Tritrichomonas mobilensis n. sp. (Zoomastigophorea: Trichomonadida) from the Bolivian Squirrel Monkey Saimiri boliviensis boliviensis1

ABSTRACT. A trichomonad flagellate, Tritrichomonas mobilensis n. sp., is described from the large intestine of the squirrel monkey, Saimiri boliviensis boliviensis. The organism has a lanceolate body 7–10.5 μm in length; a well developed undulating membrane; a stout, tubular axostyle with periaxostylar rings that terminate in a cone-shaped segment projecting from the posterior end of the cell; and a moderately wide costa. The anterior flagella are about as long as the body, and the recurrent flagellum is of the acroneme type. All its characteristics suggest that the new species belongs in the Tritrichomonas augusta type of the subfamily Tritrichomonadinae.     

Cortisol metabolism in the Bolivian squirrel monkey (Saimiri boliviensis boliviensis)

New World squirrel monkeys (Saimiri spp.) have high circulating cortisol levels but normal electrolytes and blood pressures. The goal of the present study was to gain insight into adaptive mechanisms used by Bolivian squirrel monkeys to minimize the effects of high cortisol on mineralocorticoid receptor (MR) activity and electrolyte and water balance. Aldosterone levels in serum from 10 squirrel monkeys were 17.7 +/- 3.4 ng/dl (normal range in humans, 4 to 31 ng/dl), suggesting that squirrel monkeys do not exhibit a compensatory increase in aldosterone. The squirrel monkey MR was cloned and expressed in COS-7 cells and found to have similar responsiveness to cortisol and aldosterone as human MR, suggesting that squirrel monkey MR is not inherently less responsive to cortisol. To determine whether altered metabolism of cortisol might contribute to MR protection in squirrel monkeys, serum and urinary cortisol and cortisone were measured, and a comprehensive urinary corticosteroid metabolite profile was performed in samples from anesthetized and awake squirrel monkeys. The levels of cortisone exceeded those of cortisol in serum and urine, suggesting increased peripheral 11beta-hydroxysteroid dehydrogenase 2 activity in squirrel monkeys. In addition, a significant fraction (approximately 20%) of total corticosteroids excreted in the urine of squirrel monkeys appeared as 6beta-hydroxycortisol, compared with that in man (1%). Therefore, changes in cortisol metabolism likely contribute to adaptive mechanisms used by Bolivian squirrel monkeys to minimize effects of high cortisol.     

Mating-related estradiol fluctuations during the estrous cycle of the Bolivian squirrel monkey (Saimiri boliviensis boliviensis)

The female squirrel monkey, Saimiri boliviensis, a New World monkey, has 10-day estrous cycles during the annual breeding season. Measurements of serum estradiol (E) concentrations in females housed with males in breeding pens revealed markedly higher levels than previously reported. Additionally, females in breeding pens appeared to have two distinct patterns of serum E peaks relative to the LH surge. Serum estrogen peaks averaging 5-fold greater than levels on the preceding day were observed on the same day as the LH surge, whereas other females had only a small E rise on the day of the LH surge followed by a 6-fold E rise on the next day. The serum progesterone (P) levels in all animals were depressed for 1-2 days before the LH surge but frequently started to rise on the day of the LH surge. The effect of the presence of a breeding male was examined by studying females housed in a group pen without exposure to a breeding male. In contrast to breeding-pen patterns, relatively small E rises were found in the 10 cycles observed. To further elucidate estrus-related E rises, a limited male-access paradigm was used to isolate mating-related hormone fluctuations. Pre-mating E levels had no marked rises; however, 4 h after mating, whether on the day of the LH surge or the next day, large E rises were found. These studies indicate that the LH surge in cycling squirrel monkeys is consistently preceded by a marked P nadir and associated with relatively small E rises.(ABSTRACT TRUNCATED AT 250 WORDS)     

Microsatellite polymorphisms in Bolivian squirrel monkeys (Saimiri boliviensis)

Two different approaches were used to identify new microsatellite polymorphisms among captive Bolivian squirrel monkeys (Saimiri boliviensis). In the first case, PCR primers for published human microsatellite loci were screened using genomic DNA from squirrel monkeys. Six polymorphic loci were identified using DNA samples from 19 unrelated individuals. The average heterozygosity among these six loci is 0.73. In the second set of experiments, a DNA library was created from Saimiri genomic DNA, and clones were selected from that library by screening with probes containing di-, tri-, and tetranucleotide repeats. Six novel microsatellites were identified this way, with an average heterozygosity of 0.59. Primer pairs for these six cloned microsatellites were also screened using a series of DNA samples from ten other platyrrhine species to assess the potential utility of these loci in other taxa. This study provides 12 new DNA polymorphisms that will be useful for various studies of this genus and demonstrates that both approaches can be used to develop new DNA polymorphisms in platyrrhine species.     

Meiotic characterization and sex determination system of neotropical primates: Bolivian squirrel monkey Saimiri boliviensis (primates: Cebidae)

The chromosomal sex determination system differs among platyrrhine monkeys more than any other group of primates. Although a number of studies have investigated mitotic chromosomes across platyrrhine species, the meiotic chromosomes of many genera have not yet been described. The goal of this study was to characterize the sex determination system of Saimiri boliviensis. We described for the first time the meiotic cycle, confirming the sexual system in germ cells from testicular biopsies of four adult male S. boliviensis. All specimens were weighed and testicular volume was measured. We observed 22 bivalents corresponding to 2N = 44, and a "human-like" XY bivalent was found in diakinesis/metaphase I. In addition, mitotic studies from blood samples of both sexes were performed and G- and C-banding patterns agreed with previously reported karylogy of S. boliviensis boliviensis. Further meiotic studies should be performed in New World primates based on the great value of those studies for systematic evolutionary biology and conservation programs.     

Stillbirth of twins in a squirrel monkey (Saimiri boliviensis peruviensis)

This is the first published report of twinning in a squirrel monkey (genus Saimiri). The mother survived but the twins, both male and close to full term, were stillborn     

Presence of platelet-activating factor in squirrel monkey (Saimiri boliviensis) spermatozoa: seasonal differences

Platelet-activating factor (1-O-alkyl-2-acetyl-sn-glycero-3-phosphorylcholine) (PAF) is a potent signaling phospholipid which has pleiotropic biological properties in addition to platelet activation. PAF has been detected in the spermatozoa in a number of species. The concentration of PAF is inversely related to human spermatozoal quality. There are no reports on the presence of PAF in nonhuman primate spermatozoa. Therefore, the primary objective of this study was to determine if PAF is present in the spermatozoa from the squirrel monkey (which is a seasonal breeder). A second objective was to determine if PAF levels change from the breeding to the nonbreeding season. Endogenous lipids were extracted from mature Bolivian squirrel monkeys (Saimiri boliviensis) spermatozoa and assayed for the presence of PAF by [¹²⁵I] radioimmunoassay. PAF was detected in all samples assayed. PAF levels were significantly higher (P< 0.01) during the breeding season (mean: 3.58 ng/10⁶ spermatozoa) than the nonbreeding season (mean: 0.76 ng/10⁶ spermatozoa). The data demonstrate that PAF is present in squirrel monkey spermatozoa, with higher levels found during the breeding season. Additional studies are warranted to elucidate the role of PAF in spermatozoa function. Am. J. Primatol. 45:301–305, 1998. © 1998 Wiley-Liss, Inc.     

Age-related hormonal differences in cycling squirrel monkeys (Saimiri boliviensis boliviensis)

This study was planned to evaluate the poor reproductive performance of aged squirrel monkeys in a self-sustaining breeding colony. Two groups of monkeys aged 6–8 years (Group 1), and >12 years (Group 2) were evaluated. During the midbreeding season, daily blood samples were obtained for a period of 35 days from 10 animals in each group. Blood samples were assayed for serum estradiol (E), progesterone (P), and bioassayable luteinizing hormone (bio-LH) concentrations and the data were analyzed by ANOVA (analysis of variance). Bio-LH surges were less frequent in the aged breeders (Group 2). Total P output during periovulatory period (day ?;3 to day + 3) and the total P output during the luteal phases of the estrus cycles were significantly lower in aged squirrel monkeys (Group 2, P < 0.003). Although E peaks occurred less frequently in Group 2, they had higher concentrations as compared to Group 1 (P < 0.003). Cumulative periovulatory and luteal phase E levels did not differ between the two groups. The reduction in P output in aged squirrel monkeys may interfere with proper implantation, thus contributing to the lower pregnancy rate observed in this age group. The decreased frequency of bio-LH surges indicated less frequent ovulations in the aged animals which may further impair reproduction with aging. © 1994 Wiley-Liss, Inc.     

Seasonal changes in serum dehydroepiandrosterone,androstenedione, and testosterone levels in the squirrel monkey (Saimiri boliviensis boliviensis)

The squirrel monkey (Saimiri boliviensis boliviensis) has a well-defined breeding season during which adult males undergo androgen-dependent morphological changes, with acquisition of active spermatogenesis. To assess the hormonal events of this annual cycle, blood samples were obtained weekly from ten adult males, and serum was assayed for testosterone (T), androstenedione (ΔA), and dehydroepiandrosterone (DHEA). A significant seasonal variation was noted in mean serum T (P < 0.02), ΔA (P < 0.02), and DHEA (P < 0.001) concentrations. Mean ΔA concentrations increased from a nonbreeding season nadir of 91.4 ± 12.9 ng/ml (mean ± standard error) to a prebreeding concentration of 139 ± 10.5 ng/ml and breeding season peak of 167.5 ± 15.4 ng/ml (P < 0.05). Mean DHEA concentrations increased from a nonbreeding season nadir of 8.3 ± 0.8 to a breeding season peak of 14.3 ± 1.2 (P < 0.001). Mean T levels in the nonbreeding (52.2 ± 11.6 ng/ ml) and prebreeding season (48.6 ± 7.4) were similar. However, T significantly increased during the breeding season to 103.5 ± 12.8 ng/ml (P < 0.05). Progressive changes in body weight and morphology paralleled the rise in serum ΔA levels. The pattern of peripheral serum androgen concentrations throughout the year would suggest annual activation of the hypothalamic-pituitary-adrenal and/or hypothalamic-pituitary-gonadal axes.     

Growth of skeletal components in the young squirrel monkey (Saimiri sciureus boliviensis): a longitudinal experiment

A functional skeletal criterion, as an extension of the van der Klaauw's cranial theory, was adopted in the present study. The null hypothesis tested was: "The major skeletal components of the platyrrhine body grow linearly, regardless of their functional dependence to different demands." The acceptance of the hypothesis will imply that all Saimiri skeletal growth may be satisfactorily explained by independent variables in a single equation. The rejection will suggest that such skeletal growth patterns have to be explained by variables in several different equations, and perhaps these equations may vary with the effect of sex and undernutrition. Control and undernourished squirrel monkeys were radiographed monthly for 2 years; they were also measured; and their volumetric and morphometric neurocranial, facial, and pelvic indices were calculated. The curves that best described each of the 24-point sequences were obtained. Three main growth patterns were observed: 1) Simple linear (femur length for all groups, and pelvic index for control and undernourished females), for which the simple regression equation explained more than 95% of the variation; 2) Complex linear (pelvic index for control and undernourished males, and neurocranial and facial indices for all of the groups), for which more than 95% of the variation was explained by one of the four four-function type equations; and 3) Noncorrelated with age (neurofacial index for undernourished males, and pelviofemoral index for control females and undernourished males and females), which showed nonsignificant correlations with respect to age. The food intake and the oscillations of the environmental temperature might help to explain the undulating growth trajectory observed in the complex linear components.     

Neonatal activity and state control differences among three squirrel monkey subspecies (Saimiri sciureus sciureus,S. boliviensis boliviensis,and S. boliviensis peruviensis)

Squirrel monkeys are a long-standing biomedical model, with multiple species and subspecies housed in research facilities. Few studies have examined the developmental differences between these subspecies, which may affect research outcomes. The primate neonatal neurobehavioral assessment was completed at 2 weeks of age with 279 dam-reared squirrel monkeys (188 Saimiri boliviensis boliviensis, 45 S. b. peruviensis, and 46 Saimiri. sciureus sciureus). Activity, orientation to stimuli, state control, and motor maturity scores, as well as startle responses and number of vocalizations were compared across subspecies and sex using factorial analysis of covariance (ANCOVAs) controlling for birthweight. There were no differences in orientation or motor maturity scores (p > .05) among the three subspecies or between sexes; however, there were significant subspecies differences in motor activity and state control scores. Of the three subspecies, S. s. sciureus has the lowest state control and activity scores (p < .05). They also had the most exaggerated startle response/aversion to a sudden loud noise, vocalized significantly less, and were less likely to resist restraint during the assessment (p < .05). The three subspecies of squirrel monkeys did not differ in motor development and attention to external stimuli but were significantly different in state control and activity levels. Overall S. s. sciureus were less active, agitated, irritable, and easier to console compared to S. b. boliviensis and S. b. peruviensis. This supports field research on socioecology which documented different social structure and behavior in wild populations of S. s. sciureus compared to S. b. boliviensis and S. b. peruviensis.     

Phenotypic and Functional Characterization of Lymphocytes from Different Age Groups of Bolivian Squirrel Monkeys (Saimiri boliviensis boliviensis)

Due to many physiological and genetic characteristic similarities to humans, squirrel monkeys provide an ideal animal model specifically for studying malaria, and transmissible spongiform encephalopathies (Creutzfeldt-Jacob disease). While squirrel monkeys three years and older are generally considered adult subjects suitable for use in medical research studies, little is known about the functional properties of lymphocytes in relation to the age of these animals, which could significantly impact the quality and quantity of innate and adaptive immune responses. In this study, we investigated differences in the phenotype and function of lymphocytes subsets of young (3–4 years), adult (8–10 years) and aged (16–19 years) squirrel monkeys. In general, animals in all three age groups exhibited comparable numbers of different lymphocyte subsets except for CD20+ B cells that were significantly lower in aged relative to young animals and T cells subsets expressing both CD4 and CD8 (double positive) were significantly higher in aged relative to young animals. With increasing age, phenotypic differences in central and effector memory T cells subsets were observed, that were more pronounced for the CD8+ T cells. Despite equal proportions of CD3+ T cells among the three age groups, responses of peripheral blood mononuclear cells to T cell mitogens PHA and Con A showed lower IFN-γ producing cells in the aged group than that in the young group. Furthermore, aged animals showed significantly higher plasma levels of inflammatory cytokines IL-6, IFN-γ, TNF-α, IL-10 and IL-12. These findings suggest that while the squirrel monkeys in general share phenotypic and functional similarities of lymphocyte subsets with humans in relation to age, specific differences exist in immune function of lymphocytes between young and old animals that could potentially impact experimental outcomes for which the measurement of immunologic endpoints are critical.     

Ovarian stimulation of squirrel monkeys (Saimiri boliviensis boliviensis) using pregnant mare serum gonadotropin

The application of assisted reproductive technologies (ART) to nonhuman primates has created opportunities for improving reproductive management in breeding colonies, and for creation of new animal models by genetic modification. One impediment to the application of ART in Saimiri spp. has been the lack of an effective gonadotropin preparation for ovarian stimulation. Pregnant mare serum gonadotropin (PMSG) is inexpensive and readily available, but its repeated use in rhesus monkeys has been associated with induction of a refractory state. We have compared PMSG to recombinant human follicle stimulating hormone (rhFSH) for controlled ovarian stimulation in Bolivian squirrel monkeys. Groups of mature squirrel monkeys received rhFSH (75 IU daily) or PMSG (250 IU twice daily) by subcutaneous injection for 4 d during the breeding season (November to January) or nonbreeding season (March to September). Serum estradiol (E2) was measured daily. Follicular growth was monitored by abdominal ultrasound. During the breeding season, PMSG induced a higher E2 response than did rhFSH, with mean E2 levels being significantly higher within 3 d of stimulation. Superior follicular development in PMSG animals was confirmed by abdominal ultrasonography. During the nonbreeding season, PMSG elicited a similar increase in serum E2 levels despite the fact that basal serum E2 is typically low during the nonbreeding season. Repeated use of PMSG (< or = 3 cycles of administration) produced no attenuation of the E2 response. We conclude that PMSG is highly effective for repeated cycles of controlled ovulation stimulation in the squirrel monkey.     

Confirmation of ovulation and characterization of luteinizing hormone and progesterone secretory patterns in cycling,isosexually housed Bolivian squirrel monkeys (Saimiri boliviensis boliviensis)

In the female Bolivian squirrel monkey a much greater elevation of serum estradiol (E₂) was measured after mating than that observed in similary cycling monkeys that did not mate. This raised the possibility that cycling squirrel monkeys may not ovulate during nonmated cycles To test this hypothesis, we performed laparoscopies on nine isosexually housed, cycling monkeys to observe the ovaries after the luteinizing hormone (LH) surge, which was measured by mouse interstitial cell bioassay using LER 1909-2 as the standard. Single ovulatory stigmas were identified as well demarcated, red, punctate depressions at the center of dome-shaped elevations on the ovarian surface in eight monkeys, when laparoscopically examined 9-56 hr after the LH peak. One monkey examined laparoscopically prior to the LH surge had a large translucent cystic follicle, confirming the morphology of the mature prevulatory follicle. Mean progesterone (P) concentrations fell to a nadir 1 day prior to the LH surge and then began to rise on the LH surge. Peak P levels were found 2 days after the LH surge. In the ovulating animals in which periovulatory E₂ levels were measured, no value was greater than 800 pg/ml, indicating that the presence of follicular rupture was not sufficient to account for the elevated E₂ levels observed after mating. These data confirm ovulation and follicular rupture in the absence of mating and delineate the relationship between periovulatory LH, P, and E₂ secretory patterns in cycling squirrel monkeys.     

Age-related diffuse chronic telogen effluvium- type alopecia in female squirrel monkeys (Saimiri boliviensis boliviensis)

We investigated the diffuse alopecia affecting some female squirrel monkeys (Saimiri boliviensis boliviensis) housed in a breeding facility. We randomly selected 100 female and 10 male animals and performed a complete physical exam and a hair assessment on all animals; blood tests, trichograms, hair density; and skin biopsies in representative cases; and a dominance behavioral assessment of 50 animals. Hair coat was normal in 35 female monkeys and all 10 male animals. Of the 65 females with diffuse alopecia, 17 had mild, 22 moderate, and 26 severe hair loss. The alopecia group had a mean age of 9.6 +/- 0.6 years, whereas that of the normal group was 4.7 +/- 0.6 years (P < 0.05). The parity in the alopecia group was 4.2 +/- 0.6 but 2.0 +/- 0.6 (P < 0.05) in the normal group. There were no statistically significant differences in body weight, hemoglobin, blood urea nitrogen, serum glucose, liver aspartate aminotransaminase, or free thyroxine. The trichogram demonstrated 20.8% +/- 1.6% (mean +/- standard error) of telogen hairs in the alopecia group compared with 9.5% +/- 2.8% of the control group (P < 0.05). The hair density in the alopecia group was 52.8 +/- 4.1/cm2 and 79.6 +/- 14.3/cm2 in the control group. Skin biopsies in affected monkeys demonstrated increased telogen follicles, with no fibrosis or inflammation. There were no statistically significant differences in the dominance behavioral analysis. The findings are consistent with chronic telogen effluvium (CTE). A number of organic, behavioral, and dominance-related stress causes of CTE were excluded. CTE appears to be predominantly age-related in this population. CTE in female squirrel monkeys may serve as an animal model for human diffuse alopecia.