenberger, 1992; Silva & Downing, 1995; Souza et al., 1997; Terborgh, 1983

Primarily frugivorous

Ateles

A. belzebuth

A. chamek

A. fuscicepsc

A. geoffroyi

A. marginatusc

A paniscus

White-bellied spider monkey

Black-faced black spider monkey

Brown-headed spider monkey

Black-handed spider monkey

White-whiskered spider monkey

Black spider monkey

Total fruit 78% (18-100%), including unripe fruit 6%; seed 5% (0-19%); total leaves 16% (0-38%), including mature leaves 3%; flowers 3% (1-10%); epiphytes 2%; dead wood, buds, insects 1%

Diurnal, arboreal (salt licks on ground), fission-fusion, groups 3-35 individuals

5.0-11.0 kg females, 5.8-9.8 kg males

Chapman, 1987, 1988; Ford & Davis, 1992; Hladik, 1975; Klein & Klein, 1975, 1977; MendesPontes, 1997; Milton, 1981; Mittermeier & vanRoosmalen, 1981; Nunes, 1998; Robbins et al., 1991; Silva & Downing, 1995; Simmen & Sabatier, 1996; Symington, 1988; VanRoosmalen, 1985; VanRoosmalen & Klein, 1988; White, 1986

Primarily frugivorous, seasonally seeds or leaves important

Aotus

A. nigriceps

Southern red-necked night monkey

 

A. trivirgatus

Northern gray-necked owl monkey

Fruit (soft) 44% (16-75%), leaves 32% (5-46%), insects 13% ( 5-15%), other (especially flowers) 11%; Aotus diet similar to Callicebus but ate less vegetation, more insects in abundant season

Nocturnal, arboreal, monogamous family groups, 2-5 individuals; feed in groups 25-55 at low elevations

0.78-1.1 kg females, 0.825-1.05 kg males

Durham, 1975; Engqvist & Richard, 1991; Kinzey, 1992; Wright, 1981,1989, 1994

Callicebus

C. brunneus

C. caligatusc

C. cinerascensc

C. cupreusc

C. donacophilusc

C. dubiusc

C. hoffmannsic

C. modestusc

C. moloch

C. oenanthec

C. olallaec

C. personatus

C. torguatus

Brown titi monkey

Chestnut-bellied titi monkey

Ashy gray titi monkey

Red titi monkey

Bolivian gray titi monkey

Hershkovitz’s titi monkey

Hoffmann’s titi monkey

Bolivian titi monkey

Dusky titi monkey

Andean titi monkey

Beni titi monkey

Masked titi monkey

Collared titi or widow monkey

Fruit 61% (30-87%) (of which seeds may be as much as 28%), leaves (mostly young) 21% (2-66%), insects 12% (0-28%), flowers 2% (0-18%); when food scarce, ate 25% bamboo and vine leaves

Diurnal, arboreal, monogamous family 2-6 individuals

0.7-1.5 kg

Crandlemire-Sacco, 1988; Easley, 1984; Ford & Davis, 1992; Heiduck, 1997; Kinzey, 1977, 1981, 1992; Kinzey & Gentry, 1979; Muller, 1996; Palacios, 1997; Robinson et al., 1987; Silva & Downing, 1995; Terborgh, 1983, Wright, 1994

Cebus

C. albifrons

C. apella

C. capucinus

C. olivaceus

White-fronted capuchin

Tufted or brown capuchin

White-throated capuchin

Weeper or wedge-capped capuchin

Fruit 55% (10-95%), of which seeds are 8% (0-39%); leaves (mostly young) 8% (0-39%); insects 33% (2-100%); flowers 2% (0-14%); C. apella in Argentina ate bromeliad leaves 72%, fruit 3%, insects 25%

Diurnal, arboreal mostly, multimale/ multifemale groups of 2-40 individuals; C. apella, C. olivaceus: with alpha male

1.4-3.8 kg females, 1.3-4.8 kg males

Brown & Zunino, 1990; Chapman, 1987; Chapman & Fedigan, 1990; Ford & Davis, 1992; Hladik et al., 1971; Janson, 1985; Janson & Boinski, 1992; Mittermeier & vanRoosmalen, 1981; Peres, 1994a; Robinson, 1984; Simmen & Sabatier, 1996; Teaford & Robinson, 1989; Terborgh, 1983

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

Both fruit and seeds rank high, sometimes seeds dominate

Lagothrix

L. flavicauda

L. lagothricha

Yellow-tailed woolly monkey

Woolly monkey

Fruit 67% (6-95%), seeds 10% (0-35%); insects 7% (0-34%), leaves (mostly young) 12% (2-48%); flowers 2% (0-9%), pod exudates eaten at some sites

Diurnal, arboreal, multimale/ multifemale groups of 5-70 individuals; highlands groups 6-7; lowlands groups 10-20 individuals

3.5-6.5 kg females, 3.6-10.2 kg males

Butynski, 1982; Defler & Defler, 1996; Durham, 1975; Ford & Davis, 1992; Kinzey, 1997; Luna, 1987; Peres, 1994b; Ramirez, 1988; Robinson & Janson, 1987; Soini, 1987; Stevenson et al., 1994

Cacajao

C. calvus

C. melanocephalus

Bald uacari

Black-headed uacari

Seeds (mostly unripe) 59% (20-97%), fruit pulp 22% (1-60%), nectar 6% (0-58%), insects 5%, leaves and so on 3%; seeds of unripe fruit important as for all pithecines

Diurnal, arboreal mostly, multimale/ multifemale groups 5-30 up to 100 individuals

2.4-4.0 kg

Ayres, 1989; Barnett & Brandon-Jones, 1997; Fontaine, 1981; Ford, 1994; Kinzey, 1992; Mittermeier & Coimbra-Filho, 1977

Chiropotes

C. albinasus

C. satanas

White-nosed saki

Bearded saki

Seeds (mostly unripe) 53% (12-96%), fruit 37% (6-84.5%); leaves 2% (0-4%), flowers 5% (1-11%), insects 3% (0-24%); seed predators on 52 species and seed dispersers of 7 species; C. satanas ingest unripe fruit with hard pericarp

Diurnal, arboreal, multimale/ multifemale groups 10-30 individuals

1.9-3.3 kg females, 2.2-4.0 kg males

Ayres, 1989; Ford & Davis, 1992; Kinzey, 1992; Kinzey & Norconk, 1993; Mittermeier & vanRoosmalen, 1981; Mittermeier et al., 1983; Norconk et al., 1998; Robinson et al., 1987; van Roosmalen et al., 1981, 1988

Pithecia

P. aequatorialisc

P. albicans

P. irroratac

P. monachus

P. pithecia

Equatorial saki

Buffy saki

Bald-faced saki

Monk saki

White-faced saki

Seeds 38% (17-88%), other fruit 43% (3-51%), leaves (mostly young) 12% (0-32%), insects 1.0% (0-6%), flowers 6% (0-15%); P. monachus may eat more leaves or insects, P. pithecia more young seed ( 60%)

Diurnal, arboreal, monogomous family groups, groups 2-8; P. aequatorialis, P. monachus: cryptic

0.779-2.5 kg females, 0.964-3.1 kg males

Buchanan et al., 1981; Ford & Davis, 1992; Happel, 1982; Kinzey, 1992; Kinzey & Norconk, 1993; Mittermeier & vanRoosmalen, 1981; Norconk, 1996; Norconk & Kinzey, 1990; Norconk et al., 1998; Peres, 1993b

Primarily folivorous, some fruit, no animal prey

Alouatta

A. belzabulc

A. caraya

A. colibensisc

A. fusca

A. palliata

A. pigra

A. sarac

A. seniculus

Red-handed howler

Black-and-gold howler

Colba Island howler

Brown howler

Mantled howler

Black howler

Bolivian red howler

Red howler

A. palliata, A. seniculus, A. pigra: total leaves 54% (20-100%), including 38% young, 16% mature leaf; total fruit, especially figs, 39% (0-80%), including 34% ripe, 5% unripe; flowers 9% (0-90%); A. fusca, A. caraya: 72% leaves (45-89%); fruit 20% (2-55%); flowers 8% (0-24%)

Diurnal, arboreal (drink on ground, A. palliata can swim), 1,2 or multimales/ multifemales, groups 4-21 individuals; One-male groups common

2.4-7.6 kg females, 4.2-11.4 kg males

Bicca & Calegaro, 1994; Chapman, 1987; Crockett & Eisenberg, 1987; de Thoisy & Richard-Hansen, 1997; Estrada, 1984; Estrada & Coates-Estrada, 1986; Ford & Davis, 1992; Galetti et al., 1987; Garcia, 1994; Gaulin & Gaulin, 1982; Glander, 1978; Hladik el al., 1971; Julliot & Sabatier, 1993; Milton, 1980; 1981; Mittermeier & van Roosmalen, 1981; Neville et al., 1988; Oftedal, 1991; Prates et al., 1987; Simmen & Sabatier, 1996; Smith, 1977; Stoner, 1996; Strier, 1992.

Brachyteles

B. arachnoides

Woolly spider monkey or muriqui

Leaves 58% (range 41-93%); fruit 28% (7-59%), within which unripe seeds were 8% (0-32%); flowers 14% (0-38%)

Diurnal, arboreal, multimale/ multifemale and fission-fusion, groups 5-45 individuals

9.4 kg female, 12.1 kg male

Ford, 1994; Lemos, 1988; Milton, 1984; Neville et al., 1988; Nishimura et al., 1988; Strier, 1991, 1992

aDiet format: mean (range).

bBody weights in ranges whenever possible; single numbers are not averages but indicate that only one individual of the species has been weighed in the wild.

cNo data available from the wild but assumed to be similar to congenerics.

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

TABLE 1-4 Colobine Feeding Ecology

Scientific Name

Common Name

Dieta

Behavior

Body Weightb

References

Strongly folivorous

Colobus

C. guereza

C. vellerosusc

Abyssinian, guereza, or eastern black-and-white colobus

Geoffroy’s or white-thighed black-and-white colobus

C. guereza: young leaves and buds 64% (52-90%), mature leaves 13% (2-22%), whole fruit 15% (0-34%), flower and bud 6% (0-17.1%); seeds 1%, stems 0.5%; other 0.5%

Diurnal, arboreal mostly; C. guereza: 1 male or multimale/ multifemale group 2-50; others: multimale/ multifemale

6.8-8.92 kg females, 9.7-13.5 kg males

Clutton-Brock, 1975; McKey, 1978; Napier, 1985; Oates, 1977, 1978, 1994, Oates et al., 1994; Struhsaker, 1978a; Struhsaker & Oates, 1975

Folivorous but >30% seed-eating

Colobus

C. angolensis

C. polykomos

C. satanas

Angolan black-and-white colobus

King or western black-and-white colobus

Black colobus

Young leaves 31% (2-85%), mature leaves 18% (4-75%), fruit 8% (0-55%), seeds 35% (0-89%), flowers and buds 5% (0-31%), stems 1% (0-15%), other 1.5%

Diurnal, arboreal mostly; C. angolensis 1 male or multimale/ multifemale groups 2-50; others multimale/ multifemale

4.32-9.67 kg females, 9.7-13.5 kg males

Dasilva, 1992, 1994; Groves, 1973; Harrison & Hladik, 1986; Maisels et al., 1994; McKey, 1978; McKey & Waterman, 1982; McKey et al., 1981; Silva & Downing, 1995; Tutin et al., 1997

Strongly folivorous, some seed

Procolobus (Piliocolobus or Colobus)

P. badius

P. pennantii

P. preussic

P. rufomitratus

P. verus

Western red colobus

Pennant’s red colobus

Preuss’s red colobus

Tana river red colobus

Olive colobus

Young leaves and buds 52% (7-85%) mature leaves and petiole 16% (1-60%), fruit (especially unripe) 9% (0-41%), seeds 12% (0-31%), flowers and buds 9% (0-36%), stems and miscellaneous 1% (0-17%)

Diurnal, arboreal, multimale/ multifemale groups 5-80; P. rufomitratus, 1 male or multimale/ multifemale P. verus: 1 or 2 males + multifemale

4.2-8.2 kg females, 4.7-11.0 kg males

Brandon-Jones, 1985; Clutton-Brock, 1975; Decker, 1994; Gatinot, 1977; Maisels et al., 1994; Marsh, 1981, 1983; McKey, 1978; Mowry et al., 1996; Oates, 1988; Oates & Whitesides, 1990; Oates et al., 1994; Silva & Downing, 1995; Struhsaker, 1975, 1978a; Struhsaker & Oates, 1975; Wachter et al., 1997

Folivorous/frugivorous (>50% leaf, <50% fruit)

Nasalis

N. larvatus

N. (Simias) concolor

Proboscis monkey

Pig-tailed langur

Young leaf 45% (38-48%), mature leaves 4%, fruit 40% (17-50%), of which seeds are 15-20%, flowers and buds 3%; stems 3%; other 2.5%; insects <1%; fruit eaten usually unripe; frugivorous January-May, folivorous June-December

Diurnal, arboreal, swimmers, 1 male + multifemale and bachelor troops, groups 2-20; N. (Simias) concolor also in pairs or multimale/ multifemale

7.1-11.8 kg females, 8.8-23.6 kg males

Bennett & Davies, 1994; Bennett & Sebastian, 1988; Ross, 1992; Watanabe, 1981; Yeager, 1989

Presbytis

P. comata

P. femoralis

P. frontatac

P. hosei

P. melalophos

P. potenziani

P. rubicunda

P. thomasi

Grizzled leaf monkey

Banded leaf monkey

White-fronted leaf monkey

Hose’s leaf monkey

Mitered leaf monkey

Mentawai Island leaf monkey

Maroon leaf monkey

Thomas’s leaf monkey

Young leaves 41% (15-71%); mature leaves 4% (0-11%); fruit 42% (3-80%), of which about 7% is seeds (1-30%) and unripe fruit and seeds up to 30%; flowers and buds 10% (1-30%); other 3%; very little insect eaten <1%. P. rubicunda: seed predators

Diurnal, arboreal, male + multifemale, monogamous pairs, groups 2-21; P. melalophos: 1 male or multimale/ multifemale

3.0-6.7 kg females, 5.6-8.2 kg males

Adiputra, 1994; Aldrich-Blake, 1980; Bennett & Davies, 1994; Brandon-Jones, 1985; Chivers, 1994; Curtin, 1980; Davies, 1991; Davies et al., 1988; Goodman, 1989; Gurmaya, 1986; Leutenegger & Cheverud, 1982; MacKinnon & MacKinnon, 1980b; Rodman, 1978; Ruhiyat, 1983; Silva & Downing, 1995; Ungar, 1995; Watanabe, 1981

Pygathrix

P. nemaeus

P. nigripesc

P. (Rhinopithecus) avunculus

P. (Rhinopithecus) bieti

P. (Rhinopithecus) brelichi

P. (Rhinopithecus) roxellana

Red-shanked douc langur

Black-shanked douc langur

Tonkin snub-nosed monkey

Black or Yunnan snub-nosed monkey

Guizhou snub-nosed monkey

Sichuan golden snub-nosed monkey

Young leaves and buds 37% (7-93%), mature leaves 37% (31-88%), fruit 15% (5-47%), seeds 3% (0-15%), flowers 7% (0-28%), lichen 5% (0-50%); figs important, almost no insects

Diurnal, arboreal (some also terrestrial), multimale/ multifemale or 1 male + multifemale, groups 3-200 individuals

6.5-10 kg females, 10.9-20.3 kg males

Bennett & Davies, 1994; Bleisch & Xie, 1994; Bleisch et al., 1998; Ji & Bleisch, 1994; Kirkpatrick, 1994; Lippold, 1995; Long, 1994; Nhat, 1993, 1994; Silva & Downing, 1995

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

Semnopithecus (Presbytis)

S. entellus

Hanuman langur

In remote, wild areas: young leaves 26% (0-69%), mature leaves 26% (0-79%) fruit 34% (0-72%), of which about 3% is seeds (0-45%), flowers and buds 9% (0-43%), stem 1.6%; other 3%; more insects than other colobines; near farms: 90% of diet is cultivated crops; Himalayan subspp eat pinecones, bark, twigs during snowy winter months

Troops near temples eat offerings, raid crops; diurnal, terrestrial, and arboreal, 1 male or multimale/ multifemale, groups 11-262 individuals

6.7-15.6 kg females, 10.6-20.9 kg males

Bennett & Davies, 1994; Hladik, 1975, 1988; KarGupta & Kumar, 1994; Newton, 1992; Oppenheimer, 1977; Silva & Downing, 1995; Srivastava, 1991; Starin, 1978

Trachypithecus (Presbytis)

T. auratus

T. cristatus

T. delacouric

T. francoisic

T. geei

T. (Kasi) johnii

T. obscurus

T. phayrei

T. pileatus

T. (Kasi) vetulus

Ebony langur

Silvered langur

Delacour’s langur

Francois’s langur

Golden langur

Nilgiri langur

Dusky or spectacled leaf monkey

Phayre’s leaf monkey

Capped leaf monkey

Purple-faced leaf monkey

Young leaves and shoots 32% (9-52%), mature leaves and petioles 26% (1-61%), fruit 32% (1-55%), of which 7% is seeds (0-40%); flowers and buds 10% (0-43%), insects <1%, other 0.5%; more mature leaves than Presbytis and much of fruit eaten unripe; raids crop; T. pileatus - animal prey 1.6%, gum and termite soil

Diurnal, arboreal (some also terrestrial), 1 (some 2) male and multifemale, groups 2-40 individuals

3.0-10.9 kg females, 6.0-13.6 kg males

Aldrich-Blake, 1980; Bennett & Davies, 1994; Brandon-Jones, 1985; Brotoisworo & Dirgayusa, 1991; Chivers, 1994; Curtin, 1980; Curtin & Chivers, 1978; Fleagle, 1978; Hladik, 1975, 1977, 1988; Hladik & Hladik 1972; Islam & Husain, 1982; Kool, 1992, 1993; Kumar-Gupta & Kumar, 1994; Li, 1993; MacKinnon & MacKinnon, 1980b; Mukhergee, 1978; Oates et al., 1980; Silva & Downing, 1995; Stanford, 1988; 1991a, 1991b; Whitten, 1987, Wrangham et al., 1993

aDiet format: mean (range).

bBody weights in ranges whenever possible; single numbers are not averages but indicate that only one individual of the species has been weighed in the wild.

cNo data available from the wild but assumed to be similar to congenerics.

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.

Alternative Feeding-Ecology Methods

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.

ANALYSIS OF STOMACH CONTENTS

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

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

TABLE 1-5 Non-colobine Cercopithecine Feeding Ecology

Scientific Name

Common Name

Dieta

Behavior

Body Weightb

References

Omnivorousbut predominantly frugivorous(depending on habitat)

Macaca

M. arctoides

M. assamensisc

M. cyclopis

M. maurac

M. ochreatac

M. radiata

M. silenus

M. tonkeanac

Stump-tailed macaque

Assamese macaque

Formosan rock macaque

Celebes moor macaque

Booted macaque

Bonnet macaque

Lion-tailed macaque

Tonkean macaque

Fruit and seeds, young leaves, flowers and buds, other plant parts, gums, grass, clover, sprouts, roots, bark, resin, animal prey (insects and vertebrates), fungus, raid crops/dumps; most species, little field work; M. radiata eat temple offerings

Diurnal, arboreal and terrestrial, multimale/ multifemale, some 1 male + multifemale, group size 5-50; M. silenus: rarely on ground, but swim, as do many macaques

3.69-8.5 kg females, 4.86-12 kg males

Bynum, 1994; Krishnamani, 1994; Kurup & Kumar, 1993; Kuruville, 1980; Leutenegger & Cheverud, 1982; Richard et al., 1989; Silva & Downing, 1995; Wolfheim, 1983

M. fascicularis

M. nemestrina

M. nigra

M. sinica

Long-tailed or crab-eating macaque, or cynomolgus monkey

Pig-tailed macaque

Celebes or crested black macaque

Toque macaque

Fruit 67% (2-100%); flowers and buds 3% (0-68%); leaves 12% (1-62%); bark, roots, pith and other 6% (0-73%); grass 1%; fungi, resins and other 2%; prey items 11% (0-46%); M. fascicularis’ diet at one site was 51% temple offerings

Diurnal, arboreal and terrestrial, multimale/ multifemale, group size 10-90 individuals

M. fascicularis, M. sinica: 1.5-5.7 kg females, 3.9-8.39 kg males; M. nemestrina, M. nigra: 3.5-10.9 kg females, 6.2-14.5 kg males

Aldrich-Blake, 1980; Butynski, 1982; Caldecott, 1986a,b; Davies et al., 1983; Dittus, 1977; Hladik, 1975; Lucas & Corlett, 1991; MacKinnon & MacKinnon, 1980b; O’Brien & Kinnaird, 1997; Richard et al., 1989; Rodman, 1978; Silva & Downing, 1995; Sussman & Tattersall, 1981; Temerin et al., 1984; Ungar, 1995; Wheatley, 1982; 1987; Whitten & Whitten, 1982; Wolfheim, 1983; Yeager, 1996

M. fuscata

Japanese macaque

Fruit 47% (0-100%); flowers 5% (0-40%); leaves 22% (0-94%); herb/grass 6% (0-65%); roots, bark, twigs, and other 13% (0-95%); fungi, resins, and other 1% (0-18%); prey 9% (0-50%); winter diets high in seeds in cedar forest, high in winter buds in other habitats

Diurnal, arboreal and terrestrial, multimale/ multifemale group size 40-194 individuals

8.3-18.0 kg females, 11.0-18.0 kg males

Agetsuma, 1995a,b; Agetsuma & Nakagawa, 1998; Agetsuma & Noma, 1995; Hill, 1997; Iwamoto, 1982; Maruhashi, 1980; Nakagawa, 1997, 1989a; Suzuki, 1965

M. mulatta

M. sylvanus

Rhesus macaque

Barbary macaque

Fruit 24% (0-70%); flowers 5% (0-40%); leaves 47% (2-99%); bark, pith, roots, and other 11% (0-34%); herbs or grass 9%, (0-56%); fungi or sap 1%; prey 6% (0-66%); in some sites, M. sylvanus feed heavily on acorns and cedar leaves, cones, and cambium; M. mulatta eat temple offerings

Diurnal, multimale/ multifemale; M. sylvanus: group size 12-59 individuals; M. mulatta: group size 10-200 individuals

M. sylvanus: 10.2-11.2 kg females, 15.3-17.0 kg males; M. mulatta: 3.0-10.9 kg females, 5.08-10.9 kg males

Deag, 1983; Goldstein & Richard, 1989; Lindburg, 1977; Malik, 1986; Mehlman, 1988, 1989; Menard & Vallet, 1986; Richard, et al., 1989; Seth & Seth, 1986

M. thibetana

Tibetan macaque

Reproductive plant parts 35% (10-59%), ground-layer foods 22% (11-33%), leaves and other vegetative parts 43% (30-56%), prey not quantified; fed by humans near temples

Diurnal, mostly terrestrial, multimale/ multifemale

7.81-14.2 kg females, 10.7-13.0 kg males

Richard et al., 1989; Silva & Downing, 1995; Zhao & Deng, 1988; Zhao et al., 1991

Allenopithecus

A. nigroviridis

Allen’s swamp monkey

Fruit 81%; pith 2%; roots, flowers, nectar, animal prey (vertebrates and invertebrates) 17%; little studied

Diurnal, arboreal and terrestrial (swim), multimale/ multifemale, group size up to 40 individuals

3.7 kg female, 5.95 kg male

Gautier-Hion, 1988a,b; Zeeve, 1991

Cercocebus

C. agilisc

C. galeritus

C. torquatus

C. torquatus atys

Agile mangabey

Tana river mangabey

White-collared mangabey

Sooty mangabey

Fruit 76% (14-100%); leaves 12% (0-83%); flowers and buds 1% (0-5%); other plant parts 4% (0-50%); prey 8% (0-22%)

Diurnal, arboreal and terrestrial, multimale/ multifemale, group size 14-95 individuals

4.7-5.47 kg females, 9.2 - 10.8 kg males

Davies et al., 1983; Fleagle, 1988; Gautier-Hion, 1978, 1983; Gautier-Hion et al., 1980; Homewood, 1978; Mitani, 1989, 1991; Napier, 1981; Quris, 1975; Ross, 1991; Silva & Downing, 1995; Waser, 1984; Wolfheim, 1983

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

Cercopithecus

C. campbelli

C. dryasc

C. erythrogaster

C. erythrotis

C. hamlyni

C. mona

C. petaurista

C. preussic

C. sclateri

C. solatusc

Campbell’s guenon

Dryas guenon

White-throated guenon

Red-eared guenon

Owl-faced monkey

Mona monkey

Lesser spot-nosed guenon

Preuss’s monkey

Sclater’s guenon

Sun-tailed guenon

Fruit (and seeds) 54.6-90%, animal prey 5.0-25%, leaves 6.0 -18.9%, flowers 3-6%, gums 1.9-2.8%, shoots, mushrooms, nectar; eat more leaves when fruit is scarce; raid crops; many species little studied

Diurnal, arboreal (C. campbelli most terrestrial of all the guenons); 1 male, multifemale; group size: C. campbelli, C. hamlyni, C. preussi., C. solatus 2-15; C. erythrogaster, C. erythrotis, C. mona, C. petaurista, C. sclateri 4-35; C. sclateri multimale/ multifemale

1.8-4.5 kg females, 2.4-7.0 kg males

Bourliere et al., 1970; Caldecott, 1986a; Colyn, 1994; Napier, 1981; Oates, 1985; Silva & Downing, 1995; Wolfheim, 1983

C. ascanius

C. cephus

C. mitis

C. neglectus

C. nicitans

C. pogonias

C. wolfi

Red-tailed guenon

Mustached guenon

Blue monkey

DeBrazza’s monkey

Putty-nosed or greater

spot-nosed guenon

Crowned guenon

Wolf’s guenon

Fruit 67% (5-100%) (seed only 8%); leaves 15% (0-96%); flowers 4% (0-51%); bark, pith, and other 2% (0-30%), fungi 2% (0-39%), invertebrates 14% (0-45%); C. mitis eat bamboo; C. pogonias eat more prey when food is scarce; C. mitis in southern Africa: fruit 21%; leaves 27%; cambium, pith, twigs 46%; fungi 6%; invertebrates less than 1%

Diurnal; arboreal; 1 male-multifemale groups. (C. neglectus; some monogamous pairs); group size: C. ascanius, C. cephus, C. neglectus: 5-35; C. mitis, C. nictitans: 7-70; C. pogonias, C. wolfi: 1-19 individuals

C. ascanius, C. cephus, C. pogonias, C. wolfi: 2.4-3.4 kg females, 3.2-4.8 kg males; C. mitis, C. neglectus, C. nictitans: 2.7-8 kg females, 4-9.99 kg males

Beeson, 1989; Butynski, 1982, 1990; Colyn, 1994; Conklin et al., 1998; Cords, 1986, 1987; Gautier-Hion, 1978, 1980, 1983, 1988a; Gautier-Hion & Gautier, 1974, 1978, 1979; Gautier-Hion et al., 1980; Kaplin & Moermond, 1998; Kaplin et al., 1998; Lawes, 1991; Lawes et al., 1990, Moreno-Black & Maples, 1977; Napier, 1981; Rudran, 1978; Schlichte, 1978; Silva & Downing, 1995; Struhsaker, 1978b, 1980; Tutin et al. 1997; Wahome et al., 1993; Wolfheim, 1983; Wrangham et al., 1993

C. diana

Diana monkey

Fruit 39%; leaves 10%; flowers and buds 12%; bark, pith, and so on 1%; fungi 10%; invertebrates 31%; some reports claim more fruit or leaf

Diurnal, arboreal, 1 male-multifemale, group size 5-50 individuals

4.3-7.1 kg

Oates & Whitesides, 1990; Ross, 1991; Silva & Downing, 1995; Wachter et al., 1997; Wolfheim, 1983

C. lhoesti

L’Hoest’s monkey

Fruit 42% (22-80%), leaves 19%, herbs 35% (because are terrestrial), flowers 4%, prey 9%

Diurnal, terrestrial, somewhat arboreal, 1 male-multifemale, group size 5-17 individuals

3-4 kg females, 6-7 kg males

Colyn, 1994; Kaplin & Moermond, 1998; Silva & Downing, 1995; Wolfheim, 1983

Chlorocebus

C. (Cercopithecus) aethiops

Vervet, grivet, green, or tantalus monkey

Fruit 46%; leaves 23% (more mature leaves than young); flowers and buds 10%; bark, twig, or pith 6%; fungi or gums 3%; grass 1%; prey 13%, raid crops; take handouts

Diurnal, terrestrial and arboreal; multimale/ multifemale, group size 5-76 individuals

1.5-5.23 kg females, 3.1-8 kg males

Butynski, 1982; Davies et al., 1983; Dunbar & Dunbar, 1974; Galat & Galat-Luong, 1977, 1978; Harrison, 1983, 1984; Kavanagh, 1978; Moreno-Black & Maple, 1977; Napier, 1981; Silva & Downing, 1995; Whitten, 1983, 1988; Wolfheim, 1983; Wrangham & Waterman, 1981

Erythrocebus

E. patas

Patas monkey

Fruit 20% (5-34%); leaves 17% (6-27%); flowers and buds 36% (7-65%); stems, shoots and pith 3%; sap and gum 10%; prey 16% (except Kenya: fruit and seeds 6%, leaves 3%, flowers 7%, gum 39%, prey 43%).

Diurnal, mostly terrestrial, 1 male-multifemale, group size 5-34 individuals

4.08-7.1 kg females, 7.48-12.6 kg males

Isbell, 1998; Koster, 1985; Nakagawa, 1989b; Napier, 1981; Olson & Chism, 1984; Silva & Downing, 1995

Lophocebus

L. (Cercocebus) albigena

L. aterrimus

Grey-cheeked mangabey

Black mangabey

Fruit 69% (21-91%), up to 32% of which was figs; leaves 7% (0-65%); flowers and buds 4% (0-35%); bark, pith, or stems 3% (0-22%); other plant parts 1% (0-33%); prey 17% (2-44%); raid crops

Diurnal, arboreal, occasionally come to ground to drink, multimale/ multifemale, group size 6-28 individuals

L. albigena: 5.4-6.4 kg females, 6.8-8.98 kg males; L. aterrimus: 13.0-18.0 kg females, 21.0 kg male

Conklin-Brittain et al., 1998; Davies et al., 1983; Freeland, 1979; Gautier-Hion, 1977, 1978, 1983; Gautier-Hion et al., 1980; Horn, 1987; Mitani, 1991; Napier, 1981; Olupot et al., 1997; Olupot, 1998; Silva & Downing, 1995; Struhsaker, 1978b; Tutin et al., 1997; Waser, 1975, 1977, 1984

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

Mandrillus

M. leucophaeus

M. sphinx

Drill

Mandrill

Fruit 71% (42-99%); leaves 9%; flowers 4% (0-47%); stems, pith, or bark 5%; sap or gum 3%(0-26%); fungi 3% (0-52%); grass or crops 3% (0-23%); prey 6% (0-27%); roots; mandrills are seed predators and raid crops

Diurnal, arboreal and largely terrestrial; M. leucophaeus 1 male, multifemale (up to 20), group size 14-179; M. sphinx multimale/ multifemale

M. leucophaeus: 6.9-10.0 kg females, 17.0 kg male; M. sphinx: 11.5 kg female, 26.9 kg male

Fleagle, 1988; Gautier-Hion, 1978; Gautier-Hion et al., 1980; Harvey et al., 1987; Hoshino, 1985; Jouventin, 1975; Lahm, 1986; Norris, 1988; Rogers et al., 1996; Tutin et al., 1997; Wolfheim, 1983

Miopithecus

M. talapoin

Dwarf guenon or southern talapoin monkey

Fruit 52% (0-90%); leaves and shoots 5% (0-22%); flowers 2%; stems, pith or bark 4% (0-10%); grass or crops 8% (0-80%); prey 35% (0-50%); fungus; raid crops

Diurnal, arboreal, swim, multimale/ multifemale, group size 60 to 112 individuals

0.745-1.12 kg females, 1.0-1.38 kg males

Butynski, 1982; Gautier-Hion, 1971, 1973, 1988a; Gautier-Hion et al., 1980; Gonzalez-Kirchner, 1994; Napier, 1981; Wrangham et al., 1993

Papio hamadryas

P. h. anubis

P. h. cynocephalus

P. h. papio

P. h. ursinus

Olive baboon

Yellow baboon

Guinea baboon

Chacma baboon

Fruit and seeds 46% (0-86%); grass, sedge, herb 16% (0-97%); corms or roots 10% (0-85%); tree leaves 10% (0-61%); flowers 8% (0-27%); exudates or sap 4% (0-15%); other plant parts 6% (0-19%); prey 7% (0-72%); raid farms; beg from tourists; P. h. ursinus near sea eat crab

Diurnal, mostly terrestrial, part arboreal; multimale/ multifemale group size 7-200; P. h. papio: rudimentary fission-fusion

7.9-18.6 kg females, 14.1-43.6 kg males

Butynski, 1982; Byrne et al., 1993; Dunbar & Dunbar, 1974; Hamilton et al., 1978; Harding, 1976; Harvey et al., 1987; Moreno-Black & Maples, 1977; Napier, 1981; Norton et al., 1987; Post, 1982; Rhine et al., 1989; Ross, 1991; Rowell, 1966; Silva & Downing, 1995; Stacey, 1986; Whiten et al., 1990; Wolfheim, 1983

Exceptional Diets

Papio hamadryas hamadryas

Hamadryas baboon (5 subspecies)

Only one study found quantifying diet: fruit or pods with seeds 44%, fig fruit 13%, grass seeds 6%, grass plants 17%, leaves 10%, flowers 6%, roots 5%; prey consumption not quantified

Diurnal, terrestrial, fission-fusion, 1 male + multifemales, group size foraging 25-38, troops up to 750

12.0 kg female, 21.3 kg male

Boug et al., 1994; Fleagle, 1988; Wolfheim, 1983

Theropithecus gelada

Gelada baboon

Grass leaves 62% (0-93%), grass root or stem 13% (0-67%), grass seed 13% (0-70%), fruit 3% (0-7%), tree leaves 6% (0-62%), herbs and flowers 2% (0-8%), other roots or bulbs 1% (0-3%), prey 0.1%; raid crops

Diurnal, terrestrial, multimale/ multifemale; group size: 3-20 reproductive unit, band 30-300

11.7-13.6 kg females, 20.0 kg male

Dunbar & Dunbar, 1974; Dunbar, 1976, 1977; Fleagle, 1988; Iwamoto, 1979; Napier, 1981; Silva & Downing, 1995; Stammbach, 1987

aDiet format: mean (range).

bBody weights in ranges whenever possible; single numbers are not averages but indicate that only one individual of the species has been weighed in the wild.

cNo data available from the wild but assumed to be similar to congenerics.

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

FECAL ANALYSIS

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.

FOOD REMNANTS

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

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

TABLE 1-6 Ape Feeding Ecology

Scientific Name

Common Name

Dieta

Behavior

Body Weightb

References

The Small Apes

Hylobates

H. (Bunopithecus) hoolock

H. agilis

H. klossii

H. lar

H. pileatus

H. (Nomascus) gabriellaec

H. (Nomascus) leucogenysc

Hoolock or white-browed gibbon

Dark-handed or agile gibbon

Kloss’s gibbon

White-handed gibbon

Pileated or capped gibbon

Golden-cheeked gibbon

Chinese white-cheeked gibbon

All fruit 72% (38-100%) (30% is fig), flowers 6% (0-24%); leaves (and shoots, petiole, and other 15% (0-62%) (mostly young leaves), prey 7% (0-25%); honey; leaf galls

Diurnal, arboreal, monogamous with offspring, group size 2-12

4.4-8.6 kg females, 4.5-10 kg males

Ahsan, 1994; Aldrich-Blake, 1980; Alfred, 1992; Choudhury, 1990; Ellefson, 1974; Gittins, 1982; Islam & Feeroz, 1992; Leutenegger & Cheverud, 1982; MacKinnon & MacKinnon, 1980a, 1980b; Mitani, 1990; Mukhergee, 1986; Palombit, 1997; Raemaekers, 1978, 1979, 1984; Roonwal & Mohnot, 1977; Silva & Downing, 1995; Ungar, 1995; Whitten, 1982, 1984; Wolfheim, 1983

H. moloch

H. muelleri

Silvery Javan gibbon

Mueller’s Bornean gibbon

Fruit 60% (range 56-62%), flowers 2% (0-4%), leaves 37% (32-44%), prey 1% (0-2%)

Same

5-8 kg

Kappeler, 1984; Leighton, 1987; Robbins et al., 1991; Rodman, 1978; Silva & Downing, 1995

H. (Nomascus) concolor

Black gibbon

Fruits 21%, flowers 7%, leaves 11%, leaf buds and shoots 61%, bamboo

Same

4.5-9 kg

Lan, 1993; Liu et al., 1989; Sheeran, 1993; Sheeran & Mootnick, 1995; Yang & Zuu, 1990

H.(Symphalangus) syndactylus

Siamang

Fruit 40% (6-59%) (figs are 28%), flowers 6% (0-32%), leaves 49% (24-70%) (42% young leaves), prey 5%

Same

9-11.14 kg females, 10.4-14.77 kg males

Aldrich-Blake, 1980; Chivers, 1974, 1977; Chivers et al., 1975; Curtin & Chivers, 1978; MacKinnon & MacKinnon, 1978, 1980b; Palombit, 1997; Raemaekers, 1978, 1979, 1984; Silva & Downing, 1995

The Great Apes

Pongo

P. abelii

Sumatran orangutan

Fruit 74% (22-98%) (seeds were 26% in the fruit category), leaves and shoots 15% (7-42%), bark and wood 4% (0-16%), insects 5% (0-40%, includes search time), other (including flowers) 2%, eat succulent fruits and large fruits with hard husk

Diurnal, arboreal mostly, males solitary, females travel with offspring, group size 1-3 individuals

33-45 kg females, 75-91 kg males

MacKinnon, 1974; Rijksen, 1978 ; Ungar, 1995; Wolfheim, 1983

P. pygmaeus

Borneo orangutan

Fruit 62% (0-100%), flowers 4% (0-60%), leaves and shoots 19% (0-77%), pith 1% (0-22%), bark and wood 11% (0-73%), insects 2% (0-27%), other 3% (0-41%)

Same

33-45 kg females, 75-91 kg males

Hamilton & Galdikas, 1994, Galdikas & Teleki, 1981; Knott, 1999, 1998, 1996; Leighton, 1993; MacKinnon, 1974; Rodman, 1977, 1978, 1988; Silva & Downing, 1995; Suzuki, 1994; Wheatley, 1982

Gorilla gorilla

G. g. beringei

Mountain gorilla

Pith, shoots, leaves and stems of herbs and shrubs 91% (range 85-96%); wood or bark 2% (0-7%) roots 1% (0-4%); flowers 2% (0-3%); fruit 1% (0-2%); dung 0.5% (0-2%); prey 1% (0-1%); fungus and miscellaneous 2% (0-5%)

1 male (occasionally 2), multifemale group size about 9 individuals

83-98 kg females, 159-278 kg males

Fossey, 1974; Fossey & Harcourt, 1977; Goodall, 1977; Silva & Downing, 1995; Vedder, 1984; Watts, 1984, 1996; Wolfheim, 1983

G. g. gorilla

Western lowland gorilla

Pith, shoots, and stems of herbs and shrubs 17% (7-43%); leaves 21% (6-34%); bark 5% (0-32%); roots 1% (0-4%); flowers 1% (0-6%); seeds 4% (1-13%); fruit 48% (17-68%); prey 1% (0-4%); miscellaneous 2% (0-11%)

Diurnal, terrestrial, some arboreal; 1 male, multifemale; group size 3-21

72 kg female, 139-170 kg males

Kuroda, 1992; Kuroda et al., 1996, Nishihara, 1992, 1995; Remis, 1995, 1997; Rodgers et al., 1990; Sabater Pi, 1966, 1977; Tutin 1996; Tutin et al., 1984, 1991, 1997; Tutin & Fernandez, 1993; Williamson et al., 1990

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

G. g. graueri

Eastern lowland gorilla

Pith, shoots, and stems of herbs and shrubs 19% (11-33%), leaves 41% (17-51%), bark 13% (0-29%), root 2% (0-5%), flowers 2% (0-3%), fruit 23% (9-47%), miscellaneous 1% (0-29%)

Diurnal, arboreal and terrestrial, 1 male, multifemale group

71-75 kg females, 140-168 kg males

Casimir, 1975; Goodall, 1977; Silva & Downing, 1995; Yamagiwa et al., 1992, 1994, 1996

Pan

P. paniscus

Bonobo or pygmy chimpanzee

Fruit 52% (1-100%), flower 2% (0-7%), seed 3% (0-6%), leaves 14% (0-28%), terrestrial herbaceous vegetation 24% (0-55%), bark or root 2% (0-11%), prey 2% (0-3%), fungus, honey; do not hunt or eat monkeys

Diurnal, arboreal and terrestrial, multimale/ multifemale group size 6-15 foraging parties, communities 50-120 individuals

31-34 kg females, 39 kg male

Badrian et al., 1981; Badrian & Malenky, 1984; Hashimoto et al., 1998; Kano, 1983; Kano & Mulavwa, 1984; Malenky & Stiles, 1991; Nishida a & Hiraiwa-Hasegawa, 1987; Silva & Downing, 1995; Uehara, 1990; Wolfheim, 1983

P. troglodytes

Chimpanzee

Fruit 64% (19-99%), seeds 3% (0-30%); flowers 2% (0-18%), leaves 16% (0-56%) (mostly young), pith, stem, and stalk 7% (0-27%), bark/ cambium 2% (0-26%), gum, gall, root, wood, fungus, miscellaneous 2% (0-41%), and all prey items 4% (0-28%); will eat monkeys

Diurnal; arboreal and terrestrial; multimale/ multifemale group size 7-25 females, 5-16 males, fission-fusion

32-68 kg females, 40-80 kg males

Conklin-Brittain et al., 1998; Galdikas & Teleki, 1981; Ghiglieri, 1984; Goodall, 1996; Hladik, 1973, 1977; Isabirye-Basuta, 1989; Kuroda, 1992; Kuroda, et al., 1996; Matsumoto-Oda & Hayashi, 1999; McGrew et al., 1981; Newton-Fisher, 1999; Peters & O’Brien, 1981; Sabater-Pi, 1979; Sugiyama & Koman, 1987; Suzuki, 1969; Tutin & Fernandez, 1993; Tutin et al., 1984, 1991, 1997; van Lanwick-Goodall, 1968; Wrangham, 1977; Wrangham et al., 1998; Yamagiwa et al., 1992

aDiet format: mean (range).

bBody weights in ranges whenever possible; single numbers are not averages but indicate that only one individual of the species has been weighed in the wild.

cNo data available from the wild but assumed to be similar to congenerics.

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).

Reporting Feeding Behavior

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

FEEDING TIME

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.

MASS OF FOOD AS PERCENTAGE OF TOTAL DIET MASS

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.

Feeding-Ecology Tables

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

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

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.

PLANT-FEEDING STRATEGIES

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.

INSECT FORAGING AND FEEDING

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.

ADDITIONAL CONSIDERATIONS

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.

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

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.

HOW TO USE THIS INFORMATION

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.

DIGESTIVE STRATEGIES

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

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

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).

Faunivores

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).

Frugivores

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

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

Primate Gastrointestinal Tracts

FIGURE 1-1 Tarsier

FIGURE 1-2 Squirrel Monkey

Stevens and Hume, 1995

Reprinted with the permission of Cambridge University Press

FIGURE 1-3 Night Monkey

Stevens and Hume, 1995

Reprinted with the permission of Cambridge University Press

FIGURE 1-4 Wolly Monkey

Stevens and Hume, 1995

Reprinted with the permission of Cambridge University Press

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

Primate Gastrointestinal Tracts

FIGURE 1-5 Vervet Monkey

Stevens and Hume, 1995

Reprinted with the permission of Cambridge University Press

FIGURE 1-6 Macaque

Stevens and Hume, 1995

Reprinted with the permission of Cambridge University Press

FIGURE 1-7 Baboon

Stevens and Hume, 1995

Reprinted with the permission of Cambridge University Press

FIGURE 1-8 Bush Baby

Stevens and Hume, 1995

Reprinted with the permission of Cambridge University Press

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

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).

Folivores

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

TABLE 1-7 Form of Foregut in Genera of Subfamily Colobinae

Form of Foregut

Genus

Source

Presaccus absent (tripartite)

Colobus

Polack, 1908; Stevens and Hume, 1995

 

Semnopithecus

Ayer, 1948

Trachypithecus

Otto, 1835; Kuhn, 1964

Presbytis

Caton, 1990

Presaccus present (quadripartite)

Procolobus

Hill, 1952; Kuhn, 1964

 

Rhinopithecus

Ye et al., 1983

Pygathrix

Edwards, 1995; Höllihn, 1971; Pilliet and Boulart, 1898

Nasalis

Höllihn, 1971; Langer, 1988; Martin, 1837

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.

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

Primate Gastrointestinal Tracts

FIGURE 1-9 Northern Douc Langur

Edwards, 1995

FIGURE 1-10 Columbus Monkey

Stevens and Hume, 1995

Reprinted with the permission of Cambridge University Press

FIGURE 1-10 Chimpanzee

Stevens and Hume, 1995

Reprinted with the permission of Cambridge University Press

FIGURE 1-10 Orangutan

Stevens and Hume, 1995

Reprinted with the permission of Cambridge University Press

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

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).

IMPLICATIONS FOR FEEDING PROGRAMS IN CAPTIVITY

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-

Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

TABLE 1-8 Examples of Food Consumed by Primates in Zoos and in the Wild (Oftedal and Allen, 1997)

Food Type

Dry Matter, %

Crude Protein, %

Fiber Fractionsa

 

NDF, %

ADF, %

AL, %

Ca, %

P, %

Market produce used in primate dietsb

Apples

12.8

2.3

17.4

12.6

3.8

0.0

0.0

Green beans

10.7

17.9

28.0

25.1

2.2

0.4

0.4

Cabbage

8.9

14.7

20.6

21.9

1.7

0.6

0.3

Carrots

12.2

7.7

15.2

16.5

1.5

0.2

0.4

Kale

12.3

32.5

19.3

24.7

4.6

0.9

0.4

Foods eaten in the wild by red howler monkeys (Alouatta seniculus)c

Flowers

25.1

14.4

50.6

35.8

17.1

0.5

0.3

Fruits

23.7

7.0

53.8

35.2

16.6

0.6

0.2

Mature leaves

36.5

16.6

57.2

40.5

20.4

1.4

0.1

Young leaves

32.2

21.2

54.4

36.4

21.1

0.3

0.3

Note: all values, except dry matter, are expressed on a dry matter basis.

aNDF = neutral detergent fiber; ADF = acid detergent fiber; AL = acid lignin.

bAll data except calcium and phosphorus from Oftedal et al., 1982; calcium and phosphorus values from USDA Standard Release 14.

cUnpublished data of M.S. Edwards, S.D. Crissey, O.T. Oftedal, and R. Rudran, as cited in Oftedal, 1991.

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).

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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×

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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
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Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
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Page 22
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 23
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 24
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 25
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 26
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 27
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 28
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 29
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 30
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 31
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 32
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 33
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 34
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 35
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 36
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 37
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 38
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 39
Suggested Citation:"1 Feeding Ecology, Digestive Strategies, and Implications for Feeding Programs in Captivity." National Research Council. 2003. Nutrient Requirements of Nonhuman Primates: Second Revised Edition. Washington, DC: The National Academies Press. doi: 10.17226/9826.
×
Page 40
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This new release presents the wealth of information gleaned about nonhuman primates nutrition since the previous edition was published in 1978. With expanded coverage of natural dietary habits, gastrointestinal anatomy and physiology, and the nutrient needs of species that have been difficult to maintain in captivity, it explores the impact on nutrition of physiological and life-stage considerations: infancy, weaning, immune function, obesity, aging, and more. The committee also discusses issues of environmental enrichment such as opportunities for foraging.

Based on the world's scientific literature and input from authoritative sources, the book provides best estimates of nutrient requirements. The volume covers requirements for energy: carbohydrates, including the role of dietary fiber; proteins and amino acids; fats and fatty acids; minerals, fat-soluble and water-soluble vitamins; and water. The book also analyzes the composition of important foods and feed ingredients and offers guidelines on feed processing and diet formulation.

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