Squirrel Monkeys (Saimiri)

Last modified on September 6, 2010

Taxonomy

Reproduction

Anatomy

Normal biology

    Steroid resistance

Housing and husbandry

    Common diseases

Research techniques

    Behavioral research

    Parasite research

Taxonomy

There is debate over the proper taxonomy of squirrel monkeys. Some taxonomists place them in their own family, Saimurinae{4488}. Nowak{4048} lists five genera (S. boliviensis, S. vanzolinii, S. sciureus, S. ustus and S. oerstedii) but reports that based on teeth, haircoat, biochemical data and behavior, S. sciureus and S. oerstedii may be the only two. The most commonly used phenotypic characteristic used for identification is the patch of white over the eyes. S. sciureus are called "gothic arch" monkeys because the white hair over their eyes is a pointed arch; they are usually gray-green agouti elsewhere. Gothic arch monkeys originate from countries north of the Amazon river, i.e. Brazil, Colombia and the Guianas. S. boliviensis are "roman arch" because their white patches are rounded; they usually have black crowns. Roman arch monkeys come from south of the Amazon river, usually Peru and Bolivia{4488}. Precise identification requires karyotyping. All squirrel monkeys have 44 (diploid) chromosomes. The acrocentric chromosome number varies from 5 to 7. Different types respond differently to both natural and experimentally-induced infection. Also, interbreeding can result in infertile gametes due to the pericentric inversions that result in different karyotypes.{4071}{4762}

Reproduction

Because understanding of squirrel monkey biology, specifically reproduction, was inadequate, the US supported several research endeavors in order to maintain the species for use in research. In 1980 the NIH awarded a grant to the U. of South Alabama to establish the Squirrel Monkey Breeding and Research Resource (SMBRR), currently the only federally supported breeding resource in the US. They breed several types, including S. boliviensis boliviensis, S. boliviensis peruviensis, and S. sciureus sciureus.{4071}

In the wild, squirrel monkeys congregate in large multimale/multifemale groups of up to 50 or more, varying with the habitat. Groups disperse during the day to forage, rejoin for a rest period, then forage again until gathering for the night. In captivity, only one or two males should be housed with a group because of aggression. Four types of vocalizations have been recorded: smooth chucks (affiliative), bent mast chucks (caller ID), peeps (spread out to forage) and twitters (troop movement). One unique feature of squirrel monkey behavior is seasonal sexual segregation; males remain in the periphery until breeding season. Breeding season is a distinct 3-month season. Both sexes gain weight although the "fatted male" is associated with increased spermatogenesis. Birth season 6 months later occurs when food is most available, and may be synchronized in the group. When moved to the Northern hemisphere, humidity and photoperiod are thought to influence a change in breeding season. Infants spend up to 30% of time with allomothers during their first 6 months. Usually allomothers are young adult females 4-6 years old.{4074,4762}

In the laboratory, breeding is usually done by forming groups. Individual mating schemes in which the male and female are placed together for several hours are not generally successful.{4488}

Ovulation can be induced in females with 4 days of FSH followed by HCG 12 hours later, and laparoscopic harvest. Semen can be collected by training, vibrostimulation or electroejaculation.{4072} 

With practice, pregnancy can be determined by palpation at 28-35 days. The fetus will be marble-sized. Vaginal cytology, chorionic gonadotropin or ultrasound are also effective. The females will be visually obvious as pregnant by 10 weeks. Birth almost always occurs at night; a female found with signs of labor during the day is assumed to require C section.{4488} Squirrel monkey infants are very prone to hypothermia and must be kept at 80°F or higher for the first few weeks.{4762} Dystocia is relatively common because of their large head size and large fetal size. A dam that is weak or depressed, fetal distress evidenced by a heart rate <180bpm, failure to progress labor in 2 hours, or breach presentation are indications for C section. Since the dam frequently rejects the newborn, foster or nursery rearing can be achieved.{4072} However, members of a group will vigorously defend a weak infant, presenting management problems.{4488}

At birth, infants typically weigh 100 grams, approximately 17% of their mother's weight. A healthy infant will actively participate in its own delivery; when the shoulders and arms emerge, it grabs onto the mother's abdomen and pulls itself out.{4762} They cling to the mother immediately. They are completely dependent upon their mothers for sustenance for 6-8 weeks, and will continue to nurse for 3-4 more months. From 6 months until 2-3 years of age young squirrel monkeys form peer groups.{4488}

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Anatomy

Males from different regions vary considerably in size. Roman arch males from Peru are the smallest, ranging from 700-900 grams non-fatted. Roman arch males from Bolivia are the largest, ranging from 800-1200 grams non-fatted.{4488}

Females are less variable, ranging from 550-750 grams. They reach adult size and reproductive maturity in 3.5 years, whereas males require 5 years. Females remain reproductively active until about 16 years of age. They usually reproduce only once every other year. In captivity, squirrel monkeys can live for more than 20 years.{4488}

Gender identification: females often have a false scrotum. Infant females have an enlarged clitoris that can be mistaken for a penis. The best guide is to look for the vaginal slit.{4488}

Normal biology

Steroid Resistance

It was reported in 1968 that squirrel monkeys have high circulating levels of cortisol, compared with humans. It appears that they have a normal pituitary-adrenal axis, but at a higher set point. Practically, squirrel monkeys require 50-fold more dexamethasone to achieve 50% suppression of plasma cortisol, compared to cynos. Callitrichids (marmosets and tamarins) also have consistently high cortisol; but other cebids do not.{4073}  There is variation in hormone levels (specifically glucagon and cortisol) depending on origin of the squirrel monkey subtype{4488}.

Total cortisol (free+bound) in squirrel monkeys is 10 times higher than in humans. Only free cortisol can diffuse into target cells, and again this level is much higher: in squirrel monkeys >30% of cortisol is free, whereas in humans only 4-6% is free. This translates to levels of free cortisol that are 100 times greater. Large amounts of unmetabolized cortisol are thus excreted in the urine. The high cortisol levels are driven by high adrenocorticotropin, low levels of cortisol binding globulin that is of low affinity, low metabolic clearance, and high levels of hydroxysteroid dehydrogenase that convert inactive cortisone to active cortisol.  Finally, the glucocorticoid receptor has 20-fold lower affinity than that of humans or rhesus, leading to end-organ resistance.{4073}  

Continuous cell lines have been established to provide DNA, mRNA, and protein from squirrel monkeys for study of glucocorticoid resistance. The cells are B lymphoblasts transformed with Epstein-Barr virus. The glucocorticoid receptor has been cloned and sequenced, thinking that the difference lay in amino acid changes. This turned out to be incorrect; factors in the cytosol such as components of the receptor complex appear to account for the reduced binding affinity for cortisol. In particular, differences between monkey and human immunophilins FKBP 51 and 52 have been identified. FKBP 51 is 10 times higher in squirrel monkey cells and FKBP 52 is half of human levels. The high levels of 51 appear to be most important. They appear to have developed 25-50 million years ago.{4073}  

Squirrel monkeys also have high levels of other steroids, and their monocytes secrete low levels of IL-1b and high levels of TGF-b. They are relatively resistant to progesterone.{4073}  

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Housing and Husbandry

Usually, groups of same-sex monkeys are housed together in the laboratory. Same-sex groups can be formed all at once, after a 1-month period of single housing. Multiple males housed together are not usually aggressive unless there are females nearby. Males will tend to withdraw from interactions with females and young if caging allows it, but their canine teeth can cause severe slashing injuries. Inter-female aggression is more common than inter-male, but is less severe. Since males prefer to live with other males, multi-male social groupings are desirable. Provision of visual blinds will allow the males to hide from others. In breeding colonies, males are usually housed together and placed with the females only during the 2-3 month breeding season.{4488}

After a group is formed, it should be monitored for aggression. Usually this results from one animal that initiates excitement in the others; if this animal is removed and then gradually re-introduced the aggression subsides within a few days.{4488}

Caging should allow for multiple perches and lots of vertical space for these arboreal animals. Signs of boredom include circling and head shaking. Ambient temperature should range from 23-30°C with relative humidity of 40-60%. {4488}

Diet should include 5040 New World Primate biscuits, vegetables, fruit, and mealworms.{4072} High-protein diet should be used (24-26%), with 6% fat, and 2.5-3.5% fiber. Care should be taken with supplemental fruit to ensure the animals are consuming enough of the protein diet.{4488} They require dietary vitamin D₃. They also have a high requirement for folic acid (200ug/day); deficiencies result in megaloblastic anemia, low birth weight and stillbirths.{4762} Squirrel monkeys will often examine each biscuit at feeding time and throw it on the floor to eat later, so if the slats are too wide some provision might be made to keep the animals from wasting food and being hungry. They should be fed twice a day. Foraging boards are a good method of enrichment.{4488}

Vitamin C deficiency can lead to cephalhematoma in advanced stages.{4072}  Even as recently as 1990, mistakes in manufacture of diet resulted in irreversible cephalhematoma in a colony of squirrel monkeys{3718}. Addition of sodium hexametaphosphate to the diet (by coating the biscuits with it) has been shown to slow accumulation of calculus on their teeth. Unfortunately, the teeth must first be cleaned in order for the HMP to work effectively, as it acts by complexing with calcium in the plaque{4554}. 

Monkeys can be handled using leather gloves. They can be trained to enter transport cages on command; since they do not like to enter dark places the sides or top should be made of wire mesh. Blood samples can be collected from the femoral vein of unsedated animals, and injections administered.{4488}

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Common diseases

Zoonoses

Viral diseases

Parasites

Miscellaneous

The Squirrel Monkey in Research 

(ILAR Journal 41(1), 2000)

Advantages of squirrel monkeys over Old World NHPs include small size, ease of handling, need for smaller doses of rare compounds, easy adaptation to the laboratory, and reduced risk of zoonosis to employees because they don't carry herpes B.{4071}

Squirrel monkeys have been used in atherosclerosis research since they develop fatty streaks and plaques on atherogenic diets. They also develop cholelithiasis on those diets. They are currently used for neurobehavioral research, malaria vaccine research, Creutzfeldt-Jacob disease research (their PrP is 93.8% homologous to human PrP sequence), studies of the biomechanics of labor and delivery (it was a surprise that fetal rotation through the pelvis was the same as in humans), pelvic organ prolapse (which increases with age and parity), and emphysema (effects of retinoic acid on elastase-induced emphysema).{4071,4762}   

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Research Techniques

Pertinent things to remember about squirrel monkeys are that they require vitamin D₃, the females lack menses, and both sexes have marked seasonal characteristics such as "fatting" in males. They can be carriers of Herpesvirus saimiri (which is oncogenic in other NHPs and transforms human T lymphocytes) and H. tamarinus (causing fatal disease in Aotus and other New World monkeys); and that they are less likely to contract tuberculosis than Old World primates. One must be careful to validate which species is used, because there are differences among species/subspecies such as body weight, susceptibility to gallstone formation, endocrine responses, growth and development, and malaria susceptibility. Individual identification is by tattoo, neck tag or microchip. Age of wild-caught animals can be estimated from dental eruption.{4072}

Squirrel monkeys are prone to hypothermia and hypoglycemia when they are anesthetized or debilitated. Awake squirrel monkeys should have temperatures of 38°-39.5°C, although it can increase to 41°C if they struggle. At room temperatures <26°C, they will increase metabolic heat production. If the temperature exceeds 35°C, they may be at risk for heat stroke, since they have few means of compensating{4488}. Monkeys with temperatures of less than 37.7°C are seriously ill. Normal glucose is 80±28 mg/dl; unconscious animals should be given 20% dextrose by stomach tube at a dose of 1ml/infant, 3-5ml/juvenile or 10ml/adult. Concentrated IV glucose is not recommended. Orogastric or nasogastric intubation can be achieved with a 5Fr feeding tube. Blood sampling sites include the femoral vein and lateral tail vein; infusions can be made through the saphenous vein. No more than 10ml/kg should be sampled at a time. On some studies (i.e. malaria), monkeys that become anemic following blood loss can be treated with iron dextran, folic acid, and vitamin B complex.{4072}

Isoflurane is the recommended anesthetic agent.{4072} Ketamine at 10mg/kg can also be used. Oxymorphone at 0.025mg/kg tid is used for analgesia following major surgery.{4488}

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Behavioral Research

This is discussed in the Research Methodology section.

Parasite Research

Parasites studied in squirrel monkeys include toxoplasmosis (which caused 100% morbidity and 30% mortality in a colony), Encephalitozoon cuniculi (they are quite susceptible), Tritrichomonas mobilensis (a naturally occurring parasite), filaria such as Dipetalonema (experimental), trypanosomiasis (68% are infected with T. rangeli and T. cruzi), Babesia microti (a human pathogen for which the squirrel monkey serves as a good model), Leishmania donovani (for which squirrel monkeys are a good model due to protracted course of infection), and a variety of schistosomes. However, the most frequent use in parasitic research is for malaria.{4075} The Bolivian squirrel monkey is the best model for studies of P. falciparum Indochina I. The others have varying responses to infection with P. vivax, underscoring the importance of correct species identification.{4762} 

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

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