'Ripple effects' of urban environmental characteristics on cognitive performances in Eurasian red squirrels.

Urban areas are expanding exponentially, leading more species of wildlife living in urban environments. Urban environmental characteristics, such as human disturbance, induce stress for many wildlife and have been shown to affect some cognitive traits, such as innovative problem-solving performance. However, because different cognitive traits have common cognitive processes, it is possible that urban environmental characteristics may directly and indirectly affect related cognitive traits (the ripple effect hypothesis). We tested the ripple effect hypothesis in urban Eurasian red squirrels residing in 11 urban areas that had different urban environmental characteristics (direct human disturbance, indirect human disturbance, areas of green coverage and squirrel population size). These squirrels were innovators who had previously repeatedly solved a food extraction task (the original task). Here, we examined whether and how urban environmental characteristics would directly and indirectly influence performance in two related cognitive traits, generalisation and (long-term) memory. The generalisation task required the innovators to apply the learned successful solutions when solving a similar but novel problem. The memory task required them to recall the learned solution of the original task after an extended period of time. Some of the selected urban environmental characteristics directly influenced the task performance, both at the population level (site) and at individual levels. Urban environmental characteristics, such as increased direct and indirect human disturbance, decreased the proportion of success in solving the generalisation task or the memory task at the population (site) level. Increased direct human disturbance and less green coverage increased the solving efficiency at individual levels. We also found an indirect effect in one of the urban environmental characteristics, indirect human disturbance, in the generalisation task, but not the memory task. Such an effect was only seen at the individual level but not at the population level; indirect human disturbance decreased the first original latency, which then decreased the generalisation latency across successes. Our results partially support the ripple effect hypothesis, suggesting that urban environmental characteristics are stressors for squirrels and have a greater impact on shaping cognitive performance than previously shown. Together, these results provide a better understanding of cognitive traits that support wildlife in adapting to urban environments.

Social interactions and information use by foraging seabirds.

What do seabirds perceive about the world? How do they do so? And how do they use the information available to them to make foraging decisions? Social cues provide seabirds with information about the location of prey. This can, of course, be passive and not involve higher-order cognitive processes (e.g. simple conspecific or heterospecific attraction). However, seabirds display many behaviours that promote learning and the transmission of information between individuals: the vast majority of seabirds are colonial living, have an extended juvenile phase that affords them time to learn, routinely form intra- and interspecific associations, and can flexibly deploy a combination of foraging tactics. It is worth evaluating their foraging interactions in light of this. This review describes how seabirds use social information both at the colony and at sea to forage, and discusses the variation that exists both across species and amongst individuals. It is clear that social interactions are a critical and beneficial component of seabird foraging, with most of the variation concerning the way and extent to which social information is used, rather than whether it is used. While it may seem counterintuitive that large groups of potential competitors congregating at a patch can result in foraging gains, such aggregations can alter species dynamics in ways that promote coexistence. This review explores how competitive interference at a patch can be mitigated by behavioural modifications and niche segregation. Utilising others for foraging success (e.g. via social cues and facilitation at a patch) is likely to make population declines particularly damaging to seabirds if the quantity or quality of their social foraging interactions is reduced. Environmental changes have the potential to disrupt their social networks and thus, how these species obtain food and transfer information.

Environmental conditions shape learning in larval zebrafish.

Growing evidence reveals notable phenotypic plasticity in cognition among teleost fishes. One compelling example is the positive impact of enriched environments on learning performance. Most studies on this effect have focused on juvenile or later life stages, potentially overlooking the importance of early life plasticity. To address this gap, we investigated whether cognitive plasticity in response to environmental factors emerges during the larval stage in zebrafish. Our findings indicate that larvae exposed to an enriched environment after hatching exhibited enhanced habituation learning performance compared to their counterparts raised in a barren environment. This work underscores the presence of developmental phenotypic plasticity in cognition among teleost fish, extending its influence to the very earliest stages of an individual's life.

Environmental harshness does not affect the propensity for social learning in great tits, Parus major.

According to the harsh environment hypothesis, natural selection should favour cognitive mechanisms to overcome environmental challenges. Tests of this hypothesis to date have largely focused on asocial learning and memory, thus failing to account for the spread of information via social means. Tests in specialized food-hoarding birds have shown strong support for the effects of environmental harshness on both asocial and social learning. Whether the hypothesis applies to non-specialist foraging species remains largely unexplored. We evaluated the relative importance of social learning across a known harshness gradient by testing generalist great tits, Parus major, from high (harsh)- and low (mild)-elevation populations in two social learning tasks. We showed that individuals use social learning to find food in both colour-associative and spatial foraging tasks and that individuals differed consistently in their use of social learning. However, we did not detect a difference in the use or speed of implementing socially observed information across the elevational gradient. Our results do not support predictions of the harsh environment hypothesis suggesting that context-dependent costs and benefits as well as plasticity in the use of social information may play an important role in the use of social learning across environments. Finally, this study adds to the accumulating evidence that the harsh environment hypothesis appears to have more pronounced effects on specialists compared to generalist species.

Learning modifies attention during bumblebee visual search.

Abstract: The role of visual search during bee foraging is relatively understudied compared to the choices made by bees. As bees learn about rewards, we predicted that visual search would be modified to prioritise rewarding flowers. To test this, we ran an experiment testing how bee search differs in the initial and later part of training as they learn about flowers with either higher- or lower-quality rewards. We then ran an experiment to see how this prior training with reward influences their search on a subsequent task with different flowers. We used the time spent inspecting flowers as a measure of attention and found that learning increased attention to rewards and away from unrewarding flowers. Higher quality rewards led to decreased attention to non-flower regions, but lower quality rewards did not. Prior experience of lower rewards also led to more attention to higher rewards compared to unrewarding flowers and non-flower regions. Our results suggest that flowers would elicit differences in bee search behaviour depending on the sugar content of their nectar. They also demonstrate the utility of studying visual search and have important implications for understanding the pollination ecology of flowers with different qualities of reward. Significance statement: Studies investigating how foraging bees learn about reward typically focus on the choices made by the bees. How bees deploy attention and visual search during foraging is less well studied. We analysed flight videos to characterise visual search as bees learn which flowers are rewarding. We found that learning increases the focus of bees on flower regions. We also found that the quality of the reward a flower offers influences how much bees search in non-flower areas. This means that a flower with lower reward attracts less focussed foraging compared to one with a higher reward. Since flowers do differ in floral reward, this has important implications for how focussed pollinators will be on different flowers. Our approach of looking at search behaviour and attention thus advances our understanding of the cognitive ecology of pollination. Supplementary Information: The online version contains supplementary material available at 10.1007/s00265-024-03432-z.

'Hallucination': Hospital Ecologies in COVID's Epistemic Instability.

Historians and ethnographers have described biomedicine as a modernist project that imagines accumulating ever-more stable knowledge over time. This project broke down in heavily hit hospitals at the onset of the COVID-19 pandemic in the U.S., when bureaucratic, physical and knowledge structures collapsed. A combination of terror, a partially characterized disease entity and clinicians' inability to operate without disease models drove them to draw on rapidly changing and contradictory information via social media, changing medical practice minute-to-minute. The result was a unique form of knowing described as "hallucination": a hyperreal, unstable ecology of imagined viral particles distributed in physical spaces, transforming with each text message and tweet. The nature, experience and practice of this ecology sheds light on what happens when instability comes to otherwise stable places.

Food-caching mountain chickadees can learn abstract rules to solve a complex spatial-temporal pattern.

The use of abstract rules in behavioral decisions is considered evidence of executive functions associated with higher-level cognition. Laboratory studies across taxa have shown that animals may be capable of learning abstract concepts, such as the relationships between items, but often use simpler cognitive abilities to solve tasks. Little is known about whether or how animals learn and use abstract rules in natural environments. Here, we tested whether wild, food-caching mountain chickadees (Poecile gambeli) could learn an abstract rule in a spatial-temporal task in which the location of a food reward rotated daily around an 8-feeder square spatial array for up to 34 days. Chickadees initially searched for the daily food reward by visiting the most recently rewarding locations and then moving backward to visit previously rewarding feeders, using memory of previous locations. But by the end of the task, chickadees were more likely to search forward in the correct direction of rotation, moving away from the previously rewarding feeders. These results suggest that chickadees learned the direction rule for daily feeder rotation and used this to guide their decisions while searching for a food reward. Thus, chickadees appear to use an executive function to make decisions on a foraging-based task in the wild. VIDEO ABSTRACT.

Adaptive phenotypic plasticity induces individual variability along a cognitive trade-off.

Animal species, including humans, display patterns of individual variability in cognition that are difficult to explain. For instance, some individuals perform well in certain cognitive tasks but show difficulties in others. We experimentally analysed the contribution of cognitive plasticity to such variability. Theory suggests that diametrically opposed cognitive phenotypes increase individuals' fitness in environments with different conditions such as resource predictability. Therefore, if selection has generated plasticity that matches individuals' cognitive phenotypes to the environment, this might produce remarkable cognitive variability. We found that guppies, Poecilia reticulata, exposed to an environment with high resource predictability (i.e. food available at the same time and in the same location) developed enhanced learning abilities. Conversely, guppies exposed to an environment with low resource predictability (i.e. food available at a random time and location) developed enhanced cognitive flexibility and inhibitory control. These cognitive differences align along a trade-off between functions that favour the acquisition of regularities such as learning and functions that adjust behaviour to changing conditions (cognitive flexibility and inhibitory control). Therefore, adaptive cognitive plasticity in response to resource predictability (and potentially similar factors) is a key determinant of cognitive individual differences.

No evidence of social learning in a socially roosting butterfly in an associative learning task.

Insects may acquire social information by active communication and through inadvertent social cues. In a foraging setting, the latter may indicate the presence and quality of resources. Although social learning in foraging contexts is prevalent in eusocial species, this behaviour has been hypothesized to also exist between conspecifics in non-social species with sophisticated behaviours, including Heliconius butterflies. Heliconius are the only butterfly genus with active pollen feeding, a dietary innovation associated with a specialized, spatially faithful foraging behaviour known as trap-lining. Long-standing hypotheses suggest that Heliconius may acquire trap-line information by following experienced individuals. Indeed, Heliconius often aggregate in social roosts, which could act as 'information centres', and present conspecific following behaviour, enhancing opportunities for social learning. Here, we provide a direct test of social learning ability in Heliconius using an associative learning task in which naive individuals completed a colour preference test in the presence of demonstrators trained to feed randomly or with a strong colour preference. We found no evidence that Heliconius erato, which roost socially, used social information in this task. Combined with existing field studies, our results add to data which contradict the hypothesized role of social learning in Heliconius foraging behaviour.

The contribution of executive functions to sex differences in animal cognition.

Cognitive sex differences have been reported in several vertebrate species, mostly in spatial abilities. Here, I review evidence of sex differences in a family of general cognitive functions that control behaviour and cognition, i.e., executive functions such as cognitive flexibility and inhibitory control. Most of this evidence derives from studies in teleost fish. However, analysis of literature from other fields (e.g., biomedicine, genetic, ecology) concerning mammals and birds reveals that more than 40% of species investigated exhibit sex differences in executive functions. Among species, the direction and magnitude of these sex differences vary greatly, even within the same family, suggesting sex-specific selection due to species' reproductive systems and reproductive roles of males and females. Evidence also suggests that sex differences in executive functions might provide males and females highly differentiated cognitive phenotypes. To understand the evolution of cognitive sex differences in vertebrates, future research should consider executive functions.

It Began in Ponds and Rivers: Charting the Beginnings of the Ecology of Fish Cognition.

But fish cognitive ecology did not begin in rivers and streams. Rather, one of the starting points for work on fish cognitive ecology was work done on the use of visual cues by homing pigeons. Prior to working with fish, Victoria Braithwaite helped to establish that homing pigeons rely not just on magnetic and olfactory cues but also on visual cues for successful return to their home loft. Simple, elegant experiments on homing established Victoria's ability to develop experimental manipulations to examine the role of visual cues in navigation by fish in familiar areas. This work formed the basis of a rich seam of work whereby a fish's ecology was used to propose hypotheses and predictions as to preferred cue use, and then cognitive abilities in a variety of fish species, from model systems (Atlantic salmon and sticklebacks) to the Panamanian Brachyraphis episcopi. Cognitive ecology in fish led to substantial work on fish pain and welfare, but was never left behind, with some of Victoria's last work addressed to determining the neural instantiation of cognitive variation.

Angling gear avoidance learning in juvenile red sea bream: evidence from individual-based experiments.

Angling gear avoidance learning is a possible factor that contributes to the vulnerability of caught-and-released fish to angling. Whereas past studies suggested angling gear avoidance learning, they were based on large-scale experiments on groups of fish and unable to verify learning accurately. Details of avoidance learning are also unclear. The present study investigated angling gear avoidance learning through a series of individual-based experiments using red sea bream (Pagrus major) juveniles. Fish avoided angling gear after only one or two catches while showing feeding motivation for pellets, representing avoidance learning for angling gear. Most of the experienced fish avoided krill attached to a fishing line, but not krill alone or pellets presented near the angling gear. Experienced fish were less vulnerable to angling than control fish. Approximately half of the experienced fish kept the memory of angling gear 2 months after learning. The learning effect through the catch-and-release procedure would reduce catchability and the value of fishery-dependent stock assessments.

Space in Hand and Mind: Gesture and Spatial Frames of Reference in Bilingual Mexico.

Speakers of many languages prefer allocentric frames of reference (FoRs) when talking about small-scale space, using words like "east" or "downhill." Ethnographic work has suggested that this preference is also reflected in how such speakers gesture. Here, we investigate this possibility with a field experiment in Juchitán, Mexico. In Juchitán, a preferentially allocentric language (Isthmus Zapotec) coexists with a preferentially egocentric one (Spanish). Using a novel task, we elicited spontaneous co-speech gestures about small-scale motion events (e.g., toppling blocks) in Zapotec-dominant speakers and in balanced Zapotec-Spanish bilinguals. Consistent with prior claims, speakers' spontaneous gestures reliably reflected either an egocentric or allocentric FoR. The use of the egocentric FoR was predicted-not by speakers' dominant language or the language they used in the task-but by mastery of words for "right" and "left," as well as by properties of the event they were describing. Additionally, use of the egocentric FoR in gesture predicted its use in a separate nonlinguistic memory task, suggesting a cohesive cognitive style. Our results show that the use of spatial FoRs in gesture is pervasive, systematic, and shaped by several factors. Spatial gestures, like other forms of spatial conceptualization, are thus best understood within broader ecologies of communication and cognition.

Performance of horned puffins (Fratercula corniculata) on an object permanence task.

Cognition influences how individuals interact with the environment, affecting the ecology of species. Gaining insight into the proficiency of relevant cognitive abilities provides an indication of the processes necessary for a species' survival and reproduction. Many birds have "slow" life-histories and complex social environments suggestive of high cognitive ability. Little, however, is known about the cognition of most birds with these traits, thus studying cognition in seabirds with these traits provides insight into how slow life-histories and complex social environments relate more generally to predicting cognitive ability. Object permanence is a cognitive ability shared by highly intelligent animals and could be an ecologically relevant ability for many seabirds. I used a simple experimental setup in a semi-controlled environment to test object permanence in captive horned puffins (Fratercula corniculata) by hiding a reward to be retrieved, first partially and then completely. I discovered that the horned puffins performed poorly on the object permanence task when the reward was hidden completely. I discuss briefly how the slow life-histories of many seabirds probably evolved due to the stochastic conditions associated with their marine environment, which in turn may cause an energetic bottleneck that limits the allocation of resources to certain cognitive abilities.

Heliconiini butterflies can learn time-dependent reward associations.

For many pollinators, flowers provide predictable temporal schedules of resource availability, meaning an ability to learn time-dependent information could be widely beneficial. However, this ability has only been demonstrated in a handful of species. Observations of Heliconius butterflies suggest that they may have an ability to form time-dependent foraging preferences. Heliconius are unique among butterflies in actively collecting pollen, a dietary behaviour linked to spatio-temporally faithful 'trap-line' foraging. Time dependency of foraging preferences is hypothesized to allow Heliconius to exploit temporal predictability in alternative pollen resources. Here, we provide the first experimental evidence in support of this hypothesis, demonstrating that Heliconius hecale can learn opposing colour preferences in two time periods. This shift in preference is robust to the order of presentation, suggesting that preference is tied to the time of day and not due to ordinal or interval learning. However, this ability is not limited to Heliconius, as previously hypothesized, but also present in a related genus of non-pollen feeding butterflies. This demonstrates time learning likely pre-dates the origin of pollen feeding and may be prevalent across butterflies with less specialized foraging behaviours.

Archerfish vision: Visual challenges faced by a predator with a unique hunting technique.

Archerfish are well-known for their ballistic hunting behaviour, in which they shoot down aerial prey with a well-aimed jet of water. This unique hunting strategy poses several challenges for visual systems. Archerfish face significant distortion to the appearance of targets due to refraction at the air/water interface, they search for prey against a complex background of foliage, they change prey targeting behaviour as conditions change, and they must make high speed decisions to avoid competition. By studying how archerfish have overcome these challenges, we have been able to understand more about fundamental problems faced by visual systems and the mechanisms used to solve them. In some cases, such as when searching for targets, the visual capabilities of archerfish are functionally similar to those of humans, despite significant differences in neuroanatomy. In other cases, the particular challenge faced by archerfish magnifies fundamental problems generally faced by visual systems, such as recognizing objects given strong viewpoint dependent changes to appearance. The efficiency of archerfish retrieving fallen prey to avoid kleptoparasitism, demonstrates that their visual processing excels in both speed and accuracy. In this review, we attempt to provide an overview of the many facets of visually driven behaviour of archerfish, and how they have been studied. In addition to their hunting technique, archerfish are ideal for visual processing experiments as they can be quickly trained to perform a range of non-ecologically relevant tasks. Their behavioural flexibility moreover, introduces the opportunity to study how experience-dependence and choice affects visual processing.

Multiple factors affect discrimination learning performance, but not between-individual variation, in wild mixed-species flocks of birds.

Cognition arguably drives most behaviours in animals, but whether and why individuals in the wild vary consistently in their cognitive performance is scarcely known, especially under mixed-species scenarios. One reason for this is that quantifying the relative importance of individual, contextual, ecological and social factors remains a major challenge. We examined how many of these factors, and sources of bias, affected participation and performance, in an initial discrimination learning experiment and two reversal learning experiments during self-administered trials in a population of great tits and blue tits. Individuals were randomly allocated to different rewarding feeders within an array. Participation was high and only weakly affected by age and species. In the initial learning experiment, great tits learned faster than blue tits. Great tits also showed greater consistency in performance across two reversal learning experiments. Individuals assigned to the feeders on the edge of the array learned faster. More errors were made on feeders neighbouring the rewarded feeder and on feeders that had been rewarded in the previous experiment. Our estimates of learning consistency were unaffected by multiple factors, suggesting that, even though there was some influence of these factors on performance, we obtained a robust measure of discrimination learning in the wild.

Personality traits covary with individual differences in inhibitory abilities in 2 species of fish.

In a number of animal species, individuals differ in their ability to solve cognitive tasks. However, the mechanisms underlying this variability remain unclear. It has been proposed that individual differences in cognition may be related to individual differences in behavior (i.e., personality); a hypothesis that has received mixed support. In this study, we investigated whether personality correlates with the cognitive ability that allows inhibiting behavior in 2 teleost fish species, the zebrafish Danio rerio and the guppy Poecilia reticulata. In both species, individuals that were bolder in a standard personality assay, the open-field test, showed greater inhibitory abilities in the tube task, which required them to inhibit foraging behavior toward live prey sealed into a transparent tube. This finding reveals a relationship between boldness and inhibitory abilities in fish and lends support to the hypothesis of a link between personality and cognition. Moreover, this study suggests that species separated by a relatively large phylogenetic distance may show the same link between personality and cognition, when tested on the same tasks.

Isolating the effects of ontogenetic niche shift on brain size development using pumpkinseed sunfish ecotypes.

A functional relationship between relative brain size and cognitive performance has been hypothesized. However, the influence of ontogenetic niche shifts on cognitive performance is not well understood. Increases in body size can affect niche use but distinguishing nonecologically relevant brain development from effects associated with ecology is difficult. If survival is enhanced by functional changes in ecocognitive performance over ontogeny, then brain size development should track ontogenetic shifts in ecology. We control for nonecologically relevant brain size development by comparing brain growth between two ecotypes of Pumpkinseed sunfish whose ecologies diverge over ontogeny from a shared juvenile niche. Brain size differs between ecotypes from their birth year onwards even though their foraging ecology appears to diverge at age 3. This finding suggests that the eco-cognitive requirements of adult niches shape early life brain growth more than the requirements of juvenile ecology.

Animal cognition in the field: performance of wild vervet monkeys (Chlorocebus pygerythrus) on a reversal learning task.

Increasingly, researchers are moving animal cognitive research into wild field settings. A field-based approach offers a valuable complement to laboratory-based studies, as it enables researchers to work with animals in their natural environments and indicates whether cognitive abilities found in captive subjects are generalizable to wild animals. It is thus important to field-based research to clarify which cognitive tasks can be replicated in wild settings, which species are suitable for testing in the wild, and whether replication produces similar results in wild animals. To address these issues, we modified a well-known lab test for field applications. The transfer index (TI) is a reversal learning task that tests whether animals rely on more associative or rule-based learning strategies (Rumbaugh in Primate behavior: developments in field and laboratory research. Academic Press, Inc., New York, pp. 2-66, 1970). In this paper, we detail changes needed to use a TI-like task in the field, here referred to as the Field Reversal Index (FRI). We tested a sample of nine wild vervet monkeys (Chlorocebus pygerythrus) on the FRI task at Lake Nabugabo, Uganda. We show that wild primates can successfully be tested on reversal learning paradigms, and present findings that reinforce previous conclusions from captive experiments. Our results indicate that vervets, like other cercopithecoids, rely on associative learning rather than rule-based learning. Further, our results are consistent with previous research that reports improved performance post-reversal in younger individuals relative to older individuals. The FRI enables researchers to test animals both in the wild and in captivity to facilitate direct comparisons between the learning abilities of captive and wild animals.