Response to novelty inSaimiri andCallicebus: Influence of social context

Responses to novel objects by pair-livingSaimiri andCallicebus and grouplivingSaimiri were investigated in two experiments. In the first, titis and squirrel monkeys were tested in the presence and absence of an opposite-sexed pairmate. The species were differentially affected by the absence of the pairmate: titis of both sexes were distressed and object interest was attenuated; squirrel monkeys were not distressed and object scores (particularly females') increased. Nonsocial differences in object exploration principally involved the tempo and mode of investigation; squirrel monkeys were quicker and more vigorous than titis. In the second experiment, presence of a novel object was found to attract and arouse grouplivingSaimiri, as indicated by the change in the frequency and nature of social interactions and spatial distribution. Within- and between-sex social interactions reflected the typical female nucleus-peripheral male pattern seen inSaimiri groups in other environments. Species differences in investigatory patterns were considered to be contributing elements in the maintenance of distinctive life-styles.     

Squirrel monkeys' response to inequitable outcomes indicates a behavioural convergence within the primates

Although several primates respond negatively to inequity, it is unknown whether this results from homology or convergent processes. Behaviours shared within a taxonomic group are often assumed to be homologous, yet this distinction is important for a better understanding of the function of the behaviour. Previous hypotheses have linked cooperation and inequity responses. Supporting this, all species in which inequity responses have been documented are cooperative. In this study, we tested this hypothesis by investigating the response to inequity in squirrel monkeys, which share a phylogenetic family with capuchin monkeys, but do not cooperate extensively. Subjects exchanged tokens to receive food rewards in conditions in which the level of effort required and reward received varied. Squirrel monkeys did not respond negatively to inequity. However, the monkeys were sensitive to the variation present in the task; male subjects showed a contrast effect and, as in previous studies, subjects were more sensitive to differences in reward in the context of a task than when rewards were given for free. Taken with other results, these results support the hypothesis that a negative response to inequity evolved convergently in primates, probably as a mechanism for evaluating outcomes relative to one's partners in cooperative species.     

Natural conceptual behavior in squirrel monkeys (saimiri sciureus): An experimental investigation

Natural conceptual discriminations have been tested in many different species, including pigeons and a variety of non-human primates. The ability of four male squirrel monkeys (Saimiri sciureus) to learn and use the natural concept ‘squirrel monkey’ was investigated in this study. After a training phase, subjects were presented with novel stimuli in transfer and test trials. All subjects performed at a rate significantly above chance on the first test trial (p<.001), indicating that squirrel monkeys can utilize natural concepts in the laboratory.     

Which senses play a role in nonhuman primate food selection? A comparison between squirrel monkeys and spider monkeys

In order to optimize foraging efficiency and avoid toxicosis, animals must be able to detect, discriminate, and learn about the predictive signals of potential food. Primates are typically regarded as animals that rely mainly on their highly developed visual systems, and little is known about the role that the other senses may play in food selection. It was therefore the aim of the present study to assess which senses are involved in the evaluation of food by two species of New World primates: the squirrel monkey and the spider monkey. To this end, six animals per species were repeatedly presented with both familiar and novel food items, and their behavior was videotaped and analyzed. To obtain a further indication of the relative importance of visual and chemosensory cues, the animals were also presented with familiar food items that were experimentally modified in color, odor, or both color and odor. The results demonstrate that squirrel monkeys and spider monkeys use olfactory, gustatory, and tactile cues in addition to visual information to evaluate novel food, whereas they mainly inspect familiar food items visually prior to consumption. Our findings also show that in both species the use of nonvisual cues decreased rapidly with repeated presentations of novel food, suggesting a fast multimodal learning process. Further, the two species clearly differ in their relative use of nonvisual cues when evaluating novel or modified food, with spider monkeys relying more on olfactory cues than squirrel monkeys, and squirrel monkeys relying more on tactile cues compared to spider monkeys.     

Measures of body size and growth in rhesus and squirrel monkeys subjected to long-term dietary restriction

Although many studies have reported the robust effects of dietary restriction (DR) in retarding numerous aging processes in rodents, little is known about the outcomes of reducing caloric intake of a nutritious diet on aging in primates. Most primate studies have concerned the effects of malnutrition. We hypothesized that DR influences aging processes in primate species as it does in rodents. In the present study, 24 male rhesus (Macaca mulatta) monkeys (ages 0.6–5 years) and 25 male squirrel (Saimiri sp.) monkeys (ages 0.3–10 years) were provided diets formulated differently for each species but both fortified with vitamins and minerals (40% above recommended levels) as controls (approximating ad libitum levels) or experimentals (about 30% below the level of diet provided controls of comparable age and body weight). The results reported here concern the hypothesis that DR imposed during various developmental stages in these two primate species would affect morphometric parameters obtained at different occasions during the first 5 years of the study. Groups of older monkeys (rhesus: 18–25 years, n = 3; squirrel: 10–15 years, n = 4) were also included as controls for comparative purposes. Among groups of rhesus monkeys begun on DR prior to 6 years of age, growth in body weight and crown-rump length was reduced about 10–20% beginning after 1 year on the diet, with estimated food intake being reduced about 30–35% over this period. Measures of skin-fold thickness and various body circumference measures were also reduced in experimental groups of rhesus monkeys. In contrast, the DR regimen involving a different diet produced little impact on comparable measures in squirrel monkeys, with the estimated food intake being reduced only about 20–25% over this period. However evidence of divergence in some morphometric parameters in squirrel monkeys was beginning to emerge in young groups (<5 years(after 3 yers on the diet. © 1995 Wiley-Liss, Inc.     

Ca<Superscript>2+</Superscript> responses induced by adrenergic agonists in preadipocytes of mouse and ground squirrel (<Emphasis Type="Italic">Spermophillus undulates</Emphasis>)

Brown adipose tissue of small animals in the cold is able to increase several fold its mass and ability for non-shivering thermogenesis. Adrenergic agonists play a crucial role in the stimulation of the tissue hyperplasia and thermoregulation. In this work, a comparative study of the Ca²⁺ signaling in mouse and ground squirrel brown preadipocytes was carried out. The goal of this study was to elucidate what features of the Ca²⁺ signaling in ground squirrel preadipocytes allow the hibernators to control brown fat hyperplasia in the absence of cold stress. This knowledge would enable us to find ways to control human body mass and to treat diabetes mellitus type two. Low concentrations (0.3–3 μM for mouse cells and 1–10 μM for ground squirrel cells) of the selective α₁- and β-adrenergic agonists cirazoline and isoproterenol, respectively, induced slow Ca²⁺ responses with linear kinetics in brown preadipocytes of both species. High concentrations of the agonists (10–500 μM) caused Ca²⁺ responses with exponential kinetics in ground squirrel brown preadipocytes and suppressed the responses in mouse preadipocytes. Dose-response curves for the agonists were bell-shaped for both mouse and ground squirrel preadipocytes. It should be noted that in preadipocytes of both species β-adrenergic agonist induced stronger responses than α₁-adrenergic agonist did. On the other hand, the responses evoked in ground squirrel brown preadipocytes by both agonists were two orders of magnitude stronger than the responses in mouse preadipocytes. Treatment of the cells with forskolin demonstrated that brown preadipocytes of a ground squirrel had a strong positive feedback in Ca²⁺ signaling, whereas mouse preadipocytes had a negative feedback. The difference found in the preadipocyte Ca²⁺ signaling may explain the different strategies employed in the two species for the regulation of their body fat mass and survival in the cold.     

The selfish nature of generosity: harassment and food sharing in primates

Animals may share food to gain immediate or delayed fitness benefits. Previous studies of sharing have concentrated on delayed benefits such as reciprocity, trade and punishment. This study tests an alternative model (the harassment or sharing-under-pressure hypothesis) in which a food owner immediately benefits because sharing avoids costly harassment from a beggar. I present an experiment that varies the potential ability of the beggar to harass, and of the owner to defend the food, to examine the effects of harassment on food sharing in two primate species: chimpanzees (Pan troglodytes) and squirrel monkeys (Saimiri boliviensis). For both species, high levels of harassment potential significantly increased both beggar harassment and sharing by the owner. Food defensibility did not affect harassment or sharing. Interestingly, squirrel monkeys and chimpanzees shared equally frequently with conspecifics despite a much higher natural sharing rate in chimpanzees. These results suggest that harassment can play a significant role in primate food sharing, providing a simple alternative to reciprocity. The selfish nature of harassment has implications for economic, psychological and evolutionary studies of cooperative systems.     

Tonic immobility in the squirrel monkey (Saimiri sciureus)

Tonic immobility and several accompanying behavioral changes were examined in the squirrel monkey (Saimiri sciureus). It was found that either the occurrence of a loud noise immediately before induction or the presence of a stuffed Cooper's hawk increased the duration of immobility in some subjects. Subspecies differences in durations of immobility were also found. The number of inductions required to produce immobility in squirrel monkeys were unusually large, and were negatively correlated with duration of the response. Behavioral variables accompanying tonic immobility showed qualitative differences when compared to what is known concerning their relation to immobility in other species. The findings support the belief that tonic immobility evolved as a predator defense in squirrel monkeys or one of their ancestors, but suggest that it no longer plays an active role in their survival.     

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.     

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)     

Dietary Profile of <Emphasis Type="Italic">Rhinopithecus bieti</Emphasis> and Its Socioecological Implications

To enhance our understanding of dietary adaptations and socioecological correlates in colobines, we conducted a 20-mo study of a wild group of Rhinopithecus bieti (Yunnan snub-nosed monkeys) in the montane Samage Forest. This forest supports a patchwork of evergreen broadleaved, evergreen coniferous, and mixed deciduous broadleaved/coniferous forest assemblages with a total of 80 tree species in 23 families. The most common plant families by basal area are the predominantly evergreen Pinaceae and Fagaceae, comprising 69% of the total tree biomass. Previous work has shown that lichens formed a consistent component in the monkeys’ diet year-round (67%), seasonally complemented with fruits and young leaves. Our study showed that although the majority of the diet was provided by 6 plant genera (Acanthopanax, Sorbus, Acer, Fargesia, Pterocarya, and Cornus), the monkeys fed on 94 plant species and on 150 specific food items. The subjects expressed high selectivity for uncommon angiosperm tree species. The average number of plant species used per month was 16. Dietary diversity varied seasonally, being lowest during the winter and rising dramatically in the spring. The monkeys consumed bamboo shoots in the summer and bamboo leaves throughout the year. The monkeys also foraged on terrestrial herbs and mushrooms, dug up tubers, and consumed the flesh of a mammal (flying squirrel). We also provide a preliminary evaluation of feeding competition in Rhinopithecus bieti and find that the high selectivity for uncommon seasonal plant food items distributed in clumped patches might create the potential for food competition. The finding is corroborated by observations that the subjects occasionally depleted leafy food patches and stayed at a greater distance from neighboring conspecifics while feeding than while resting. Key findings of this work are that Yunnan snub-nosed monkeys have a much more species-rich plant diet than was previously believed and are probably subject to moderate feeding competition.     

Comparative normal levels of serum triiodothyronine and thyroxine in nonhuman primates.

Normative values were obtained for triiodothyronine and thyroxine from four species of Old World primate (chimpanzees, rhesus monkeys, African green monkeys and talopoin monkeys) and a single species of New World primate (squirrel monkeys) represented by two subspecies, Colombian and Bolivian. The Bolivian squirrel monkeys exhibited the lowest values for both triiodothyronine and thyroxine. Male talapoins had the highest levels of thyroxine. Significant differences were found in levels of triiodothyronine and thyroxine between males and females of the same species and between the two subspecies of squirrel monkeys. Triiodothyronine:thryroxine ratios were consistently lower in the males of all species examined.     

Partner's behavior, not reward distribution, determines success in an unequal cooperative task in capuchin monkeys

It was recently demonstrated that capuchin monkeys notice and respond to distributional inequity, a trait that has been proposed to support the evolution of cooperation in the human species. However, it is unknown how capuchins react to inequitable rewards in an unrestricted cooperative paradigm in which they may freely choose both whether to participate and, within the bounds of their partner's behavior, which reward they will receive for their participation. We tested capuchin monkeys with such a design, using a cooperative barpull, which has been used with great success in the past. Contrary to our expectations, the equity of the reward distribution did not affect success or pulling behavior. However, the behavior of the partner in an unequal situation did affect overall success rates: pairs that had a tendency to alternate which individual received the higher-value food in unequal reward situations were more than twice as successful in obtaining rewards than pairs in which one individual dominated the higher-value food. This ability to equitably distribute rewards in inherently biased cooperative situations has profound implications for activities such as group hunts, in which multiple individuals work together for a single, monopolizable reward.     

Difference in food selection between patas monkeys (Erythrocebus patas) and tantalus monkeys (<Emphasis Type="Italic">Cercopithecus aethiops tantalus</Emphasis>) in Kala Maloue National Park,Cameroon, in relation to nutrient content

Phytochemical or nutrient analyses of primate diets have revealed clues to their food selection in a single species. On the other hand, few interspecific comparisons of phytochemical or nutrient composition of primate diets have been made, although diets are considered to differ in phytochemical or nutrient content from primate species to species, since different species have different body weights and different morphological and physiological characteristics. I compared the nutrient content of diet between patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus) living sympatrically in Cameroon. Patas subsisted on a smaller number of food items, most of which were also tantalus food items. Then, I compared the protein–fiber ratio and the available energy content of the food items eaten by patas (patas foods) with those items eaten only by tantalus (tantalus foods). Both variables were higher in patas than tantalus foods, although there was no significant difference in available energy of plant foods. Next, when I performed discriminant analysis for patas foods and tantalus foods, employing the above two variables, a discriminant function with positive coefficients for both variables was obtained. The mean discriminant-function score of patas foods was higher than that of tantalus foods. Despite being somewhat larger in weight, patas selectively fed on a smaller number of foods of higher quality than did tantalus. I discuss why the results are inconsistent with a well known body weight–diet relationship (Jarman–Bell principle). Energy-efficient locomotion enables patas to exploit not only small dispersed food items of high quality but also areas where high-quality foods are distributed in clumps. Electronic Publication     

Gustatory responsiveness to monosodium glutamate and sodium chloride in four species of nonhuman primates

The taste responsiveness of six squirrel monkeys, five pigtail macaques, four olive baboons and four spider monkeys to monsodium glutamate (MSG) and to sodium chloride was assessed in two-bottle preference tests of brief duration (2 min). When given the choice between tap water and defined concentrations of the two tastants dissolved in tap water, the animals were found to significantly discriminate concentrations of MSG as low as 2 mM (spider monkeys and olive baboons), 50 mM (pigtail macaques) and 300 mM (squirrel monkeys) from the solvent. With sodium chloride, taste preference thresholds were found to be 1 mM (spider monkeys), 20 mM (pigtail macaques), 50 mM (olive baboons), and 200 mM (squirrel monkeys), respectively. Across-species comparisons of the degree of preference for MSG and sodium chloride displayed by the four primate species showed the same order of spider monkeys>olive baboons>pigtail macaques>squirrel monkeys. When presented with equimolar concentrations of different tastants, all four species preferred sucrose as well as a mixture of sucrose and sodium chloride over MSG, and--at least at one concentration--they preferred MSG over sodium chloride. The results support the assertion that the taste responsiveness of the four primate species to MSG and sodium chloride might reflect an evolutionary adaptation to their respective dietary habits.     

Use of spatial, visual, and olfactory information during foraging in wild nocturnal and diurnal anthropoids: A field experiment comparing Aotus, Callicebus, and Saguinus

Early in their evolution, the ancestors of anthropoid primates radiated from a nocturnal to a diurnal niche. Foraging during the night differs from foraging during the day in terms of the availability of light and color cues, and in the movement of odor molecules through the canopy. In this study, we compared the ability of nocturnal and diurnal New World monkeys to use perceptual cues (i.e., the sight or smell of food) and spatial information (place predictability) in within-patch foraging decisions. An experimental field study was conducted on wild groups of night monkeys (Aotus nigriceps), tamarins (Saguinus imperator imperator and S. fuscicollis weddelli), and titi monkeys (Callicebus cupreus) at the Zoobotanical Park/UFAC, Rio Branco, Brazil. Our research design included the construction of feeding stations located in the home range of the study groups. Each feeding station consisted of eight visually identical feeding platforms located in a circular arrangement. In all test settings, two platforms at each feeding station contained a food reward (banana), and the remaining six platforms contained a sham reward (yellow plastic or inaccessible banana). In the night-monkey experiments, each feeding platform was illuminated by a 40-W red bulb to aid the researcher in observing their behavior. When the location of reward sites was predictable over time, individuals in all four species successfully relocated food rewards based solely on spatial information. Each species was also successful in using visual information to distinguish real from sham food rewards. However, only night monkeys and one group of emperor tamarins used olfactory information alone to locate food rewards. Overall, the species' performances did not clearly differentiate Aotus from diurnal New World primates in these experiments.     

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.     

Olfactory Discrimination Ability for Aliphatic Esters in Squirrel Monkeys and Humans

Using a behavioral paradigm designed to simulate olfactory-guidedforaging, the ability of five squirrel monkeys to distinguishiso-amyl acetate from n-and iso-forms of other acetic esters(ethyl acetate to decyl acetate) and from other esters carryingthe iso-amyl group (iso-amyl propionate to iso-amyl capronate)was investigated. We found (i) that all five animals were clearlyable to discriminate between all odor pairs tested; (ii) a significantnegative correlation between discrimination performance andstructural similarity of odorants in terms of differences incarbon chain length of both the aliphatic alcohol group andthe aliphatic acid group of the esters; and (iii) that iso-and n-amyl acetate were perceived as qualitatively similar despitedifferent steric conformation. Using a triple-forced choiceprocedure, 20 human subjects were tested on the same tasks inparallel and showed a very similar pattern of discriminationperformance compared with the squirrel monkeys. Thus, the resultsof this study provide evidence of well-developed olfactory discriminationability in squirrel monkeys for aliphatic esters and supportthe assumption that human and non-human primates may share commonprinciples of odor quality perception. Chem. Senses 22: 457–465,1997.     

Social organization of a stable natal group of captive Guyanese squirrel monkeys (<Emphasis Type="Italic">Saimiri sciureus sciureus</Emphasis>)

Socioecological models suggest competition for food, foraging efficiency, predation, infanticide risk, and the costs of dispersal regulate primate social structure and organization. Wild populations of squirrel monkeys (Saimiri spp.) appear to conform to the predictions of the predation/competition socioecological model (Sterck et al. in Behav Ecol Sociobiol 41:291–309, 1997) and the dispersal/foraging efficiency model (Isbell in Kinship and behavior in primates. Oxford University, New York, pp 71–108, 2004). However, squirrel monkeys in captivity are reported to maintain patterns of social behavior observed in their wild conspecifics despite different food distribution, predation risk, and dispersal options. This behavioral similarity suggests squirrel monkeys’ social behavior has limited flexibility to respond to environmental changes. In this study, we experimentally evaluated the flexibility of social behavior within a captive group of S. sciureus. First, we determined whether dominance and affiliative relationships observed under normal laboratory conditions (with abundant, widely distributed, food; no dispersal option; and no predators) better matched published reports of relationships among wild conspecifics or the predictions of the predation/competition model. Second, we made preferred food items defensible to determine whether dominance interactions would become more frequent and linear, as predicted by the model. The model correctly predicted rates of dominance behavior in both conditions and a linear hierarchy in the defensible food condition but did not predict the consistent affiliative relationships and linear dominance hierarchy observed in normal lab conditions. Although hierarchies were linear and male dominant, manipulating food distribution changed the dominant individual within each sex. Our findings suggest interaction rates adapt more rapidly than social structure to environmental changes in Saimiri and recommend caution in interpreting tests of socioecological models.     

Insect-catching behavior in socially inexperienced infant squirrel monkeys

Insects are an essential component of squirrel monkey natural food. Eight of ten socially inexperienced infant squirrel monkeys, during their 2nd and 3rd month of age, directed their attention to living insects or film presentations of moving insects. They attempted to catch them with gradually improving success, and on at least two occasions consumed them. For comparison, group-living squirrel monkeys begin to eat solid food around their 2nd month of age, continuing with some nursing until about 11 or 13 months, and were only at this age seen to successfully catch and eat insects. Thus, as infant squirrel monkeys proved to be able to catch and eat insects before their first experience with conspecifics, an innate basis for this behavior can be assumed.