Old World monkeys

Last modified on May 26, 2010

Taxonomy    Anatomy    Physiology    Behavior

Uses in Research    Common Diseases

Taxonomy

Suborder Anthropoidea
    Infraorder Catarrhini, 21 genera (narrow, downward-facing nostrils, diurnal, hindlimbs longer than forelimbs, short tails, flat nails, ischial callosities){4048}
        Superfamily Cercopithecoidea
            Family Cercopithecidae

Subfamily Cercopithecinae (molars with low rounded cusps, closely-spaced orbits, frugivorous, have cheek pouches, short tails, arms and legs nearly the same length, well-developed thumbs)

Cercopithecus neglectus (deBrazza's monkeys), 
which are seriously endangered in Kenya.{4048}

1. Macaques (20 species of Macaca; primarily Asian except for the Barbary macaque M. sylvanus)

2. Baboons (8 species including Papio, Mandrillus, Theropithecus, Africa)

3. Mangabeys (5 species including Cercocebus, Lophocebus)

4. Guenons (24 species including Chlorocebus and Cercopithecus) (from the French word for "fright", a characteristic grimace) 
5. Patas monkey (Erythrocebus patas)

6. Talapoins (Miopithecus)

 

Subfamily Colobinae (leaf-monkeys, folivorous, shearing molars, multi-chamber stomachs, widely spaced orbits, long legs, short/absent thumbs, very long tails, no cheek pouches)

1. African colobus monkeys (Colobus and Procolobus) Colobus guereza gallarum

Colobus guereza gallarum at left.

 

2. Asian langurs (Presbytis, Trachypithecus, Semnopithecus, Nasalis larvatus, Simias, Pygathrix, Rhinopithecus)

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Macaque Anatomy

Macaca fuscataMacaca fuscata, the Japanese macaque, has a beard, long whiskers, and long dense fur. While traditionally protected in Japan, its habitat is being deforested and people are killing them because of crop destruction.

 

 

 

 

Macaca nigra, at right, is the Celebes ape.Macaca nigra Note the crown-shaped mass of black hair on top of the head. This species develops diabetes mellitus spontaneously.{2765}

Bonnet macaques (M. radiata) inhabit southern India, in contrast to rhesus (M. mulatta) which live in the north of the country. The species is considered endangered{4018}. 

Rhesus macaques are considered sacred by the Hindus.{4048} The species is found from sea level to altitudes of 2500 meters and in all types of habitat. Crab-eating macaques (cynomolgus or M. fascicularis) seem to prefer coastal mangrove areas, where they eat shellfish, crabs and crustaceans exposed by the tides. Both species are good swimmers. A group of cynos was introduced to Mauritius (560 miles east of Madagascar in the southwest Indian Ocean) in the 16th century by Dutch sailors, and now numbers 25,000-35,000.{4048}

Guenon Taxonomy and Anatomy

In the genus Chlorocebus there are four allopatric species: C. sabaeus (the green monkey found in Senegal and Ghana, C. tantalus, C. aethiops (the grivet, found in Sudan and Ethiopia), and C. pygerythrus (the vervet, found in Ethiopia, Angola, and South Africa). Many authorities consider them all subspecies of C. aethiops. They differ from Cercopithecus in some minor cephalic bone structure. Some 17th-century escaped pets (C. sabaeus) have populated islands in the West Indies.{4048}

The genus Cercopithecus includes 20 species, among which are the De Brazza's monkey (C. neglectus), L'hoest's monkey (C. lhoesti), Diana monkey (C. diana) and many others.{4048} Erythrocebus patas is a gentle monkey of larger size than most guenons{4163}.

Guenons have cheek pouches, roundish heads, slender bodies, long hind limbs and a long tail. The tail of young animals is prehensile, but adults use it only for balance. Nostrils are close together and they often have beards. Ischial callosities are much smaller than those of macaques and baboons, and there is no sexual swelling during estrus{4163}. Guenons prefer riverine woodland but are limited only by the need for water and sleeping trees (they are diurnal). They do well in marginal habitats such as secondary growth, agricultural areas and swamps. They are partly terrestrial and are good swimmers.{4048}

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Macaque Physiology

Papio cynocephalus anubisPapio cynocephalus anubis at right.

For more information on nutrient requirements of rhesus macaques, click here to go to the Resource Management section. Macaques are largely frugivorous, and they also eat nuts, flowers, bark, insects, eggs and small vertebrates.{4048} In captivity, semipurified diets meet most of the nutritional needs of Old World monkeys. Information on mineral needs is somewhat lacking, as is knowledge of the nutrition of species other than common laboratory species. Supplementation is unnecessary as long as a complete diet is provided and used within 90 days of the milling date. 

Vitamin C is required at a dose of 25mg/kg for a growing rhesus monkey. Caloric requirements range from 100-300 kCal/kg for infants to 50-120 kCal/kg for adults. This translates to approximately 2-3 times the amount of food on a per kg basis needed by young growing animals.{2765} In 1990 scurvy was diagnosed in 19 rhesus monkeys (Macaca mulatta) and four squirrel monkeys (Saimiri sciureus) from a colony of nonhuman primates maintained on a commercial diet. Signs of weakness, reluctance to move, gingival hemorrhage, bruising, proximal and distal metaphyseal fractures, weight loss and anemia appeared in juvenile and young adult rhesus monkeys over a 2 week period. Clinical signs subsided after 5 days of vitamin C therapy. At the same time, cephalhematoma and weakness developed in squirrel monkeys, which failed to respond to treatment. These cases were associated with manufacturer's admitted error in preparation of the commercially prepared monkey diet{3718}.

Most primates require 1ml water/kCal gross energy consumed per day. For an adult rhesus macaque, approximately 80 ml/kg/day is required.{2765}

Baboons have three blood groups: A, B and AB (CL Davis 2001).

Reproduction

Menarche occurs at around 2 years of age. All Old World monkeys menstruate, and many show external signs of it. The pigtailed macaque and baboon also have marked changes in their perineal skin during their menstrual cycle. Males generally mature about a year later (age 4-7) than females (2½-4 years{4048}){2765}. In the wild, females have breeding seasons with several estrous cycles; the cycles average 28 days for rhesus and 24-52 days for cynos. Estrus lasts about 9 days. There is usually a birth every two years; in captivity a rhesus may become pregnant again soon after giving birth. Female rhesus undergo menopause at around age 25.{4048}

For mating, the female is generally taken to the male's cage. Pregnancy can be palpated as early as 24 days; hormone assays and ultrasound can also be used. Nursery rearing techniques have been well established, if they are needed. During the first 24 hours infants are fed 5% dextrose, and switched to human formula after that. Infants can learn to self-feed in a week, and be started on cereal mixed with formula after 3 weeks.{2765

Species{2765} Rhesus Cyno Bonnet Baboon
Menarche, yrs 2 2 2.75 2
Female sexual maturity, yrs 3-4 3-4 5 5-6
Estrous cycle length, days 28 24-52 28 28
Gestation, days 161-175 161-175 161-174 164-186
Birthweight, kg 0.4-0.55 0.4-0.55   0.4-0.55
Weaning age, months 1-9 1-9 6  

Reproductive physiology of the bonnet macaque (M. radiata) has been described. Menarche occurs at around 32 months of age, but there is no obvious "sex skin". Age at first conception is usually 5 years. Gestation is 168 (161-174) days. These macaques breed year-round, with most during the July-October rainy season in India. In the laboratory, housing the animals in humidified (55-65%) rooms prevented "summer amenorrhea". Cycles are much more regular in the laboratory if a male is housed in the same room with the females. Unlike other macaques, bonnet macaques exhibit a cervical mucus discharge from days 8-12 of their 28-day cycle, with ovulation occurring on days 11 or 12. This mucus discharge corresponds to levels of estradiol 17ß of over 200pg/ml. For use in breeding programs, normally cycling females with estradiol 17ß levels of >200pg/ml on days 9-10 become pregnant 80-85% of the time within 3 exposures to a proven fertile male. Females do not cycle during lactation; infants are weaned at 6 months of age.{4018}

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Guenon Physiology

Average weight of adult male Chlorocebus is 7.0 kg, and of females 5.6 kg. Males have a light red penis and a blue scrotum. They eat fruit, cultivated plants, insects, crustaceans, bird eggs and small vertebrates; in some places such as Senegal they hunt for crabs. 

The estrous cycle lasts about 30 days, and gestation is 5½ months. Females usually have young every year. Weaning is completed at 8.5 months of age.{4048}

Macaque Behavior

In the wild, macaques generally live in large groups of up to a couple hundred animals. Females stay in their families, and males stay at the periphery or live in all-male groups. Social status of the young is dependent upon the rank of their mothers.{4048}

Vocalizations include a shrill bark for alarm, barking or screeching in response to aggression, screaming when under attack, a growl of aggression, and a squawk for surprise.{4048}

In laboratory-reared macaques, behavioral testing is commonly performed using the Brazelton Neonatal Assessment Scale, which is discussed in the experimental methodology section.

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Guenon Behavior

Guenons live in large groups with several adults of each sex in the group. The social hierarchy revolves around females. They are territorial, but generally avoid serious conflicts.{4048}

Uses in Research

Obviously, uses of NHPs in research are many and varied. Some specific examples from the recent literature are:

Cercocebus atys, the sooty mangabey, is naturally susceptible to leprosy.{2765} They may be asymptomatic carriers of SIV. Their endangered status complicates extensive use for research.{4163} An article in Nature suggested that human HIV-2 originated in sooty mangabeys (CL Davis 2001).

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Common diseases

Enteric

Enteric disease is the primary cause of morbidity and mortality in colonies, particularly caused by Shigella flexneri, S. sonnei and S. boydii. Clinical signs vary; acute colitis may progress to dysentery (loss of necrotic colonic mucosa), but a more common picture is subacute to chronic diarrhea occurring intermittently. Young animals become carriers. Campylobacter jejuni is another cause of primate diarrhea, particularly in patas monkeys. It may respond to 7-14 days of erythromycin. Salmonella localizes in the ileum, and is less common in primates. Diarrhea, acute deaths and abortion may be caused by Yersinia pseudotuberculosis and Y. enterocolitica, for which wild birds and rodents are reservoirs. Contaminated food may be a source of infection for primates. Cold enrichment of cultures is needed to confirm the presence of the organism. Treatment with chloramphenicol, trimethoprim-sulfa, gentamicin or kanamycin may be effective.{2765}

Enteric infections of macaques{4762}

Agent

Clinical signs

Treatment

Shigella

Diarrhea, blood, mucus; depression, hunched

Enrofloxacin 5mg/kg, fluids

Campylobacter

Mucohemorrhagic diarrhea, hyponatremia, hypochloremia, acidosis

Usually self-limiting

Salmonella

Diarrhea, fever

Usually multidrug resistant, carriers

Yersinia

Diarrhea, vomiting, blood-stained feces, depression, pain, dehydration, abortion/stillbirths

Usually unsuccessful, try chloramphenicol 100mg/kg div TID

Helicobacter

Anorexia, vomiting, or chronic diarrhea

Triple: amoxicillin, metronidazole, bismuth

Lawsonia intracellularis

Mild or transient diarrhea, abdominal distension, anemia; or may die with no signs (reported only once?)

None

Giardia

Diarrhea, vomiting, may be steatorrhea

Metronidazole, furozolidine

Entamoeba histolytica

Worse in young and NWM; anorexia, vomiting, severe diarrhea/hemorrhage, ulcerative colitis, flask-shaped ulcers, amebic abscesses in other sites

Metronidazole, diiodohydroxyquin, tetracycline, chloroquin, chloramphenicol, paromomycin

Cryptosporidium

Usually in immunocompromised (SIV)-infected; intractable, profuse, watery diarrhea, ADR, mesenteric ln enlargement, villous atrophy

Supportive

Balantidium coli

ADR, watery diarrhea, tenesmus, rectal prolapse

Metronidazole, tetracycline, diiodohydroxyquin

Strongyloides fulleborni or stercoralis

Diarrhea +/- hemorrhage +/- mucus

Ivermectin, thiabendazole, mebendazole, levamisole, pyrantel pamoate

Oesophagostomum

Weight loss, diarrhea, poor doer

Thiabendazole, levamisole, mebendazole

Ascaris lumbricoides

Subclinical

Mebendazole, pyrantel pamoate

Trichuris spp.

Anorexia, mucoid or watery diarrhea

Mebendazole, dichlorvos, levamisole, flubendazole

Folic acid deficiency

Megaloblastic anemia, weight loss, petechia, gingivitis, diarrhea

Nutritional

 

Acute gastric dilatation (bloat) occasionally occurs. Potential causes include poor husbandry or perhaps an infectious agent such as Clostridium perfringens. Animals in restraint chairs bloat more frequently than those kept in corrals or pens. This is an emergency situation; treatment includes passing a stomach tube and supportive care. Animals recovering from bloat should be placed on a restricted diet for 7-10 days.{2765}

NHPs ingest foreign bodies and may also develop trichobezoars, both of which cause diarrhea, anorexia and weight loss.{2765}

Polychlorinated biphenyls (PCBs) are a component of some concrete sealers. Old World monkeys housed on such concrete surfaces have developed photophobia, palpebral edema, alopecia, gingivitis, periodontitis, diarrhea and emaciation. A characteristic squint is produced by distension of the ducts of the Meibomian glands.{2765}

Respiratory

Respiratory diseases of macaques {4762}
Agent Clinical signs Treatment
Streptococcus pneumoniae

Panophthalmitis, conjunctivitis; lethargy, incoordination, head pressing; depressed reflexes; ataxia, tremors, nuchal rigidity, nystagmus; peracute death

Penicillin, ampicillin, ceftriaxone

Klebsiella pneumoniae

Anorexia, adipsia; listlessness, reluctance to move; peracute death. Pneumonia, meningitis, air sacculitis, septicemia, peritonitis, enteritis in all NHP species.

Very difficult, fulminating.

Nocardia asteroides

Dyspnea, epistaxis; chronic weight loss, abdominal distension; chronic diarrhea; lethargy; coma. Looks like TB: lungs, granulomas

None

Moraxella catarrhalis

Epistaxis, mucohemorrhagic nasal discharge, sneezing, periorbital swelling in cynos

Long-acting penicillin

Mycobacterium tuberculosis or bovis

Cough, fatigue, dyspnea, weight loss, cutaneous abscesses, liver and spleen enlargement

None

Morbillivirus (measles)

Rash, facial hyperemia, cough, conjunctivitis, pneumonia; gastroenteritis

None

The second most common cause of morbidity and mortality in primate colonies is respiratory disease (at least it was in 1984!). Pneumonia causes facial cyanosis, and animals sit upright holding onto the cage bars to assist in respiration. Rapid, shallow respiration is observed, with radiographic consolidation. Viral infections such as measles should be ruled out. Bacterial causes include Klebsiella pneumoniae, Streptococcus pneumoniae (which may also cause meningitis), Bordetella bronchiseptica, and Pasteurella multocida.{2765}  

Tetanus causes early signs of depression, dysphagia, stiffening and adduction of the pectoral limbs and a hopping gait. Trismus, piloerection, and extensor rigidity follow; risus sardonicus is the term for facial spasm that leads to flattening of the ears. Death is due to respiratory paralysis. Tetanus antitoxin and treatment of local wounds is essential; routine immunization should be considered, with two doses given 4-12 months apart.{2765}

Tuberculosis poses the most insidious threat to colonies of Old World monkeys. Infection with M. tuberculosis or M. bovis is progressive and usually fatal. It is not a naturally-occurring disease of NHPs, but is contracted from humans. Route of exposure is inhalation. Delayed hypersensitivity, the basis of the intradermal test, takes at least 3 weeks to develop after exposure. A 90-day quarantine with TB testing using mammalian old tuberculin (1500 units, but who assays it?) every 2 weeks is the method of choice for detection. M. avium and related organisms of the MAIS group cause granulomatous enteritis and mesenteric lymphadenitis, although this is rare and sporadic.{2765}

Parasites: In NHPs with diarrhea, large numbers of protozoans are frequently seen, particularly Trichomonas and Giardia. They may be the cause, but are more likely an incidental finding or a sequel to the initial cause. Oral metronidazole (50mg/kg sid x 5-10 days) is helpful. Animals imported from other countries may be infected with malaria. African primates may be infected with a malarial organism called Hepatocystis kochi. Pneumocystis carinii is occasionally found in immunosuppressed macaques with pneumonia. Nematodes such as whipworms (Trichuris) are frequently found in baboons. Strongyloides fulleborni, which can be contracted through ingestion, skin penetration, or autoinfection, can cause serious outbreaks in NHPs. The most common nematode of Old World NHPs, though, is Oesophagostomum. Animals are infected through ingestion, and the larvae penetrate the large intestine producing nodules which rupture. Thiabendazole kills mature worms in the intestine, but not the larvae in the nodules. Anatrichosoma cutaneum is found in the nasal mucosa of the rhesus; usually the infection is inapparent, but cutaneous eruptions may be noticed in the hands, feet and face of cynomolgus monkeys. Finally, the lung mite, Pneumonyssus simicola, is a very common find in wild-caught NHPs, although mild to moderate infestations do not cause severe disease.{2765

Fungal: Candida albicans, a skin saprophyte, causes white plaques on the dorsum of the tongue and oral cavity. Coccidioides immitis, found the dry Southwest US, infects animals via spore inhalation and has infected Old World monkeys.{2765}

Viral: Too often viruses that cause no signs of disease in their natural hosts cause fatal outbreaks in other species. Examples from Old World primates and man include Marburg/Ebola, measles, herpesvirus B, simian hemorrhagic fever, yellow fever, and simian varicella virus.{2765}

Any pox-like disease is reportable to the CDC. In Old World monkeys, monkeypox causes outbreaks of high morbidity but low mortality. Yaba in macaques and baboons causes subcutaneous nodules 4-6cm in diameter that resolve spontaneously. OrTeCa pox (BEMP) causes raised nodules .5-1.5cm in diameter involving the epidermis, but not vesiculating. All these are zoonotic.{2765}

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©1999, Janet Becker Rodgers, DVM, MS, DipACLAM, MRCVS

All rights reserved.

Comments? Send an email to janet.rodgers@vet.ox.ac.uk