The role of food transfers in wild golden lion tamarins (Leontopithecus rosalia) : support for the informational and nutritional hypothesis

Funding; The research was supported in part by a grant from the John Templeton Foundation (40128) and the European Research Council (232823), to KN Laland, and is in compliance with ASAB and ICMBio guidelines.Callitrichidae is a unique primate family not only in terms of the large number of food transfers to infants but also for the prevalence of transfers that are initiated by the adults. It has been hypothesized that, as well as provisioning infants, callitrichid food transfers might function to teach the receiver what food types to eat. If food provisioning has a teaching function, we would expect successful food transfers to be more likely with food types that are novel to the juveniles. We would also expect juveniles to learn about foods from those transfers. We introduced different types of food (some familiar, some novel) to wild groups of golden lion tamarins (Leontopithecus rosalia). While novel foods were not more successfully transferred than familiar food in the experiment, transfers were more successful (i.e., the receiver obtained food) when the donor had previous experience with that food. Moreover, we found evidence suggesting that food transfers influenced the future foraging choices of juveniles. Our findings are consistent with the first and third criteria of the functional definition of teaching, which requires that tutors (the adults) modify their behavior in the presence of a naïve individual (a juvenile), and that the naïve individual learns from the modified behavior of the demonstrator. Our findings are also consistent with the provisioning function of food transfer. Social learning seems to play an important role in the development of young tamarins’ foraging preferences.Publisher PDFPeer reviewe

The effect of auditory enrichment, rearing method and social environment on the behavior of zoo-housed psittacines (Aves: Psittaciformes); implications for welfare

The psychological and physiological effects of different genres of music are well documented in humans. These concepts have also been studied in kenneled dogs and some exotic animals, implying that animals may experience benefits similar to those of humans. This study tested the hypothesis that auditory enrichment changed the behavior of ten zoo-housed psittacines. All animals were exposed to six conditions of auditory stimulation; a ‘control’ (no auditory stimulation), and ‘experimental’ conditions, during which animals were presented with commercially-available CDs of classical music, pop music, natural rainforest sounds, parrot sounds and a talking radio. Each type of stimulation lasted two days, with a wash-out day between different stimulation conditions. We recorded key parameters relating to the birds’ social environment – whether they were group or single-housed and whether they had been hand or parent-reared. The parrots’ behaviour was recorded every minute for a 25 min period seven times a day using instantaneous sampling. The incidence of calm vocalisations and the level of preening changed with the different conditions. Birds exposed to rainforest and talking radio preened more than control birds. Birds exposed to several genres of auditory stimulation expressed fewer calm vocalisations than control birds. A further finding from this study was that hand-reared birds exhibited dramatically increased incidences of stereotypic behavior, more learned vocalisation and interacted less with enrichment than parent-reared and the implications of hand rearing for welfare are discussed. Similarly solo housed birds showed changes in behavior compared to group housed, such as less preening and more stereotypic behaviour. Hand reared, solo housed parrots express less normal behavior and maybe at risk of impaired welfare

Multi-network-based diffusion analysis reveals vertical cultural transmission of sponge tool use within dolphin matrilines

Behavioural differences among social groups can arise from differing ecological conditions, genetic predispositions and/or social learning. In the past, social learning has typically been inferred as responsible for the spread of behaviour by the exclusion of ecological and genetic factors. This ‘method of exclusion’ was used to infer that ‘sponging’, a foraging behaviour involving tool use in the bottlenose dolphin (Tursiops aduncus) population in Shark Bay, Western Australia, was socially transmitted. However, previous studies were limited in that they never fully accounted for alternative factors, and that social learning, ecology and genetics are not mutually exclusive in causing behavioural variation. Here, we quantified the importance of social learning on the diffusion of sponging, for the first time explicitly accounting for ecological and genetic factors, using a multi-network version of ‘network-based diffusion analysis'. Our results provide compelling support for previous findings that sponging is vertically socially transmitted from mother to (primarily female) offspring. This research illustrates the utility of social network analysis in elucidating the explanatory mechanisms behind the transmission of behaviour in wild animal populations

Social network analysis shows direct evidence for social transmission of tool use in wild chimpanzees

The authors are grateful to the Royal Zoological Society of Scotland for providing core funding for the Budongo Conservation Field Station. The fieldwork of CH was funded by the Leverhulme Trust, the Lucie Burgers Stichting, and the British Academy. TP was funded by the Canadian Research Chair in Continental Ecosystem Ecology, and received computational support from the Theoretical Ecosystem Ecology group at UQAR. The research leading to these results has received funding from the People Programme (Marie Curie Actions) and from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007–2013) REA grant agreement n°329197 awarded to TG, ERC grant agreement n° 283871 awarded to KZ. WH was funded by a BBSRC grant (BB/I007997/1).Social network analysis methods have made it possible to test whether novel behaviors in animals spread through individual or social learning. To date, however, social network analysis of wild populations has been limited to static models that cannot precisely reflect the dynamics of learning, for instance, the impact of multiple observations across time. Here, we present a novel dynamic version of network analysis that is capable of capturing temporal aspects of acquisition-that is, how successive observations by an individual influence its acquisition of the novel behavior. We apply this model to studying the spread of two novel tool-use variants, "moss-sponging'' and "leaf-sponge re-use,'' in the Sonso chimpanzee community of Budongo Forest, Uganda. Chimpanzees are widely considered the most "cultural'' of all animal species, with 39 behaviors suspected as socially acquired, most of them in the domain of tool-use. The cultural hypothesis is supported by experimental data from captive chimpanzees and a range of observational data. However, for wild groups, there is still no direct experimental evidence for social learning, nor has there been any direct observation of social diffusion of behavioral innovations. Here, we tested both a static and a dynamic network model and found strong evidence that diffusion patterns of moss-sponging, but not leaf-sponge re-use, were significantly better explained by social than individual learning. The most conservative estimate of social transmission accounted for 85% of observed events, with an estimated 15-fold increase in learning rate for each time a novice observed an informed individual moss-sponging. We conclude that group-specific behavioral variants in wild chimpanzees can be socially learned, adding to the evidence that this prerequisite for culture originated in a common ancestor of great apes and humans, long before the advent of modern humans.Publisher PDFPeer reviewe

Integrating Genetic, Environmental, and Social Networks to Reveal Transmission Pathways of a Dolphin Foraging Innovation

Cultural behavior, which is transmitted among conspecifics through social learning [ 1 ], is found across various taxa [ 2 , 3 , 4 , 5 , 6 ]. Vertical social transmission from parent to offspring [ 7 ] is thought to be adaptive because of the parental generation being more skilled than maturing individuals. It is found throughout the animal kingdom, particularly in species with prolonged parental care, e.g., [ 8 , 9 ]. Social learning can also occur among members of the same generation [ 4 , 10 , 11 ] or between older, non-parental individuals and younger generations [ 7 ] via horizontal or oblique transmission, respectively. Extensive work on primate culture has shown that horizontal transmission of foraging behavior is biased toward species with broad cultural repertoires [ 12 ] and those with increased levels of social tolerance [ 13 , 14 ], such as great apes. Vertical social transmission has been established as the primary transmission mechanism of foraging behaviors in the Indo-Pacific bottlenose dolphin ( Tursiops aduncus) population of Shark Bay, Western Australia [ 6 , 9 , 15 , 16 ]. Here, we investigated the spread of another foraging strategy, “shelling” [ 17 ], whereby some dolphins in this population feed on prey trapped inside large marine gastropod shells. Using a multi-network version of “network-based diffusion analysis” (NBDA), we show that shelling behavior spreads primarily through non-vertical social transmission. By statistically accounting for both environmental and genetic influences, our findings thus represent the first evidence of non-vertical transmission of a foraging tactic in toothed whales. This research suggests there are multiple transmission pathways of foraging behaviors in dolphins, highlighting the similarities between cetaceans and great apes in the nature of the transmission of cultural behaviors

Diffusion dynamics of socially learned foraging techniques in squirrel monkeys

Social network analyses [1-5] and experimental studies of social learning [6-10] have each become important domains of animal behavior research in recent years yet have remained largely separate. Here we bring them together, providing the first demonstration of how social networks may shape the diffusion of socially learned foraging techniques [11]. One technique for opening an artificial fruit was seeded in the dominant male of a group of squirrel monkeys and an alternative technique in the dominant male of a second group. We show that the two techniques spread preferentially in the groups in which they were initially seeded and that this process was influenced by monkeys' association patterns. Eigenvector centrality predicted both the speed with which an individual would first succeed in opening the artificial fruit and the probability that they would acquire the cultural variant seeded in their group. These findings demonstrate a positive role of social networks in determining how a new foraging technique diffuses through a population

Data from: Environmental complexity influences association network structure and network-based diffusion of foraging information in fish shoals

Socially transmitted information can significantly affect the ways in which animals interact with their environments. We used network-based diffusion analysis, a novel and powerful tool for exploring information transmission, to model the rate at which sticklebacks (Gasterosteus aculeatus) discovered prey patches, comparing shoals foraging in open and structured environments. We found that for groups in the open environment, individuals tended to recruit to both the prey patch and empty comparison patches at similar times, suggesting that patch discovery was not greatly affected by direct social transmission. In contrast, in structured environments we found strong evidence that information about prey patch location was socially transmitted and moreover that the pathway of information transmission followed the shoals’ association network structures. Our findings highlight the importance of considering habitat structure when investigating the diffusion of information through populations and imply that association networks take on greater ecological significance in structured than open environments

Data from: Environmental complexity influences association network structure and network-based diffusion of foraging information in fish shoals

Socially transmitted information can significantly affect the ways in which animals interact with their environments. We used network-based diffusion analysis, a novel and powerful tool for exploring information transmission, to model the rate at which sticklebacks (Gasterosteus aculeatus) discovered prey patches, comparing shoals foraging in open and structured environments. We found that for groups in the open environment, individuals tended to recruit to both the prey patch and empty comparison patches at similar times, suggesting that patch discovery was not greatly affected by direct social transmission. In contrast, in structured environments we found strong evidence that information about prey patch location was socially transmitted and moreover that the pathway of information transmission followed the shoals’ association network structures. Our findings highlight the importance of considering habitat structure when investigating the diffusion of information through populations and imply that association networks take on greater ecological significance in structured than open environments