Pleistocene diversification of living squirrel monkeys (Saimiri spp.) inferred from complete mitochondrial genome sequences

In order to enhance our understanding of the evolutionary history of squirrel monkeys (Saimiri spp.), we newly sequenced and analyzed data from seven complete mitochondrial genomes representing six squirrel monkey taxa. While previous studies have lent insights into the taxonomy and phylogeny of the genus, phylogenetic relationships and divergence date estimates among major squirrel monkey clades remain unclear. Using maximum likelihood and Bayesian procedures, we inferred a highly resolved phylogenetic tree with strong support for a sister relationship between Saimiri boliviensis and all other Saimiri, for monophyly of Saimiri oerstedii and Saimiri sciureus sciureus, and for Saimiri sciureus macrodon as the sister lineage to the S. oerstedii/S. s. sciureus clade. We inferred that crown lineages for extant squirrel monkeys diverged around 1.5 million years ago (MYA) in the Pleistocene Epoch, with other major clades diverging between 0.9 and 1.1 MYA. Our results suggest a relatively recent timeline of squirrel monkey evolution and challenge previous conceptions about the diversification of the genus and its expansion into Central America.     

Biologic data of Macaca mulatta, Macaca fascicularis, and Saimiri sciureus used for research at the Fiocruz primate center

Physiological parameters of laboratory animals used for biomedical research is crucial for following several experimental procedures. With the intent to establish baseline biologic parameters for non-human primates held in closed colonies, hematological and morphometric data of captive monkeys were determined. Data of clinically healthy rhesus macaques (Macaca mulatta), cynomolgus monkeys (Macaca fascicularis), and squirrel monkeys (Saimiri sciureus) were collected over a period of five years. Animals were separated according to sex and divided into five age groups. Hematological data were compared with those in the literature by Student's t test. Discrepancies with significance levels of 0.1, 1 or 5% were found in the hematological studies. Growth curves showed that the sexual dimorphism of rhesus monkeys appeared at an age of four years. In earlier ages, the differences between sexes could not be distinguished (p < 0.05). Sexual dimorphism in both squirrel monkeys and cynomolgus monkeys occurred at an age of about 32 months. Data presented in this paper could be useful for comparative studies using primates under similar conditions.     

Studies of the Sal I strain of Plasmodium vivax in the squirrel monkey (Saimiri sciureus)

The Sal I strain of Plasmodium vivax was successfully adapted to three phenotypes of the squirrel monkey, Saimiri sciureus. Through five linear blood passages, parasitemias in excess of 200,000/mm3 blood were attained; Bolivian phenotype Saimiri appear to develop higher peak parasitemias. Sporozoites of the Sal I strain inoculated intravenously produced patent parasitemias in all five squirrel monkeys challenged, with prepatent periods ranging from 21 to 38 days. Anopheles freeborni and An. gambiae were the most susceptible of eight anopheline species fed on infected squirrel monkeys. As a model for in vivo studies of P. vivax the Sal I strain in Saimiri has great potential.     

Ecological and Social Factors Affecting the Vocal Behavior of Adult Female Squirrel Monkeys

Focal recordings of the vocalizations of squirrel monkeys, Saimiri sciureus, occupying an undisturbed Peruvian habitat were collected to evaluate the importance of both the ecological and social functions of female vocal behavior. The rates and sequences of six call types were examined by context: single, double, and multiple chuck, peep, tweet, and tweet-chuck. In contrast to laboratory studies, our findings emphasize the primacy of ecological functions in the wild, where calling permits females to operate as a convoy of spatially separated individuals in an arboreal habitat where visual contact is limited. Chuck calls are probably best interpreted as contact calls. The rate of chucks and tweet-chucks increased when the nearest adult female was > 5 m away. However, call production did not predict a change in the spatial separation between a female and her nearest adult female. During travel, the rate of single and double chucks was greater and the rate of multiple chucks was reduced. No direct relationship was found between foraging activities and vocal behavior. Although secondary, social factors did have a subtle effect on vocal behavior: the larger the social alliance of a female, the lower the rate and repetitiveness of her chuck vocalizations. We also consider the role of variations in vocalization rates among primates and the differing conclusions of field and captive studies of squirrel monkey vocal behavior.     

Reconciliation in captive Guyanese squirrel monkeys (Saimiri sciureus)

The tendency for agonistic interaction to increase the probability of friendly interaction between social partners has been demonstrated across a range of Old World primates. While research on such post-conflict behavior proceeds into an hypothesis-testing phase, new comparative information must accumulate to provide full phylogenetic perspective on primate social behavior. Data from New World and prosimian primates are yet extremely limited. We studied captive squirrel monkeys (Saimiri sciureus) via post-conflict (PC) and matched control (MC) observations and analyzed results using both the PC-MC and time-rule methods. Former opponents maintaining affiliative relationships soon engaged in friendly interaction following large proportions of agonistic interactions, whereas non-affiliated individuals, including virtually all male-female pairs, reconciled conflicts rarely. Close-proximity approaching and huddling contact constituted the principal modes of post-conflict amicability. Agonistic interactions of relatively high intensity were most likely to be reconciled and most likely to be reconciled via physical contact. High vulnerability of Saimiri to predation may have favored this species' strong inclination to reconcile soon after agonistic interaction. Research on free-living populations of this and other primate species is needed to illuminate similarities and differences across taxa.     

Distribution, ecology, life history, genetic variation, and risk of extinction of nonhuman primates from Costa Rica

We examined the association between geographic distribution, ecological traits, life history, genetic diversity, and risk of extinction in nonhuman primate species from Costa Rica. All of the current nonhuman primate species from Costa Rica are included in the study; spider monkeys (Ateles geoffroyi), howling monkeys (Alouatta palliata), capuchins (Cebus capucinus), and squirrel monkeys (Saimiri oerstedii). Geographic distribution was characterized accessing existing databases. Data on ecology and life history traits were obtained through a literature review. Genetic diversity was characterized using isozyme electrophoresis. Risk of extinction was assessed from the literature. We found that species differed in all these traits. Using these data, we conducted a Pearson correlation between risk of extinction and ecological and life history traits, and genetic variation, for widely distributed species. We found a negative association between risk of extinction and population birth and growth rates; indicating that slower reproducing species had a greater risk of extinction. We found a positive association between genetic variation and risk of extinction; i.e., species showing higher genetic variation had a greater risk of extinction. The relevance of these traits for conservation efforts is discussed.     

Disparate Data Sets Resolve Squirrel Monkey (Saimiri) Taxonomy: Implications for Behavioral Ecology and Biomedical Usage

Squirrel monkeys (Saimiri spp.) are the most commonly used neotropical (platyrrhine) monkeys in biomedical research; however, no consensus exists as to the phylogenetic relationships amongst geographic variants or whether these variants represent species or subspecies. Here we report a strongly supported squirrel monkey phylogeny, congruent across multiple data sets, including new field data and the first molecular (mtDNA) cladogram. These data support species-level classification for the three major groups in this study. Approximately the same amount of molecular divergence exists among Saimiri oerstedii, S. sciureus, and S. boliviensis. The S. sciureus/S. oerstedii ancestor diverged from S. boliviensis and shortly thereafter S. sciureus and S. oerstedii diverged. Until now, lack of a robust taxonomy has hindered exploitation of the massive potential of Saimiri for comparative studies. No other primate genus displays such widely divergent, genetically-based social behaviors. Our taxonomy also provides robust support for previous warnings against the widespread use of hybrid squirrel monkeys as research models.     

Taste preference thresholds for food-associated sugars in the squirrel monkey (Saimiri sciureus)

The purpose of this study was to determine taste preference thresholds for four different food-associated sugars inSaimiri sciureus. Using a two-bottle test three male squirrel monkeys were found to significantly prefer 10 mM sucrose, 40 mM fructose, 90 mM glucose, and 100 mM lactose over tap water. Presentation of suprathreshold sugar solutions led to marked concentration-dependent and monotonically increasing polydipsia. The results showed the squirrel monkey to prefer lower sugar concentrations compared to other non-human primates and thus support the assumption that this species may use sweetness as a criterion for food selection.     

Diversity, Geographic Distribution and Conservation of Squirrel Monkeys, Saimiri (Primates, Cebidae), in the Floodplain Forests of Central Amazon

Eleven taxa of primates are found in the floodplains of the western portion of the central Brazilian Amazon, protected in part by the Mamirauá Sustainable Development Reserve. The taxonomy of the squirrel monkeys, the number of taxa, and their geographic distributions are still poorly understood. Here we investigate differentiation among the taxa of this genus in Mamirauá, examining their morphology and geographic distribution. We registered 333 points of occurrence of squirrel monkeys and examined 117 specimens deposited in scientific collections. The results of the morphological analyses were generally in good agreement with field observations. Together they indicate the existence of three taxa: Saimiri vanzolinii, Saimiri sciureus macrodon, and S. s. cassiquiarensis. The restricted range of Saimiri vanzolinii in the southeastern portion of the reserve covers an area of 870 km², and it is among the smallest of the distribution areas for any Neotropical primate species. Saimiri sciureus cassiquiarensis has a disjunct distribution, crossing the Japurá River to the right bank into the reserve in two places, and S. s. macrodon is the squirrel monkey ranging widely in the northwest of Mamirauá. There are three areas of parapatry: one between Saimiri vanzolinii and Saimiri sciureus macrodon and two between S. vanzolinii and S. s. cassiquiarensis. We recommend that anthropogenic changes in the region be monitored, and conservation measures be taken to protect these primates, especially considering the endemism and very restricted range of Saimiri vanzolinii and its consequent vulnerability to extinction.     

Behavioural evidence of sex-linked colour vision polymorphism in the squirrel monkey Saimiri ustus

Squirrel monkeys, like most Neotropical primates, display a sex-linked colour vision polymorphism. Here we assess the colour perception of 8 Saimiri ustus by a behavioural paradigm using Munsell colour chips as discriminating stimuli. A random variation in brightness assured that discriminations were based on colour rather than brightness cues. Results indicate that all males showed random performances when presented with stimuli which, in previous experiments with human colour-blind individuals and dichromatic non-human primates, proved to be difficult to discriminate. Females behaved as trichromats. The different phenotypes in S. ustus may offer diverse advantages in feeding ecology and are in agreement with the existence of vision polymorphism, as described for other species of squirrel monkeys.     

Primates got personality,too: Toward an integrative primatology of consistent individual differences in behavior

In recent years, research on animal personality has exploded within the field of behavioral ecology. Consistent individual differences in behavior exist in a wide range of species, and these differences can have fitness consequences and influence several aspects of a species' ecology. In comparison to studies of other animals, however, there has been relatively little research on the behavioral ecology of primate personality. This is surprising given the large body of research within psychology and biomedicine showing that primate personality traits are heritable and linked to health and life history outcomes. In this article, I bring together theoretical perspectives on the ecology and evolution of animal personality with an integrative review of what we know about primate personality from studies conducted on captive, free‐ranging, and wild primates. Incorporating frameworks that emphasize consistency in behavior into primate behavioral ecology research holds promise for improving our understanding of primate behavioral evolution.     

Nutritional and Health Status of Woolly Monkeys

Woolly monkeys (Lagothrix lagotricha and L. flavicauda) are threatened species in the wild and in captivity. Numerous zoological institutions have historically kept Lagothrix lagotricha spp., but only a few of them have succeeded in breeding populations. Therefore the majority of institutions that formerly kept Lagothrix lagotricha are no longer able or willing to do so. Captive populations of the species have frequent health problems, most significantly hypertension and related disorders. Researchers have conducted free-ranging dietary and behavior studies with respect to woolly monkeys, but have established no concrete link between diet or nutrients and captive health problems. The available literature we discuss indicates that researchers need to examine the link further. In addition, it is critical to the survival of the primates to be able to keep breeding populations in captivity owing to increasing natural pressures such as deforestation and hunting. Therefore, better understanding of the captive and free-ranging behavior and health parameters of the species is vital to ensure their survival and to maintain forest health and diversity. Researchers need to conduct large-scale research studies comparing the health and complete diet of individuals in the wild and captivity to resolve health problems facing the species in captivity.     

Increased production of 11beta-hydroxysteroid dehydrogenase type 2 in the kidney microsomes of squirrel monkeys (Saimiri spp.)

In squirrel monkeys (Saimiri spp.), cortisol circulates at levels much higher than those seen in man and other Old World primates, but squirrel monkeys exhibit no physiologic signs of the mineralocorticoid effects of cortisol. These observations suggest that squirrel monkeys have mechanisms for protection of the mineralocorticoid receptor (MR) from these high levels of cortisol. We previously showed that the serum cortisol to cortisone ratio in these animals is low relative to that in human serum, suggesting that production of the MR protective enzyme, 11beta-hydroxysteroid dehydrogenase type 2 (11beta-HSD2), is increased in squirrel monkeys. Here, we directly evaluate whether increased production of 11beta-HSD2, which inactivates cortisol to cortisone, is a mechanism for protection of MR. In vitro assays showed that 11beta-HSD2 activity in squirrel monkey kidney microsomes was 3 to 7 times higher than that seen in kidney microsomes from pig or rabbit. 11beta-HSD2 protein detected by Western blot analysis was 4 to 9 times greater in squirrel monkey microsomes than in pig or rabbit microsomes. Comparison of the effect of expression of either human or squirrel monkey 11beta-HSD2 on MR transactivation activity showed similar inhibition of MR response to cortisol by both enzymes, indicating that the intrinsic activities of the human and squirrel monkey enzymes are similar. These findings suggest that one mechanism by which squirrel monkeys protect the MR from activation by high cortisol levels in the kidney is by upregulation of 11beta-HSD2 activity through increased production of the enzyme.     

Vitamin C deficiency in captive nonhuman primates fed commercial primate diet

Scurvy was diagnosed in 19 rhesus monkeys (Macaca mulatta) and four squirrel monkeys (Saimiri sciureus) from a colony of nonhuman primates maintained on a commercial diet. Signs of weakness, reluctance to move, gingival hemorrhage, bruising, proximal and distal metaphyseal fractures, weight loss and anemia appeared in juvenile and young adult rhesus monkeys over a 2 week period. Clinical signs subsided after 5 days of vitamin C therapy. At the same time, cephalohematomas and weakness developed in squirrel monkeys, which failed to respond to treatment. These cases were associated with manufacturer's admitted error in preparation of the commercially prepared monkey diet.     

Serum and urine biochemical diversity among adult wild-caught Aotus nancymae and Saimiri peruviensis

Serum and urine analytes were compared between adult wild-caught owl monkeys (Aotus nancymae) and adult wild-caught squirrel monkeys (Saimiri peruviensis) to determine if normative clinical pathology data were similar. An objective of the study was to confirm that species of neotropical primates are distinct with regard to physiologic parameters, and should not be considered interchangeable in biomedical research. Significant differences (P < 0.05) were noted in many serum and urine analytes between the two groups. The results suggest that reference data for wild-caught owl monkeys are not applicable to squirrel monkeys, and the differences are sufficiently large to be of clinical significance. These findings illuminate the diversity among species of neotropical primates.     

Spontaneous pulmonary adenocarcinoma and subcutaneous cavernous hemangiomas arising in a squirrel monkey (Saimiri sciureus)

Benign and malignant pulmonary tumors have been reported in both Old World and New World monkeys but are uncommon. Hemangiomas are also rarely reported in nonhuman primates. Here we present a case of two primary neoplasms (a papillary adenocarcinoma of bronchioloalveolar origin and multiple cavernous subcutaneous hemangiomas) arising in an aged squirrel monkey (Saimiri sciureus).     

Leukemic histiocytic sarcoma in a captive common squirrel monkey (Saimiri sciureus) with Saimiriine Gammaherpesvirus 2 (Rhadinovirus), Saimiri sciureus lymphocryptovirus 2 (Lymphocryptovirus) and Squirrel monkey retrovirus (β-Retrovirus) coinfection

Hematopoietic neoplasia other than lymphoma and leukemia is uncommon among non-human primates. Herein, we provide the first evidence of occurrence of leukemic histiocytic sarcoma in a captive common squirrel monkey with Saimiriine Gammaherpesvirus 2 (Rhadinovirus), Saimiri sciureus lymphocryptovirus 2 (Lymphocryptovirus), and Squirrel monkey retrovirus (β-Retrovirus) coinfection.     

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.