ABSTRACT
Despite increasing interest in the evolution of inhibitory control, few studies have examined the validity of widespread testing paradigms, the long-term repeatability and the heritability of this cognitive ability in the wild. We investigated these aspects in the inhibitory control performance of wild toutouwai (North Island robin; Petroica longipes), using detour and reversal learning tasks. We assessed convergent validity by testing whether individual performance correlated across detour and reversal learning tasks. We then further evaluated task validity by examining whether individual performance was confounded by non-cognitive factors. We tested a subset of subjects twice in each task to estimate the repeatability of performance across a 1-year period. Finally, we used a population pedigree to estimate the heritability of task performance. Individual performance was unrelated across detour and reversal learning tasks, indicating that these measured different cognitive abilities. Task performance was not influenced by body condition, boldness or prior experience, and showed moderate between-year repeatability. Yet despite this individual consistency, we found no evidence that task performance was heritable. Our findings suggest that detour and reversal learning tasks measure consistent individual differences in distinct forms of inhibitory control in toutouwai, but this variation may be environmentally determined rather than genetic.
ABSTRACT
Although animal personality research may have applied uses, this suggestion has yet to be evaluated by assessing empirical studies examining animal personality and conservation. To address this knowledge gap, we performed a systematic review of the peer-reviewed literature relating to conservation science and animal personality. Criteria for inclusion in our review included access to full text, primary research articles, and relevant animal conservation or personality focus (i.e., not human personality studies). Ninety-two articles met these criteria. We summarized the conservation contexts, testing procedures (including species and sample size), analytical approach, claimed personality traits (activity, aggression, boldness, exploration, and sociability), and each report's key findings and conservation-focused suggestions. Although providing evidence for repeatability in behavior is crucial for personality studies, repeatability quantification was implemented in only half of the reports. Nonetheless, each of the 5 personality traits were investigated to some extent in a range of conservations contexts. The most robust studies in the field showed variance in how personality relates to other ecologically important variables across species and contexts. Moreover, many studies were first attempts at using personality for conservation purposes in a given study system. Overall, it appears personality is not yet a fully realized tool for conservation. To apply personality research to conservation problems, we suggest researchers think about where individual differences in behavior may affect conservation outcomes in their system, assess where there are opportunities for repeated measures, and follow the most current methodological guides on quantifying personality.
Aunque la investigación sobre la personalidad animal puede tener usos aplicados, esta propuesta aún no ha sido evaluada mediante el análisis de estudios empíricos que examinan la personalidad animal y la conservación. Realizamos una revisión sistemática de la literatura revisada por pares relacionada con las ciencias de la conservación y la personalidad animal para abordar este vacío en el conocimiento. Los criterios para la inclusión dentro de nuestra revisión incluyen el acceso al texto completo, artículos de investigación primaria y un enfoque relevante en la conservación animal o en la personalidad (es decir, no estudios sobre la personalidad humana). Noventa y dos artículos cumplieron con estos criterios y de ellos resumimos los contextos de conservación, procedimientos de análisis (incluyendo el tamaño de la muestra y de la especie), estrategia analítica, características declaradas de la personalidad (actividad, agresión, audacia, exploración y sociabilidad) y los hallazgos más importantes de cada reporte y sus sugerencias enfocadas en la conservación. Aunque proporcionar evidencias para la repetitividad en el comportamiento es crucial para los estudios de personalidad, la cuantificación de la repetitividad sólo se implementó en la mitad de los reportes. Sin embargo, cada una de las cinco características de la personalidad se investigaron hasta cierto punto dentro de una gama de contextos de la conservación. Los estudios más sólidos en el campo mostraron varianza en cómo la personalidad se relaciona con otras variables de importancia ecológica a través de las especies y los contextos. Además, muchos estudios fueron los primeros intentos del uso de la personalidad con propósitos de conservación en un sistema dado de estudios. En general, parece que la personalidad todavía no es una herramienta completamente realizada para la conservación. Para poder aplicar la investigación sobre la personalidad a los problemas de conservación, sugerimos que los investigadores piensen en dónde pueden afectar las diferencias individuales en el comportamiento a los resultados de la conservación dentro de su sistema, evalúen en dónde hay oportunidades para repetir medidas y sigan las guías metodológicas más actuales sobre la cuantificación de la personalidad.
Subject(s)
Behavior, Animal , Conservation of Natural Resources , Animals , PersonalityABSTRACT
Tool set use is rare in the animal kingdom. Previously, only primates were known to use multiple tools with different functions to achieve a single goal. New research now reveals the convergent evolution of tool set use in wild parrots.
Subject(s)
Parrots , Tool Use Behavior , Animals , Motor Activity , PrimatesABSTRACT
Despite decades of comparative research, how selection shapes the evolution of cognitive traits remains poorly understood [1-3]. Several lines of evidence suggest that natural selection acts on spatial memory in food-caching species [3-6]. However, a link between reproductive fitness and spatial memory ability has yet to be demonstrated in any caching species [1, 3, 6]. Here, we show that memory performance influences reproductive success differentially for males and females in a caching songbird, the New Zealand robin (Petroica longipes). Males' memory performance in a spatial task during winter influenced their subsequent breeding success; individuals with more accurate performance produced more fledglings and independent offspring per nesting attempt. Males with superior memory performance also provided an increased proportion of large prey items to chicks in the nest and spent less time flying while foraging and provisioning. No such effects were found for females. Previous research reveals that trade-offs may constrain selection and act to maintain variation in cognitive traits [7]. The gender dimorphism in the reproductive benefits of robin memory performance suggests an additional role for divergent selection between the sexes in constraining runaway selection on male memory ability [8], ultimately maintaining variation in this cognitive trait.
Subject(s)
Memory , Nesting Behavior , Reproduction , Songbirds/physiology , Animals , Female , Male , New Zealand , Sex FactorsABSTRACT
The requirements of living in social groups, and forming and maintaining social relationships are hypothesized to be one of the major drivers behind the evolution of cognitive abilities. Most empirical studies investigating the relationships between sociality and cognition compare cognitive performance between species living in systems that differ in social complexity. In this review, we ask whether and how individuals benefit from cognitive skills in their social interactions. Cognitive abilities, such as perception, attention, learning, memory, and inhibitory control, aid in forming and maintaining social relationships. We investigate whether there is evidence that individual variation in these abilities influences individual variation in social relationships. We then consider the evolutionary consequences of the interaction between sociality and cognitive ability to address whether bi-directional relationships exist between the two, such that cognition can both shape and be shaped by social interactions and the social environment. In doing so, we suggest that social network analysis is emerging as a powerful tool that can be used to test for directional causal relationships between sociality and cognition. Overall, our review highlights the importance of investigating individual variation in cognition to understand how it shapes the patterns of social relationships.This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'.
Subject(s)
Behavior, Animal , Cognition , Social Behavior , Animals , Biological Variation, IndividualABSTRACT
Hoarding or caching behaviour is a widely-used paradigm for examining a range of cognitive processes in birds, such as social cognition and spatial memory. However, much is still unknown about how caching develops in young birds, especially in the wild. Studying the ontogeny of caching in the wild will help researchers to identify the mechanisms that shape this advantageous foraging strategy. We examined the ontogeny of food caching behaviour in a wild New Zealand passerine, the North Island robin (Petroica longipes). For 12-weeks following fledging, we observed 34 juveniles to examine the development of caching and cache retrieval. Additionally, we compared the caching behaviour of juveniles at 12 weeks post-fledging to 35 adult robins to determine whether juveniles had developed adult-like caching behaviour by this age. Juveniles began caching mealworms shortly after achieving foraging independency. Multivariate analyses revealed that caching rate increased and handling time decreased with increasing age. Juveniles spontaneously began retrieving caches as soon as they had begun to cache and their retrieval rates then remained constant throughout their ensuing development. Likewise, the number of sites used by juveniles did not change with age. Juvenile sex, caregiver sex and the duration of post-fledging parental care did not influence the development of caching, cache retrieval, the number of cache sites used and the time juveniles spent handling mealworms. At 12 weeks post-fledging, juveniles demonstrated levels of caching, cache retrieval and cache site usage that were comparable to adults. However, juvenile prey handling time was still longer than adults. The spontaneous emergence of cache retrieval and the consistency in the number of cache sites used throughout development suggests that these aspects of caching in North Island robins are likely to be innate, but that age and experience have an important role in the development of adult caching behaviours.
Subject(s)
Behavior, Animal/physiology , Feeding Behavior/physiology , Hoarding , Songbirds/physiology , Animals , Female , Male , New ZealandABSTRACT
For the past two decades, behavioural ecologists have documented consistent individual differences in behavioural traits within species and found evidence for animal "personality". It is only relatively recently, however, that increasing numbers of researchers have begun to investigate individual differences in cognitive ability within species. It has been suggested that cognitive test batteries may provide an ideal tool for this growing research endeavour. In fact, cognitive test batteries have now been used to examine the causes, consequences and underlying structure of cognitive performance within and between many species. In this review, we document the existing attempts to develop cognitive test batteries for non-human animals and review the claims that these studies have made in terms of the structure and evolution of cognition. We argue that our current test battery methods could be improved on multiple fronts, from the design of tasks, to the domains targeted and the species tested. Refining and optimising test battery design will provide many benefits. In future, we envisage that well-designed cognitive test batteries may provide answers to a range of exciting questions, including giving us greater insight into the evolution and structure of cognition.
Subject(s)
Cognition , Psychometrics/methods , Animals , Behavior, Animal , Individuality , Psychometrics/trendsABSTRACT
In many species that have bi-parental care, food-sharing males provide vital nutritional resources to their mates during reproduction. However, it is currently unknown whether females can signal specific desires to their mates, or if males can cater to female desire in the wild. Here we investigate whether and how wild male North Island robins (Petroica longipes) respond to changes in their mates' desires and nutritional need when sharing food. We demonstrate that wild female robins' desire for particular foods changes over short time periods; when given the choice between two types of insect larvae, females prefer the type they have not recently eaten. In our experiments, wild male robins preferentially shared the larvae type that their mate was most likely to desire and also increased the quantity of food shared if she had begun incubating. Males catered to their mates' desire when female behaviour was the only cue available to guide their choices. This is the first evidence that females may behaviourally communicate their specific food desires to their mates, enabling males to cater to fine-scale changes in their mates' nutritional requirements in the wild. Such a simple behaviour-reading mechanism has the potential to be widespread among other food-sharing species.
Subject(s)
Food Preferences , Sexual Behavior, Animal , Songbirds/physiology , Animals , Female , MaleABSTRACT
Developing cognitive tasks to reliably quantify individual differences in cognitive ability is critical to advance our understanding of the fitness consequences of cognition in the wild. Several factors may influence individual performance in a cognitive task, with some being unrelated to the cognitive ability that is the target of the test. It is therefore essential to assess how extraneous factors may affect task performance, particularly for those tasks that are frequently used to quantify individual differences in cognitive ability. The current study therefore measured the performance of wild North Island robins in two tasks commonly used to measure individual differences in avian cognition: a novel motor task and a detour reaching task. The robins' performance in the motor task was affected by prior experience; individuals that had previously participated in a similar task that required a different motor action pattern outperformed naïve subjects. By contrast, detour reaching performance was influenced by an individual's body condition, suggesting that energetic state may affect inhibitory control in robins. Designing tasks that limit the influence of past experience and developing means of standardising motivation across animals tested in the wild remain key challenges to improving current measurements of cognitive ability in birds.
Subject(s)
Animals, Wild/physiology , Cognition/physiology , Songbirds/physiology , Animals , Female , Individuality , Male , Motor Activity , Task Performance and AnalysisABSTRACT
Despite recent efforts to characterize innovative individuals within a species, we still know very little about the ontogeny of innovation ability. A number of studies have found that innovation rates are correlated with personality traits, such as neophilia and exploration. Juvenile birds are frequently more neophilic and explorative, yet few studies have found evidence of age-related differences in innovative problem-solving success. Here, we show consistently higher innovation efficiency in juveniles of a wild, omnivorous parrot species across a variety of tasks and contexts. We tested 104 kaka (Nestor meridionalis), ranging in age from four months to 13 years. Twenty-four individuals participated in all three of our problem-solving tasks, two of which involved a familiar feeder and one an entirely novel apparatus. Juveniles were the most efficient problem-solvers in all three tasks. By contrast, the adults' success was context dependent and limited to the novel apparatus, which did not require modification of a pre-learned behavioural response. This suggests greater behavioural flexibility in the juvenile birds, who also showed higher persistence and exploratory diversity than adults. These traits may enable young kaka to discover efficient foraging techniques, which are then maintained throughout adulthood.
Subject(s)
Cognition , Learning , Parrots/physiology , Problem Solving , AnimalsABSTRACT
In recent years, we have investigated the possibility that Eurasian jay food sharing might rely on desire-state attribution. The female's desire for a particular type of food can be decreased by sating her on it (specific satiety) and the food sharing paradigm can be used to test whether the male's sharing pattern reflects the female's current desire. Our previous findings show that the male shares the food that the female currently wants. Here, we consider 3 simpler mechanisms that might explain the male's behavior: behavior reading, lack of self-other differentiation and behavioral rules. We illustrate how we have already addressed these issues and how our food sharing paradigm can be further adapted to answer outstanding questions. The flexibility with which the food sharing paradigm can be applied to rule out alternative mechanisms makes it a useful tool to study desire-state attribution in jays and other species that share food.
ABSTRACT
Following nest destruction, the laying of physiologically committed eggs (eggs that are ovulated, yolked, and making their way through the oviduct) in the nests of other birds is considered a viable pathway for the evolution of obligate interspecific brood parasitism. While intraspecific brood parasitism in response to nest predation has been experimentally demonstrated, this pathway has yet to be evaluated in an interspecific context. We studied patterns of egg laying following experimental nest destruction in captive zebra finches, Taeniopygia guttata, a frequent intraspecific brood parasite. We found that zebra finches laid physiologically committed eggs indiscriminately between nests containing conspecific eggs and nests containing heterospecific eggs (of Bengalese finches, Lonchura striata vars. domestica), despite the con- and heterospecific eggs differing in both size and coloration. This is the first experimental evidence that nest destruction may provide a pathway for the evolution of interspecific brood parasitism in birds.
ABSTRACT
Pilfering corvids use observational spatial memory to accurately locate caches that they have seen another individual make. Accordingly, many corvid cache-protection strategies limit the transfer of visual information to potential thieves. Eurasian jays (Garrulus glandarius) employ strategies that reduce the amount of visual and auditory information that is available to competitors. Here, we test whether or not the jays recall and use both visual and auditory information when pilfering other birds' caches. When jays had no visual or acoustic information about cache locations, the proportion of available caches that they found did not differ from the proportion expected if jays were searching at random. By contrast, after observing and listening to a conspecific caching in gravel or sand, jays located a greater proportion of caches, searched more frequently in the correct substrate type and searched in fewer empty locations to find the first cache than expected. After only listening to caching in gravel and sand, jays also found a larger proportion of caches and searched in the substrate type where they had heard caching take place more frequently than expected. These experiments demonstrate that Eurasian jays possess observational spatial memory and indicate that pilfering jays may gain information about cache location merely by listening to caching. This is the first evidence that a corvid may use recalled acoustic information to locate and pilfer caches.
Subject(s)
Auditory Perception , Feeding Behavior/psychology , Passeriformes , Spatial Memory , Visual Perception , Animals , Female , Male , Passeriformes/physiologyABSTRACT
Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.
Subject(s)
Brain/physiology , Cognition , Primates/physiology , Animals , Biological Evolution , Brain/anatomy & histology , Diet , Humans , Learning , Likelihood Functions , Models, Statistical , Organ Size , Phylogeny , Primates/anatomy & histology , Problem Solving , Selection, Genetic , Social Behavior , Species SpecificityABSTRACT
Humans' predictions of another person's behaviour are regularly influenced by what they themselves might know or want. In a previous study, we found that male Eurasian jays (Garrulus glandarius) could cater for their female partner's current desire when sharing food with her. Here, we tested the extent to which the males' decisions are influenced by their own current desire. When the males' and female's desires matched, males correctly shared the food that was desired by both. When the female's desire differed from their own, the males' decisions were not entirely driven by their own desires, suggesting that males also took the female's desire into account. Thus, the male jays' decisions about their mates' desires are partially biased by their own desire and might be based upon similar processes as those found in humans.
Subject(s)
Feeding Behavior/physiology , Food , Motivation , Social Behavior , Songbirds/physiology , Animals , Female , MaleABSTRACT
Choice by exclusion involves selecting a rewarded stimulus by rejecting alternatives that are unlikely to be rewarded. It has been proposed that in corvids, exclusion is an adaptive specialization for caching that, together with object permanence and observational spatial memory, enhances a bird's ability to keep track of the contents of caches. Thus, caching species are predicted to perform well in tasks requiring exclusion. We tested this prediction by assessing the performance of Eurasian jays (Garrulus glandarius), a highly specialized cacher, in a two-way object choice task in which food was hidden in 1 of 2 cups. Consistent with the corvids' capacity for observational spatial memory, jays were highly accurate when shown the location of the food reward. However, the jays failed to exclude the empty cup when shown its contents. This failure to select the baited cup when shown the empty cup was possibly due to jays attending to the experimenter's movements and erroneously selecting the empty cup by responding to these local enhancement cues. To date, no corvids have been tested in an auditory two-way object choice task. Testing exclusion in the auditory domain requires that a bird use the noise produced when the baited cup is shaken to locate the reward. Although jays chose the baited cup more frequently than predicted by chance, their performance did not differ from trials controlling for the use of conflicting cues provided by the experimenter. Overall, our results provide little support for the hypothesis that caching has shaped exclusion abilities in corvids.
Subject(s)
Auditory Perception/physiology , Behavior, Animal/physiology , Choice Behavior/physiology , Passeriformes/physiology , Reward , Visual Perception/physiology , Animals , Cues , Food/statistics & numerical data , Random Allocation , Task Performance and AnalysisABSTRACT
State-attribution is the ability to ascribe to others an internal life like one's own and to understand that internal, psychological states such as desire, hope, belief, and knowledge underlie others' actions. Despite extensive research, comparative studies struggle to adequately integrate key factors of state-attribution that have been identified by evolutionary and developmental psychology as well as research on empathy. Here, we develop a behavioral paradigm to address these issues and investigate whether male Eurasian jays respond to the changing desire-state of their female partners when sharing food. We demonstrate that males feed their mates flexibly according to the female's current food preference. Critically, we show that the males need to see what the female has previously eaten to know what food she will currently want. Consequently, the males' sharing pattern was not simply a response to their mate's behavior indicating her preference as to what he should share, nor was it a response to the males' own desire-state. Our results raise the possibility that these birds may be capable of ascribing desire to their mates.
Subject(s)
Passeriformes/physiology , Animals , Behavior, Animal , Female , Food , Male , Social BehaviorABSTRACT
Food-storing corvids use many cache-protection and pilfering strategies. We tested whether Eurasian jays (Garrulus glandarius) reduce the transfer of auditory information to a competitor when caching and pilfering. We gave jays a noisy and a quiet substrate to cache in. Compared with when alone, birds cached less in the noisy substrate when with a conspecific that could hear but could not see them caching. By contrast, jays did not change the amount cached in the noisy substrate when they were with a competitor that could see and hear them caching compared with when they were alone. Together, these results suggest that jays reduce auditory information during caching as a cache-protection strategy. By contrast, as pilferers, jays did not attempt to conceal their presence from a cacher and did not prefer a silent viewing perch over a noisy one when observing caching. However, birds vocalized less when watching caching compared with when they were alone, when they were watching a non-caching conspecific or when they were watching their own caches being pilfered. Pilfering jays may therefore attempt to suppress some types of auditory information. Our results raise the possibility that jays both understand and can attribute auditory perception to another individual.