ABSTRACT
Cognition is defined as the processes by which animals collect, retain and use information from their environment to guide their behaviour. Thus cognition is essential in a wide range of ...behaviours, including foraging, avoiding predators and mating. Despite this pivotal role, the evolutionary processes shaping variation in cognitive performance among individuals in wild populations remain very poorly understood. Selection experiments in captivity suggest that cognitive traits can have substantial heritability and can undergo rapid evolution. However only a handful of studies have attempted to explore how cognition influences life‐history variation and fitness in the wild, and direct evidence for the action of natural or sexual selection on cognition is still lacking, reasons for which are diverse. Here we review the current literature with a view to: (i) highlighting the key practical and conceptual challenges faced by the field; (ii) describing how to define and measure cognitive traits in natural populations, and suggesting which species, populations and cognitive traits might be examined to greatest effect; emphasis is placed on selecting traits that are linked to functional behaviour; (iii) discussing how to deal with confounding factors such as personality and motivation in field as well as captive studies; (iv) describing how to measure and interpret relationships between cognitive performance, functional behaviour and fitness, offering some suggestions as to when and what kind of selection might be predicted; and (v) showing how an evolutionary ecological framework, more generally, along with innovative technologies has the potential to revolutionise the study of cognition in the wild. We conclude that the evolutionary ecology of cognition in wild populations is a rapidly expanding interdisciplinary field providing many opportunities for advancing the understanding of how cognitive abilities have evolved.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
In human societies, cultural norms arise when behaviours are transmitted through social networks via high-fidelity social learning. However, a paucity of experimental studies has meant that there is ...no comparable understanding of the process by which socially transmitted behaviours might spread and persist in animal populations. Here we show experimental evidence of the establishment of foraging traditions in a wild bird population. We introduced alternative novel foraging techniques into replicated wild sub-populations of great tits (Parus major) and used automated tracking to map the diffusion, establishment and long-term persistence of the seeded innovations. Furthermore, we used social network analysis to examine the social factors that influenced diffusion dynamics. From only two trained birds in each sub-population, the information spread rapidly through social network ties, to reach an average of 75% of individuals, with a total of 414 knowledgeable individuals performing 57,909 solutions over all replicates. The sub-populations were heavily biased towards using the technique that was originally introduced, resulting in established local traditions that were stable over two generations, despite a high population turnover. Finally, we demonstrate a strong effect of social conformity, with individuals disproportionately adopting the most frequent local variant when first acquiring an innovation, and continuing to favour social information over personal information. Cultural conformity is thought to be a key factor in the evolution of complex culture in humans. In providing the first experimental demonstration of conformity in a wild non-primate, and of cultural norms in foraging techniques in any wild animal, our results suggest a much broader taxonomic occurrence of such an apparently complex cultural behaviour.
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DOBA, IJS, IZUM, KILJ, KISLJ, NUK, PILJ, PNG, SAZU, SBMB, SIK, UILJ, UKNU, UL, UM, UPUK
Animals can learn about the value of resources and predation risk by exploring novel environments or exploring novel stimuli in their regular environments. Still, there is a disconnect in the way ...that exploration has been defined and measured; exploration is defined in terms of information acquisition, while measured in terms of movement speed and diversity of contacted items in a novel environment. If exploration is indeed a measurement of information gathering, fast explorers should seek to reduce uncertainty about their environment more than slow explorers. Exploration speed has also been linked to behavioral plasticity, where fast explorers move fast but collect less detailed information, thereby forming routines and expressing less plasticity than slow explorers. We test these two hypotheses by comparing exploration in a novel environment to individuals' attraction to novelty and behavioral plasticity. Our results support the view that exploration is a measurement of information‐gathering tendencies as fast explorers were more likely to collect novel information, which should reduce uncertainty further than sampling familiar information sources, compared with slower explorers. Furthermore, faster explorers switched to sampling novel information more quickly than slow explorers when the value of the familiar option decreased, opposing the widely held view that faster explorers present more routine‐like behavior. By providing familiar and novel foraging options in close spatial contiguity, we demonstrate an attraction to novelty in faster explorers that cannot be confounded by activity rate, thereby suggesting that these individuals seek to reduce uncertainty. In conclusion, our results support the biological validity of the term “exploration” through its association with information gathering.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Neophobia, defined as the fear of novelty, can be exhibited when individuals encounter unfamiliar stimuli in their environment. Neophobia has been shown to both increase and decrease when individuals ...are with conspecifics. An increase in latency to contact new objects can be explained by the negotiation hypothesis, which proposes that individuals in groups will negotiate who will approach novelty first, thereby delaying the first contact. This negotiation process could co‐occur with and mask a potential effect of risk dilution, where individuals in groups should approach novel objects faster due to lower perceived risk in a social than non‐social context. Here, we aimed to test the risk dilution hypothesis using an experimental set‐up that precluded negotiation among group members by physically separating dyads during social trials. We presented zebra finches (Taeniopygia guttata) with different novel objects in both social and non‐social contexts. We also repeated the presentation of each object to investigate, for the first time to our knowledge, the effect of social context on the change in neophobia over repeated encounters (i.e., habituation). We found that social context increased the latency to approach a novel object upon first presentation of objects (i.e., increased neophobia), but these latencies decreased faster over repeated presentations of the objects (i.e., faster habituation) compared to the non‐social context. These results do not provide support for the risk dilution hypothesis regarding first encounters with objects (neophobia) but seem to support it over repeated object presentations (habituation). This suggests that the effect of social context is different on neophobia and habituation, possibly because they recruit different cognitive mechanisms. Future studies should investigate the impact of ecological and social conditions on decision‐making upon first versus subsequent encounters with a novel object in social animals, as both processes can impact fitness costs and benefits of novelty responses.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Survival depends on appropriate behavioural and physiological responses to danger. In addition to active ‘fight‐flight’ defence responses, a passive ‘freeze‐hide’ response is adaptive in some ...contexts. However, the physiological mechanisms determining which individuals choose a given defence response remain poorly understood. We examined the relationships among personality, metabolic performance and physiological stress responses across an environmental gradient in the olive flounder, Paralichthys olivaceus. We employed four behavioural assays to document the existence of two distinct behavioural types (‘bold’ and ‘shy’) in this species. We found consistent metabolic differences between individuals of a given behavioural type across an environmental gradient: shy individuals had overall lower aerobic scope, maximum metabolic rate and standard metabolic rate than bold individuals in both high (25 ppt) and low (3 ppt) salinity. These behavioural and metabolic differences translated into divergent physiological responses during acute stress: shy individuals adopted a passive ‘freeze‐hide’ response by reducing their oxygen consumption rates (akin to shallow breathing) whereas bold individuals adopted an active ‘fight‐flight’ response by increasing their rates of respiration. These distinct defence strategies were repeatable within individuals between salinity treatments. Although it has been suggested theoretically, this is the first empirical evidence that the metabolic response to stressful situations differs between bold and shy individuals. Our results emphasize the importance of incorporating physiological measures to understand the mechanisms driving persistent inter‐individual differences in animals.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Cognition and covariance in the producer–scrounger game Reichert, Michael S.; Morand‐Ferron, Julie; Kulahci, Ipek G. ...
Journal of animal ecology,
November 2021, 2021-11-00, 20211101, Volume:
90, Issue:
11
Journal Article
Peer reviewed
Open access
The producer–scrounger game is a key element of foraging ecology in many systems. Producing and scrounging typically covary negatively, but partitioning this covariance into contributions of ...individual plasticity and consistent between individual differences is key to understanding population‐level consequences of foraging strategies. Furthermore, little is known about the role cognition plays in the producer–scrounger game.
We investigated the role of cognition in these alternative foraging tactics in wild mixed‐species flocks of great tits and blue tits, using a production learning task in which we measured individuals’ speed of learning to visit the single feeder in an array that would provide them with a food reward. We also quantified the proportion of individuals’ feeds that were scrounges (‘proportion scrounged’); scrounging was possible if individuals visited immediately after a previous rewarded visitor. Three learning experiments—initial and two reversal learning—enabled us to estimate the repeatability and covariance of each foraging behaviour.
First, we examined whether individuals learned to improve their scrounging success (i.e. whether they obtained food by scrounging when there was an opportunity to do so). Second, we quantified the repeatability of proportion scrounged, and asked whether proportion scrounged affected production learning speed among individuals. Third, we used multivariate analyses to partition within‐ and among‐individual components of covariance between proportion scrounged and production learning speed.
Individuals improved their scrounging success over time. Birds with a greater proportion scrounged took longer to learn their own rewarding feeder. Although multivariate analyses showed that covariance between proportion scrounged and learning speed was driven primarily by within‐individual variation, that is, by behavioural plasticity, among‐individual differences also played a role for blue tits.
This is the first demonstration of a cognitive trait influencing producing and scrounging in the same wild system, highlighting the importance of cognition in the use of alternative resource acquisition tactics. The results of our covariance analyses suggest the potential for genetic differences in allocation to alternative foraging tactics, which are likely species‐ and system‐dependent. They also point to the need to control for different foraging tactics when studying individual cognition in the wild.
Individual birds can learn to scrounge better, and this might affect how they learn to find food on their own.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Individuals vary in their cognitive performance. While this variation forms the foundation of the study of human psychometrics, its broader importance is only recently being recognized. Explicitly ...acknowledging this individual variation found in both humans and non-human animals provides a novel opportunity to understand the mechanisms, development and evolution of cognition. The papers in this special issue highlight the growing emphasis on individual cognitive differences from fields as diverse as neurobiology, experimental psychology and evolutionary biology. Here, we synthesize this body of work. We consider the distinct challenges in quantifying individual differences in cognition and provide concrete methodological recommendations. In particular, future studies would benefit from using multiple task variants to ensure they target specific, clearly defined cognitive traits and from conducting repeated testing to assess individual consistency. We then consider how neural, genetic, developmental and behavioural factors may generate individual differences in cognition. Finally, we discuss the potential fitness consequences of individual cognitive variation and place these into an evolutionary framework with testable hypotheses. We intend for this special issue to stimulate researchers to position individual variation at the centre of the cognitive sciences.
This article is part of the theme issue ‘Causes and consequences of individual differences in cognitive abilities’.
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BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
Understanding dominance hierarchies is an important aspect of many studies of animal groups. Collecting the necessary data requires a large amount of time and effort to detect only a small number of ...interactions. Here, we assess the viability of extracting interactions from a temporal data stream of arrival and departures to a feeder equipped with a radio‐frequency identifier antenna. We show that the interactions extracted from this type of data can create similar dominance hierarchies to those produced by analysing video data of interactions. Additionally, we assessed the amount of temporal data required to obtain a dominance hierarchy and discuss the advantages and disadvantages of utilising temporal data streams to generate dominance hierarchies of animal groups. The code to extract the dominance interactions and test the correlation between different dominance hierarchies is included in the Supporting Information.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Group living commonly helps organisms face challenging environmental conditions. Although a known phenomenon in humans, recent findings suggest that a benefit of group living in animals generally ...might be increased innovative problem-solving efficiency. This benefit has never been demonstrated in a natural context, however, and the mechanisms underlying improved efficiency are largely unknown. We examined the problem-solving performance of great and blue tits at automated devices and found that efficiency increased with flock size. This relationship held when restricting the analysis to naive individuals, demonstrating that larger groups increased innovation efficiency. In addition to this effect of naive flock size, the presence of at least one experienced bird increased the frequency of solving, and larger flocks were more likely to contain experienced birds. These findings provide empirical evidence for the "pool of competence" hypothesis in nonhuman animals. The probability of success also differed consistently between individuals, a necessary condition for the pool of competence hypothesis. Solvers had a higher probability of success when foraging with a larger number of companions and when using devices located near rather than further from protective tree cover, suggesting a role for reduced predation risk on problem-solving efficiency. In contrast to traditional group living theory, individuals joining larger flocks benefited from a higher seed intake, suggesting that group living facilitated exploitation of a novel food source through improved problem-solving efficiency. Together our results suggest that both ecological and social factors, through reduced predation risk and increased pool of competence, mediate innovation in natural populations.
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BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
Understanding the ecology and evolution of personality and cognition requires the development of new tools to measure individual and species differences in behavioural and cognitive performances in ...wild populations. Furthermore, such tools should facilitate collection of large sample sizes, evaluate the repeatability of measured traits and allow direct comparison of species performances across a variety of behavioural tasks.
Here we present a RFID‐based feeder (OpenFeeder) designed to run visual cognitive tasks in wild animals. We illustrate the flexibility of the tool showing performances of three wild passerine species (Parus major, Cyanistes caeruleus and Poecile palustris) in an associative learning task.
We recorded performances of a large number of individuals (>300) in the wild and showed both interspecific and intraspecific differences in associative learning. We also found moderate to high repeatability in individual differences in associative learning in each species.
We show that the OpenFeeder is a flexible tool to record performance in multiple cognitive and behavioural tasks in free‐ranging animals across a variety of passerine species. The design, firmware and software are open source to facilitate use in a wide variety of species and thus allow continuous improvement of the system and development of new behavioural and cognitive tasks. In doing so, we hope that this tool will be used by a large community of cognitive ecologists and comparative psychologists for both within and across species studies. Furthermore, our system should facilitate replication of results across populations along large‐scale environmental gradients to improve our understanding of the role ecology plays in the evolution of cognitive traits.
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FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
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