Age differences and developmental trends in alarm peep responses by squirrel monkeys (Saimiri sciureus)

Alarm calls can code for different classes of predators or different types of predatory threat. Acoustic information can also encode the urgency of threat through variations in acoustic features within specific alarm call types. Squirrel monkeys (Saimiri sciureus) produce an alarm call, known as the alarm peep, in highly threatening situations. Infant squirrel monkeys appear to have an innate predisposition to respond to alarm peeps but require experience to associate alarm peeps with the appropriate type of predatory threat [Herzog & Hopf, American Journal of Primatology 7:99-106, 1984]. Little is known about age-related differences in the type or frequency of response to alarm peeps, or the development of alarm peep response in infants. The purpose of this study was to test experimentally the response strategies of different age classes of squirrel monkey to the playback of alarm peeps that were produced by infants, juveniles, or adults. Results suggest that infants, juveniles, and female subadults respond more frequently to alarm peeps than do adult females. Infant squirrel monkeys showed different behavioral strategies in response to alarm peeps as a function of age. Adult females differentiate between infant and adult alarm peeps by responding more frequently to the alarm peeps of adult females. These data demonstrate that squirrel monkeys use acoustic information to discern when to respond to the alarm peeps from conspecifics, and that infants gradually develop an adult-like response to alarm peeps over the first year of development.     

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.     

Hypoglycemia of squirrel monkey neonates: implications for infant survival

Neonatal deaths are a serious problem in breeding colonies of squirrel monkeys. Seriously ill neonates in our colony are always hypoglycemic on presentation. To determine normal glucose values for squirrel monkey infants of various ages, serum glucose determinations were done at 1, 3, 7, 10, 14 days and 1 month of age using a standard laboratory test for serum glucose. Glucose concentration increased from a low of 49 +/- 3 mg/dl (Mean +/- SEM) at 1 day (n = 21) to 109 +/- 4 mg/dl at 1 month of age (n = 17). Glucose values for 1, 3 and 7 day-old infants were significantly lower than 1 month-old infants (P less than .05). To provide a time-averaged indication of blood glucose, glycosylated hemoglobin (GHb) measurements were made at 1 day, 1 week, 2 weeks, 1 month, 2 months, 1 year of age and in adults (greater than 3 years of age). GHb values ranged from 2.6% +/- 0.1 for 1 day old infants (n = 13) to 4.0 +/- 0.2 for adults (n = 10) with a steady increase during the first 2 months of life. Animals 1 year of age and younger had significantly lower glycosylated hemoglobin than adults. These studies indicate that blood glucose concentration is significantly lower in squirrel monkey neonates than in older infants, juveniles and adults. Maternal rejection, trauma, and associated problems occur commonly in socially reared squirrel monkeys. The marginal hypoglycemic state of these infants places them at high risk for clinical hypoglycemia as a sequel to such perturbations.     

Responses of mother squirrel monkeys to dead infants

The responses of mother squirrel monkeys to infants were examined by testing the mothers with bodies of their own and other infants. Mothers whose infants were stillborn or died at one day of age showed strong and equivalent maternal responses to all the bodies with which they were presented, while those whose infants died after two weeks of age responded mainly to the body of their own infant. These results suggest that the female squirrel monkey becomes more selective in responding to the body of a dead infant with the passage of time after parturition. The female's post-parturient condition appears to be the prime cause for changes in her responsiveness, although other factors related to the infant's growth and development might also be important.Supported by Grant HD 04905 from the National Institute of Child Health and Human Development.     

TRICHOMONIASIS—Clinical Trial of Metronidazole (Flagyl?)

Metronidazole was given in various dosage regimens to 97 patients having microscopically diagnosed trichomoniasis.At the first examination after treatment all 97, including 76 to whom metronidazole had been given orally only, were found by culture and wet smear to be free of trichomonads.Reexamination of the 65 patients followed up for periods ranging from two weeks to 14 months revealed reappearance of trichomonads in eight cases.Nineteen husbands were treated. No patient had a recurrence after treatment of the husband.No effect of metronidazole on pregnancy or on fetal development was seen. Side effects, noted in 19 cases (20 per cent), generally were mild and transient and in no case were severe enough to terminate therapy before cure was effected.     

Population recognition of infant isolation peeps in the squirrel monkey

Infants from three populations of squirel monkeys with different pelage, behaviour patterns and physiological patterns emitted two forms of isolation peeps. Offspring from Peruvian and Bolivian stock produced isolation peeps previously described as belonging to ‘Roman Arch’ monkeys, whereas the Guyanese population produced isolation peeps previously described as belonging to ‘Gothic Arch’ monkeys. Playbacks of isolation peeps from, infants of each population to groups of adult monkeys revealed a population specificity in the response to infant calls. Peruvian, and Bolivian adults responded with increased activity, decreased huddling and increased approach to the speaker only when isolation peeps of Peruvian and Bolivian infants were broadcast. Guyanese adult monkeys showed similar responses to the isolation peeps of Guyanese infants. These are the first reported data indicating that the long-recognized vocal differences in squirrel monkey populations are responded to differentially. The results also support a major taxonomic division between the Gothic Arch and Roman Arch populations with the other morphological and physiological differences within these populations reflecting secondary divisions.     

Do Adult Male Spider Monkeys (Ateles geoffroyi) Preferentially Handle Male Infants?

Infant tolerance by adult males has been observed in many primate species with multimale–multifemale mating systems, but males do not usually initiate interactions with infants. In male philopatric species, such as spider monkeys, adult males within a community exhibit high levels of cooperation and affiliation, and they might therefore be motivated to create bonds with potential future allies. Based on this hypothesis we predicted that adult male spider monkeys would participate in infant handling more than adult females and they would preferentially direct handling toward male infants. Between January 2008 and July 2010, we collected 884?h of observation on a community of wild spider monkeys at Runaway Creek Nature Reserve in Belize. During this period we observed 120 incidences of affiliative interactions between infants and adults other than their mother. The adult initiated the majority of nonmother adult–infant interactions (78?%). All available infants (5 males, 7 females) were handled during the study. All 9 of the community adult males handled infants but only 7 of 14 adult females did so. Adult males handled infants significantly more often than did adult females and males also handled young infants more often than older infants. Significant infant sex differences in handling appeared in infants >6?mo when adult males handled males significantly more than females. The patterns of infant handling among age–sex class dyads reflect the affiliative social patterns that we see in adult spider monkeys. These results provide support for the hypothesis that adult males preferentially handle male infants as a strategy for fostering social bonds.     

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.     

Social organization of captive monandrous squirrel monkey groups (Saimiri sciureus).

1 adult male and 4 adult female squirrel monkeys were observed together as a group, isolated from all other monkeys. 3 of the 4 females were deafened for a previous experiment. Deafening, however, had no apparent, permanent effect on social behavior. Social dominance hierarchy was evaluated in a variety of situations. The results were compared with those of a similar set of observations on the females prior to the introduction of the male. Before the male was introduced, the dyadic interactions involving food stealing, body grasping, and sexual behaviors were indicative of a female linear rank order. After the male was introduced, the rank order among the females generally remained intact, with the male becoming the highest ranking member in the group. The noteworthy exception to the stability involved the highest ranking female, whose position in the hierarchy was threatened. Heterosexual interactions predominated. Homosexual behavior was also observed, although appreciably reduced in frequency as compared to the all-female group situation. A similar rank order hierarchy was observed in a second group of squirrel monkeys comprised of 1 adult male and 4 adult females. None of these monkeys was deaf.     

Leishmania donovani: cellular and humoral immune responses after primary and challenge infections in squirrel monkeys, Saimiri sciureus

Cellular and humoral immune responses were studied in squirrel monkeys after primary and challenge infection with a Khartoum strain (WR 378) of Leishmania donovani. Each of 7 squirrel monkeys, Saimiri sciureus, was inoculated intravenously with 5 X 10(7) amastigotes/kg body weight, and one other monkey (control) was inoculated with uninfected hamster spleen homogenate. Five infected monkeys recovered from visceral leishmaniasis and two infected monkeys died. Three of the five squirrel monkeys which recovered from the primary infection demonstrated acquired resistance when challenged with an intravenous inoculation of 1.0 X 10(8) amastigotes of L. donovani/kg of body weight. Each of these same three monkeys, the two remaining monkeys which recovered from the primary infection and an uninfected control monkey, were challenged subsequently with an intradermal injection of 2.2 X 10(7) promastigotes of L. braziliensis panamensis (WR539) and developed cutaneous lesions. The reactivity of peripheral blood leukocytes from infected squirrel monkeys to phytohemagglutinin was depressed 2 to 10 weeks after infection, and the reactivity to concanavalin A was not affected. Data on responses to pokeweed mitogen were inconclusive. Reactivity to leishmanial antigens was detected at 12 weeks after infection, which coincided with a marked decrease or disappearance of parasites in liver imprints. Two of five surviving squirrel monkeys developed weak delayed skin test responses to leishmanin antigens after 23 weeks; the three remaining monkeys were anergic during the primary infection but developed strong delayed skin test responses to leishmanin antigens at 7 weeks after a challenge with L. donovani. All squirrel monkeys inoculated with L. donovani developed a hyperproteinemia, hypergammaglobulinemia, hypoalbuminemia, and a reversal of the albumin/globulin ratio between 4 to 18 weeks after infection. Plasma IgM and IgG levels were increased between 2 to 18 weeks after infection; much of this increase was due to IgG. Class-specific antileishmanial antibodies, with generally low IgM and high IgG titers, reached a maximum after 14 and 16 weeks, respectively. A correlation was observed between concentration of gamma-globulins and plasma IgM and IgG levels, but not gamma-globulin concentrations and maximum titers of class-specific antileishmanial antibodies. Squirrel monkeys challenged with L. donovani again developed hyperproteinemia, hypergammaglobulinemia, and increased concentrations of plasma IgM and IgG which correlated with high titers of IgG class-specific antileishmanial antibody 4 weeks after reinoculation.(ABSTRACT TRUNCATED AT 400 WORDS)     

Babysitting behavior by age/sex classification in squirrel monkeys (Saimiri sciureus)

The aunting behavior in a captive group of 22 squirrel monkeys containing three infants was done in terms of the age/sex classification of those animals involved. The time course of the aunting phenomena and the type and intensity of the interactions between the mothers and the aunts were recorded. Males as well as females were observed to ascertain if the babysitters were sex specific. Observations were gathered before, during, and after a particular threat to any monkey who was carrying an infant. Three categories of protective behavior (protect, retreat, and nothing) were tabulated. The results indicated that most aunting and protection occurred between infant ages 2-1/2-5 weeks when the infants were growing rapidly but not as yet socially self-sufficient. Mothers protected infants the most against juveniles, then subadult males, and least against other adult females. Subadult males were occasionally observed to carry and protect older infants. Aunting behavior was discussed in terms of the selective pressures by which it may have evolved.     

Notes on pregnancy,delivery, and infant survival in captive squirrel monkeys

A survey is given on 13 pregnancies in captive squirrel monkeys including 3 reported elsewhere. Observations of sexual behavior suggest a gestation period of 24 to 26 weeks which confirms former estimations. In 8 pregnancies the presentation of the fetus was determined by X-ray and measurements on fetal growth are given. Three deliveries were observed and motion pictures in artificial or infrared light were taken. Behavior and physical changes during pregnancy, and behavior of mother, infant, and group members during delivery and early postnatal period are described. Of the 6 live born infants 4 did not survive the weaning period and 2 have not yet been weaned.Attempts to provide the monkeys with sufficient protein and to eliminate accidents are discussed.     

Detection and cultivation of intestinal trichomonads of squirrel monkeys (Saimiri sciureus)

Routine examinations of fecal samples from squirrel monkeys suggested that intestinal trichomonads might be common inhabitants of these animals. In pursuit of these observations, microscopic examination of fecal suspensions and cultures have demonstrated a 100% incidence of trichomonads in 30 arbitrarily selected animals from a colony of more than 300 housed in groups of ten. The most prominent species was Pentatrichomonas hominis. A not yet fully characterized tritrichomonad was also found on several occasions. The main obstacle in establishing individual strains in culture was the presence of bacterial and fungal flora in the samples. Nevertheless, abundant cultures were obtained from 28 animals by inoculation of fecal suspensions into tissue cultures with appropriately formulated medium and high concentration of antibiotics. In several unattended cultures maintained at room temperature, the flagellates retained motility for at least 4 months. This long survival may explain the widespread occurrence of the parasites within a confined animal community.     

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.     

Male behavior through the breeding season in Saimiri boliviensis boliviensis

The Bolivian squirrel monkey (Saimiri boliviensis boliviensis) is a seasonal breeder. Male squirrel monkeys show distinct morphological and behavioral changes prior to and during the breeding season. A “fatting syndrome” includes increased body weight, increased levels of androgens, and in the Bolivian subspecies, an increasingly active role in the social organization of the group. In this study, the behavior of ten adult male Bolivian squirrel monkeys was analyzed over a 6-month period prior to, during, and after the breeding season. Each was housed as the only adult male in a breeding unit with six to ten adult females and one juvenile male. Employing a principle components method, 11 behavioral clusters were generated from 27 responses. Their activity clusters were identified as follows: sexual activity that showed a peak around the time of peak conceptions; excitatory activity that was initially high but decreased throughout the breeding season; and maintenance activity that did not change across the breeding season. The changing social behavior of the male squirrel monkey parallels physiological changes and is correlated with changing androgen levels.     

The repeated procedure of weaning and peer group formation causes accumulation of stress and changes of plasma cortisol level and natural killer activity in squirrel monkeys (Saimiri sciureus)

The psychological stress was evaluated in repeated and unrepeated procedures of weaning as well as forming peer group in squirrel monkeys. The repeated procedure included the process of increasing the period of separation or formation stepwise during four weeks. The plasma cortisol levels and natural killer (NK) activities were monitored during experiment to evaluate the stress in infant monkeys. The plasma cortisol level rapidly increased two to three times as much as basal level and kept high levels throughout experiment in repeated group. In the infants of unrepeated group, significant increase of cortisol level and decrease of NK activity were observed in day-1, but both of them returned to the basal level at day-7. Both cortisol level and NK activity did not show any change with exception of decrease in NK activity at day-7 in infants who were introduced into peer group without repeated procedure. On the other hand, both cortisol level and NK activity increased during the repeated procedure. These results indicate that both weaning and forming peer group induce the psychological stress in infant squirrel monkeys, resulting in changes of plasma cortisol level and NK activity. Repeating the procedure of separation or introduction applied in this study caused the accumulation of stress. Although plasma cortisol level increased in infants exposed to both weaning and forming peer group, the changing pattern of NK activity differed between them. This finding suggests that social or psychological stress show two different effects on immune function, suppression, and enhancement depending on the level of stress.     

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.     

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.     

Vigilance during play in squirrel monkeys

Play by young squirrel monkeys (Saimiri boliviensis) may put them and other troop members at risk for predation because youngsters are noisy, separated from adults, and not vigilant when at play. In a study using separated groups of adults and 1-year-old juveniles caged outdoors, we found that adult female squirrel monkeys become more vigilant during periods of spontaneous play among juveniles. This behavioral response could be obtained with auditory cues (play vocalizations) alone. Five times as much vigilance activity was directed toward an area from which threat or disturbance was likely to come as was directed toward the juveniles themselves. These results suggest both an adaptive, compensatory increase in adult vigilance during play and a function for play vocalizations. Additional functions for play vocalizations remain to be investigated.