Avian Cognition Research Articles

Cues to individuality in Greylag Goose faces: algorithmic discrimination and behavioral field tests

Cues to individuality, and the corresponding capacity for individual-level discrimination, can allow individually specific investment by conspecifics into offspring, partners, neighbors or competitors. Here we investigated possible cues to individuality via faces in an ancient avian lineage, the Greylag Goose (Anser anser). Konrad Lorenz could famously name each Greylag Goose in ‘his’ flock from a photograph. Confirming this anecdotal observation, we developed facial recognition software that can reliably (~ 97% accuracy) assign a goose face to a goose ID within a database, using bill morphology normalized during photo preparation. To explore conspecific detection of individuality cues, we erected life-size photos of geese and measured subjects’ responses to photos of themselves (unfamiliar goose), their partner, and another flock mate. Geese displayed significantly greater affiliative response to photos of their partners, providing evidence that geese can use two-dimensional images as cues to determine social category (partner/non-partner) and/or individual-level recognition. Our methods provide novel approaches to automatically detect and monitor geese and to test avian cognition. Our approach may also create new opportunities for species monitoring approaches more generally using photographic images and citizen-science engagement.

What do zebra finches learn besides singing? Systematic mapping of the literature and presentation of an efficient associative learning test

The process of learning in birds has been extensively studied, with a focus on species such as pigeons, parrots, chickens, and crows. In recent years, the zebra finch has emerged as a model species in avian cognition, particularly in song learning. However, other cognitive domains such as spatial memory and associative learning could also be critical to fitness and survival, particularly during the intensive juvenile period. In this systematic review, we provide an overview of cognitive studies on zebra finches, with a focus on domains other than song learning. Our findings indicate that spatial, associative, and social learning are the most frequently studied domains, while motoric learning and inhibitory control have been examined less frequently over 30 years of research. All of the 60 studies included in this review were conducted on captive birds, limiting the generalizability of the findings to wild populations. Moreover, only two of the studies were conducted on juveniles, highlighting the need for more research on this critical period of learning. To address this research gap, we propose a high-throughput method for testing associative learning performance in a large number of both juvenile and adult zebra finches. Our results demonstrate that learning can occur in both age groups, thus encouraging researchers to also perform cognitive tests on juveniles. We also note the heterogeneity of methodologies, protocols, and subject exclusion criteria applied by different researchers, which makes it difficult to compare results across studies. Therefore, we call for better communication among researchers to develop standardised methodologies for studying each cognitive domain at different life stages and also in their natural conditions.

A brain atlas of the carrion crow (Corvus corone).

Corvidae, passerine songbirds such as jays, crows, and ravens known as corvids, have become model systems for the study of avian cognition. The superior cognitive capabilities of corvids mainly emerge from a disproportionally large telencephalon found in these species. However, a systematic mapping of the neuroanatomy of the corvid brain, and the telencephalon in particular, is lacking so far. Here, we present a brain atlas of the carrion crow, Corvus corone, with special emphasis on the telencephalic pallium. We applied four staining techniques to brain slices (Nissl, myelin, combination of Nissl and myelin, and tyrosine hydroxylase targeting catecholaminergic neurons). This allowed us to identify brain nuclei throughout the brain and delineate the known pallial subdivisions termed hyperpallium, entopallium, mesopallium, nidopallium, arcopallium, and hippocampal complex. The extent of these subdivisions and brain nuclei are described according to stereotaxic coordinates. In addition, 3D depictions of pallial regions were reconstructed from these slices. While the overall organization of the carrion crow's brain matches other songbird brains, the relative proportions and expansions of associative pallial areas differ considerably in agreement with enhanced cognitive skills found in corvids. The presented global organization of the crow brain in stereotaxic coordinates will help to guide future neurobiological studies in corvids.

Avian cognition and the implications for captive parrot welfare

AbstractPreviously assumed to be unintelligent animals, many species of birds display high levels of cognition and may even possess conscious awareness. In particular, both corvids and parrots have been the focus of cognitive research including studies on problem-solving, social intelligence, and sentience. Despite their similar neural architecture and cognitive abilities, the laws regarding these two families of birds differ greatly. In the United States, it is illegal to keep corvids as pets. Parrots, however, are one of the most commonly kept pets in America, although their care in captivity remains largely unregulated. Captive parrots suffer from a number of medical and psychological issues and experience high rates of neglect and abandonment. At the same time, wild parrot populations are dwindling due both to habitat loss and capture for the pet trade. This review examines the novel findings on avian cognition and applies them to the potential ethical implications of keeping parrots in captivity. In addition, suggestions for future directions are presented, including the development of legislation to protect captive and wild parrots.

Wild skuas can use acoustic cues to locate hidden food.

Among animals, the visual acuity of several predatory bird species is probably the most outstanding. This, and the ease with which visually based tasks are administered, has led researchers to predominantly use the visual modality when studying avian cognition. Some wild skua populations routinely use acoustic cues emitted by their prey during foraging. In this study, we thus assessed whether this species was able to locate hidden food using acoustic cues alone (training phase). During the subsequent test phase, we investigated the capacity of successful individuals to choose the correct baited container in four conditions: (i) baited (shaking the baited container), (ii) full information (shaking both containers), (iii) exclusion (shaking the empty container), and (iv) control (shaking neither container). Four out of ten subjects succeeded in locating the baited container in the training phase. During the test phase, most subjects chose the baited container significantly more than the empty container in the baited and full information condition, while their performance was at chance level in the control condition. When no sound emanated from the empty container in the exclusion condition, one out of four skuas chose the baited container with more accuracy than predicted by chance. As this bird chose correctly on the first trial and during the first five trials, its performance is unlikely due to learning processes (learning to exclude the empty container). Although further tests are necessary to draw firm conclusions, our results open the way for assessing further this species' reasoning abilities in the wild.

ManyBirds: A multi-site collaborative Open Science approach to avian cognition and behavior research

Comparative cognitive and behavior research aims to investigate cognitive evolution by comparing performance in different species to understand how these abilities have evolved. Ideally, this requires large and diverse samples; however, these can be difficult to obtain by single labs or institutions, leading to potential reproducibility and generalization issues with small, less representative samples. To help mitigate these issues, we are establishing a multi-site collaborative Open Science approach called ManyBirds, with the aim of providing new insight into the evolution of avian cognition and behavior through large-scale comparative studies, following the lead of exemplary ManyPrimates, ManyBabies and ManyDogs projects. Here, we outline a) the replicability crisis and why we should study birds, including the origin of modern birds, avian brains and convergent evolution of cognition; b) the current state of the avian cognition field, including a ‘snapshot’ review; c) the ManyBirds project, with plans, infrastructure, limitations, implications and future directions. In sharing this process, we hope that this may be useful for other researchers in devising similar projects in other taxa, like non-avian reptiles or mammals, and to encourage further collaborations with ManyBirds and related ManyX projects. Ultimately, we hope to promote collaboration between ManyX projects to allow for wider investigation of the evolution of cognition across all animals, including potentially humans.

Vultures as an overlooked model in cognitive ecology.

Despite important recent advances in cognitive ecology, our current understanding of avian cognition still largely rests on research conducted on a few model taxa. Vultures are an ecologically distinctive group of species by being the only obligate carrion consumers across terrestrial vertebrates. Their unique scavenging lifestyle suggests they have been subject to particular selective pressures to locate scarce, unpredictable, ephemeral, and nutritionally challenging food. However, substantial variation exists among species in diet, foraging techniques and social structure of populations. Here, we provide an overview of the current knowledge on vulture cognition through a comprehensive literature review and a compilation of our own observations. We find evidence for a variety of innovative foraging behaviors, scrounging tactics, collective problem-solving abilities and tool-use, skills that are considered indicative of enhanced cognition and that bear clear connections with the eco-social lifestyles of species. However, we also find that the cognitive basis of these skills remain insufficiently studied, and identify new research areas that require further attention in the future. Despite these knowledge gaps and the challenges of working with such large animals, we conclude that vultures may provide fresh insight into our knowledge of the ecology and evolution of cognition.

Use of appeasement display and recruitment by an adult Striated Caracara (Phalcoboenus australis) to overcome territorial defense

Adult animals across many taxa use appeasement signaling to minimize or avoid costly conflict in social settings by jointly communicating their consent to defer and an interest to remain. When foraging, however, appeasement may not be enough to gain access to a resource controlled by a dominant conspecific. In this case, conspecific recruitment can shift the social dynamic, so the resource becomes accessible to all. Striated Caracara (Phalcoboenus australis) are Near Threatened scavenging falconids that breed in high densities on the extreme southern coasts of South America and the Falkland Islands. While juvenile caracaras recruit other caracaras to concentrated food resources, neither recruitment nor appeasement has been reported in adults. Here we describe a female adult caracara that appeared to use both appeasement signaling and recruitment to access food in another pair's defended territory on New Island, Falkland Islands. Appeasement and recruitment calls are one of several behavioral parallels that researchers have noted among Striated Caracara, Common Raven (Corvus corax), and Kea (Nestor notabilis). Although falconids are not typically considered in comparative studies of avian cognition and social behavior, we suggest that caracaras merit further attention, especially given their relationship to parrots in the clade Eufalconimorphae.

Persistent fine-tuning of egg rejection based on parasitic timing in a cuckoo host even after relaxation of parasitism pressure

Egg rejection is one of the most effective defenses to avoid avian brood parasites by hosts, and reflects avian cognition during parasite-host coevolution. However, egg rejection varies with different populations and species, or under different contexts. Here we studied the egg recognition behavior in a non-parasitized population of the red-whiskered bulbul (Pycnonotus jocosus), which has been recorded as a host of the banded bay cuckoo (Cacomantis sonneratii). By comparing its egg rejection frequency and latency between egg-laying and egg-incubation stages with a variety of nest ages, which represent different costs of cuckoo parasitism, the results show that the hosts rejected parasite eggs more frequently in the egg-laying stage than in the egg-incubation stage without a difference in latency, and accepted parasite eggs with an increase of nest age. These findings indicated that the hosts are able to adjust the intensity of their anti-parasitic responses according to the parasitic timing. A relaxation of parasitism risk and the tradeoff between parasitism risk and egg rejection cost may contribute to explaining our results.

Convergent evolution of complex cognition: Insights from the field of avian cognition into the study of self-awareness.

Pioneering research on avian behaviour and cognitive neuroscience have highlighted that avian species, mainly corvids and parrots, have a cognitive tool kit comparable with apes and other large-brained mammals, despite conspicuous differences in their neuroarchitecture. This cognitive tool kit is driven by convergent evolution, and consists of complex processes such as casual reasoning, behavioural flexibility, imagination, and prospection. Here, we review experimental studies in corvids and parrots that tested complex cognitive processes within this tool kit. We then provide experimental examples for the potential involvement of metacognitive skills in the expression of the cognitive tool kit. We further expand the discussion of cognitive and metacognitive abilities in avian species, suggesting that an integrated assessment of these processes, together with revised and multiple tasks of mirror self-recognition, might shed light on one of the most highly debated topics in the literature-self-awareness in animals. Comparing the use of multiple assessments of self-awareness within species and across taxa will provide a more informative, richer picture of the level of consciousness in different organisms.

Macphail's Null Hypothesis of Vertebrate Intelligence: Insights From Avian Cognition.

Macphail famously criticized two foundational assumptions that underlie the evolutionary approach to comparative psychology: that there are differences in intelligence across species, and that intelligent behavior in animals is based on more than associative learning. Here, we provide evidence from recent work in avian cognition that supports both these assumptions: intelligence across species varies, and animals can perform intelligent behaviors that are not guided solely by associative learning mechanisms. Finally, we reflect on the limitations of comparative psychology that led to Macphail’s claims and suggest strategies researchers can use to make more advances in the field.

Using 3D modelling and printing to study avian cognition from different geometric dimensions.

Studying animal cognition is meaningful because it helps us understand how animals adapt to the natural environment. Many birds build nests, clean their nests and reject foreign objects from their nests, which provide an optimal opportunity for studying their cognition toward foreign objects in nests. However, hand-made models used in previous studies have many deficiencies that considerably constrain our capacity to understand the evolution of avian cognition of foreign objects because they are unquantifiable and dependent on different features. We established a 3D modelling and printing method to manipulate one geometric dimension of a model while controlling for others, which allowed us to investigate avian cognition for different dimensions independently. Here we introduce this method, conduct an empirical study as an example, and discuss its applications to further studies.

Inference by exclusion in the red-tailed black cockatoo (Calyptorhynchus banksii).

Inference by exclusion is the ability to select a given option by excluding the others. When designed appropriately, tests of this ability can reveal choices that cannot be explained by associative processes. Over the past decade, exclusion reasoning has been explored in several non-human taxonomic groups, including birds, mainly in Corvids and Parrots. To increase our understanding of the taxonomic distribution of exclusion reasoning and, therefore, its evolution, we investigated exclusion performances in red-tailed black cockatoos (Calyptorhynchus banksii), an Australian relative of the Goffin cockatoo (Cacatua goffini), using a food-finding task. Cockatoos were required to find a food item hidden in 1 of the 2 experimenter's hands. Following training sessions in which they reliably selected the closed baited hand they had just been shown open, each individual was tested on 4 different conditions. Critical to demonstrating exclusion reasoning was the condition in which they were shown the empty hand and then offered a choice of both closed hands. The performance of all birds was above chance on all experimental conditions but not on an olfactory and/or cuing control condition. The results suggest that the birds might be able to infer by exclusion, although an explanation based on rule learning cannot be excluded. This first experiment in red-tailed black cockatoo highlights the potential of this species as a model to study avian cognition and paves the pathway for future investigations.

A Facet Theory Analysis of the Structure of Cognitive Performance in New Zealand Robins (Petroica longipes)

In this report we analyse the cognitive performance of New Zealand Robins (Petroica longipes) using facet theory, smallest space analysis (SSA) and partial order scalogram analysis (POSA). The data set we analyse was originally subjected to principle component analysis in order to develop a test-battery for avian cognitive performance. We extend these analyses by proposing a two facet rather than a single component solution using SSA and we characterize individual birds by their scores on all tasks using POSA. We note problems with the small sample size and call for our exploratory analyses to be replicated using a larger sample of birds and for the development of further test items using the facet theory’s tool the mapping sentence. We suggest that facet theory and the mapping sentences are research approaches suitable for conceiving, designing, analysing and developing theory that may be used within avian cognitive research. We conclude by proposing a mapping sentence for avian cognition, which forms an adaptable template for future avian cognition research.

Birds of a feather? Parrot and corvid cognition compared

Abstract The last several decades of research on avian cognition have revealed surprising parallels between the abilities of birds — most notably corvids — and great apes. Parrots, albeit far less studied, are cited alongside corvids as “feathered apes”, but are these two taxa really that similar cognitively? In this review we aim to take a step back and present the broader picture, focusing on areas where there is now data from both parrots and corvids to facilitate first comparisons on a somewhat wider scale. By charting these birds’ performance in cognitive tasks, in many of which corvids perform on par with primates, we hope to highlight understudied areas and promising directions for future research. In reviewing the literature, the general pattern that emerges shows that different corvid and parrot species indeed perform similarly in a range of cognitive tasks to the extent that one may call them “feathered apes”.

Exposure to dietary mercury alters cognition and behavior of zebra finches.

Environmental stressors can negatively affect avian cognitive abilities, potentially reducing fitness, for example by altering response to predators, display to mates, or memory of locations of food. We expand on current knowledge by investigating the effects of dietary mercury, a ubiquitous environmental pollutant and known neurotoxin, on avian cognition. Zebra finches Taeniopygia guttata were dosed for their entire lives with sub-lethal levels of mercury, at the environmentally relevant dose of 1.2 parts per million. In our first study, we compared the dosed birds with controls of the same age using tests of three cognitive abilities: spatial memory, inhibitory control, and color association. In the spatial memory assay, birds were tested on their ability to learn and remember the location of hidden food in their cage. The inhibitory control assay measured their ability to ignore visible but inaccessible food in favor of a learned behavior that provided the same reward. Finally, the color association task tested each bird’s ability to associate a specific color with the presence of hidden food. Dietary mercury negatively affected spatial memory ability but not inhibitory control or color association. Our second study focused on three behavioral assays not tied to a specific skill or problem-solving: activity level, neophobia, and social dominance. Zebra finches exposed to dietary mercury throughout their lives were subordinate to, and more active than, control birds. We found no evidence that mercury exposure influenced our metric of neophobia. Together, these results suggest that sub-lethal exposure to environmental mercury selectively harms neurological pathways that control different cognitive abilities, with complex effects on behavior and fitness.

Song learning and cognitive ability are not consistently related in a songbird.

Learned aspects of song have been hypothesized to signal cognitive ability in songbirds. We tested this hypothesis in hand-reared song sparrows (Melospiza melodia) that were tutored with playback of adult songs during the critical period for song learning. The songs developed by the 19 male subjects were compared to the model songs to produce two measures of song learning: the proportion of notes copied from models and the average spectrogram cross-correlation between copied notes and model notes. Song repertoire size, which reflects song complexity, was also measured. At 1year of age, subjects were given a battery of five cognitive tests that measured speed of learning in the context of a novel foraging task, color association, color reversal, detour-reaching, and spatial learning. Bivariate correlations between the three song measures and the five cognitive measures revealed no significant associations. As in other studies of avian cognition, different cognitive measures were for the most part not correlated with each other, and this result remained true when 22 hand-reared female song sparrows were added to the analysis. General linear mixed models controlling for effects of neophobia and nest of origin indicated that all three song measures were associated with better performance on color reversal and spatial learning but were associated with worse performance on novel foraging and detour-reaching. Overall, the results do not support the hypothesis that learned aspects of song signal cognitive ability.

Innovativeness and the effects of urbanization on risk-taking behaviors in wild Barbados birds.

The effects of urbanization on avian cognition remain poorly understood. Risk-taking behaviors like boldness, neophobia and flight distance are thought to affect opportunism and innovativeness, and should also vary with urbanization. Here, we investigate variation in risk-taking behaviors in the field in an avian assemblage of nine species that forage together in Barbados and for which innovation rate is known from previous work. We predicted that birds from highly urbanized areas would show more risk-taking behavior than conspecifics from less urbanized parts of the island and that the differences would be strongest in the most innovative of the species. Overall, we found that urban birds are bolder, less neophobic and have shorter flight distances than their less urbanized conspecifics. Additionally, we detected between-species differences in the effect of urbanization on flight distance, more innovative species showing smaller differences in flight distance between areas. Our results suggest that, within successful urban colonizers, species differences in innovativeness may affect the way species change their risk-taking behaviors in response to the urban environment.

Nest sanitation elicits egg discrimination in cuckoo hosts

Nest sanitation is a nearly universal behavior in birds, while egg discrimination is a more specific adaptation that has evolved to counter brood parasitism. These two behaviors are closely related with nest sanitation being the ancestral behavior, and it has been hypothesized to constitute a preadaptation for egg discrimination. However, previous studies found little evidence to support this hypothesis. Here, we conducted an empirical test of the association between nest sanitation and egg discrimination in the barn swallow (Hirundo rustica) by inserting a single non-mimetic model egg or a non-mimetic model egg plus half a peanut shell into host nests. Compared to the rejection rate of single model eggs, barn swallows significantly increased egg rejection frequency if a half peanut shell was simultaneously introduced. Our result for the first time shows the impact of nest sanitation on egg discrimination and demonstrates that nest sanitation can elicit egg discrimination in hosts of brood parasites. This study provided evidence for nest sanitation being a preadaptation to egg discrimination by facilitating egg rejection, thereby significantly advancing our understanding of avian cognition of foreign objects. Furthermore, we suggest that egg discrimination behavior in many accepters and intermediate rejecters may be lost or diluted. Such egg discrimination can be elicited and restored after nest sanitation, implying a sensitive and rapid phenotypic response to increased risk of parasitism. Our study offers a novel perspective for investigating the role of so-called intermediate rejecter individuals or species in the long-term coevolutionary cycle between brood parasites and their hosts.

Avian cognition: examples of sophisticated capabilities in space and song.

Although birds have traditionally and colloquially been considered less cognitively complex than mammals, and especially primates, more recent research has consistently refuted these assumptions. We argue that the impressive abilities of birds to navigate and communicate require considerable information-processing capabilities. These capacities include collecting, organizing, and selecting from a wide variety of navigational cues to orient toward and find a goal location in the spatial domain, and utilizing open-ended categorization and possibly even abstract reasoning to discriminate species-specific acoustic features of songs and calls. Furthermore, these abilities may be present across many avian species, providing evidence for domain-general cognitive facilities. We provide examples of processes in spatial learning and communication in birds, and locate them within the general literature, as evidence that the term 'bird-brain' should not be considered a pejorative.