Sleep quantitation in common marmoset, cotton top tamarin and squirrel monkey by non-invasive actigraphy

Sleep quantitation data on the Neotropical primate species, apart from the squirrel monkey, are still sparse. As such, we have quantitated sleep in the common marmosets (Callithrix jacchus), cotton top tamarins (Saguinus oedipus) and squirrel monkeys (Saimiri sciureus) reared in one primate facility simultaneously, by non-invasive actigraphy. The range in total sleep time/24h measured for male adult common marmosets, cotton top tamarins and squirrel monkeys were 713-793 min (n=4), 707-889 min (n=4) and 459-475 min (n=2) respectively. The range in sleep episode length /12h dark phase for marmosets, tamarins and squirrel monkeys were 21-52 min (n=3), 10-28 min (n=4) and 9-15 min (n=2) respectively. Since vigilance is a critical evolutionary adaptive feature of predator avoidance among Callitrichid monkeys and squirrel monkeys, the shorter ranges in sleep episode length recorded, even under captivity, in this study could be interpreted as probable indicators of such vigilance behavior during the rest phase. We hypothesize that the vigilance behavior when it exists during a primate's active phase should also prevail when it is at rest (sleep). This hypothesis deserves additional testing in female Callitrichid monkeys.     

Hepatitis A and B: serologic survey of human and nonhuman primate sera

Sera of humans and seven species of nonhuman primates were tested by radioimmunoassay and enzyme immunoassay for the presence of hepatitis A antibody, hepatitis B surface antigen and antibody to hepatitis B surface antigen. The outcome of testing a total of 276 serum or plasma specimens was as follows: with the exception of squirrel monkeys (0%) and cotton-top marmosets (0%), a considerable percentage of all other species tested had detectable antibodies to hepatitis A virus: humans 45.9%, chimpanzees 36.6%, baboons 38.2%, vervets 57.9%, cebus monkeys 40.0% and common marmosets 50.0%. Only one human and two chimpanzees were carriers of hepatitis B surface antigen. Antibodies to hepatitis B surface antigen were detected in human (11.3%), chimpanzees (29.9%), baboons (36.2%) and squirrel monkeys (5%). Chimpanzees showed an increasing prevalence of antibodies to hepatitis A virus and hepatitis B surface antigen with age.     

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.     

Serum dopamine beta-hydroxylase activity in non-human primates: phylogenetic and genetic implications

1. Serum dopamine beta-hydroxylase (DBH) activity is one to two orders of magnitude higher in man than in any other species previously studied. The high levels of human serum DBH are associated with the inherited allele DBHH. 2. DBH activity was measured in serum from gorillas, chimpanzees, orangutans, gibbons, rhesus monkeys and squirrel monkeys in an attempt to determine how recently in the course of evolution the allele DBHH had originated. 3. Of the non-human primates tested, only gorillas had high levels of serum DBH activity comparable to those found in man. 4. The genetic polymorphism responsible for evaluated serum DBH in man is probably of very recent evolutionary origin.     

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.     

Working memory of action: a comparative study of ability to selecting response based on previous action in New World monkeys (Saimiri sciureus and Callithrix jacchus)

Working memory of the outcome of one's own action is important for organizing and learning appropriate behaviors in a given condition. To examine whether non-human primates with different neocortical sizes show different abilities regarding working memory for action, the performance of squirrel monkeys (Saimiri sciureus) and common marmosets (Callithrix jacchus) in a kind of delayed-response task was compared. In this task, subjects were required to select a response based on short-term memory of the outcome of their own prior action, which requires working memory of action. These monkeys have a similar phylogenetic status (i.e. Ceboidea), but the size of the neocortex relative to the rest of the brain (relative size of the neocortex) is quite different. We found that both two species could attend to and remember their own actions and could select a response based on that memory. However, the performance level was higher for squirrel monkeys than for marmosets. These results suggest that non-human primates with differentially developed neocortices have different abilities regarding working memory of action.     

Responsiveness and Somatotopic Organization of Anterior Parietal Field 3b and Adjoining Cortex in Newborn and Infant Monkeys

Microelectrodes were used to record from somatosensory areas 3b and adjoining areas 3a and 1 in newborn monkeys. At birth, area 3b was responsive to cutaneous stimuli and had an adult-like somatotopic organization in marmosets and one squirrel monkey, while areas 1 and 3a had only limited responsiveness. In newborn macaque monkeys, cortex was unresponsive to cutaneous stimuli; however, by 1 month, areas 3b and 1 appeared to be adult-like in responsiveness and somatotopic organization.     

Responsiveness and somatotopic organization of anterior parietal field 3b and adjoining cortex in newborn and infant monkeys

Microelectrodes were used to record from somatosensory areas 3b and adjoining areas 3a and 1 in newborn monkeys. At birth, area 3b was responsive to cutaneous stimuli and had an adult-like somatotopic organization in marmosets and one squirrel monkey, while areas 1 and 3a had only limited responsiveness. In newborn macaque monkeys, cortex was unresponsive to cutaneous stimuli; however, by 1 month, areas 3b and 1 appeared to be adult-like in responsiveness and somatotopic organization.     

Androgen resistance in squirrel monkeys (Saimiri spp.)

The goal of this study was to understand the basis for high androgen levels in squirrel monkeys (Saimiri spp.). Mass spectrometry was used to analyze serum testosterone, androstenedione, and dihydrotestosterone of male squirrel monkeys during the nonbreeding (n = 7) and breeding (n = 10) seasons. All hormone levels were elevated compared with those of humans, even during the nonbreeding season; the highest levels occurred during the breeding season. The ratio of testosterone to dihydrotestosterone in squirrel monkeys is high during the breeding season compared to man. Squirrel monkeys may have high testosterone to compensate for inefficient metabolism to dihydrotestosterone. We also investigated whether squirrel monkeys have high androgens to compensate for low-activity androgen receptors (AR). The response to dihydrotestosterone in squirrel monkey cells transfected with AR and AR-responsive reporter plasmids was 4-fold, compared with 28-fold in human cells. This result was not due to overexpression of cellular FKBP51, which causes glucocorticoid and progestin resistance in squirrel monkeys, because overexpression of FKBP51 had no effect on dihydrotestosterone-stimulated reporter activity in a human fibroblast cell line. To test whether the inherently low levels of FKBP52 in squirrel monkeys contribute to androgen insensitivity, squirrel monkey cells were transfected with an AR expression plasmid, an AR-responsive reporter plasmid, and a plasmid expressing FKBP52. Expression of FKBP52 decreased the EC50 or increased the maximal response to dihydrotestosterone. Therefore, the high androgen levels in squirrel monkeys likely compensate for their relatively low 5 alpha-reductase activity during the breeding season and AR insensitivity resulting from low cellular levels of FKBP52.     

Intestinal microbial patterns of the common marmoset and rhesus macaque

The intestinal microflora of common marmosets and rhesus monkeys were compared by enumerating bacteria from the small and large intestines. Rhesus monkeys had a consistent microflora pattern manifest by higher concentrations of total and Gram-negative aerobic and facultatively anaerobic bacteria, as well as aerobic and anaerobic Lactobacilli, in the large intestine as compared to the small intestine. In contrast, the marmoset microflora were considerably more variable. Approximately two-thirds of the marmosets (designated group A) had an overall profile that resembled the rhesus monkeys, but they had significantly higher concentrations of Gram-negative microflora in their large intestines than the rhesus monkeys. The remaining marmosets (group B) had higher concentrations of bacteria in the small intestine as compared to the large intestine, with the large intestinal concentrations being significantly lower than in the rhesus monkeys and group A marmosets. Moreover, the marmosets did not have detectable levels of aerobic Lactobacilli, and anaerobic Lactobacilli concentrations were significantly lower than in the rhesus macaques. Although it is unknown why microflora differ across species, it is likely that evolutionary adaptations in anatomy and functioning of the gastrointestinal tract influence the concentration and types of bacteria residing as the normal intestinal microflora.     

Spontaneous zinc deficiency in marmosets, saguinus mystax.

Moustached marmosets, Saguinus mystax, developed alopecia, skin lesions and general debilitation approximately 6 months after being brought into our laboratory. These lesions resembled the signs of zinc deficiency in pigs, rats and squirrel monkeys. The marmosets were fed a commercial monkey diet containing 150 parts per million zinc and about 100 g of apples and oranges per week. The addition of 40 parts per million zinc to the drinking water brought about improvement in hair coat and skin condition.     

Corticotropin-releasing hormone-binding protein in primates

In humans, placental corticotropin-releasing hormone (CRH) production has been linked to the determination of gestational length, and a late gestational fall in CRH-binding protein (CRH-BP) has been linked to the onset of parturition. Expression of placental CRH mRNA is limited to primates, and only in man has a circulating CRH-BP been described. As the fall in CRH-BP in late gestation has been associated with parturition in humans, we sought to determine whether a CRH-BP circulated in the plasma of other primates. It is unclear whether maternal plasma CRH concentrations are elevated in New World monkeys and prosimians. We have therefore performed CRH plasma measurements in the blood of pregnant marmosets, in several species of lemur, and in pregnant and fetal rhesus monkeys as a positive control. Using gel chromatography, CRH-BP was detected in the human, gorilla, chimpanzee, orangutan, gibbon, macaque, squirrel monkey, and marmoset, but was absent in the mandrill, spider monkey, and lemur. CRH was detected in the plasma of pregnant marmosets and rhesus monkeys. CRH was also detected in the fetal rhesus monkey, but at lower concentrations than in maternal plasma. CRH immunoreactivity was not detectable in the plasma of pregnant lemurs or in extracts of lemur placenta. In conclusion, a circulating binding protein for CRH exists in all species of apes but occurs variably among New World and Old World monkeys and is absent in lemurs. The variable occurrence of the CRH-BP does not support a role for this protein in the mechanism of parturition in primates. Maternal CRH is elevated in the pregnant marmoset and rhesus, and may play a role in the pregnancy of New and Old World monkeys.     

Preparing New World monkeys for laboratory research

New World monkeys represent an important but often poorly understood research resource. The relatively small size and low zoonotic risk of these animals make them appealing as research subjects in a number of areas. However, historic portrayal of many of these species as difficult to manage and handle is one of the factors that has limited their use. Basic guidelines are provided on management and handling approaches for the New World monkeys most commonly used in research: marmosets, squirrel monkeys, owl monkeys, and titi monkeys. Topics include transport and acclimation to a new facility, location changes within a facility, diet changes, removal from and return to social groups, capture and restraint, handling for anesthesia, postprocedural monitoring, and staff training.     

Laterality in spontaneous motor activity of chimpanzees and squirrel monkeys

Varieties of nonmanipulative motor responses were observed in chimpanzees and squirrel monkeys. Chimpanzees displayed a right hand preference for touching their inanimate environments but used their right and left hands equally for touching their faces and their bodies. The latter result was not consistent with previous reports of a left hand preference for face touching in apes. The right hand preference for environmental touching was stronger in male than in female chimpanzees. Squirrel monkeys had a right preference for combined hand and foot responses directed to their bodies, but expressed no handedness for environmentally directed touching. These limb preferences in chimpanzees and squirrel monkeys indicate that neither precise, complex manipulation nor postural instability are necessary conditions for population level hand preferences. Factor analysis of the chimpanzee manual responses showed distinct self and environmentally directed factors. Analysis of the squirrel monkey data also showed self and environmental factors, except that body scratching had a negative loading on the environmental factor. This latter result suggests that self-scratching by squirrel monkeys is a displacement activity that suppresses manual exploration of the environment. © 1992 Wiley-Liss, Inc.     

Abundance, diversity, and patterns of distribution of primates on the Tapiche River in Amazonian Peru

This work presents data on the relative diversity, abundance, and distribution patterns of primates in a 20 km2 area of the Tapiche River in the Peruvian Amazon. Population data were collected while the study area was both inundated and dry (March to September 1997) using conventional line-transect census techniques. Survey results reflected the presence of 11 primate species, but population parameters on only eight of the species will be presented, including saddleback tamarins (Saguinus fuscicollis), Bolivian squirrel monkeys (Saimiri boliviensis), brown capuchins (Cebus apella), white-fronted capuchins (Cebus albifrons), monk sakis (Pithecia monachus), red titi monkeys (Callicebus cupreus), red uakaris (Cacajao calvus), and red howler monkeys (Alouatta seniculus). Woolly monkeys (Lagothrix lagotricha), night monkeys (Aotus nancymaae), and pygmy marmosets (Callithrix pygmaea) were also seen in the area. The data for the smaller-bodied primates is similar to that reported almost 18 years earlier, but the data for the larger-bodied primates reflect a loss in the number of animals present in the area. Pressure from hunters and the timber industry may account for declining numbers of large-bodied primates, while it appears that natural features peculiar to the conservation area contribute to the patchy pattern of distribution.     

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.     

Head-cocking and visual perception in primates

To examine the phyletic distribution and ontogeny of ‘head-cocking’ (rotating the cranium about the longitudinal body axis while orienting in a fixed direction) in primates, I conducted observations on 229 individuals of 40 different species. Head-cocking in primates typically occurs during visual inspection of objects. The response is primarily characteristic of diminutive species that lack ocular dominance columns in the visual striate cortex (e.g. marmosets, squirrel monkeys), and is most frequently observed during infancy.     

Phylogenomics of species from four genera of New World monkeys by flow sorting and reciprocal chromosome painting

Background

The taxonomic and phylogenetic relationships of New World monkeys (Platyrrhini) are difficult to distinguish on the basis of morphology and because diagnostic fossils are rare. Recently, molecular data have led to a radical revision of the traditional taxonomy and phylogeny of these primates. Here we examine new hypotheses of platyrrhine evolutionary relationships by reciprocal chromosome painting after chromosome flow sorting of species belonging to four genera of platyrrhines included in the Cebidae family: Callithrix argentata (silvered-marmoset), Cebuella pygmaea (pygmy marmoset), Callimico goeldii (Goeldi's marmoset) and Saimiri sciureus (squirrel monkey). This is the first report of reciprocal painting in marmosets.

Results

The paints made from chromosome flow sorting of the four platyrrhine monkeys provided from 42 to 45 hybridization signals on human metaphases. The reciprocal painting of monkey probes on human chromosomes revealed that 21 breakpoints are common to all four studied species. There are only three additional breakpoints. A breakpoint on human chromosome 13 was found in Callithrix argentata, Cebuella pygmaea and Callimico goeldii, but not in Saimiri sciureus. There are two additional breakpoints on human chromosome 5: one is specific to squirrel monkeys, and the other to Goeldi's marmoset.

Conclusion

The reciprocal painting results support the molecular genomic assemblage of Cebidae. We demonstrated that the five chromosome associations previously hypothesized to phylogenetically link tamarins and marmosets are homologous and represent derived chromosome rearrangements. Four of these derived homologous associations tightly nest Callimico goeldii with marmosets. One derived association 2/15 may place squirrel monkeys within the Cebidae assemblage. An apparently common breakpoint on chromosome 5q33 found in both Saimiri and Aotus nancymae could be evidence of a phylogenetic link between these species. Comparison with previous reports shows that many syntenic associations found in platyrrhines have the same breakpoints and are homologous, derived rearrangements showing that the New World monkeys are a closely related group of species. Our data support the hypothesis that the ancestral karyotype of the Platyrrhini has a diploid number of 2n = 54 and is almost identical to that found today in capuchin monkeys; congruent with a basal position of the Cebidae among platyrrhine families.

     

非人灵长类动物种质冷冻保存研究进展和展望

非人灵长类动物是生物多样性的重要组成部分,也是生物医学研究的珍贵实验动物,然而,由于人类活动、栖息地破坏、狩猎和遗传隔离等原因,许多非人灵长类动物的野生种群数量急剧下降,甚至处于灭绝的边缘。种质冷冻保存对拯救非人灵长类动物和保存遗传物质资源具有重要意义。本文综述了新大陆猴、旧大陆猴和巨猿等类群动物精子、卵子、胚胎和性腺组织等种质冷冻保存的研究进展,介绍了狨猴、松鼠猴、恒河猴、食蟹猴和黑猩猩等种质冷冻保存的主要方法,并对未来种质冷冻保存的研究方向进行了讨论。     

Forelimb dimensions and goniometry of the wrist and fingers in tufted capuchin monkeys (Cebus apella): Developmental and comparative aspects

Adult capuchin monkeys use precision grips during manipulation of small objects, although their thumbs have been classified as pseudo-opposable. We investigated the physical properties of the hands to increase our understanding of manual function in capuchins. Forelimb dimensions and joint mobility (goniometric) measurements were obtained from adult, juvenile, and infant tufted capuchins (Cebus apella). Compared to adult squirrel monkeys, adult capuchins exhibited less flexibility of the wrist and digits. Capuchins of all ages had proportionally longer hands than squirrel monkeys, and capuchins more than 7 weeks old had proportionally longer thumbs than squirrel monkeys. Growth of the arms and hands was asynchronous. The duration of growth of the thumb was particularly prolonged, extending into early adulthood. Age-related changes in flexibility were apparent in most indices, and were greatest at the metacarpophalangeal joints. It is unknown to what extent the characteristics of growth, forelimb dimensions, and goniometry presented by capuchins are shared with other species, or if they contribute to the capuchin's unusual prehensive capacities. However, the marked differences between adult capuchins and squirrel monkeys in these metrics, and between capuchins and rhesus in the growth patterns of the digits, suggest that variation across taxa in these characteristics can be considerable.