Available and unavailable decoys in capuchin monkeys (Sapajus spp.) decision-making.

Decision-making has been observed to be systematically affected by decoys, i.e., options that should be irrelevant, either because unavailable or because manifestly inferior to other alternatives, and yet shift preferences towards their target. Decoy effects have been extensively studied both in humans and in several other species; however, evidence in non-human primates remains scant and inconclusive. To address this gap, this study investigates how choices in capuchin monkeys (Sapajus spp.) are affected by different types of decoys: asymmetrically dominated decoys, i.e., available and unavailable options that are inferior to only one of the other alternatives, and phantom decoys, i.e., unavailable options that are superior to another available alternative. After controlling for the subjective strength of initial preferences and the distance of each decoy from its target in attribute space, results demonstrate a systematic shift in capuchins' preference towards the target of both asymmetrically dominated decoys (whether they are available or not) and phantom decoys, regardless of what options is being targeted by such decoys. This provides the most comprehensive evidence to date of decoy effects in non-human primates, with important theoretical and methodological implications for future comparative studies on context effects in decision-making.

Context-effect bias in capuchin monkeys (Sapajus spp.): exploring decoy influences in a value-based food choice task.

Decision making is known to be liable to several context effects. In particular, adding a seemingly irrelevant alternative (decoy) to a set of options can modify preferences: typically, by increasing choices towards whatever option clearly dominates the decoy (attraction effect), but occasionally also decreasing its appeal and generating a shift in the opposite direction (repulsion effect). Both types of decoy effects violate rational choice theory axioms and suggest dynamic processes of preference-formation, in which the value of each alternative is not determined a priori, but it is instead constructed by comparing options during the decision process. These effects are well documented, both in humans and in other species: e.g., amoebas, ants, honeybees, frogs, birds, cats, dogs. However, evidence of decoy effects in non-human primates remains surprisingly mixed. This study investigates decoy effects in capuchin monkeys (Sapajus spp.), manipulating time pressure across different conditions, to test whether such effects require time-consuming comparative processes among available alternatives. Whereas the time-dependent nature of decoy effects is a robust finding in the human literature, this is its first investigation in non-human animals. Our results show that capuchins exhibit an attraction effect with decoys targeting their preferred food, and that this effect disappears under time pressure; moreover, we observe preliminary evidence of a repulsion effect when decoys target instead the less-preferred food, possibly due to the larger distance between decoy and target in the attribute space. Taken together, these results provide valuable insight on the evolutionary roots of comparative decision making.

State-dependent risky choices in primates: Variation in energy budget does not affect tufted capuchin monkeys' (Sapajus spp.) risky choices.

Economic models predict that rational decision makers' choices between a constant, "safe" option and a variable, "risky" option leading, on average, to the same payoff, should be random. However, a wealth of research has revealed that, when faced with risky decisions, both human and nonhuman animals deviate from economic rationality. According to the risk-sensitivity theory, individuals should prefer a safe option when they are in a positive energy state and a risky option when they are in a negative energy state. The abundance/risk hypothesis proposes that individuals should prefer risky options when diet quality exceeds their nutritional requirements. We tested how energy budget affects decision making under risk by presenting 22 capuchins belonging to two colonies (IT: N = 12, US: N = 10) with a risky choice task. Capuchins had to choose between a constant option (always four food items) and a variable option (one or seven food items with a 50% probability) in two conditions. In the Low-energy condition capuchins were tested before their main meal, whereas in the High-energy condition they were tested following a high-caloric meal. In neither colony did we find a significant difference between conditions, suggesting that the energy budget did not affect risk preferences. However, we found differences between colonies in their general response to risky choices: US capuchins were more risk-prone after selecting a safe option than a risky option and after selecting a bad (one food item) than a good (seven food items) risky option, whereas this did not hold true in IT capuchins. Furthermore, in the IT colony, males were more risk-prone under the High-energy condition compared to the Low-energy condition. Subtle differences in individual characteristics, management conditions, or stochastic founder effects may be implied, with relevant consequences for the outcomes of research on risky decision-making across laboratories.

Complementary feeding approach and maternal responsiveness in 8- and 12-month-old Italian infants: A longitudinal study.

In Western countries, infants are usually introduced to solids through spoon-fed puréed foods (parent-led weaning, PLW). However, an alternative approach known as "baby-led weaning" (BLW), in which infants usually participate in family meals and eat independently, is becoming increasingly popular. We investigated the relationship between the type of complementary feeding approach and maternal responsiveness to infant feeding cues in a longitudinal sample of 178 infants observed at 8 and 12 months. Mothers reported the complementary feeding method used and, from video-recorded meals, we coded the proportion of time infants self-fed and rated maternal responsiveness by means of the Responsiveness to Child Feeding Cues Scale (Hodges et al., 2013). Responsiveness to infant receptiveness and fullness cues were significantly correlated at 8 months, but not at 12 months, when unresponsiveness decreased for receptiveness but remained stable for fullness cues. Thus, as infants got older, mothers were increasingly tuned in to their receptiveness cues. However, we did not observe the same pattern for fullness cues, perhaps because mothers were concerned that their infants did not eat enough. Moreover, at both time points, mothers were more responsive to infants' receptiveness than fullness cues, possibly due to an evolutionary drive to protect infants from starvation. Finally, responsiveness to fullness, but not responsiveness to receptiveness, was positively related to the proportion of infant self-feeding, but there were no significant differences in responsiveness depending on the self-reported complementary feeding approach. Thus, a weaning style that emphasizes independent feeding, regardless of whether this is labeled as BLW, may promote more infant-centered maternal responses at the end of the meal, with potential implications for promoting infant self-regulation not only at mealtimes, but also in other domains.

Baby-led weaning in Italy and potential implications for infant development.

Baby-led weaning is an approach to complementary feeding that emphasizes an infant's ability to self-feed rather than being spoon fed, and to eat minimally-processed foods rather than puréed foods. This study aimed to investigate the variability in infant feeding practices and the possible association with developmental milestones in an Italian population. A sample of 1245 mothers of 6-12 month-old infants completed an online survey about complementary feeding and their infant's attainment of developmental milestones. Infants' eating of family food was positively related to self-feeding and to a lower consumption of puréed foods. As in previous studies in the UK and New Zealand, a baby-led weaning style was positively associated with breastfeeding, exposure to complementary foods around six months of age, earlier exposure to both finger and family foods, and higher interest in family food and shared family meals. Infants who were introduced to solid foods using a baby-led weaning approach were more likely to have met important developmental milestones; when controlling for covariates, percentage of family feeding was positively associated with sitting unsupported at an earlier age and a low spoon-feeding style was associated with crawling at an earlier age. These data suggest that baby-led weaning should be defined more comprehensively. Moreover, its potential influence on developmental domains beyond diet and eating behavior warrants future targeted exploration.

An infant-led approach to complementary feeding is positively associated with language development.

The timing and strategy with which parents first introduce their infants to solid foods may be an important predictor of subsequent developmental outcomes. Recent years have seen a decline in the prevalence of traditional parent-led feeding of soft, puréed food and a rise in the prevalence of infant-led complementary feeding. Although there has been some research espousing the benefits of infant-led complementary feeding for improving food fussiness and self-regulation, there has been little exploration of this approach that may impact on other developmental outcomes in children. The current study explores whether aspects of the infant-led approach, specifically the child eating unaided and consuming finger foods and eating with the family, are related to child language outcomes. One hundred thirty one parents of children aged 8-24 months completed questionnaires about their approach to complementary feeding, their current feeding practices, their child's experiences with family foods and child language comprehension/production. The findings suggest that an approach to complementary feeding which promotes infant autonomy in feeding (i.e., eating finger foods rather than puréed foods) and consuming more family foods is related to more advanced child language production and comprehension. Specifically, the prevalence of eating family foods mediated the relationship between eating unaided at the onset of the complementary feeding period and later language outcomes. This study is the first to find a significant relationship between different approaches to introducing solid foods and child language outcomes and these findings highlight the potential for different complementary feeding approaches to influence behaviour beyond mealtimes.

Evolutionary origins of money categorization and exchange: an experimental investigation in tufted capuchin monkeys (Sapajus spp.).

Money is a cultural artefact with a central role in human society. Here, we investigated whether some features of money may be traced back to the exchange habits of nonhuman animals, capitalizing on their ability to flexibly use tokens in different domains. In Experiment 1, we evaluated whether capuchins can recognize token validity. Six subjects were required to exchange with the experimenter valid/familiar tokens, valid/unfamiliar tokens, invalid tokens, and no-value items. They first exchanged a similar number of valid/familiar and valid/unfamiliar tokens, followed by exchanges of invalid tokens and no-value items. Thus, as humans, capuchins readily recognized token validity, regardless of familiarity. In Experiment 2, we further evaluated the flexibility of the token-food association by assessing whether capuchins could engage in reverse food-token exchanges. Subjects spontaneously performed chains of exchanges, in which a food item was exchanged for a token, and then the token was exchanged for another food. However, performance was better as the advantage gained from the exchange increased. Overall, capuchins recognized token validity and successfully engaged in chains of reverse and direct exchanges. This suggests that-although nonhuman animals are far from having fully-fledged monetary systems-for capuchins tokens share at least some features with human money.

The evolution of self-control.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Do tufted capuchin monkeys play the odds? Flexible risk preferences in Sapajus spp.

As humans, several non-human animal species avoid risk, defined as "variability in rate of gain". However, non-human primate studies revealed a more complicated picture, with different species ranging from risk aversion to risk proneness. Within an ecological rationality framework, a species' feeding ecology should influence its risk preferences, as it has been shown in bonobos and chimpanzees. Although the feeding ecology hypothesis is promising, it has not been yet verified in species other than apes. Here, we aimed to assess whether this hypothesis holds true in tufted capuchin monkeys (Sapajus spp.). Ten capuchins were presented with choices between a "safe" option and a "risky" option in three conditions differing for the probability of receiving the larger reward when selecting the risky option. Similarly to chimpanzees, capuchins were risk prone. However, capuchins' behaviour was not the result of a bias towards the choice of the risky option, since-when facing options with different probabilities of obtaining the larger outcome-they were able to flexibly modify their preferences. Capuchins' decision-making under risk mirrors their risk-prone behaviour in the wild, where they often rely on unpredictable and/or hazardous food sources, thus satisfying the feeding ecology hypothesis.

When is it worth waiting for? Food quantity, but not food quality, affects delay tolerance in tufted capuchin monkeys.

When faced with choices between smaller sooner options and larger later options (i.e. intertemporal choices), both humans and non-human animals discount future rewards. Apparently, only humans consistently show the magnitude effect, according to which larger options are discounted over time at a lower rate than smaller options. Most of the studies carried out in non-human animals led instead to negative results. Here, we tested ten tufted capuchin monkeys (Sapajus spp.) in a delay choice task to evaluate whether they show a magnitude effect when choosing between different quantities of the same food or when the options are represented by high- and low-preferred foods in different conditions. Whereas food quality did not play a role, we provided the first evidence of an effect of the reward amount on temporal preferences in a non-human primate species, a result with potential implications for the validity of comparative studies on the evolution of delay tolerance. In contrast with human results, but as shown in other animal species, capuchins' choice of the larger later option decreased as the amount of the smaller sooner option increased. Capuchins based their temporal preferences on the quantity of the smaller sooner option, rather than on that of the larger later option, probably because in the wild they virtually never have to choose between the above two options at the same time, but they more often encounter them consecutively. Thus, paying attention to the sooner option and deciding on the basis of its features may be an adaptive strategy rather than an irrational response.

Chimpanzees (Pan troglodytes) can wait, when they choose to: a study with the hybrid delay task.

Self-control has been studied in nonhuman animals using a variety of tasks. The inter-temporal choice (ITC) task presents choices between smaller-sooner (SS) and larger-later (LL) options. Using food amounts as rewards, this presents two problems: (a) choices of the LL option could either reflect self-control or instead result from animals' difficulty with pointing to smaller amounts of food; (b) there is no way to verify whether the subjects would not revert their choice for the LL option, if given the opportunity to do so during the ensuing delay. To address these problems, we have recently introduced a new protocol, the hybrid delay task, which combines an initial ITC with a subsequent accumulation phase in which selection of the SS option leads to its immediate delivery, but choice of the LL option then leads to one-by-one presentation of those items that continues only as long as the subject does not eat any of the accumulated items. The choice of the LL option therefore only reflects self-control when the number of items obtained from LL choices during the accumulation phase is higher than what could be received in the SS option. Previous research with capuchin monkeys demonstrated that their apparent self-control responses in the ITC task may have overestimated their general self-control abilities, given their poor performance in the hybrid delay task. Here, chimpanzees instead demonstrated that their choices for the LL option in the ITC phase of the hybrid delay task were confirmed by their ability to sustain long delays during accumulation of LL rewards.

Do displacement activities help preschool children to inhibit a forbidden action?

Displacement activities are commonly recognized as behavioral patterns, mostly including self-directed actions (e.g., scratching, self-touching), that often occur in situations involving conflicting motivational tendencies. In ethology, several researchers have suggested that displacement activities could facilitate individuals in dealing with the stress experienced in a frustrating context. In child developmental research, some authors have assessed whether distraction strategies could help children to inhibit a dominant response during delay of gratification tasks. However, little is known about the displacement activities that young children may produce in such situations. This study was aimed at investigating whether displacement activities had an effect on preschool children's ability to postpone an immediate gratification (i.e., interacting with an attractive toy, a musical box), thereby functioning as regulators of their emotional state. To this end, we administered 143 2- to 4-year-olds with a delay maintenance task and related their performance with displacement activities they produced during the task and with actions with an external object. Children's latency to touch the musical box was positively related to their rate of displacement activities. However, the rate of displacement activities increased progressively as long as the children were able to inhibit the interaction with the musical box. In addition, the rate of displacement activities during the first 1 min of test did not predict the ability of children to inhibit the interaction with the box. These results suggest that displacement activities represented a functionless by-product of motivational conflict rather than a strategy that children used to inhibit their response to an attractive stimulus.

Monomorphic region of the serotonin transporter promoter gene in New World monkeys.

Genetic variation in the human serotonin system has long been studied because of its functional consequences and links to various neuropsychiatric and behavior-related disorders. Among non-human primates, the common marmosets (Callithrix jacchus) and tufted capuchins monkeys (Cebus apella) are becoming increasingly used as models to study the effects of genes, environments, and their interaction on physiology and complex behavior. In order to investigate the independent functions of and potential interactions between serotonin-related genes, anxiety and neuropsychiatric disorders, we analyzed the presence and variability of the serotonin transporter gene-linked polymorphic region (5-HTTLPR) in marmoset and capuchin monkeys. By PCR and using heterologous primers from the human sequence, we amplified and then sequenced the corresponding 5-HTT region in marmosets and capuchins. The resulting data revealed the presence of a tandem repeat sequence similar to that described in humans, but unlike humans and other Old World primates, no variable length alleles were detected in these New World monkeys, suggesting that if serotonin transporter is involved in modulating behavior in these animals it does so through different molecular mechanisms.

The presence of a potential competitor modulates risk preferences in rats.

Although both human and non-human animals, in everyday life, deal with risky decisions in a social environment, few studies investigated how social dimension influences risk preferences (i.e., if consequences on others feeds back over own choice). Here, we assessed whether the presence of a conspecific, acting as a potential competitor for the same food resource, influenced risky decision-making in male rats. Subjects received a series of choices between a safe option (always yielding a small yet optimal reward, solely to itself) and a risky option (yielding a larger but suboptimal reward, one third of times to itself and two third of times delivered to the other half cage); rats were tested twice, both alone and paired with a conspecific, recipient of own-lost food and hence acting as potential competitor. Results showed that focal subjects were more risk-prone when paired with a conspecific than when tested alone. However, rats exhibited also a higher motivational conflict with a competing bystander present than alone: data suggest that the primary drive was to increase "own" food rather than either a competitive or prosocial tendency. Overall, for rats tested in a risky-choice task, a competitive social context increased the salience and attractiveness of larger food outcomes, as observed in humans and great apes. This led to the economically irrational response of selecting the "binge-but-risky" option, notwithstanding uncertainty about the actual recipient of such food.

Online Assessment of Motor, Cognitive, and Communicative Achievements in 4-Month-Old Infants.

Remote methods for data collection allow us to quickly collect large amounts of data, offering several advantages as compared to in-lab administration. We investigated the applicability of an online assessment of motor, cognitive, and communicative development in 4-month-old infants based on several items of the Bayley Scales of Infant Development, 3rd edition (BSID-III). We chose a subset of items which were representative of the typical developmental achievements at 4 months of age and that we could administer online with the help of the infant's caregiver using materials which were easily available at home. Results showed that, in a sample of infants tested live (N = 18), the raw scores of the BSID-III were significantly correlated with the raw scores of a subset of items corresponding to those administered to a sample of infants tested online (N = 53). Moreover, for the "online" participants, the raw scores of the online assessment did not significantly differ from the corresponding scores of the "live" participants. These findings suggest that the online assessment was to some extent comparable to the live administration of the same items, thus representing a viable opportunity to remotely evaluate infant development when in-person assessment is not possible.

Searching for a Relationship between Early Breastfeeding and Cognitive Development of Attention and Working Memory Capacity.

Previous research consistently reported that subjects that were exclusively breastfed (eBF) vs. not-exclusively breastfed (neBF) during infancy (0-6 months) showed increased scores of general intelligence measures (e.g., the intelligence quotient). However, the existent literature largely neglected whether breastfeeding also affects specific cognitive processes, such as attention and working memory (WM) capacity. We tested whether eBF vs. neBF subjects showed performance differences in relation to these two core cognitive functions. The Attention Network Test (ANT), to measure alerting, orienting, and conflict, and the Change Colour Task (CCT), to measure visuospatial WM capacity, were administered to 144 participants divided according to age (6-, 10-, and 18-year-old participants) and breastfeeding (eBF or neBF during 0-6 months of life). Importantly, the sub-groups were homogenous in terms of maternal education, a factor potentially affecting the relation between breastfeeding and cognition. While we found increased performance as a function of participants' age in both tasks, we failed to observe effects related to breastfeeding, as evidenced by Bayesian analyses. These findings highlight for the first time that the pattern of nutrition provided during early infancy does not appear to affect the development of attention and WM capacity, at least starting from the age considered in the present study.

Infant sleep and development: Concurrent and longitudinal relations during the first 8 months of life.

Sleep is an essential function of human life, underlying both biological and cultural processes. Dramatic changes in sleep occur during infancy, in terms of night awakenings, which tend to diminish over time, and day/night sleep duration, with newborns sleeping up to 16-17 h per day and gradually decreasing to 9-13 h between 6 and 11 months of age. Remarkably, research indicates that changes in infant sleep are in interaction with important acquisitions in other domains of child development. In the present study, we aimed at investigating concurrent and longitudinal relations between sleep and cognitive maturation during infancy, by collecting data on 156 infants at 4 and 8 months of age. Infants' sleep was assessed through the Brief Infant Sleep Questionnaire (BISQ; Sadeh, 2004), whereas cognitive maturation was evaluated using the Developmental Profile™ 3 (Alpern 2007). We also examined infants' language understanding through the short form of the Italian version of the MacArthur-Bates Communicative Development Inventory (MCDI-SF): Words and Gestures (Caselli, Bello, Rinaldi, Stefanini, & Pasqualetti, 2015; Fenson et al., 2000). Finally, information about infants' temperament and maternal practices potentially relevant for sleep quality, such as the use of a pacifier at nighttime, co-sleeping and exclusive breastfeeding, was detected. Results showed that night and day sleep were differently related to infants' development at 4 and 8 months of age, but there were no robust longitudinal relationships.

Tokens improve capuchin performance in the reverse-reward contingency task.

In humans and apes, one of the most adaptive functions of symbols is to inhibit strong behavioural predispositions. However, to our knowledge, no study has yet investigated whether using symbols provides some advantage to non-ape primates. We aimed to trace the evolutionary roots of symbolic competence by examining whether tokens improve performance in the reverse-reward contingency task in capuchin monkeys, which diverged from the human lineage approximately 35 Ma. Eight capuchins chose between: (i) two food quantities, (ii) two quantities of 'low-symbolic distance tokens' (each corresponding to one unit of food), and (iii) two 'high-symbolic distance tokens' (each corresponding to a different amount of food). In all conditions, subjects had to select the smaller quantity to obtain the larger reward. No procedural modifications were employed. Tokens did improve performance: five subjects succeeded with high-symbolic distance tokens, though only one succeeded with food, and none succeeded with low-symbolic distance tokens. Moreover, two of the five subjects transferred the rule to novel token combinations. Learning effects or preference reversals could not account for the successful performance with high-symbolic distance tokens. This is, to our knowledge, the first demonstration that tokens do allow monkeys to inhibit strong behavioural predispositions, as occurs in chimpanzees and children.

Economic behaviours among non-human primates.

Do we have any valid reasons to affirm that non-human primates display economic behaviour in a sufficiently rich and precise sense of the phrase? To address this question, we have to develop a set of criteria to assess the vast array of experimental studies and field observations on individual cognitive and behavioural competences as well as the collective organization of non-human primates. We review a sample of these studies and assess how they answer to the following four main challenges. (i) Do we see any economic organization or institutions emerge among groups of non-human primates? (ii) Are the cognitive abilities, and often biases, that have been evidenced as underlying typical economic decision-making among humans, also present among non-human primates? (iii) Can we draw positive lessons from performance comparisons among primate species, humans and non-humans but also across non-human primate species, as elicited by canonical game-theoretical experimental paradigms, especially as far as economic cooperation and coordination are concerned? And (iv) in which way should we improve models and paradigms to obtain more ecological data and conclusions? Articles discussed in this paper most often bring about positive answers and promising perspectives to support the existence and prevalence of economic behaviours among non-human primates. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.