Understanding the Role of Naive Learners in Cultural Change.

AbstractA change to a population's social network is a change to the substrate of cultural transmission, affecting behavioral diversity and adaptive cultural evolution. While features of network structure such as population size and density have been well studied, less is understood about the influence of social processes such as population turnover-or the repeated replacement of individuals by naive individuals. Experimental data have led to the hypothesis that naive learners can drive cultural evolution by better assessing the relative value of behaviors, although this hypothesis has been expressed only verbally. We conducted a formal exploration of this hypothesis using a generative model that concurrently simulated its two key ingredients: social transmission and reinforcement learning. We simulated competition between high- and low-reward behaviors while varying turnover magnitude and tempo. Variation in turnover influenced changes in the distributions of cultural behaviors, irrespective of initial knowledge-state conditions. We found optimal turnover regimes that amplified the production of higher reward behaviors through two key mechanisms: repertoire composition and enhanced valuation by agents that knew both behaviors. These effects depended on network and learning parameters. Our model provides formal theoretical support for, and predictions about, the hypothesis that naive learners can shape cultural change through their enhanced sampling ability. By moving from experimental data to theory, we illuminate an underdiscussed generative process that can lead to changes in cultural behavior, arising from an interaction between social dynamics and learning.

callsync: An R package for alignment and analysis of multi-microphone animal recordings.

To better understand how vocalisations are used during interactions of multiple individuals, studies are increasingly deploying on-board devices with a microphone on each animal. The resulting recordings are extremely challenging to analyse, since microphone clocks drift non-linearly and record the vocalisations of non-focal individuals as well as noise. Here we address this issue with callsync, an R package designed to align recordings, detect and assign vocalisations to the caller, trace the fundamental frequency, filter out noise and perform basic analysis on the resulting clips. We present a case study where the pipeline is used on a dataset of six captive cockatiels (Nymphicus hollandicus) wearing backpack microphones. Recordings initially had a drift of ~2 min, but were aligned to within ~2 s with our package. Using callsync, we detected and assigned 2101 calls across three multi-hour recording sessions. Two had loud beep markers in the background designed to help the manual alignment process. One contained no obvious markers, in order to demonstrate that markers were not necessary to obtain optimal alignment. We then used a function that traces the fundamental frequency and applied spectrographic cross correlation to show a possible analytical pipeline where vocal similarity is visually assessed. The callsync package can be used to go from raw recordings to a clean dataset of features. The package is designed to be modular and allows users to replace functions as they wish. We also discuss the challenges that might be faced in each step and how the available literature can provide alternatives for each step.

Social demonstration of colour preference improves the learning of associated demonstrated actions.

We studied how different types of social demonstration improve house sparrows' (Passer domesticus) success in solving a foraging task that requires both operant learning (opening covers) and discrimination learning (preferring covers of the rewarding colour). We provided learners with either paired demonstration (of both cover opening and colour preference), action-only demonstration (of opening white covers only), or no demonstration (a companion bird eating without covers). We found that sparrows failed to learn the two tasks with no demonstration, and learned them best with a paired demonstration. Interestingly, the action of cover opening was learned faster with paired rather than action-only demonstration despite being equally demonstrated in both. We also found that only with paired demonstration, the speed of operant (action) learning was related to the demonstrator's level of activity. Colour preference (i.e. discrimination learning) was eventually acquired by all sparrows that learned to open covers, even without social demonstration of colour preference. Thus, adding a demonstration of colour preference was actually more important for operant learning, possibly as a result of increasing the similarity between the demonstrated and the learned tasks, thereby increasing the learner's attention to the actions of the demonstrator. Giving more attention to individuals in similar settings may be an adaptive strategy directing social learners to focus on ecologically relevant behaviours and on tasks that are likely to be learned successfully.

The ontogeny of social networks in wild great tits (Parus major).

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.

Multilevel Bayesian analysis of monk parakeet contact calls shows dialects between European cities.

Geographic differences in vocalizations provide strong evidence for animal culture, with patterns likely arising from generations of social learning and transmission. Most studies on the evolution of avian vocal variation have predominantly focused on fixed repertoire, territorial song in passerine birds. The study of vocal communication in open-ended learners and in contexts where vocalizations serve other functions is therefore necessary for a more comprehensive understanding of vocal dialect evolution. Parrots are open-ended vocal production learners that use vocalizations for social contact and coordination. Geographic variation in parrot vocalizations typically take the form of either distinct regional variations known as dialects or graded variation based on geographic distance known as clinal variation. In this study, we recorded monk parakeets (Myiopsitta monachus) across multiple spatial scales (i.e., parks and cities) in their European invasive range. We then compared calls using a multilevel Bayesian model and sensitivity analysis, with this novel approach allowing us to explicitly compare vocalizations at multiple spatial scales. We found support for founder effects and/or cultural drift at the city level, consistent with passive cultural processes leading to large-scale dialect differences. We did not find a strong signal for dialect or clinal differences between parks within cities, suggesting that birds did not actively converge on a group level signal, as expected under the group membership hypothesis. We demonstrate the robustness of our findings and offer an explanation that unifies the results of prior monk parakeet vocalization studies.

Evidence for vocal signatures and voice-prints in a wild parrot.

In humans, identity is partly encoded in a voice-print that is carried across multiple vocalizations. Other species also signal vocal identity in calls, such as shown in the contact call of parrots. However, it remains unclear to what extent other call types in parrots are individually distinct, and whether there is an analogous voice-print across calls. Here we test if an individual signature is present in other call types, how stable this signature is, and if parrots exhibit voice-prints across call types. We recorded 5599 vocalizations from 229 individually marked monk parakeets (Myiopsitta monachus) over a 2-year period in Barcelona, Spain. We examined five distinct call types, finding evidence for an individual signature in three. We further show that in the contact call, while birds are individually distinct, the calls are more variable than previously assumed, changing over short time scales (seconds to minutes). Finally, we provide evidence for voice-prints across multiple call types, with a discriminant function being able to predict caller identity across call types. This suggests that monk parakeets may be able to use vocal cues to recognize conspecifics, even across vocalization types and without necessarily needing active vocal signatures of identity.

Group-level differences in social network structure remain repeatable after accounting for environmental drivers.

Individuals show consistent between-individual behavioural variation when they interact with conspecifics or heterospecifics. Such patterns might underlie emergent group-specific behavioural patterns and between-group behavioural differences. However, little is known about (i) how social and non-social drivers (external drivers) shape group-level social structures and (ii) whether animal groups show consistent between-group differences in social structure after accounting for external drivers. We used automated tracking to quantify daily social interactions and association networks in 12 colonies of zebra finches (Taeniopygia guttata). We quantified the effects of five external drivers (group size, group composition, ecological factors, physical environments and methodological differences) on daily interaction and association networks and tested whether colonies expressed consistent differences in day-to-day network structure after controlling for these drivers. Overall, we found that external drivers contribute significantly to network structure. However, even after accounting for the contribution of external drivers, there remained significant support for consistent between-group differences in both interaction (repeatability R: up to 0.493) and association (repeatability R: up to 0.736) network structures. Our study demonstrates how group-level differences in social behaviour can be partitioned into different drivers of variation, with consistent contributions from both social and non-social factors.

Increased initial task difficulty drives social foragers to develop sub-optimal conformity instead of adaptive diversity.

The extent to which animal societies exhibit social conformity as opposed to behavioural diversity is commonly attributed to adaptive learning strategies. Less attention is given to the possibility that the relative difficulty of learning a task socially as opposed to individually can be critical for social learning dynamics. Here we show that by raising initial task difficulty, house sparrows previously shown to exhibit adaptive social diversity become predominantly conformists. The task we used required opening feeding well covers (easier to learn socially) and to choose the covers with the rewarding cues (easy to learn individually). We replicated a previous study where sparrows exhibited adaptive diversity, but did not pre-train the naive sparrows to open covers, making the task initially more difficult. In sharp contrast to the previous study results, most sparrows continued to conform to the demonstrated cue even after experiencing greater success with the alternative rewarding cue for which competition was less intense. Thus, our study shows that a task's cognitive demands, such as the initial dependency on social demonstration, can change the entire learning dynamics, causing social animals to exhibit sub-optimal social conformity rather than adaptive diversity under otherwise identical conditions.

The presence of air sac nematodes in passerines and near-passerines in southern Germany.

Major climatic changes in conjunction with animal movement may be associated with the spread of parasites and their vectors into new populations, with potentially important consequences for population persistence. Parasites can evolve to adapt to unsuitable ecological conditions and take up refuge within new host species, with consequences for the population growth of the new host species. One parasite species that has likely been increasing its geographic range, and potentially infecting new hosts, is the recently described air sac nematode Serratospiculoides amaculata, in great tits (Parus major) in Slovakia. In this study, we screened wild birds for potential air sac nematode infection in a woodland area of southern Germany. We identified four additional host species: Eurasian nuthatch, great spotted woodpecker, greenfinch and robin. As infection by this group of nematodes can be highly pathogenic, we recommend further investigation into its potential risk to these populations.

Manipulating actions: A selective two-option device for cognitive experiments in wild animals.

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.

Social network analysis reveals context-dependent kin relationships in wild sulphur-crested cockatoos Cacatua galerita.

A preference to associate with kin facilitates inclusive fitness benefits, and increased tolerance or cooperation between kin may be an added benefit of group living. Many species exhibit preferred associations with kin; however, it is often hard to disentangle active preferences from passive overlap, for example caused by limited dispersal or inheritance of social position. Many parrots exhibit social systems consisting of pair-bonded individuals foraging in variably sized fission-fusion flocks within larger communal roosts of hundreds of individuals. Previous work has shown that, despite these fission-fusion dynamics, individuals can exhibit long-term preferred foraging associations outside their pair bonds. Yet the underlying drivers of these social preferences remain largely unknown. In this study, we use a network approach to examine the influence of kinship on social associations and interactions in wild, communally roosting sulphur-crested cockatoos, Cacatua galerita. We recorded roost co-membership, social associations and interactions in 561 individually marked birds across three neighbouring roosts. We then collected genetic samples from 205 cockatoos, and conducted a relationship analysis to construct a kinship network. Finally, we tested correlations between kinship and four social networks: association, affiliative, low-intensity aggression and high-intensity aggression. Our result showed that while roosting groups were clearly defined, they showed little genetic differentiation or kin structuring. Between roost movement was high, with juveniles, especially females, repeatedly moving between roosts. Both within roosting communities, and when visiting different roosts, individuals preferentially associated with kin. Supporting this, individuals were also more likely to allopreen kin. However, contrary to expectation, individuals preferred to direct aggression towards kin, with this effect only observed when individuals shared roost membership. By measuring social networks within and between large roosting groups, we could remove potential effects of passive spatial overlap on kin structuring. Our study reveals that sulphur-crested cockatoos actively prefer to associate with kin, both within and between roosting groups. By examining this across different interaction types, we further demonstrate that sulphur-crested cockatoos exhibit behavioural and context-dependent interaction rules towards kin. Our results help reveal the drivers of social association in this species, while adding to the evidence for social complexity in parrots.

Is bin-opening in cockatoos leading to an innovation arms race with humans?

Foraging innovations can give wild animals access to human-derived food sources1. If these innovations spread, they can enable adaptive flexibility2 but also lead to human-wildlife conflicts3. Examples include crop-raiding elephants4 and long-tailed macaques that steal items from people to trade them back for food5. Behavioural responses by humans might act as a further driver on animal innovation2,6, even potentially leading to an inter-species 'innovation arms-race'7, yet this is almost entirely unexplored. Here, we report a potential case in wild, urban-living, sulphur-crested cockatoos (Cacatua galerita; henceforth cockatoos), where the socially-learnt behaviour of opening and raiding of household bins by cockatoos8 is met with increasingly effective and socially-learnt bin-protection measures by human residents.

Cultural diffusion dynamics depend on behavioural production rules.

Culture is an outcome of both the acquisition of knowledge about behaviour through social transmission, and its subsequent production by individuals. Acquisition and production are often discussed or modelled interchangeably, yet to date no study has explored the consequences of their interaction for cultural diffusions. We present a generative model that integrates the two, and ask how variation in production rules might influence diffusion dynamics. Agents make behavioural choices that change as they learn from their productions. Their repertoires may also change, and the acquisition of behaviour is conditioned on its frequency. We analyse the diffusion of a novel behaviour through social networks, yielding generalizable predictions of how individual-level behavioural production rules influence population-level diffusion dynamics. We then investigate how linking acquisition and production might affect the performance of two commonly used inferential models for social learning; network-based diffusion analysis, and experience-weighted attraction models. We find that the influence that production rules have on diffusion dynamics has consequences for how inferential methods are applied to empirical data. Our model illuminates the differences between social learning and social influence, demonstrates the overlooked role of reinforcement learning in cultural diffusions, and allows for clearer discussions about social learning strategies.

The performance of field sampling for parasite detection in a wild passerine.

Parasites can impact the behavior of animals and alter the interplay with ecological factors in their environment. Studying the effects that parasites have on animals thus requires accurate estimates of infections in individuals. However, quantifying parasites can be challenging due to several factors. Laboratory techniques, physiological fluctuations, methodological constraints, and environmental influences can introduce measurement errors, in particular when screening individuals in the wild. These issues are pervasive in ecological studies where it is common to sample study subjects only once. Such factors should be carefully considered when choosing a sampling strategy, yet presently there is little guidance covering the major sources of error. In this study, we estimate the reliability and sensitivity of different sampling practices at detecting two internal parasites-Serratospiculoides amaculata and Isospora sp.-in a model organism, the great tit Parus major. We combine field and captive sampling to assess whether individual parasite infection status and load can be estimated from single field samples, using different laboratory techniques-McMaster and mini-FLOTAC. We test whether they vary in their performance, and quantify how sample processing affects parasite detection rates. We found that single field samples had elevated rates of false negatives. By contrast, samples collected from captivity over 24 h were highly reliable (few false negatives) and accurate (repeatable in the intensity of infection). In terms of methods, we found that the McMaster technique provided more repeatable estimates than the mini-FLOTAC for S. amaculata eggs, and both techniques were largely equally suitable for Isospora oocysts. Our study shows that field samples are likely to be unreliable in accurately detecting the presence of parasites and, in particular, for estimating parasite loads in songbirds. We highlight important considerations for those designing host-parasite studies in captive or wild systems giving guidance that can help select suitable methods, minimize biases, and acknowledge possible limitations.

Machine learning reveals cryptic dialects that explain mate choice in a songbird.

Culturally transmitted communication signals - such as human language or bird song - can change over time through cultural drift, and the resulting dialects may consequently enhance the separation of populations. However, the emergence of song dialects has been considered unlikely when songs are highly individual-specific, as in the zebra finch (Taeniopygia guttata). Here we show that machine learning can nevertheless distinguish the songs from multiple captive zebra finch populations with remarkable precision, and that 'cryptic song dialects' predict strong assortative mating in this species. We examine mating patterns across three consecutive generations using captive populations that have evolved in isolation for about 100 generations. We cross-fostered eggs within and between these populations and used an automated barcode tracking system to quantify social interactions. We find that females preferentially pair with males whose song resembles that of the females' adolescent peers. Our study shows evidence that in zebra finches, a model species for song learning, individuals are sensitive to differences in song that have hitherto remained unnoticed by researchers.

Innovation and geographic spread of a complex foraging culture in an urban parrot.

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.

A deepening understanding of animal culture suggests lessons for conservation.

A key goal of conservation is to protect biodiversity by supporting the long-term persistence of viable, natural populations of wild species. Conservation practice has long been guided by genetic, ecological and demographic indicators of risk. Emerging evidence of animal culture across diverse taxa and its role as a driver of evolutionary diversification, population structure and demographic processes may be essential for augmenting these conventional conservation approaches and decision-making. Animal culture was the focus of a ground-breaking resolution under the Convention on the Conservation of Migratory Species of Wild Animals (CMS), an international treaty operating under the UN Environment Programme. Here, we synthesize existing evidence to demonstrate how social learning and animal culture interact with processes important to conservation management. Specifically, we explore how social learning might influence population viability and be an important resource in response to anthropogenic change, and provide examples of how it can result in phenotypically distinct units with different, socially learnt behavioural strategies. While identifying culture and social learning can be challenging, indirect identification and parsimonious inferences may be informative. Finally, we identify relevant methodologies and provide a framework for viewing behavioural data through a cultural lens which might provide new insights for conservation management.

Population turnover facilitates cultural selection for efficiency in birds.

Culture, defined as socially transmitted information and behaviors that are shared in groups and persist over time, is increasingly accepted to occur across a wide range of taxa and behavioral domains.1 While persistent, cultural traits are not necessarily static, and their distribution can change in frequency and type in response to selective pressures, analogous to that of genetic alleles. This has led to the treatment of culture as an evolutionary process, with cultural evolutionary theory arguing that culture exhibits the three fundamental components of Darwinian evolution: variation, competition, and inheritance.2-5 Selection for more efficient behaviors over alternatives is a crucial component of cumulative cultural evolution,6 yet our understanding of how and when such cultural selection occurs in non-human animals is limited. We performed a cultural diffusion experiment using 18 captive populations of wild-caught great tits (Parus major) to ask whether more efficient foraging traditions are selected for, and whether this process is affected by a fundamental demographic process-population turnover. Our results showed that gradual replacement of individuals with naive immigrants greatly increased the probability that a more efficient behavior invaded a population's cultural repertoire and outcompeted an established inefficient behavior. Fine-scale, automated behavioral tracking revealed that turnover did not increase innovation rates, but instead acted on adoption rates, as immigrants disproportionately sampled novel, efficient behaviors relative to available social information. These results provide strong evidence for cultural selection for efficiency in animals, and highlight the mechanism that links population turnover to this process.

Social network architecture and the tempo of cumulative cultural evolution.

The ability to build upon previous knowledge-cumulative cultural evolution-is a hallmark of human societies. While cumulative cultural evolution depends on the interaction between social systems, cognition and the environment, there is increasing evidence that cumulative cultural evolution is facilitated by larger and more structured societies. However, such effects may be interlinked with patterns of social wiring, thus the relative importance of social network architecture as an additional factor shaping cumulative cultural evolution remains unclear. By simulating innovation and diffusion of cultural traits in populations with stereotyped social structures, we disentangle the relative contributions of network architecture from those of population size and connectivity. We demonstrate that while more structured networks, such as those found in multilevel societies, can promote the recombination of cultural traits into high-value products, they also hinder spread and make products more likely to go extinct. We find that transmission mechanisms are therefore critical in determining the outcomes of cumulative cultural evolution. Our results highlight the complex interaction between population size, structure and transmission mechanisms, with important implications for future research.

Connecting the data landscape of long-term ecological studies: The SPI-Birds data hub.

The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long-term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and ecological processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad-scale global issues (e.g. climate change). To solve data integration issues and enable a new scale of ecological and evolutionary research based on long-term studies of birds, we have created the SPI-Birds Network and Database (www.spibirds.org)-a large-scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI-Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting. SPI-Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collaboration and synthesis. We provide community-derived data and meta-data standards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata languages (e.g. ecological meta-data language). The encouraging community involvement stems from SPI-Bird's decentralized approach: research groups retain full control over data use and their way of data management, while SPI-Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community-specific hubs (such as ours, COMADRE for animal demography, etc.) will aid much-needed large-scale ecological data integration.