There is extensive evidence that the spread of innovation via social learning can facilitate uptake of new foraging behaviours in populations. In comparison, social learning about novel food types has received comparatively little attention. Yet the adoption of novel food is vital to persistence in, or colonisation of, novel environments. Here, we present a novel food (almonds in the shell, coloured either blue or red) in a two-option and control cultural diffusion experiment to five neighbouring roosts of 705 individually-marked sulphur-crested cockatoos (Cacatua galerita) living in a highly urbanised environment. From 4 initially trained individuals, a total of 349 individuals across all roosts learned to feed on the novel food within 10 days of first exposure. Using network-based diffusion-analysis (N = 214 learners out of 322 individuals with available social information), we demonstrated that this spread occurred almost exclusively through social learning, with information spreading through social network ties. Second, using experience-weighted attraction models, we described age-differences in social learning strategies, with juveniles, but not adults, exhibiting a conformist bias to prefer the most frequently chosen food colour. Third, when analysing 539 opening techniques of the novel food by 147 individuals across the five roosts, we found that opening techniques were more similar between roost communities when the distance between sites was small, or the degree of movement between sites was high. In addition, when focusing on a subset for which social association data were available (273 openings by 78 individuals), techniques tended to be more similar between close associates. Taken together, our study suggests that the adoption of novel food in urban-living sulphur-crested cockatoos is facilitated by social transmission of knowledge through networks, with food choice further influenced in juveniles by a conformist learning bias. Social networks influenced both food choice and acquisition of foraging techniques within and between roosting communities, leading to differences at surprisingly local scales. The utilisation of new food resources is a fundamental component of adaptive behavioural responses to novel environments. Our study demonstrates how cognitive and social influences can be vital determinants of this adaptive flexibility.

Given rapid urbanization across the globe, coping with humans is an important aspect of life in the modern world for most animals. Although human presence is often accompanied by human-associated predators such as dogs, the effects of humans and dogs on animal physiology are rarely considered together. Here, we leverage over 4500 measures of fecal glucocorticoid metabolite (FGM) measurements, a biomarker of stress physiology, collected from more than 1200 marked California ground squirrels (Otospermophilus beecheyi) at two sites differing in human activity. Drawing on 12 years of study, we explored the effects of dispersal status, human presence, and dog activity on FGMs in juveniles and adults to uncover the multiple factors contributing to individual and population-level differences in FGMs. Longitudinal data on between-site dispersal revealed site-level effects on FGMs. FGMs decreased after individuals dispersed to the less disturbed site, but generally increased after dispersers moved to the more disturbed site. Detailed cross-sectional data from the more disturbed site further revealed age- and mass-dependent responses to human and dog activity. Whereas dog activity failed to predict juvenile FGMs, juvenile FGMs were highest for individuals trapped in areas with high human activity. In contrast, dogs represented a major stressor for adult animals, but the effects of dogs on adult FGMs were generally shielded by human presence. Together, these findings uncover the complex relationships among anthropogenic factors, stress physiology, and habitat selection over multiple spatial and temporal scales in wild animals living in a human-influenced world.

Abstract Human-influenced environments pose challenges but also provide wildlife with anthropogenic resources. Individuals vary widely in their ability to exploit such resources, often as a function of behavioural type. However, we lack a clear understanding of how variation in behavioural traits influences stages of resource exploitation required to use anthropogenic resources. Using fully automated foraging puzzles, we examined how boldness and sociability influenced three aspects of resource exploitation – discovery, problem-solving, and overall performance – in two wild populations of California ground squirrels ( Otospermophilus beecheyi ). Bolder individuals discovered the resource earlier, solved the task faster and achieved higher performance, indicating that boldness promotes efficient exploitation of anthropogenic resources across multiple stages in the process. Greater sociability and more opportunities to observe conspecifics solving the task led to faster problem-solving, consistent with evidence for observational learning. Squirrels in the recreational-use population – with regular exposure to humans and anthropogenic food – were faster to discover the resource than those in a trail-use population – where human exposure was transient and no anthropogenic food available. Problem-solving latency and performance were consistent between populations. Our findings highlight how individual variation in behavioural traits drives performance in novel ecological contexts, providing a mechanistic understanding of behavioural plasticity in human-influenced environments.

In many animal species, the juvenile period is under strong selection, leading to a concentration of social learning during this stage as an efficient strategy for young individuals to acquire skills essential for survival. However, as social learning is not always adaptive, juveniles need to be strategic in when, who, and what to copy. In species with extended parental care, parents are often preferred sources of information, leading to stable intergenerational transmission of knowledge. However, little is known about transmission pathways in species with limited periods of parental care, and their implication for cultural inheritance. Here, we investigate social learning strategies during development in a model species with a dependence period of a few weeks, the great tit (Parus major). Using fully automated two-option foraging puzzles, we diffused knowledge about the puzzle through breeding populations and then constrained parental individuals' choices such that parents either (1) both had knowledge of the same option, (2) had conflicting knowledge of the two options, or (3) had no knowledge of how to solve the puzzle. We then tracked solving behavior of 229 newly fledged juveniles over 10 weeks. Parental solving frequency during dependence strongly predicted knowledge acquisition by offspring, suggesting intergenerational cultural inheritance. However, detailed investigation of learning pathways revealed siblings as the most important role models for social learning, followed by nonparental adults and parents. Furthermore, offsprings' option choices were not predicted by parental choices, but instead influenced by the broader social environment, with evidence for a conformist learning bias. Overall, by using large-scale experimental manipulation of parental behavior, our study offers new insights into social learning pathways and mechanisms of cultural inheritance in r-selected species with limited parental care and multiple offspring. Our findings provide a stark contrast to most previously studied systems exhibiting multigenerational cultures, where cultural transmission overwhelmingly occurs from parents to offspring, and give insights into the more variable transmission routes that might occur across socially learning species.

Dietary flexibility allows animals to respond adaptively to food pulses in the environment. Here we document the novel emergence of widespread hunting of California voles and carnivorous feeding behavior by California ground squirrels. Over two months in the twelfth year of a long-term study on the squirrel population, we document 74 events of juvenile and adult ground squirrels of both sexes depredating, consuming, and/or competing over vole prey. Our video footage, photographic evidence, and direct observations of marked individual squirrels provide insights into the ecological circumstances favoring behavioral flexibility in foraging associated with a decadal peak in vole abundance. Digital video images related to the article are available at http://www.momo-p.com/showdetail-e.php?movieid=momo241126ob01a

Sociality impacts many biological processes and can be tightly linked to an individual's fitness. To maximize the advantages of group living, many social animals prefer to associate with individuals that provide the most benefits, such as kin, familiar individuals, or those of similar phenotypes. Such social strategies are not necessarily stable over time but can vary with changing selection pressures. In particular, young individuals transitioning to independence should continuously adjust their social behavior in light of developmental changes. However, social strategies exhibited during adolescence in animals are understudied, and the factors underlying social network formation during ontogeny remain elusive. Here, we tracked associations of wild great tits (Parus major) during the transition to independence and across their first year of life. Both spatial and social factors predicted dyadic associations. During the transition to independence in spring, fledglings initially preferred to associate with siblings and peers over non-parent adults. We found no evidence for preferred associations among juveniles of similar age or fledge weight during that time but weak evidence for some potential inheritance of the parental social network. By autumn, after juveniles had reached full independence, they exhibited social strategies similar to those of adults by establishing stable social ties based on familiarity that persisted through winter into the next spring. Overall, this research demonstrates dynamic changes in social networks during ontogeny in a species with a fast life history and limited parental care, which likely reflect changes in selective pressures. It further highlights the importance of long-term social bonds based on familiarity in this species. Social networks of juvenile birds change dramatically during the transition to independence. While they initially prefer to associate with other juveniles, by autumn, their social strategies resemble those of adults. Like adults, first-year birds establish long-term social bonds with familiar individuals that persist over time, which highlights the importance of stable social bonds with others.

Abstract This chapter considers ‘social learning’, broadly defined as learning that is facilitated by observation of, or interaction with, another individual (or its products). Of most interest is social learning that results in ‘social transmission’: the observer adopting behaviour patterns matching those of the demonstrator. It looks at a number of different social learning processes, from simple processes like local enhancement to cognitively complex processes like imitation. Social learning is not always adaptive. Individuals need to employ strategies on when, who, and what is beneficial to copy rather than relying on personal information. A variety of experimental set-ups—ranging from simple diffusion to cross-fostering or translocation studies—in combination with statistical methods such as matrix regressions, network-based diffusion analysis or experience-weighted attraction models provide powerful tools to detect and measure the importance of social learning across species and contexts and identify typical pathways of transmission.

Advances in biologging technologies have significantly improved our ability to track individual animals' behaviour in their natural environment. Beyond observations, automation of data collection has revolutionized cognitive experiments in the wild. For example, radio-frequency identification (RFID) antennae embedded in 'puzzle box' devices have allowed for large-scale cognitive experiments where individuals tagged with passive integrated transponder (PIT) tags interact with puzzle boxes to gain a food reward, with devices logging both the identity and solving action of visitors. Here, we extended the scope of wild cognitive experiments by developing a fully automated selective two-option foraging device to specifically control which actions lead to a food reward and which remain unrewarded. Selective devices were based on a sliding-door foraging puzzle, and built using commercially available low-cost electronics. We tested it on two free-ranging PIT-tagged subpopulations of great tits Parus major as a proof of concept. We conducted a diffusion experiment where birds learned from trained demonstrators to get a food reward by sliding the door either to the left or right. We then restricted access of knowledgeable birds to their less preferred side and calculated the latency until birds produced solutions as a measure of behavioural flexibility. A total of 22 of 23 knowledgeable birds produced at least one solution on their less preferred side after being restricted, with higher-frequency solvers being faster at doing so. In addition, 18 of the 23 birds reached their solving rate from prior to the restriction on their less preferred side, with birds with stronger prior side preference taking longer to do so. We therefore introduce and successfully test a new selective two-option puzzle box, providing detailed instructions and freely available software that allows reproducibility. It extends the functionality of existing systems by allowing fine-scale manipulations of individuals' actions and opens a large range of possibilities to study cognitive processes in wild animal populations.

As an important determinant of reproductive success, avian nest building is under strong selection and requires behavioral plasticity to optimize conditions in which offspring develop. Learning is a one form of plasticity that allows adaptation to the local environment. Birds may refine nest-building behavior with personal experience or use social information to guide their choices. While there is mounting evidence for an effect of experience-based learning on nest building and social information use when selecting nesting material in the laboratory, experimental evidence for social information use in wild birds is lacking. Here, we provided sources of two differently colored wool as nest lining material in a wild mixed-species community of tits (Paridae sp.) to investigate experimentally (i) whether females use social information to locate lining materials and (ii) whether preferences for specific materials (here color) are socially influenced. We investigated pathways of social transmission through a foraging association and a spatial breeding network using the time of arrival at the wool in a network-based diffusion analysis. Our results gave evidence that birds learned about the location of lining resources from foraging associates. Furthermore, we found significant non-random clustering of wool colors in nest boxes across the study area, suggestive of a social influence on selecting lining materials. Taken together, we provide quantitative evidence for a role of social information use in both finding and selecting lining material in wild tits and demonstrate that social information use constitutes an important factor towards behavioral plasticity in nest building in wild birds.Significance statementAs vessels of reproduction, avian nests are under strong selection to provide optimized conditions for developing offspring. Learning is one mechanism that allows individuals to adapt to local environmental conditions. Previous work has shown that nest-building birds use both social information and personal experience to refine their nests. Yet, evidence for social information use for nest construction in the wild has been purely anecdotal and experimental evidence lacking. Here, we demonstrate for the first time experimentally that in wild tits (Paridae sp.), females rely on social information from their foraging associates to locate and choose material to line their nests. This research highlights the importance of social information use as a potential mechanism of behavioral plasticity in wild nest-building birds.

Social structuring from assortative associations may affect individual fitness, as well as population-level processes. Gaining a broader understanding of social structure can improve our knowledge of social evolution and inform wildlife conservation. We investigated association patterns and community structure of female Indo-Pacific bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia, assessing the role of kinship, shared culturally transmitted foraging techniques, and habitat similarity based on water depth. Our results indicated that associations are influenced by a combination of uni- and biparental relatedness, cultural behaviour and habitat similarity, as these were positively correlated with a measure of dyadic association. These findings were matched in a community level analysis. Members of the same communities overwhelmingly shared the same habitat and foraging techniques, demonstrating a strong homophilic tendency. Both uni- and biparental relatedness between dyads were higher within than between communities. Our results illustrate that intraspecific variation in sociality in bottlenose dolphins is influenced by a complex combination of genetic, cultural, and environmental aspects.

Recent well-documented cases of cultural evolution towards increasing efficiency in non-human animals have led some authors to propose that other animals are also capable of cumulative cultural evolution, where traits become more refined and/or complex over time. Yet few comparative examples exist of traits increasing in complexity, and experimental tests remain scarce. In a previous study, we introduced a foraging innovation into replicate subpopulations of great tits, the 'sliding-door puzzle'. Here, we track diffusion of a second 'dial puzzle', before introducing a two-step puzzle that combines both actions. We mapped social networks across two generations to ask if individuals could: (1) recombine socially-learned traits and (2) socially transmit a two-step trait. Our results show birds could recombine skills into more complex foraging behaviours, and naïve birds across both generations could learn the two-step trait. However, closer interrogation revealed that acquisition was not achieved entirely through social learning-rather, birds socially learned components before reconstructing full solutions asocially. As a consequence, singular cultural traditions failed to emerge, although subpopulations of birds shared preferences for a subset of behavioural variants. Our results show that while tits can socially learn complex foraging behaviours, these may need to be scaffolded by rewarding each component. This article is part of a discussion meeting issue 'The emergence of collective knowledge and cumulative culture in animals, humans and machines'.

The emergence, spread, and establishment of innovations within cultures can promote adaptive responses to anthropogenic change. We describe a putative case of the development of a cultural adaptation to urban environments: opening of household waste bins by wild sulphur-crested cockatoos. A spatial network analysis of community science reports revealed the geographic spread of bin opening from three suburbs to 44 in Sydney, Australia, by means of social learning. Analysis of 160 direct observations revealed individual styles and site-specific differences. We describe a full pathway from the spread of innovation to emergence of geographic variation, evidencing foraging cultures in parrots and indicating the existence of cultural complexity in parrots. Bin opening is directly linked to human-provided opportunities, highlighting the potential for culture to facilitate behavioral responses to anthropogenic change.

Investigations into cooperative partner choice should consider both potential and realised partners, allowing for the comparison of traits across all those available. Male bottlenose dolphins form persisting multi-level alliances. Second-order alliances of 4–14 males are the core social unit, within which 2–3 males form first-order alliances to sequester females during consortships. We compared social bond strength, relatedness and age similarity of potential and realised partners of individual males in two age periods: (i) adolescence, when second-order alliances are formed from all available associates, and (ii) adulthood, when first-order allies are selected from within second-order alliances. Social bond strength during adolescence predicted second-order alliance membership in adulthood. Moreover, males preferred same-aged or older males as second-order allies. Within second-order alliances, non-mating season social bond strength predicted first-order partner preferences during mating season consortships. Relatedness did not influence partner choice on either alliance level. There is thus a striking resemblance between male dolphins, chimpanzees and humans, where closely bonded non-relatives engage in higher-level, polyadic cooperative acts. To that end, our study extends the scope of taxa in which social bonds rather than kinship explain cooperation, providing the first evidence that such traits might have evolved independently in marine and terrestrial realms.

Cultural behavior, which is transmitted among conspecifics through social learning [1], is found across various taxa [2-6]. 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. VIDEO ABSTRACT.

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.

Network-based diffusion analysis (NBDA) has become a widely used tool to detect and quantify social learning in animal populations. NBDA infers social learning if the spread of a novel behavior follows the social network and hence relies on appropriate information on individuals' network connections. Most studies on animal populations, however, lack a complete record of all associations, which creates uncertainty in the social network. To reduce this uncertainty, researchers often use a certain threshold of sightings for the inclusion of animals (which is often arbitrarily chosen), as observational error decreases with increasing numbers of observations. Dropping individuals with only few sightings, however, can lead to information loss in the network if connecting individuals are removed. Hence, there is a trade-off between including as many individuals as possible and having reliable data. We here provide a tool in R that assesses the sensitivity of NBDA to error in the social network given a certain threshold for the inclusionof individuals. It simulates a social learning process through a population and then tests the power of NBDA to reliably detect social learning after introducing observational error into the social network, which is repeated for different thresholds. Our tool can help researchers using NBDA to select a threshold, specific to their data set, that maximizes power to reliably quantify social learning in their study population.

Homophilous behaviour plays a central role in the formation of human friendships. Individuals form social ties with others that show similar phenotypic traits, independently of relatedness. Evidence of such homophily can be found in bottlenose dolphins ( Tursiops aduncus) in Shark Bay, Western Australia, where females that use marine sponges as foraging tools often associate with other females that use sponges. 'Sponging' is a socially learned, time-consuming behaviour, transmitted from mother to calf. Previous research illustrated a strong female bias in adopting this technique. The lower propensity for males to engage in sponging may be due to its incompatibility with adult male-specific behaviours, particularly the formation of multi-level alliances. However, the link between sponging and male behaviour has never been formally tested. Here, we show that male spongers associated significantly more often with other male spongers irrespective of their level of relatedness. Male spongers spent significantly more time foraging, and less time resting and travelling, than did male non-spongers. Interestingly, we found no difference in time spent socializing. Our study provides novel insights into the relationship between tool use and activity budgets of male dolphins, and indicates social homophily in the second-order alliance composition of tool-using bottlenose dolphins.

Male alliances are an intriguing phenomenon in the context of reproduction since, in most taxa, males compete over an indivisible resource, female fertilization. Adult male bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia, form long-term, multilevel alliances to sequester estrus females. These alliances are therefore critical to male reproductive success. Yet, the long-term processes leading to the formation of such complex social bonds are still poorly understood. To identify the criteria by which male dolphins form social bonds with other males, we adopted a long-term approach by investigating the ontogeny of alliance formation. We followed the individual careers of 59 males for 14 years while they transitioned from adolescence (8-14 years of age) to adulthood (15-21 years old). Analyzing their genetic relationships and social associations in both age groups, we found that the vast majority of social bonds present in adolescence persisted through time. Male associations in early life predict alliance partners as adults. Kinship patterns explained associations during adolescence but not during adulthood. Instead, adult males associated with males of similar age. Our findings suggest that social bonds among peers, rather than kinship, play a central role in the development of adult male polyadic cooperation in dolphins.

One of many challenges in the conservation of biodiversity is the recent trend in the frequency and intensity of extreme climatic events [1]. The Shark Bay World Heritage Area, Western Australia, endured an unprecedented marine heatwave in 2011. Catastrophic losses of habitat-forming seagrass meadows followed [2], along with mass mortalities of invertebrate and fish communities [3]. Our long-term demographic data on Shark Bay’s resident Indo-Pacific bottlenose dolphin (Tursiops aduncus) population revealed a significant decline in female reproductive rates following the heatwave. Moreover, capture–recapture analyses indicated 5.9% and 12.2% post-heatwave declines in the survival of dolphins that use tools to forage and those that do not, respectively. This implies that the tool-using dolphins may have been somewhat buffered against the cascading effects of habitat loss following the heatwave by having access to a less severely affected foraging niche [4]. Overall, however, lower survival has persisted post-heatwave, suggesting that habitat loss following extreme weather events may have prolonged, negative impacts on even behaviourally flexible, higher-trophic level predators.