ILAR Journal Online, Volume 31(1) 1989: Perspectives on Animal Use

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ILAR Journal V31(1) 1989
Perspectives on Animal Use

The Squirrel Monkey in Biomedical Research
Christian R. Abee

Dr. Abee is professor and chairman of the Department of Comparative Medicine, University of South Alabama, Mobile. He is a member of the ILAR Committee on Animal Models and Genetic Stocks.

Introduction

Squirrel monkeys are the most commonly used South American primates in biomedical research. Members of the genus Saimiri, they are native to equatorial South America and a small part of Central America. The squirrel monkey's natural range extends from coastal areas of eastern Brazil and French Guiana (east) to Peru (west); Columbia, Venezuela, and Guyana (north); and Bolivia and central Brazil (south). There are also two small, isolated habitats of squirrel monkeys in Central America on the western coasts of Panama and Costa Rica. Squirrel monkeys consist of four species and nine subspecies (Hershkovitz, 1984); however, only two species (S. sciureus and S. boliviensis) comprising three subspecies have been used to any great extent in biomedical research.

Squirrel monkeys have the largest range of all New World primates. They are also the most plentiful. Frequently, wild populations are found living in close proximity to human settlements, which indicates that they are among the most adaptable of the neotropical primates. Their habitat includes altitudes from sea level to 2,000 meters. The South American habitat of the squirrel monkey spans many thousands of miles throughout the Amazon Basin. Figure 1, a modified depiction from the work of Hershkovitz (1984), shows the distribution of Saimiri spp. throughout their natural range.

Historical Perspectives

The first research report citing the squirrel monkey was published in 1933 (Klüver). Squirrel monkeys were first recognized as potentially important laboratory animals because they were readily available, easy to handle and maintain in the laboratory, and more closely related to humans phylogenetically than non-primate laboratory species. Later, they were found to develop some diseases that resemble important maladies of humans.

In 1949, the National Heart Institute awarded a grant to establish a breeding colony of squirrel monkeys (Goss et al., 1968). The purpose of this project was to determine whether the squirrel monkey would adapt to laboratory breeding conditions. They found that squirrel monkeys adapted well to the laboratory; however, early attempts at breeding were not successful. It was not until 10 years later that limited breeding success was observed in this colony. The squirrel monkey gained popularity during the 1960s and 1970s beginning with the observation that squirrel monkeys had naturally occurring aortic and coronary atherosclerosis (Middleton et al., 1964).

Although research using the squirrel monkey has changed over the years, it remains an important animal in biomedical research. Between 1986 and October 1988, more than 1,000 articles on the squirrel monkey appeared in scientific journals and books (Primate Information Center, Regional Primate Research Center, University of Washington, Seattle, personal communication, 1988). Table I summarizes the subject areas of articles that describe the use of squirrel monkeys. Interestingly, their use has shifted from cardiovascular/metabolic disease research in the 1960s to neuroscience, pharmacology, and behavioral research in more recent years.

Availability of Squirrel Monkeys for Research

Developing a stable supply of squirrel monkeys and developing methods to optimize reproduction in captivity have become important issues in biomedical research. These animals were once plentiful and available at modest cost from a number of commercial sources and countries of origin, but this is no longer the case. In recent years, supplies of squirrel monkeys have steadily decreased, and only one subspecies--S. boliviensis peruviensis--is currently available from the wild. Occasionally, S. sciureus macrodon also may be available in limited numbers.

The constantly changing availability of squirrel monkeys provides an excellent example of the fragile relationship between geopolitics and biomedical research. The first squirrel monkey to be imported in large numbers for research was the Brazilian/Colombian type (S. sciureus), which became the most common laboratory squirrel monkey of the 1960s and early 1970s. The supply of this species ceased rather abruptly in the 1970s when both countries decided to stop allowing exportation. The next squirrel monkey to be imported for research was the Bolivian type (S. boliviensis boliviensis). At about the same time, the Peruvian type (S. boliviensis peruviensis) also began to appear in the laboratory. In the early 1980s, supplies of these squirrel monkeys became scarce as Bolivia stopped exportation. The Guyanese-type squirrel monkey (S. sciureus) became the predominant squirrel monkey in research for several years during the 1980s. This moved the research community full circle back to S. sciureus. In the past two years, Guyana has stopped exportation of squirrel monkeys. Thus, it has been very difficult to maintain continuity in multiyear research programs that depend on a continuous supply of a particular species of squirrel monkey.

The single remaining source of feral squirrel monkeys is through the Pan-American Health Organization (PAHO). PAHO, supported by contracts from the National Institutes of Health (NIH) and the U.S. Agency for International Development, provides support for a primate breeding and trapping facility in Iquitos, Peru. This facility is operated under the authority of the Peruvian government and is considered a means for developing conservation strategies, as well as providing limited numbers of squirrel monkeys and other South American primates for research purposes. Squirrel monkeys available through PAHO can be requested by contacting the Interagency Research Animal Committee (IRAC).¹Because this source is supported by a joint governmental effort between the United States and Peru, special approvals are required to obtain these animals for research. There are approximately 300 squirrel monkeys imported into the United States from Peru each year.

Laboratory-born squirrel monkeys of known age, history, and pedigree are highly desirable for some kinds of research. The NIH provides support for one breeding resource of squirrel monkeys, which is the colony maintained at the Primate Research Laboratory of the University of South Alabama College of Medicine. This research resource was established in 1980 with the following objectives: provide a resource of expertise on the squirrel monkey; carry out research aimed at optimizing captive reproduction; and provide laboratory-born, well-defined squirrel monkeys for NIH-supported research. This breeding colony has grown from approximately 235 animals in 1980 to more than 400 in 1988. Although this colony is the only NIH-supported resource of squirrel monkeys in the United States, there are also a number of small, institutionally supported breeding colonies at various U.S. research centers and academic institutions. Animals produced from these colonies are used primarily to meet specific research needs within each institution.

Squirrel monkeys are occasionally available from laboratories no longer using them in research. The Primate Supply Information Clearinghouse of the Regional Primate Research Center at the University of Washington lists the availability of such animals weekly. Through this mechanism, use of the limited supply of previously imported squirrel monkeys is made more efficient.

Taxonomic and Genetic Considerations

All Saimiri spp. were once considered to be a single species with several geographic races or subspecies. More recently, karyotypic and phenotypic information has shown that squirrel monkeys should be separated as a single genus with four species and nine subspecies (Hershkovitz, 1984). Studies by Assis and Barros (1987), Da Silva et al. (1987), and VandeBerg et al. (1988) support the taxonomic classification of Hershkovitz.

MacLean (1964) first divided squirrel monkeys into two varieties based upon external characteristics. He described squirrel monkeys as either "gothic" or "roman" based upon the arching pattern created by the distribution of pigmented and white hair in the periocular patch (gothic: elongated, peaked arch; roman: semicircular arch). S. sciureus subspecies were described as gothic and S. boliviensis subspecies as roman. Later, S. oerstedi subspecies and, most recently, S. ustus (Hershkovitz, 1984) have been described as gothic varieties. Squirrel monkey species and subspecies each vary either morphologically, karyotypically, or both. The most obvious karyotypic difference between squirrel monkey species is the number of acrocentric autosomes. Table 2. lists differences between squirrel monkeys based upon numbers of acrocentric autosomes and periocular patch. Figure 2 depicts a breeding group of S. boliviensis boliviensis, a roman variety, imported from Santa Cruz, Bolivia. Figure 3 is a breeding group of S. sciureus, a gothic variety, imported from Guyana.

Many investigators either ignore or are unable to distinguish between species within their colonies, an error that may contribute to invalid experimental results and wasted research dollars. There is now substantial information showing that species of squirrel monkeys vary in their susceptibility to both naturally occurring and experimentally induced disease. Portman et al. (1980) showed that diet-induced cholelithiasis is species dependent in the squirrel monkey. The Brazilian-type squirrel monkey (S. sciureus) develops cholesterol gallstones by diet induction, while the Bolivian type (S. boliviensis) is resistant. The Bolivian squirrel monkey also maintains a lower mean total serum cholesterol than does the Brazilian squirrel monkey, which suggests that the metabolism of lipids and the relative distribution of plasma lipoproteins may vary between squirrel monkey species. Abee (1985) suggested that the incidence of glomerulonephritis, a common disease among Brazilian squirrel monkeys, may vary between species because the disease appears to occur less frequently in S. boliviensis. Other species differences in physiology (Coe et al., 1985; Martin and McNease, 1982), behavior (Mendoza et al., 1978), and growth and development (Ausman et al., 1985) have been described.

The difficulty researchers have in differentiating between Peruvian, Bolivian, and Guyanese squirrel monkeys based upon coat color and physical characteristics may result in their interbreeding the three species (Ariga et al., 1978). Because karyotypic variation in acrocentric autosomes of squirrel monkeys is thought to be due to inversions (Jones et al., 1973), the progeny of such matings will be heterozygous for the inversion. This inversion heterozygosity can lead to the production of abnormal gametes due to crossovers at the inversion loop during meiosis. Theoretically, as many as 50 percent of conceptions in hybrid squirrel monkeys could result in nonviable embryos-a possibility that has the potential for drastically reducing reproduction in a breeding colony.

Genetic characterization of squirrel monkeys used in research and breeding is essential. Mixing species and subspecies within experimental groups may create confounding variables, which make interpretation of data difficult or impossible. Similarly, the long-term negative effect of mixing species in breeding groups can only be estimated; however, the potential reduction in reproductive performance makes such a management decision unwise.

Squirrel Monkeys as Models in Biomedical Research

As shown in Table 1, the squirrel monkey is used in many research areas. Research uses for the squirrel monkey have expanded considerably since the publication of The Squirrel Monkey (Rosenblum and Cooper, 1968). Squirrel monkeys are used principally in two ways, as surrogates for humans and as models for studies of human diseases.

As surrogates for humans, squirrel monkeys have been used extensively in pharmacologic studies (Barrett, 1985) and in aerospace research (Beischer, 1968). As models of disease, squirrel monkeys have been used for more than 25 years to study naturally occurring or experimentally induced diseases resembling important diseases of humans. This paper will not exhaustively review all the uses of squirrel monkeys in research. Instead, it will provide an overview of major research uses in the past and focus on several emerging, contemporary research areas that utilize squirrel monkeys.

Established Research Uses for Squirrel Monkeys

Among South American primates, squirrel monkeys have been the ones most extensively used in cardiovascular research (Strickland and Clarkson, 1985). Middleton et al. (1964) reported that a high percentage of laboratory-housed Brazilian-type squirrel monkeys had aortic fatty streaks and coronary artery lesions. This report led to additional studies to determine the extent of naturally occurring atherosclerosis in free-living squirrel monkeys (Middleton et al., 1967) and studies of the incidence of atherosclerosis in squirrel monkeys compared to other primate species (Lofland et al., 1967). Dietary influences on cholesterolemic response and atherosclerosis were also described in the squirrel monkey (Clarkson et al., 1976; Lofland et al., 1970; Malinow et al., 1966).

Diet-induced cholelithiasis in Colombian/Brazilian-type squirrel monkeys was first described by Osuga and Portman (1971). Although this was the first report specifically dealing with diet induction of cholelithiasis, investigators first discovered gallstones as incidental necropsy findings in squirrel monkeys being used for studies of atherosclerosis. Clarkson et al. (1976) reported that cholelithiasis was age dependent. Adult squirrel monkeys were more susceptible than juveniles when fed cholelithogenic diets. Portman et al. (1980) found that Bolivian squirrel monkeys were resistant to diet-induced cholelithiasis.

Squirrel monkeys have been used in pharmacologic studies since the early 1960s (Kelleher et al., 1963). Barrett (1985) recently reviewed the use of the squirrel monkey in behavioral pharmacology. Using squirrel monkeys to study the effects of various drugs on behavior has increased considerably in the past 20 years. Behavioral pharmacology spans the disciplines of pharmacology and neuroscience; squirrel monkeys are thought by many to be desirable models because of the obvious anthropomorphic similarities of their nervous system and their ease of handling and trainability. Saimiri spp. have also been used extensively for neuroscience studies because of their relatively large brains, which resemble the human brain. A Stereotypic Atlas of the Squirrel Monkey's Brain (Saimiri sciureus) (Gergen and MacLean, 1962) provides a detailed, photographic series of whole-brain sections stained by the Weil-Weigert method. This atlas illustrates the anatomical features of the squirrel monkey's highly organized nervous system.

New and Emerging Uses for the Squirrel Monkey

A major discovery was made in 1984 when experimentally treated squirrel monkeys developed lesions and clinical signs resembling Parkinson's disease. Squirrel monkeys treated with MPTP (1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine), a contaminant found in an illicit drug, developed tremors, bradykinesia, and cell loss in the substantia nigra (Langston et al., 1984a,b). This finding confirmed that MPTP is a highly selective neurotoxin responsible for clinical signs and lesions similar to those observed in Parkinson's disease and that the squirrel monkey could be used as a model for this disease. Because administration of MPTP to rodents did not result in a Parkinsonian state (Chiueh et al., 1983; Johannessen et al., 1985), the squirrel monkey played an important role in elucidation of this neurotoxin. Squirrel monkeys have been used by neuroscientists in numerous studies of MPTP-induced Parkinson's disease since 1984.

Concerted efforts have been made for a number of years to find and characterize appropriate animal models for the human malarias. Plasmodium spp., responsible for malaria in humans, are rather host specific, which complicates the search for good animal models. The Bolivian squirrel monkey has been shown to be a good model for studies of the pathogenesis of P. falciparum Indochina I (Whiteley et al., 1987). Experimentally infected Bolivian squirrel monkeys had many of the same lesions and disease syndromes as those reported in the human disease. Guyanese squirrel monkeys experimentally infected at the same time were found to be less favorable models. This difference emphasizes the importance of using the appropriate squirrel monkey species.

Squirrel monkeys have been proposed as a model of genital trichomoniasis of women (Street et al., 1983). Gardner et al. (1987) repeated the initial observations made by Street et al. (1983) and provided the additional insight that hormonal status of squirrel monkeys experimentally infected with Trichomonas vaginalis is critical to successful establishment of vaginal infections. Squirrel monkeys resistant to infection during the nonbreeding season become susceptible during the breeding season. This finding suggests that elevations of ovarian hormones influence susceptibility. Failure to understand seasonality in this species could lead to erroneous conclusions about the usefulness of the squirrel monkey in studies of genital trichomoniasis. The squirrel monkey is the only known animal model for vaginal trichomoniasis caused by T. vaginalis.

A previously undescribed intestinal trichomonad (Tritrichomonas mobilensis) was discovered serendipitously during attempts to induce genital trichomoniasis in squirrel monkeys (Culberson et al., 1986). Two reports describing the properties of this parasite followed (Brady et al., 1988; Pindak et al., 1985). As studies progressed to characterize this new trichomonad, a potent, lectin-like hemagglutinin was discovered that had not been described previously in trichomonads (Pindak et al., 1987, 1988).

Clinical observations that squirrel monkeys naturally develop dental disease have led to the conclusion that they may serve as an excellent model for studies of periodontal disease (Collins et al., 1986). Several studies have characterized and determined the presence of bacteria associated with periodontal disease in squirrel monkeys (Clark et al., in press; McArthur et al., 1988; Progulske et al., 1987).

As more is learned about the biology of squirrel monkeys, new research uses for these animals will become apparent. It is clear from the broad scope of literature citing squirrel monkeys that they are important models for the study of many biomedical research issues.

Reproductive Biology of the Squirrel Monkey

Although squirrel monkeys are easily maintained in laboratory colonies, reproduction in captivity has been much less successful than for other commonly used laboratory primate species. Taub et al. (1978) reported experience with a large breeding colony of Brazilian squirrel monkeys maintained at the Bowman Gray School of Medicine. His report documents the difficulties with captive reproduction in Saimiri spp., particularly as it relates to the use of captive-born squirrel monkeys as breeders. More recently, Johnsen and Whitehair (1986) reported the experience of breeding colonies at several institutions. The collective experiences of these laboratories clearly establish that the squirrel monkey is much more difficult to breed in captivity than are most other commonly used laboratory primates. Although progress has been made, efforts to learn more about methods for improving reproduction are needed in order to provide self-sustaining breeding colonies.

The squirrel monkey is a seasonal breeder, giving birth during the summer months. Both male and female squirrel monkeys undergo physiologic changes during the breeding season. The breeding season lasts approximately three months and occurs most commonly during the winter in the northern hemisphere. Most births in the breeding colony at the University of South Alabama occur in June. Because the gestational period is approximately 150 days, the peak period for conceptions can be estimated to fall between December and January.

Table 3 is a summary of reproductive performance of a breeding colony of Bolivian squirrel monkeys (S. boliviensis boliviensis) at the Primate Research Laboratory of the University of South Alabama. It should be noted that many of these animals were also being used in various studies that may have influenced their reproductive potential. These data depict what can be expected from a combined research and breeding colony. A strict production colony might be expected to be somewhat more successful reproductively.

Reproductive Biology of the Female

For female squirrel monkeys, the breeding season is characterized by elevations in circulating levels of estradiol and progesterone associated with a series of ovulatory cycles that vary between 6 and 12 days (Diamond et al., 1984). Serum concentrations of estradiol and progesterone in S. boliviensis boliviensis increase dramatically in cycling females. Estradiol rises from peak prebreeding season levels averaging less than 95 pg/ml to levels greater than 1,000 pg/ml during the breeding season. The breeding season spans approximately three months.

Mean concentrations of progesterone during non-breeding months are less than 10 ng/ml, while sixfold or greater increases are observed during the breeding season. Although serum estradiol concentrations are subject to wide fluctuations from day to day, progesterone concentrations remain consistently elevated compared to precycling levels. Thus, elevations in serum progesterone concentration appear to be a reliable indication of cycling in the squirrel monkey (Aksel et al., 1985).

The female Bolivian squirrel monkey does not cycle in synchrony with other females in the same cage (Williams et al., 1986a), which makes prediction of cyclic events within the breeding group difficult because each female appears to be cycling independently. The fact that some adult females in the breeding groups either fail to cycle or cycle during only portions of the breeding season further complicates management of the breeding colony. Determination of which animals are capable of conceiving can only be done laparoscopically or by serial serum progesterone determinations (Aksel et al., 1985).

Reproductive Biology of the Male

Prior to the onset of the breeding season of the female, breeding-age males undergo a rapid weight gain that is distributed primarily over the upper torso. Figure 4 shows mean monthly body weights ( ± SEM) for a group of 10 male squirrel monkeys throughout the year. The shaded months correspond to the breeding season. Peak body weights are shown to occur immediately prior to the onset of the breeding season. This phenomenon is called "fatting" (Dumond, 1968; Dumond and Hutchinson, 1967).

Longitudinal studies of serum androgens and breeding behavior of males have provided some insights into endocrine changes associated with seasonality (Wiebe et al., 1988). Serum testosterone concentrations of adult male Bolivian squirrel monkeys maintained in harem cages with adult females fluctuate widely during the breeding season; however, a yearly peak occurs in the later part of the breeding season. Dehydroepiandrosterone (DHEA) levels peak early in the breeding season but decline during the remainder of the season. Androstenedione levels are quantitatively greater than testosterone, a finding that differs from observations in Old World primates and humans (Wiebe et al., 1988).

Behavior of male squirrel monkeys during the breeding season is characterized by a reduction in responses associated with aggression and an increase in sexually related responses, such as genital displays, anogenital inspection, and copulation. These responses were positively correlated with elevations in circulating levels of androstenedione (Williams et al., 1986b).

Anderson and Mason (1977) have shown that male squirrel monkeys exposed to females stimulated with exogenous estradiol show increased sexual behavior. Studies to determine whether copulations during the breeding season are associated with specific parts of the female's reproductive cycle showed that breeding attempts by the male are not random events (Williams et al., 1986a). Using a limited male access paradigm that allowed observation of all interactions between breeding males and females, all copulations were found to occur within 24 hours of predicted ovulation (based upon daily serum estradiol determinations). Males mated with no more than two females on any given day. This study provides important insights about reproduction in the male. Because squirrel monkeys are usually housed in breeding colonies as harems (one male and multiple females), random matings would be very inefficient. It appears there are cues, as yet undetermined, that influence copulatory behavior.

Abortions and Stillbirths

Abortions are a serious problem in a squirrel monkey breeding colony because all females must conceive in a relatively narrow time span due to the strict seasonal breeding pattern of this genus. Those that abort may not have another opportunity to conceive before the breeding season ends. Females that fail to become pregnant or to maintain their pregnancies cannot become pregnant again until the following year.

Diamond et al. (1985) reported that early and occult abortions may be an important factor in the reproductive efficiency of squirrel monkeys. This study revealed hormonally documented conceptions in 71 percent of animals sampled every two to four weeks during the breeding season. Early abortions were subsequently detected in 25 percent of this group. Therefore, early abortion or occult abortion may account for a large portion of the reduced breeding efficiency experienced in squirrel monkey breeding colonies compared to other primate species.

Because squirrel monkeys deliver large fetuses relative to the size of the dam, stillbirths and neonatal deaths associated with dystocia are important considerations. A retrospective study of females delivering live and stillborn fetuses revealed a highly significant difference in pelvic outlet diameter (Aksel and Abee, 1983). Those females at greatest risk for delivering stillborn fetuses had smaller pelvic outlets than did those that successfully delivered. This work has led to the first diagnostic procedure for assessing risk of stillbirth or dystocia for this species. Early detection of females at high risk for stillbirths or abortion provides the opportunity to cull such animals from the breeding colony or to prepare for surgical intervention.

Husbandry

Perhaps the single most important but often overlooked aspect of the care of laboratory primates is daily husbandry. Close attention to the basic needs of the squirrel monkey often will prevent serious problems. Daily observations during cage cleaning and feeding provide many useful clues about the condition of individual animals and the colony as a whole. The choice of functional housing designed to facilitate an effective husbandry program will minimize stress and contribute to the success of the colony. A description of the care, management, and caging usually used for squirrel monkeys has been published (Abee, 1985).

All cages used for housing squirrel monkeys in NIH-sponsored research must comply with the standards set forth in the Guide for the Care and Use of Laboratory Animals (National Research Council, 1985) and the Animal Welfare Act. Most squirrel monkeys are classified as "Group 1" small primates weighing less than 1 kg. It is recommended that they be provided a minimum of 1.6 square feet of living area and a minimum of 20 inches of cage height.

There is a growing emphasis in regulatory documents and within the research community to house squirrel monkeys in social groups. Although this effort is thought to reduce the stress of captivity in these naturally social animals, group housing can complicate husbandry of squirrel monkeys. Group pens must be designed to promote the health and well-being of these animals while allowing for adequate sanitation.

Group pens are most commonly constructed of aluminum or chain link with monolithic floors. Perches can be constructed from various materials; however, polyvinyl chloride (PVC) pipe--which is impervious to water, easily cleaned, and not thermoconductive--has been shown to be an excellent perch material (Williams et al., 1988). PVC pipe of the type used by plumbers can be cut and joined to meet the requirements of almost any cage configuration. Metal perches are less desirable because they are more thermoconductive and tend to dissipate body heat (Moreland, 1972).

Squirrel monkeys are almost entirely arboreal in their natural habitat. Because they lack ischial callosities, they are prone to developing sores if they are not provided with suitable structures on which to climb and perch. Squirrel monkeys prefer a flat, shelf-type surface for sleeping, but animals using such perches frequently develop pressure ulcers on the dorsal aspect of the tail (Clewe, 1965). By using large-diameter PVC pipe (1.5 inch), a highly desirable perch can be provided. These perches have a broad surface for sitting and lack the flat surface associated with tail sores. Williams et al. (1988) have shown that multiple levels of perches in a single cage will increase the actual living area used by the social group. This arrangement is an effective means for reducing population density within a pen without enlarging the square footage.

Using appropriate cages and cage furniture along with maintaining a husbandry program designed to meet the specific biological and psychological needs of the squirrel monkey will reduce morbidity and mortality in captivity. Also, proper maintenance of these animals will enhance the quality of information generated experimentally. Careful attention to these details prevents medical problems and therefore reduces the need for therapeutic intervention.

Conclusions

To meet the need for squirrel monkeys in future biomedical research, it is essential to improve expertise in captive reproduction and to develop more efficient methods for using available supplies of squirrel monkeys. Current studies of the reproductive biology of squirrel monkeys hold considerable promise for improving reproduction if practical management strategies can be developed from this information.

One of the more promising approaches to more efficient use of squirrel monkeys is the development of more precise genetic characterization. Genetic characterization of squirrel monkeys will allow investigators to select animals with similar genetic characteristics (VandeBerg et al., 1987). This approach may lead to the development of experimental groups with less interanimal variability, which will reduce the number of animals required in each experimental group. Also, the selection of animals for specific genetic traits that control susceptibility or resistance to disease may eventually be possible.

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¹Address: IRAC, Office of Animal Care and Use, N1H, Building 12A, Room 4003, Bethesda, MD 20892 (301/496-5424).

TABLE 1 Scientific Articles Reporting on the Squirrel Monkey, 1986-1988

Subject Area	Number of Articles
Neuroscience and ophthalmology	252
Pharmacology and therapeutics	131
Behavior	107
Parasitology	55
Dental and oral	39
Toxicology, environmental health, and space flight	37
Reproductive biology	37
Virology	34
Ecology and conservation	32
Endocrine system	26
Learning and perception	22
Metabolism and nutrition	22
General primatology	21
Immunology	17
Genetics	15
Cardiovascular	11
Gerontology	10
All other	151
Total articles	1019

SOURCE: Bibliographic search by Primate Information Center, Regional Primate Research Center, University of Washington, Seattle, 1988.

TABLE 2 Selected Taxonomic Characteristics of the Squirrel Monkey

Scientific Name	Chromosome Number (Diploid)	Acrocentric Variety^a	Autosomes
Saimiri sciureus sciureus	44	Gothic	7
S. sciureus macrodon	44	Gothic	6
S. sciureus cassiquiarensis	?	Gothic	?
S. sciureus albigena	?	Gothic	?
S. boliviensis boliviensis	44	Roman	6
S. boliviensis peruviensis	44	Roman	5
S. oerstedi oerstedi	44	Gothic	5
S. oerstedi citrinellis	?	Gothic	?
S. ustus	44	Gothic	5

^aBased on arching pattern created by distribution of pigmented and white hair in the periocular patch (gothic: elongated, peaked arch; roman: semicircular arch).

SOURCE: Adapted from Hershkovitz (1984) and Assis and Barros {1987).

TABLE 3 Reproductive Performance of the Squirrel Monkey Breeding Colony at the University of South Alabama

Year	Adult Females	Pregnancies	Conceptions (%)^a	Live Births	Stillbirths	Abortions	Fetal Wastage (%)^b
1982	185	69	37	55	8	6	20
1983	155	85	55	70	12	3	18
1984	153	58	38	46	9	3	21
1985	162	68	42	53	12	3	23
1986	168	65	39	48	8	9	26
1987	128	52	41	38	7	7	27

^aPregnant females divided by total adult females x 100.
^bStillbirths plus abortions divided by total births x 100. These include only abortions that could be documented by fetal tissue. Occult abortions could not be counted and would be considered as failures to conceive.

Figure 1 Map of South and Central America showing the distribution of the genus Saimiri throughout its natural range. This map is a modification of that presented by Hershkovitz (1984), which demonstrates speciation of the genus Saimiri. Reprinted by permission of the publisher. Copyright 1984 by Alan R. Liss, Inc.

Figure 2 A family group of Bolivian squirrel monkeys (Saimiri boliviensis boliviensis). Bolivian squirrel monkeys are classified as "roman" variety based upon the distribution of pigmented and nonpigmented periocular hair in a pattern resembling a semicircular arch.

Figure 3 A group of Guyanese squirrel monkeys (Saimiri sciureus sciureus). Guyanese squirrel monkeys are classified as "gothic" variety based upon the distribution of pigmented and nonpigmented periocular hair in a pattern resembling an elongated, peaked arch.

Figure 4 A graphic depiction of monthly body weights (group mean ± SEM) for a group of 10 adult male Bolivian squirrel monkeys. The shaded area represents the breeding season. Note that the yearly peak occurs just prior to the onset of the breeding season. This phenomenon is called "fatting."