Signatures of adaptive evolution in platyrrhine primate genomes.

The platyrrhine family Cebidae (capuchin and squirrel monkeys) exhibit among the largest primate encephalization quotients. Each cebid lineage is also characterized by notable lineage-specific traits, with capuchins showing striking similarities to Hominidae such as high sensorimotor intelligence with tool use, advanced cognitive abilities, and behavioral flexibility. Here, we take a comparative genomics approach, performing genome-wide tests for positive selection across five cebid branches, to gain insight into major periods of cebid adaptive evolution. We uncover candidate targets of selection across cebid evolutionary history that may underlie the emergence of lineage-specific traits. Our analyses highlight shifting and sustained selective pressures on genes related to brain development, longevity, reproduction, and morphology, including evidence for cumulative and diversifying neurobiological adaptations across cebid evolution. In addition to generating a high-quality reference genome assembly for robust capuchins, our results lend to a better understanding of the adaptive diversification of this distinctive primate clade.

Rearing condition may alter neonatal development of captive Bolivian squirrel monkeys (Saimiri boliviensis boliviensis).

Nursery rearing has well-known consequences for primate species. Relative to some other primate species, research has indicated a reduced impact of nursery rearing on squirrel monkeys, particularly in terms of rates, severity, and persistence of abnormal behavior. We administered the Primate Neonatal Neurobehavioral Assessment to 29 dam-reared and 13 nursery-reared squirrel monkeys (Saimiri boliviensis boliviensis) at 2 and 6 weeks of age. Mixed-model ANOVAs comparing composite scores and individual assessment items across age, rearing status, and sex revealed a number of developmental differences. Dam-reared infants scored higher on all four composite measures compared to nursery-reared infants (p < .05) indicating that nursery-reared animals had slower motor development, were less active and attentive, and were more passive than their dam-reared counterparts. Consistent with infant rhesus macaques, nursery-reared squirrel monkeys showed an increased sensitivity to tactile stimulation (p < .05). Altogether, these results suggest a disruption of species-typical development when squirrel monkey infants are reared in a nursery setting, with activity, orientation, and state control areas most affected, though experimental research is needed to determine if this is a causal relationship. Contrary to previous behavioral research, there are likely developmental differences between dam-reared infant squirrel monkeys and those reared in a nursery setting.

Individual differences in zoo-housed squirrel monkeys' (Saimiri sciureus) reactions to visitors, research participation, and personality ratings.

Understanding individual differences in captive squirrel monkeys is a topic of importance both for improving welfare by catering to individual needs, and for better understanding the results and implications of behavioral research. In this study, 23 squirrel monkeys (Saimiri sciureus), housed in an environment that is both a zoo enclosure and research facility, were assessed for (i) the time they spent by an observation window under three visitor conditions: no visitors, small groups, and large groups; (ii) their likelihood of participating in voluntary research; and (iii) zookeepers, ratings of personality. A Friedman's ANOVA and Wilcoxon post-hoc tests comparing mean times found that the monkeys spent more time by the window when there were large groups present than when there were small groups or no visitors. Thus, visitors do not seem to have a negative effect and may be enriching for certain individuals. Through GLMM and correlational analyses, it was found that high scores on the personality trait of playfulness and low scores on cautiousness, depression, and solitude were significant predictors of increased window approach behavior when visitors were present. The GLMM and correlational analyses assessing the links between personality traits and research participation found that low scores of cautiousness and high scores of playfulness, gentleness, affection, and friendliness, were significant predictors. The implications of these results are discussed in relation to selection bias and its potential confounding effect on cognitive studies with voluntary participation.

Repeated acquisition and discrimination reversal in the squirrel monkey (Saimiri sciureus).

Repeated acquisition and discrimination reversal tasks are often used to examine behavioral relations of, respectively, learning and cognitive flexibility. Surprisingly, despite their frequent use in cognitive neuroscience and behavioral pharmacology, variables that control performance under these two tasks have not been widely studied. The present studies were conducted to directly investigate the controlling variables in nonhuman primates. Squirrel monkeys were trained with a touchscreen variant of the repeated acquisition task in which a novel pair of S(+)/S(-) stimuli was presented daily. Subjects learned to discriminate the two stimuli (acquisition) and, subsequently, with the contingencies switched (reversal). Results indicate that rates of both acquisition and reversal learning increased across successive sessions, but that rate of reversal learning remained slower than acquisition learning, i.e., more trials were needed for mastery. Subsequent experiments showed this difference between the rate of learning novel discriminations and reversal was reliable for at least 5 days between acquisition and reversal and notwithstanding the interpolation of additional discriminations. Experimental analysis of the S(+)/S(-) elements of the tasks revealed that the difference in the rate of learning could not be attributed to a relatively aversive quality of the S(-) or to a relatively appetitive quality of the S(+), but, rather, to contextual control by the S(+)/S(-) stimulus complex. Thus, if either element (S(+) or S(-)) of the stimulus complex was replaced by a novel stimulus, the rate of acquisition approximated that expected with a novel stimulus pair. These results improve our understanding of fundamental features of discrimination acquisition and reversal.

The Thatcher illusion in squirrel monkeys (Saimiri sciureus).

Like humans, Old World monkeys are known to use configural face processing to distinguish among individuals. The ability to recognize an individual through the perception of subtle differences in the configuration of facial features plays an important role in social cognition. To test this ability in New World monkeys, this study examined whether squirrel monkeys experience the Thatcher illusion, a measure of face processing ability in which changes in facial features are difficult to detect in an inverted face. In the experiment, the monkeys were required to distinguish between a target face and each of the three kinds of distracter faces whose features were altered to be different from those of the target. For each of the pairs of target and distracter faces, four rotation-based combinations of upright and inverted face presentations were used. The results revealed that when both faces were inverted and the eyes of the distracter face were altered by rotating them at an angle of 180° from those of the target face, the monkeys' discrimination learning was obstructed to a greater extent than it was under the other conditions. Thus, these results suggest that the squirrel monkey does experience the Thatcher illusion. Furthermore, it seems reasonable to assume that squirrel monkeys can utilize information about facial configurations in individual recognition and that this facial configuration information could be useful in their social communications.

Positive reinforcement training in squirrel monkeys using clicker training.

Nonhuman primates in research environments experience regular stressors that have the potential to alter physiology and brain function, which in turn can confound some types of research studies. Operant conditioning techniques such as positive reinforcement training (PRT), which teaches animals to voluntarily perform desired behaviors, can be applied to improve behavior and reactivity. PRT has been used to train rhesus macaques, marmosets, and several other nonhuman primate species. To our knowledge, the method has yet to be used to train squirrel monkeys to perform complex tasks. Accordingly, we sought to establish whether PRT, utilizing a hand-box clicker (which emits a click sound that acts as the conditioned reinforcer), could be used to train adult male squirrel monkeys (Saimiri boliviensis, N = 14). We developed and implemented a training regimen to elicit voluntary participation in routine husbandry, animal transport, and injection procedures. Our secondary goal was to quantify the training time needed to achieve positive results. Squirrel monkeys readily learned the connection between the conditioned reinforcer (the clicker) and the positive reinforcer (food). They rapidly developed proficiency on four tasks of increasing difficulty: target touching, hand sitting, restraint training, and injection training. All subjects mastered target touching behavior within 2 weeks. Ten of 14 subjects (71%) mastered all tasks in 59.2 ± 2.6 days (range: 50-70 days). In trained subjects, it now takes about 1.25 min per monkey to weigh and administer an intramuscular injection, one-third of the time it took before training. From these data, we conclude that clicker box PRT can be successfully learned by a majority of squirrel monkeys within 2 months and that trained subjects can be managed more efficiently. These findings warrant future studies to determine whether PRT may be useful in reducing stress-induced experimental confounds in studies involving squirrel monkeys.

Reinforcement learning modeling reveals a reward-history-dependent strategy underlying reversal learning in squirrel monkeys.

Insight into psychiatric disease and development of therapeutics relies on behavioral tasks that study similar cognitive constructs in multiple species. The reversal learning task is one popular paradigm that probes flexible behavior, aberrations of which are thought to be important in a number of disease states. Despite widespread use, there is a need for a high-throughput primate model that can bridge the genetic, anatomic, and behavioral gap between rodents and humans. Here, we trained squirrel monkeys, a promising preclinical model, on an image-guided deterministic reversal learning task. We found that squirrel monkeys exhibited two key hallmarks of behavior found in other species: integration of reward history over many trials and a side-specific bias. We adapted a reinforcement learning model and demonstrated that it could simulate squirrel monkey-like behavior, capture training-related trajectories, and provide insight into the strategies animals employed. These results validate squirrel monkeys as a model in which to study behavioral flexibility. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

The impact of moving to a novel environment on social networks, activity and wellbeing in two new world primates.

Among the stressors that can affect animal welfare in zoos, the immediate effect of relocation to a novel environment is one that has received little attention in the literature. Here, we compare the social network, daily activity and the expression of stress-related behavior in capuchins (Cebus apella) and squirrel monkeys (Saimiri sciureus) before and just after they were relocated to a new enriched enclosure. Results showed similar immediate responses to the move in the two species. Both showed a substantial increase in the time spent resting and spent more time in the highest and "safest" part of their enclosure after relocation. Both capuchins and squirrel monkeys spent significantly more time in close proximity to other group members after relocation, compared to before. In squirrel monkeys, the structure of the social network, which was initially correlated to affiliation, was no longer so after the move. In capuchins, the network analysis showed that individuals regrouped by age, with the youngsters who were potentially more affected by stress being in the center of the network. Social network analysis helped to achieve a more complete picture of how individuals were affected by relocation. We suggest that this type of analysis should be used alongside traditional methods of observation and analysis to encompass the most complex aspects of animal behavior in times of stress and to improve welfare.

Flexibility in the use of requesting gestures in squirrel monkeys (Saimiri sciureus).

Three squirrel monkeys, trained to make a requesting gesture, were tested in the presence of a human assistant whose visual attention varied across trials. When food was available in one dish and an empty dish was nearby, the monkeys pointed overwhelmingly toward the former, regardless of where the assistant was looking. Looking at the assistant while pointing ("monitoring") peaked when she looked at them and when she attempted to engage them in joint attention. When only one dish was present, the monkeys refrained from gesturing if it was empty and if no assistant was present. They gestured more when the assistant made eye contact with them. Furthermore, when the assistant's focus of attention switched from the dish or the ceiling to the monkeys, the latter resumed pointing and increased their monitoring of the assistant. This is the first demonstration of such flexible use of an intentionally communicative requesting gesture in New World monkeys.

Investigating reactions of squirrel monkeys (Saimiri sciureus) towards unequal food distributions in a tray-pulling paradigm.

The fact that squirrel monkeys do not routinely cooperate in the wild has been proposed to explain their failure to show disadvantageous inequity aversion (i.e., negative reactions when receiving less than a partner) in an experimental exchange. Here we assessed whether the use of a tray-pulling paradigm, allowing for a larger variety of unequal testing situations, would bring additional insights into inequity aversion in this species. Squirrel monkeys were tested in pairs in which only the donor could pull a tray baited with food to within reach of itself and a recipient. Using pairs with different social relationships, we examined donors' frequencies of pulling both in the presence and absence of a recipient, as well as across three different food distributions: equal, qualitative inequity (higher-value reward for the recipient), and quantitative inequity (no food reward for the donor). Results showed that female donors pulled the tray less often in the quantitative inequity condition with an out-group female recipient than when alone. However, such discrimination was not observed when females were with female in-group and male out-group recipients. By contrast, male donors did not adjust their pull frequencies according to the recipient's presence or identity (female and male out-group recipients). These results point towards possible disadvantageous inequity aversion in female squirrel monkeys. However, alternative hypotheses such as increased arousal caused by out-group female recipients cannot be ruled out. We discuss the data in line with major theories of inequity aversion and cooperation in primates.

Longitudinal changes in DTI parameters of specific spinal white matter tracts correlate with behavior following spinal cord injury in monkeys.

This study aims to evaluate how parameters derived from diffusion tensor imaging reflect axonal disruption and demyelination in specific white matter tracts within the spinal cord of squirrel monkeys following traumatic injuries, and their relationships to function and behavior. After a unilateral section of the dorsal white matter tract of the cervical spinal cord, we found that both lesioned dorsal and intact lateral tracts on the lesion side exhibited prominent disruptions in fiber orientation, integrity and myelination. The degrees of pathological changes were significantly more severe in segments below the lesion than above. The lateral tract on the opposite (non-injured) side was minimally affected by the injury. Over time, RD, FA, and AD values of the dorsal and lateral tracts on the injured side closely tracked measurements of the behavioral recovery. This unilateral section of the dorsal spinal tract provides a realistic model in which axonal disruption and demyelination occur together in the cord. Our data show that specific tract and segmental FA and RD values are sensitive to the effects of injury and reflect specific behavioral changes, indicating their potential as relevant indicators of recovery or for assessing treatment outcomes. These observations have translational value for guiding future studies of human subjects with spinal cord injuries.

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.

Are monkeys aesthetists? Rensch (1957) revisited.

Three experiments assessed whether capuchin monkeys (Cebus apella) and squirrel monkeys (Saimiri sciureus) prefer regular and symmetrical visual patterns. Pictorial representations of faces were included in 1 stimulus set. When the monkeys could pick up and manipulate small cards bearing the stimuli, all preferences expressed by capuchins and most of those expressed by squirrel monkeys were for regular stimuli. Symmetry of the patterns was influential but not essential. Some preferences were also found for faces. When images of the patterns were presented on a touch screen, capuchins continued to express preferences especially for regular and symmetrical stimuli, but they showed some avoidance of faces. Squirrel monkeys responded less discriminatingly to the touch screen stimuli. The findings provide support for B. Rensch's (1957) claim that monkeys prefer visual stimuli that humans find aesthetically pleasing.

Inference by exclusion in lion-tailed macaques (Macaca silenus), a hamadryas baboon (Papio hamadryas), capuchins (Sapajus apella), and squirrel monkeys (Saimiri sciureus).

Previous research has suggested that several primate species may be capable of reasoning by exclusion based on the finding that they can locate a hidden object when given information about where the object is not. The present research replicated and extended the literature by testing 2 Old World monkey species, lion-tailed macaques (Macaca silenus) and a hamadryas baboon (Papio hamadryas), and 2 New World species, capuchin monkeys (Sapajus apella) and squirrel monkeys (Saimiri sciureus). The New World monkeys were tested on the traditional 2-way object choice task, and all 4 species were also tested on a more complex 3-way object choice task. In addition, the squirrel monkeys were tested on a 2-way object choice task with auditory information. The results showed that, whereas the Old World species were able to infer by exclusion on the 3-object task, some of the capuchin monkeys had difficulty on each of the 2- and 3-cup tasks. All but 1 of the squirrel monkeys failed to infer successfully, and their strategies appeared to differ between the visual and auditory versions of the task. Taken together, this research suggests that the ability to succeed on this inference task may be present throughout Old World monkey species, but is fragile in the New World species tested thus far. (PsycINFO Database Record

Judgements of ordinality and summation of number symbols by squirrel monkeys (Saimiri sciureus).

In Experiment 1, 2 squirrel monkeys (Saimiri sciureus) were given choices between all possible pairs of the arabic numbers 0, 1, 3, 5, 7, and 9, with choice of any number yielding that number of pieces of peanut as a reward. Both monkeys learned to choose the larger number in all pairings and learned to choose the largest number within a set of 4 numbers. In Experiments 2-4, the monkeys were tested on problems in which they chose between pairs of stimuli containing 2 numbers versus 2 numbers, 1 number versus 2 numbers, and 3 numbers versus 3 numbers. Both monkeys showed a significant tendency to choose the stimulus that contained the largest sum. Various tests indicated that this effect could not be explained by choice of the stimulus with the largest single number, by avoidance of the stimulus with the smallest single number, or by experimenter cuing.

Can squirrel monkeys (Saimiri sciureus) learn self-control? A study using food array selection tests and reverse-reward contingency.

Eight squirrel monkeys (Saimiri sciureus) were presented with 2 stimulus arrays, namely 1 and 4 pieces of food, but they received only the array other than the one they reached for. In this reverse-reward condition, all monkeys initially showed a strong preference for the larger array. One monkey learned to reach toward the smaller array when a large-or-none reward contingency was applied (i.e., no reward followed a reach toward the larger array, but this array was given for a reach toward the smaller array). When correction trials and time-out were added to the large-or-none procedure, all remaining monkeys except 1 learned this form of self-control. Performance was maintained when correction trials were discontinued, the original reverse-reward condition was rerun, and novel array-size pairs were presented. This study demonstrates one form of self-control in a New World primate and shows the reverse-reward procedure to be a potentially valuable method for assessing species and individual differences in self-control and numerosity-related abilities.

Assessing olfactory performance in a New World primate, Saimiri sciureus.

Using a task designed to simulate olfactory-guided foraging behavior, this study demonstrates for the first time that olfactory performance can be reliably assessed in squirrel monkeys. Small flip-top vials were fixed in random order to the arms of a climbing frame and equipped with odorized strips signalling either that they contained a peanut food reward (S+) or that they did not (S-), and three adult female monkeys were allowed 1 min to harvest as many baited nuts from this tree as possible. Given five 1-min trials per day, animals took between 15 and 25 days to reach the criterion of 80% correct choices, could readily transfer to new S+ or S- stimuli, and could remember the task even after a 1-month break. The precision and consistency of the monkeys' performance in tests of discrimination ability and sensitivity demonstrate the suitability of this paradigm for assessing olfactory function, and a first test of human subjects using the same cups and odorants showed that it may also be used to directly compare olfactory performance in human and nonhuman primates.

Sociophysiology of relationships in squirrel monkeys. I. Formation of female dyads.

Physiological and behavioral consequences of formation of female-female relationships were investigated in adult squirrel monkeys. Plasma cortisol, heart rate, and behavior were evaluated during confinement in a test cage while animals were housed alone, during the first hour of isosexual pair formation, and while animals were housed as isosexual dyads. In addition, basal cortisol levels were assessed both before and after pair formation, as were behavioral and cardiovascular responses to social and nonsocial stimulus presentations. Basal cortisol levels underwent a marked and sustained reduction following formation of pairs, independent of both dominance status and the quality of social interactions between pairmates. In contrast, adrenocortical responsiveness was not altered by social conditions, apart from a modest and transitory difference between dominant and subordinate females in their initial response to pair formation. Heart rate declined sharply during each test session, but did not reliably differentiate social conditions, stimulus conditions, or dominance status. These findings contrast with results of a parallel study of male squirrel monkeys and suggest that isosexual relationships in males and females are associated with different sociophysiological processes.

A comparison of food preferences and nutrient composition in captive squirrel monkeys, Saimiri sciureus, and pigtail macaques, Macaca nemestrina.

I assessed the occurrence of food preferences in captive squirrel monkeys and pigtail macaques and analyzed whether their preferences correlate with nutrient composition. Using a two-alternative choice test, I repeatedly presented six Saimiri sciureus and six Macaca nemestrina with all possible binary combinations of 12 types of food that are part of their diet in captivity. The two species exhibited significantly different rank orders of preference. Correlational analyses revealed that the preference ranking of the squirrel monkeys was significantly positively correlated with total energy content, irrespective of the source of energy as neither total carbohydrate content nor protein or lipid content was significantly correlated with food preference. In contrast, the preference ranking of the pigtail macaques showed a significant positive correlation with total carbohydrate content and with fructose content but not with total energy content of the food items. These results suggest that squirrel monkeys are opportunistic feeders with regard to maximizing net gain of energy, whereas pigtail macaques are not but rather seek to meet their requirements of metabolic energy by preferring foods that are high in carbohydrates.

A study of long-term odor memory in squirrel monkeys (Saimiri sciureus).

Five squirrel monkeys (Saimiri sciureus) were trained to discriminate between pairs of odors, and their ability to recognize these as positive or negative was tested at intervals of up to 7 months. Retention was excellent up to 15 weeks and remained significantly above chance even after 30 weeks. Good performance at the shorter intervals was not due to rapid relearning, although at the longer intervals considerable savings were demonstrated by the animals' ability to reach criterion more rapidly than with novel odors. Thus, squirrel monkeys possess a robust memory for odors and show flat forgetting curves consistent with reports for human subjects.