Substrate determines asymmetrical gait dynamics in marmosets (Callithrix jacchus) and squirrel monkeys (Saimiri boliviensis)

Studies of skeletal pathology indicate that injury from falling accounts for most long bone trauma in free‐ranging primates, suggesting that primates should be under strong selection to manifest morphological and behavioral mechanisms that increase stability on arboreal substrates. Although previous studies have identified several kinematic and kinetic features of primate symmetrical gaits that serve to increase arboreal stability, very little work has focused on the dynamics of primate asymmetrical gaits. Nevertheless, asymmetrical gaits typify the rapid locomotion of most primates, particularly in smaller bodied taxa. This study investigated asymmetrical gait dynamics in growing marmosets and squirrel monkeys moving on terrestrial and simulated arboreal supports (i.e., an elevated pole). Results showed that monkeys used several kinematic and kinetic adjustments to increase stability on the pole, including reducing peak vertical forces, limiting center of mass movements, increasing substrate contact durations, and using shorter and more frequent strides (thus limiting disruptive whole‐body aerial phases). Marmosets generally showed greater adjustment to pole locomotion than did squirrel monkeys, perhaps as a result of their reduced grasping abilities and retreat from the fine‐branch niche. Ontogenetic increases in body size had relatively little independent influence on asymmetrical gait dynamics during pole locomotion, despite biomechanical theory suggesting that arboreal instability is exacerbated as body size increases relative to substrate diameter. Overall, this study shows that 1) symmetrical gaits are not the only stable way to travel arboreally and 2) small‐bodied primates utilize specific kinematic and kinetic adjustments to increase stability when using asymmetrical gaits on arboreal substrates. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Gait selection and the ontogeny of quadrupedal walking in squirrel monkeys (Saimiri boliviensis)

Locomotor researchers have long known that adult primates employ a unique footfall sequence during walking. Most mammals use lateral sequence (LS) gaits, in which hind foot touchdowns are followed by ipsilateral forefoot touchdowns. In contrast, most quadrupedal primates use diagonal sequence (DS) gaits, in which hind foot touchdowns are followed by contralateral forefoot touchdowns. However, gait selection in immature primates is more variable, with infants and juveniles frequently using LS gaits either exclusively or in addition to DS gaits. I explored the developmental bases for this phenomenon by examining the ontogeny of gait selection in juvenile squirrel monkeys walking on flat and simulated arboreal substrates (i.e., a raised pole). Although DS gaits predominated throughout development, the juvenile squirrel monkeys nonetheless utilized LS gaits in one-third of the ground strides and in one-sixth of pole strides. Multiple logistic regression analyses showed that gait selection within the juvenile squirrel monkey sample was not significantly associated with either age or body mass per se, arguing against the oft-cited argument that general neuromuscular maturation is responsible for ontogenetic changes in preferred footfall sequence. Rather, lower level biomechanical variables, specifically the position of the whole-body center of mass and the potential for interference between ipsilateral fore and hindlimbs, best explained variation in footfall patterns. Overall, results demonstrate the promise of developmental studies of growth and locomotor development to serve as "natural laboratories" in which to explore how variability in morphology is, or is not, associated with variability in locomotor behavior.     

Age and seasonal effects on predator-sensitive foraging in squirrel monkeys (Saimiri sciureus): a field experiment

A field experiment was conducted to examine the effect of perceived predation risk on the use of foraging areas by juvenile and adult primates under different conditions of local food abundance. Wild squirrel monkeys, Saimiri sciureus, were observed in an experiment conducted during the dry and the wet seasons at a site in Eastern Amazonia, Brazil. Animals were presented with feeding platforms that differed in food quantity and exposure to aerial predators through varying vegetative cover. In the dry season, juveniles and adults chose platforms based solely on food quantity. However, in the wet season, juveniles foraged preferentially on high-reward platforms only if cover level also was high (i.e., potentially offered greater concealment from predators). In contrast, adults showed the same pattern of platform use regardless of season. These results indicate that age and local resource availability based on seasonality affect whether primates forage in a predator-sensitive manner. Juveniles may be more sensitive to predation risk when foraging, and individuals may take fewer risks when resource abundance is high in their environment.     

A study of correlates of hand preferences in squirrel monkeys (Saimiri sciureus)

The purpose of this study was to test the influence of sex, age, social rank, matriline membership, posture, and visual and tactual motor control on manual preferences inSaimiri sciureus. A well-established social group of 12 squirrel monkeys, aged 2 to 14 yrs and consisting of two matrilines with social rank known for each animal, was presented with four different food-reaching tasks and assessed for hand preferences with a minimum of 100 reaches per animal. Frequency of occurrence of hand preferences at the group level and degree of hand preferences at the individual level depended on posture and on whether the reaching act took place under visual or tactual guidance. Sex, age, social rank, and matriline membership were not found to determine frequency of occurrence, direction or degree of hand preferences with the exception of one task in which a significant negative correlation between the degree of hand preference and age was found. Nine out of 12 monkeys showed task-dependent changes in the hand they used preferentially while only three animals preferred the same hand in all four tasks. Significant preferences for the use of right or left hand on a given task were distributed almost equally between individuals. Thus, the results of this study suggest task-specific demands like posture and/or whether reaching was visually or tactually guided to be the major correlates of hand preferences in food-reaching tasks in squirrel monkeys.     

Hemobartonellosis in squirrel monkeys (Saimiri sciureus) in a domestic breeding colony: case report and preliminary study

Infection with Hemobartonella sp was diagnosed in a colony-born squirrel monkey with normocytic, normochromic anemia and pronounced punctate erythrocytic basophilic stippling on Wright's-Giemsa stained blood films. The diagnosis was confirmed using transmission electron microscopy. Two randomly selected colony-born squirrel monkeys were splenectomized in an effort to activate and detect possible latent hemobartonellosis . One monkey became parasitemic 12 days following splenectomy. The second monkey was inoculated on day 14 with 1 ml of whole blood from an infected, but nonparasitemic monkey and developed overt parasitemia 3 days later (day 17 following splenectomy). Infections in the latter two monkeys were confirmed using scanning electron microscopy.     

Elevation in plasma glucagon levels in response to stress in squirrel monkeys: comparisons of two subspecies (Saimiri sciureus boliviensis and Saimiri sciureus sciureus)

Bolivian (Bo) and Brazilian (Br) squirrel monkeys (SMs) were captured and restrained to determine patterns of glucagon and glucose response. In both subspecies, plasma glucagon and glucose levels rose rapidly in response to restraint procedures; glucagon levels in BrSMs and glucose levels in both subspecies returned to basal values in 15 minutes. The magnitude of the glucagon and glucose responses differed significantly between BoSMs and BrSMs.     

Postnatal changes of IgG and IgM levels in squirrel monkeys (Saimiri sciureus)

Serum IgG and IgM levels were measured in domestically bred squirrel monkeys (Saimiri sciureus) ranging in age from 0 days to 42 months, as well as in adult squirrel monkeys from the wild estimated to be 60 months or older. The results indicated that the transplacental transfer of IgG occurs in the squirrel monkey but the transferability is lower in the squirrel monkey than in the cynomolgus monkey. Immune response in the squirrel monkey occurs just after birth, as shown by IgM production.     

Sequences and timing of dental eruption in Bolivian captive-born squirrel monkeys (Saimiri sciureus)

Squirrel monkeys, colony-born from Bolivian parents, were studied to establish the sequences and timing of eruption for deciduous and permanent teeth. Infants were born with a naked gingiva, and in only one monkey was di₁ present at birth. The eruption of the lower deciduous teeth preceded their upper counterparts with the exception of di2, dc, and dpm2. No significant differences were found between the right and left quadrants of the mandible and maxilla. No significant sexual differences were found in the age of eruption. By the age of 14 weeks, all deciduous teeth had erupted. The sequence of eruption of the replacement teeth was different from that of milk teeth. The differences lie in the delayed eruption of canine teeth and in the inverted sequence, from the back to the front, of the premolar series. Significant sexual differences were found in total eruption (TE) for PM₃ and I² (P < 0.05) and highly significant differences (P < 0.01) in TE and initial eruption (IE) for C¹, females being more precocious than males. The age at which monkeys completed dental eruption was highly variable, 103–119 weeks for males and 89–112 weeks for females. Differences were found when our results were compared with those of Long and Cooper [1968] for Colombian squirrel monkeys.     

Comparison of rectal and tympanic core body temperature measurement in adult Guyanese squirrel monkeys (Saimiri sciureus sciureus)

Background Measuring core body temperature in a manner that is safe for animals and veterinary personnel is an important part of a physical examination. For nonhuman primates, this can involve increased restraint, additional stress, as well as the use of anesthetics and their deleterious effects on body temperature measurements. The purpose of this study was to compare two non‐invasive methods of infrared tympanic thermometry to standard rectal thermometry in adult squirrel monkeys. Methods Tympanic temperatures were collected from 37 squirrel monkeys and compared to rectal temperatures using a human and veterinary infrared tympanic thermometer. Results Compared with rectal temperature measurements, the human tympanic thermometer readings were not significantly different, while the veterinary tympanic thermometer measurements were significantly higher (P < 0.05). There were no differences between sexes. Conclusions The tympanic thermometer designed for use in humans can be used in adult squirrel monkeys as an alternative to rectal thermometry for assessing core body temperature.     

Hysterosalpingography: a technique to aid in assessment of reproductive fitness of female squirrel monkeys (Saimiri sciureus)

A hysterosalpingography method was developed to examine the uterine cavity and oviducts of potential additions to our squirrel monkey breeding colony and those animals within the colony with a history of infertility. Females to be examined were anesthetized and placed in dorsal recumbency. A needle was inserted transabdominally into the body of the uterus, the cervix was sealed with a clamp applied vaginally, and water soluble contrast media was infused into the uterine cavity with sufficient pressure to fill the oviducts. Radiographs were obtained during infusion resulting in visualization of the uterine cavity and the lumina of the oviducts. The ovaries were visualized as they were surrounded by contrast media draining from the fimbriae of the oviducts. Hysterosalpingography proved to be a useful method for clinical evaluation of reproductive potential of female squirrel monkeys. It also has provided a means to diagnose causes of infertility associated with dysfunction of the oviducts.     

Prenatal growth of long bones in rhesus and squirrel monkeys (Macaca mulatta and Saimiri sciureus)

Fetal long bone growth was studied from 59 radiographs representing 35 macaques and 79 radiographs representing 16 squirrel monkeys. From lateral abdominal radiographs of pregnant females total lengths of long bone shadows were measured to the nearest millimeter with a sliding caliper. A linear regression line was fitted to the data for each species. The high correlation coefficients (min. = 0.92) indicated not only that over 80% of the variance in longbone length was associated with the regression but also that linear regression was an acceptable model. It was determined that the macaque long bones grew more rapidly prenatally than the squirrel monkey long bones. Saimiri long bones grew at a faster rate during the second half of gestation than would be expected considering that the macaque long bones were approximately twice the length of Saimiri long bones at birth and that the duration of their gestation was about the same. Thus squirrel monkeys must achieve a greater percentage of their birth size during the second half of gestation.     

Seasonal changes of serum concentrations of estradiol and progesterone in Bolivian squirrel monkeys (Saimiri sciureus)

Serial measurements of estradiol (E2) and progesterone (P) were used to describe the ovarian cycle of the Bolivian squirrel monkey. Group-caged, sexually mature female squirrel monkeys, housed with males, were sampled daily between 0900 and 1100 hr. Sampling was carried out during the breeding and nonbreeding seasons, for periods of 19–20 days from September 1981 to May 1982. Seasonal differences in serum concentrations of E2 and P were found with low levels of E2 and P and an absence of preovulatory surges of E2 during the nonbreeding season. This pattern was also observed in some animals during the breeding season. An abrupt increase in serum P concentrations in December appeared to signal the onset of cycling. Cycling animals had well-defined peaks of E2 (450–9,500 pg/ml) followed by increasing levels of P, which were >200 ng/ml in some animals. After the breeding season, E2 and P levels returned to their initially low levels. Levels of both steroids in cycling animals were higher than those reported for other primates and for previous measurements made in squirrel monkeys. Cycle length based on time interval between consecutive E2 peaks varied from 6–12 days.     

Demography of squirrel monkeys (Saimiri sciureus) in captive environments and its effect on population growth

Understanding which life-history variables have the greatest influence on population growth rate has great ecological and conservation importance. Applying models of population regulation and demographic mechanisms can aid management and conservation of both wild and captive populations. By comparisons of sensitivity, elasticity, and life-table response analyses, we identified demographic processes that were most likely to produce changes in population size (via prospective analyses) and the traits that actually influenced population changes (via retrospective analyses) among sexes, zoological facilities, and generations of captive squirrel monkey populations (Saimiri sciureus). Variation in life-history traits occurs within each group analyzed. Those traits that vary the most include age at maturity, age at last reproduction, and fertility. Zoos with increasing population growth rates maintain earlier ages of maturity, later ages of last reproduction, high rates of juvenile and adult survival, and most importantly greater fertility, reflecting shorter inter-birth intervals. Using prospective analyses, juvenile and adult survivals were predicted to be demographic traits with the greatest effect on population growth. Surprisingly, and despite predictions, retrospective analyses revealed that fertility was the life-history characteristic trait that contributed the most to changes in population size.     

Cranial growth in Saimiri sciureus (Cebidae) and its alteration by nutritional factors: A longitudinal study

Ten male Saimiri sciureus boliviensis (Cebidae), born at the Centro Argentino de Primates (CAPRIM), were grown in captivity. At weaning (6 months old), five individuals were fed ad libitum on a 20% protein diet (controls). The other five animals were fed ad libitum on a 5% protein diet (malnourished). Animals were radiographed monthly. The length, width, and height of the anterior, middle, and posterior components of the neurocranium, and those of the masticatory, respiratory, and optic components of the face were measured. A pattern of high growth rate was observed in both the three facial and the middle neural components. The anterior and posterior neural components showed a pattern of low rate of growth. The growth behavior of each variable was also different. Lengths grew more than widths and heights in the facial components, whereas widths grew more than heights and lengths in the neurocranium. Malnutrition delayed growth in size and altered the normal shape changes. High-patterned variables, such as masticatory and respiratory lengths, and the anterior and middle neural widths were particularly affected. The masticatory and the middle neural components underwent the greatest growth arrest. The optic and the respiratory components suffered a mild effect. The anterior and the posterior neural components were affected to a lesser degree. Am J Phys Anthropol 102:545–554, 1997. © 1997 Wiley-Liss, Inc.     

Hematologic values of normal Bolivian squirrel monkeys (Saimiri sciureus): a comparison between wild-caught and laboratory-bred male animals

Complete and differential blood counts were conducted on 23 male squirrel monkeys (Saimiri sciureus) of Bolivian origin. The sample included 9 laboratory-bred and 14 wild-caught adult monkeys weighing between 600 and 1,500 g. The means of total white blood cell (WBC) counts, total hemoglobin and hematocrits of laboratory-bred animals were found to be significantly different from those of wild-caught monkeys (p less than 0.01). Other hematologic parameters showed no significant differences between the two experimental groups. 3 of 14 (21.0%) wild-caught animals each had 1 reactive lymphocyte and 7% of the same group had 10 nucleated erythrocytes per 100 WBC. No reactive lymphocytes or nucleated erythrocytes were observed in laboratory-bred animals. The importance of these baseline data and the basis for the differences observed between laboratory and wild-caught monkeys are discussed within the context of experimental studies involving primates in which hematologic parameters are valuable.     

Biochemical and hormonal correlates of dominance and social behavior in all-male groups of squirrel monkeys (Saimiri sciureus)

This study examined the relationship between dominance rank and several physiological and behavioral measures in stable, captive, all-male squirrel monkey groups. Four groups, each containing three males, were observed for 12 weeks during the breeding season. Relative dominance ranking among males in each group was based on the direction of agonistic behaviors displayed. For each subject, whole blood serotonin (WBS), plasma testosterone (T), and cortisol (C) were sampled 4 to 6 times over the course of the study. Samples were separated by 1- to 2-week intervals. Each group had a stable linear dominance hierarchy. WBS had small intraanimal variance and was positively related to dominance rank. In contrast, T and C were highly variable within subjects and were unrelated to dominance rank. Among alpha males, concentrations of T and C were positively correlated, and WBS and C were negatively correlated. The effect of dominance rank on the relationship between within-animal fluctuations in WBS, T, and C and behavior was also assessed. In dominant, but not subordinate subjects, intraanimal fluctuations in WBS correlated with agonistic behavior initiated, and fluctuations in C and T correlated with huddling. In beta and gamma males, C was related to agonism received, and in gamma males to food stealing received. Dominance status also affected endocrine response to the stress of capture but not the rate of sneezing. Sneezing was positively correlated with T concentrations irrespective of dominance rank. These results extend the association between WBS and dominance rank previously reported in Old World monkeys to a New World monkey species, support previous suggestions that mean T and C titers are not reflective of dominance rank in well-established groups, and indicate that dominance rank affects adrenocortical response to the stress associated with capture and anesthesia.     

Taxonomy of squirrel monkeys genus Saimiri (Cebidae,platyrrhini): A preliminary report with description of a hitherto unnamed form

Two groups of squirrel monkeys, genus Saimiri, are distinguished by external characters. The first, or Roman type, contains Saimiri boliviensis of upper Amazonia south of the Rio Marañón-Amazonas, with two subspecies of which S. boliviensis peruviensis is described as new. The second group, or Gothic type, contains three species: Saimiri sciureus with four subspecies distributed over much of tropical South America, Saimiri ustus of Brazil between the south bank Amazonian Rios Purús and Xingu, and S. oerstedi isolated on a Pacific coastal area straddling Costa Rica and Panamá. The geographic range of S. sciureus overlaps parts of those of S. ustus and S. boliviensis. Incomplete karyotypic data indicate that the diploid number of chromosomes for the genus is 44. Geographic variation is characterized by reduction from seven to six or five paired acrocentric autosomes through pericentric inversion with reciprocal increase in number of paired submetacentric or subtelocentric autosomes. Geographic distribution, behavior, sexual dimorphism including dichromatism, and hybridization are discussed. Ventral guide hairs for orientation of subprecocial newborn toward the maternal mammae are described. Distinguishing characters of species and subspecies are provided in a key. The taxons are listed with the taxonomy of each discussed, their geographic distribution plotted and mapped.     

Adaptation of the Plasmodium falciparum FCB strain for in vitro and in vivo analysis in squirrel monkeys (Saimiri sciureus)

The asexual blood stages of the Plasmodium falciparum parasite are responsible for inducing the clinical symptoms and the most severe presentations of malaria infection that causes frequent mortality and morbidity in tropical and subtropical areas of the world, making the blood stages of infection a key target of new malaria treatment and prevention strategies. Progress towards the development of more effective treatment and prevention strategies has been hindered by the limited availability of infection models that permit the sequential analysis of blood stage parasites in vitro followed by in vivo analysis to confirm therapeutic benefits. To advance a model for in vitro and in vivo analysis of blood stage parasites, we examined nine laboratory strains of P. falciparum to determine which strains could adapt to growth in vivo in splenectomized squirrel monkeys (Saimiri sciureus). Only one of the nine laboratory strains tested, the FCB strain, adapted to in vivo growth. Morphological analysis show that the adapted ring-stage parasites have a different morphology from original parasites cultured in vitro, and more often they were found to localize at the edge of the infected red blood cell. No remarkable differences were observed for both trophozoites and schizonts. The adapted strain can be cultured back in vitro similar to the original parasite, indicating that the adapted parasite can develop both in vitro and in vivo. This squirrel monkey-adapted P. falciparum parasite is expected to be suitable and is advantageous for the research and development of vaccines and antimalarial drugs.     

Excretion and measurement of estradiol and progesterone metabolites in the feces and urine of female squirrel monkeys (Saimiri sciureus)

The first objective of the present study was to determine the metabolic form and rate of excretion of ovarian hormone metabolites in the urine and feces of female squirrel monkeys injected with radiolabeled progesterone (Po) and estradiol. The major portion of the urinary metabolites of both hormones was excreted within 16-24 hr post-injection. Estrogen and Po isotopes in feces exhibited an excretion peak at 16 hr post-injection. The majority of recovered radiolabel of both hormones was excreted in feces. Chromatographic separation of fecal extractions indicated that the major estrogen metabolites in feces are in the free as opposed to the conjugated form. The radioactivity and immunoreactivity for estrone and estradiol (E(1) and E(2), respectively) in eluates of fecal samples subjected to celite co-chromatography indicated that both free E(1) and E(2) exist as excretion products in the feces of female squirrel monkeys. The major radioactive peaks for Po metabolites showed peaks in the elution profile at or very near the Po standard, and corresponded with the celite co-chromatography elution profile of Po standard when subjected to enzyme immunoassay (EIA). The second objective was to validate the application of EIA systems to measure fecal metabolites. Reproductive events of one female squirrel monkey across one annual reproductive cycle are described using the endocrine profile generated from fecal steroid assays. Examination of this profile confirmed that longitudinal fecal sampling and steroid hormone metabolite measurement in feces was not only feasible and practical, but accurately detected known reproductive events as well.