To thrive in rapidly changing environments, including those induced by humans, animals must respond quickly to relevant information about their surroundings (Barrett et al., 2019). Climate change or human-induced invasions of species novel to the area, as well as the introduction of human artifacts into the environment can affect different species in myriad ways, for example, bringing new threats, disruptions, competition, or novel resource opportunities. Adaptive behavioral responses to such changes can include effectively avoiding new predators, maintaining the high competitive ability, and exploiting novel resources (Barrett et al., 2019; Jesmer et al., 2018; Gruber et al., 2019; Sih et al., 2011). For long-lived species, fast, learned behavioral adaptations are crucial for survival when circumstances change too rapidly for genetic adaptation to suffice. Whilst transmission mechanisms of genetic adaptation are well understood, our understanding of how behavioural adaptations arise and spread is murky, and the role of individual heterogeneity in a group remains underexplored (Jolles et al., 2020).

Research has identified two main classes of behavioral responses to novel stimuli in animals. These are neophobia and exploration (Forss et al., 2017; Carter et al., 2012). Neophobia refers to the avoidance of novelty, which could expose individuals to risky situations such as entering unknown home ranges of predators or ingesting toxins. Neophobia is common in response to potential novel foods (Modlinska and Pisula, 2018). Exploration, on the other hand, involves behaviors that seek information about novel stimuli. Obtaining novel information directly from the environment requires overcoming neophobia and engaging in exploration, tendencies for which may vary between individuals (Jolles et al., 2020). If this information is used, it can facilitate innovation. (Kummer and Goodall, 1985) defined innovation as, ‘a solution to a novel problem, or a novel solution to an old one,’ and ‘a new ecological discovery such as a food item not previously part of the group.’ Behavioral innovations can, therefore, allow species with slow generational turnover to adapt their behavior quickly to changing circumstances, for example, to exploit a novel resource introduced into the current habitat (e.g. McLennan and Hockings, 2014). To innovate, however, it is necessary to go beyond obtaining information through exploration. Individuals must interact with the environment in novel ways, either using novel behaviors with known environmental features, or performing familiar behaviours on novel aspects of the environment, which additionally requires behavioural plasticity (Brosnan and Hopper, 2014). This plasticity can also be highly variable, both between individuals of a species, and within individuals across time (Modlinska and Pisula, 2018). Given the risks associated with novelty and innovation, it is likely only beneficial to innovate when necessary; and motivation based on the physiological states of individuals is likely important in variation in innovation within species (Brosnan and Hopper, 2014; Sol, 2015). Moreover, neophobia and motivation to innovate may vary over time according to an individual’s current needs, developmental status, and transient environmental conditions (Modlinska and Pisula, 2018; Sol, 2015). For example, innovation might be more likely in juveniles who may be less neophobic due to their need to learn about their environment before adulthood, or in dispersing individuals who need to find a new home territory. Accordingly, dispersing individuals may go through a transitory exploratory behavioral syndrome (Sih et al., 2012) at the time of dispersal making them more likely to innovate during that period. Greater behavioral flexibility (‘…adaptive change in the behavior of an animal, in response to changes in the external or internal environment…,’ including stopping or starting a behavior Brown and Tait, 2014) is an important requisite for innovation and is apparent in both juvenile (Kumpan et al., 2020) and dispersing male (Bono et al., 2018) vervet monkeys.

On the other hand, if innovative conspecifics or individuals that uniquely possess particular knowledge are present, individuals can save energy and avoid risks by learning socially from them. Indeed, many studies of diverse species in captivity have found that observing a conspecific eating a novel food reduces neophobic responses (Forss et al., 2017; Modlinska and Pisula, 2018). A study on wild jackdaws found the same (Greggor et al., 2016), and similarly, wild baboons with a ‘bold’ personality handled a novel food for longer after seeing a demonstrator do so (though ‘shy’ baboons did not) (Carter et al., 2014). Further investigation is required in the wild, since the risk for foraging animals to ingest toxins via unknown foods can be high, whilst this risk is diminished in captivity due to human feeding with edible food only. Indeed, captivity and increased exposure to human artifacts appear to increase exploration of novel objects in vervet monkeys (Forss et al., 2022), suggesting differences in risk-taking due to familiarity with human provisions. In addition, individual differences, such as age or sex, of the demonstrating conspecifics may be important (Kendal et al., 2018) and more work is needed on the topic. Moreover, in several species, dispersing individuals have been hypothesized to import information or behavioral innovations, upon immigration, into new groups (O’Malley et al., 2012; Biro et al., 2003; Barrett et al., 2017; Perry, 2003; Péter et al., 2022; McDougall et al., 2010; Gunst et al., 2007). For example, one study reports an immigrant vervet monkey providing spatial knowledge to his new group of a remaining water hole, during a drought, in a neighboring territory (McDougall et al., 2010). Detailed work in capuchins suggests the involvement of immigrants in both creating and spreading innovations in social and foraging domains (Barrett et al., 2017; Perry, 2003). Male Japanese macaques have been suspected to transfer stone handling patterns between troops (Gunst et al., 2007). While these studies show that dispersing individuals might facilitate the spread of information at the population level, experimental evidence focusing on multiple groups is sparse, resulting in a small pool of evidence.

Within wild groups, animals can use social information to guide foraging decisions. Many social learning studies in primates have focused on visual access to information (e.g. Bono et al., 2018; Carter et al., 2014; Barrett et al., 2017; Canteloup et al., 2021; van de Waal et al., 2010; Grampp et al., 2019, and see review in Whiten, 2019). However, for Cercopithecoid monkeys, detailed olfactory information, in a foraging context, may also be acquired through muzzle contact behavior – the act of one individual bringing their muzzle into very close proximity with another’s (Laidre, 2009; Drapier et al., 2002; Chauvin and Thierry, 2005; Nord et al., 2021). Indeed, previous studies found that, whilst foraging, muzzle contacts were most commonly initiated by infants and juveniles towards adults (Nord et al., 2021; Lycett and Henzi, 1992), which supports their function in information acquisition as young animals are still learning about their dietary repertoire, and adults are likely the most reliable sources of information. (Nord et al., 2021) also suggest that, due to the necessary close proximity, social tolerance may constrain information transmission in this modality, which can be affected by age, sex, and rank. In the presence of novel resources, muzzle contacts may be useful to adults as well as youngsters. Experimental research into this mode of information transmission in the presence of a novel resource is now required.

Vervet monkeys (Chlorocebus pygerythrus) are a species that thrive in natural, urban, and agricultural habitats, and are widely distributed throughout eastern sub-Saharan Africa (Turner et al., 2019). Their diverse habitats, including those highly modified by humans, make them an ideal species in which to investigate adaptation to novel environmental conditions. They live in multi-male multi-female troops, with philopatric females, and males dispersing multiple times during their lives. Frequently dispersing males may serve as vectors of information between groups. In addition, if dispersal triggers an increase in exploratory behavior, necessary to seek novelty in order to leave one group to join a new one, around the dispersal period they may also become more likely innovators in novel environments (Sol, 2015), potentially facilitating behavioral adaptation to diverse habitats across their geographical range (Turner et al., 2019). In a previous study by our team (Canteloup et al., 2021), in 2018, two groups (NH, KB) of wild vervet monkeys were provided with a novel food that required extraction (peanuts in shells, Figure 1A) before consumption. The aim of this initial study was to test whether vervet monkeys socially learned how to extract peanuts from their shells, and from whom they did learn. The results supported social transmission of the opening techniques used to extract peanuts, based on visual attention to demonstrators, and that vervet monkeys socially learned the technique that yielded the highest observed payoff and that was demonstrated by higher-ranked individuals (Canteloup et al., 2021). Here, we replicated the same experimental paradigm in 2019 and 2020 in three more groups (AK, BD, LT) after some males from the initially studied groups dispersed to other studied groups. The aim was to investigate whether dispersing males could trigger the uptake of an innovation in their new groups. Specifically, we took advantage of the natural dispersals of males from groups already accustomed to extracting and eating peanuts (Canteloup et al., 2021) into groups that never had. This endeavor afforded us the opportunity to also observe innovation, which subsequently inspired hypotheses about the potential role of dispersal in innovation, building upon the work of others (Brosnan and Hopper, 2014; Sol, 2015). Our observations of innovation are limited in number, but further testing of the hypotheses we propose as a result of our exploratory analysis that we present may aid our understanding of animal innovation.

Figure 1

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The present study addressed the following questions: First, (1a) Who innovated and how did it affect the extent to which the innovation was adopted by the group? We expected, when the innovators or initiators (in case of immigrant males importing the innovation) were adults rather than juveniles or infants, greater neophobia reduction and, therefore, faster and more widespread uptake of the novel food, in agreement with the three phases in the ontogeny of social learning in primates (Whiten and van de Waal, 2018). Next, to further our understanding of the uptake of innovations, we assessed (1b) whether socio-demographic characteristics (age, sex, rank) of group members predicted their adoption of the innovation at the first exposure, and across all four exposures after the first eating event. We expected adoption of the innovation to be more likely in younger monkeys due to previous findings that juveniles take more risks (Fairbanks, 1993), are less neophobic (Benson-Amram et al., 2013; Bergman and Kitchen, 2009; Miller et al., 2015; Sherratt and Morand-Ferron, 2018), and generally tend to learn faster (Kumpan et al., 2020) than adults.

Second, we experimentally investigated the function of muzzle contact behavior in novel food information acquisition. Specifically, we tested (2a) the effects of the amount of exposure to the food (and, therefore, familiarity with it) and the number of monkeys eating it on the rate of muzzle contacts. We expected that the rate of muzzle contacts would decrease as monkeys had more exposure to peanuts, if there were many monkeys eating. This would provide evidence for the function of muzzle contact in obtaining novel food information, by showing the dependence of muzzle contact rate on individuals developing their own knowledge of it through more group exposures and through eating the food. We also analyzed (2b) whether individuals’ knowledge of the food, and their age, sex, and rank predicted initiating and being targets of muzzle contacts. We expected an effect of knowledge, specifically for naïve monkeys to initiate more, and knowledgeable monkeys to be targeted more, with muzzle contact being a medium to obtain information about what conspecifics are eating. When referring to knowledge we are referring to the individuals’ own knowledge acquired in this specific case that peanuts are a food source. We do not invoke any more complex cognitive skills such as inference of the knowledge of others beyond what is observable of a conspecific eating the novel food. As in Nord et al., 2021, we also expected effects of age, with juveniles more likely initiators and adults more likely targets, as these are the theoretically predicted directions of social information transfer (Whiten and van de Waal, 2018), under the rationale that adults should have the most reliable information. Given the close proximity required to initiate muzzle contacts, we also expected low-ranked individuals to be less likely to initiate muzzle contacts, as they are tolerated by fewer group members (Nord et al., 2021).

We refer to the group AK differentially as AK₁₉ and AK₂₀, representing their status in 2019 and 2020, respectively, as 40% of the group composition changed between years due to dispersals, deaths, and changes in age categories (see Supplementary file 1a and detailed description in Materials and methods).

Across the experiment, a total of 81/164 vervet monkeys in all five groups, learned to successfully extract and eat peanuts during four exposures from each group’s first eating event (Table 1).

When presented with the novel food, multiple individuals (2–16 individuals) in all groups (except BD where the knowledgeable immigrant approached the box first and immediately started eating) approached the box, looked at the peanuts, and retreated without touching any (visual inspection; Table 2); and at least one group member (1–7 individuals) approached and handled, sniffed or nibbled the peanuts before rejecting them and retreating from the box (contact inspection; Table 2).

Who innovated and how did it affect the extent to which the innovation was adopted by the group?

When tested in 2018, in NH, a naïve immigrant male, Avo, was the third monkey to approach the box, and innovated extracting and eating peanuts during the group’s first exposure to the novel food. In KB a naïve infant male, Aar, was the 16^th monkey to approach the box (across all the exposures) and innovated at the group’s third exposure.

In 2019, in BD, a knowledgeable immigrant male, Pro (who emigrated from NH, Figure 1B), was the first to approach the box and started extracting and eating immediately at the first exposure. In LT, an immigrant male, Bab, was the 17^th monkey to approach the box and innovate during the group’s first exposure. In AK, no monkeys innovated in 2019 (AK₁₉), but in 2020 (AK₂₀), at the group’s second exposure (but the first with a knowledgeable immigrant), Yan (also emigrating from NH; Figure 1B), was the fourth to approach the box and the first to extract and eat peanuts (Supplementary file 1a).

During the first exposures to peanuts in BD, LT and NH, when new immigrant males initiated eating peanuts, we observed that the following percentages of these groups started to extract and eat peanuts during that exposure: BD: 31% (group n=65); LT: 20% (group n=25); NH: 9% (group n=35; Figure 2A). In the first exposures in AK₁₉ and KB, no monkeys started to extract and eat peanuts. After an immigrant male ate in AK₂₀, at the second exposure in that group, 30% (group n=20) of the group followed during that exposure (Figure 2A). When an infant innovated at the third exposure in KB, no other group members followed during that exposure (Figure 2A). The immigrant who innovated in NH left the group after the group’s first exposure, leaving just two juveniles who had also started eating at the first exposure. After four exposures from the first eating event in all groups, the percentages of each group extracting and eating peanuts were: 95% in AK₂₀; 66% in BD; 21% in KB; 84% in LT; and 20% in NH (Figure 2B).

Figure 2

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Muzzle contact rate across repeated exposure to novel food

We recorded a total of 498 muzzle contacts initiated by 64 different individuals in all four study groups during the first four exposures from the first eating event.

Regarding the rate of muzzle contacts across exposures, we found a significant interaction between the number of monkeys eating and exposure number (Model 3, Table 3). The main effects of exposure number and the number of monkeys eating were also significant but are not interpretable in this model due to the presence of the interaction. The significant interaction shows that the effect of exposure number depends on the number of monkeys eating (Figure 3). In Figure 3A and B, we can see that whilst muzzle contact rate decreased across the exposures, this decrease was less extreme when more monkeys were eating. This suggests that whilst muzzle contacts decreased as the food become, overall, more familiar in the group, it was still dependent on how many opportunities for muzzle contacts there were, i.e., the number of individuals eating, suggesting a potential social function of muzzle contacts. Conditional R²=0.91, meaning that model 3 explains a significant amount of variance (Table 4). Max. VIF = 4.36, for the variable no. monkeys eating (z-score), suggesting low collinearity and the dispersion test was not significant (p=0.57), meaning that data were not over or underdispersed.

Figure 3

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By exposing five groups of wild vervet monkeys to a novel extractive foraging problem, we created conditions under which to (1) observe innovation by individuals, and the uptake of transmission of knowledge within and between groups, and (2) assess the function and patterns of muzzle contact behavior in the context of encountering a novel food. We found evidence of immigrant males as fast innovators, and as potential vectors of information between groups. We observed faster uptake of the innovation in groups when new immigrant males, rather than infants or juveniles, ate first. We found effects of age and rank on uptake of the food, both during the first exposure, and over four exposures, with juveniles and high-rankers eating the novel food more readily than adults and low-rankers. Furthermore, as groups had more exposure to the food, if many monkeys had started to eat peanuts and olfactory contact with novel food increased, the rate of muzzle contacts decreased. Initiating muzzle contacts was influenced by prior knowledge of the food, age, and rank, and being targeted by muzzle contacts was influenced by knowledge and age. Below we discuss the contributions of these results to perspectives on the potential value of dispersing individuals in the innovation and transmission of behavioural adaptations to novel circumstances within populations.

All data and code used for analyses are freely available at: https://doi.org/10.5281/zenodo.7376673.

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Author details

1. Pooja Dongre

   1. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
   2. Inkawu Vervet Project, Mawana Game Reserve, KwaZulu Natal, South Africa

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-6957-3972

2. Gaëlle Lanté

   1. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
   2. University of Poitiers, Poitiers, France

   Contribution

   Data curation, Formal analysis

   Competing interests

   No competing interests declared

3. Mathieu Cantat

   Inkawu Vervet Project, Mawana Game Reserve, KwaZulu Natal, South Africa

   Contribution

   Data curation

   Competing interests

   No competing interests declared

4. Charlotte Canteloup

   1. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
   2. Inkawu Vervet Project, Mawana Game Reserve, KwaZulu Natal, South Africa
   3. Laboratory of Cognitive & Adaptive Neurosciences, CNRS - UMR 7364, University of Strasbourg, Strasbourg, France

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Writing – review and editing, Supervision, Writing – original draft

   Competing interests

   No competing interests declared

   Additional information

   Joint last authorships

   "This ORCID iD identifies the author of this article:" 0000-0001-5462-081X

5. Erica van de Waal

   1. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
   2. Inkawu Vervet Project, Mawana Game Reserve, KwaZulu Natal, South Africa

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Methodology, Writing – review and editing

   For correspondence

   erica.vandewaal@unil.ch

   Competing interests

   No competing interests declared

   Additional information

   Joint last authorships

   "This ORCID iD identifies the author of this article:" 0000-0001-7778-418X

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