Sometimes slower is better: slow-exploring birds are more sensitive to changes in a vocal discrimination task

Animal personality, defined as consistent individual differences across context and time, has attracted much recent research interest in the study of animal behaviour. More recently, this field has begun to examine how such variation arose and is maintained within populations. The habitat-dependent selection hypothesis, which posits that animals with differing personality types may fare better (i.e. have a fitness advantage) in different habitats, suggests one possible mechanism. In the current experiment, we tested whether slow- and fast-exploring black-capped chickadees (Poecile atricapillus), determined by performance in a novel environment exploration task, perform differentially when the demands of an acoustic operant discrimination (cognitive) task were altered following successful task acquisition. We found that slow-exploring birds learn to reverse previously learned natural category rules more quickly than faster exploring conspecifics. In accordance with the habitat-dependent selection hypothesis, and previous work with great tits (Parus major), a close relative of the black-capped chickadee, our results suggest that fast-exploring birds may perform better in stable, predictable environments where forming a routine is advantageous, while slow-exploring birds are favoured in unstable, unpredictable environments, where task demands often change. Our results also support a hypothesis derived from previous work with great tits; slow-exploring birds may be generally more flexible (i.e. able to modify their behaviour in accordance with changes in environmental stimuli) in some learning tasks.     

Personality and urbanization: behavioural traits and <Emphasis Type="Italic">DRD4</Emphasis> SNP830 polymorphisms in great tits in Barcelona city

Most examples of adaptation to the urban environment relate to plasticity processes rather than to natural selection. Personality, however, defined as consistent individual differences in behaviour related to exploration, caution, and neophobia, is a good behavioural candidate character to study natural selection in relation to the urban habitat due to its heritable variation. The aim of this paper was to analyse variation in personality by comparing urban and forest great tits Parus major using standard tests of exploratory behaviour and boldness. We studied personality in 130 wild great tits captured in Barcelona city and nearby forests and found that urban birds were more explorative and bolder towards a novel object than forest birds. Genotype frequencies of the DRD4 SNP830 polymorphism, a gene region often associated with personality variation, varied significantly between forest and urban birds. Behavioural scores, however, were not correlated with this polymorphism in our population. Exploration scores correlated to boldness for forest birds but not for urban birds. Our findings suggest that the novel selection pressures of the urban environment favour the decoupling of behavioural traits that commonly form behavioural syndromes in the wild.     

Zebra finches are bolder in an asocial, rather than social, context

Despite an expanding interest in animal personalities, the influence of social interactions and sex differences on individual differences in behaviour remains poorly understood. Using the social zebra finch (Taeniopygia guttata), we tested for behavioural differences in exploration of a novel environment and objects, between individuals of both sexes in relation to a social context; the presence of three male companions, three female companions or no companion birds. We predicted that the presence of conspecific companions should result in focal birds reacting to novelty by exploring more extensively because the companion birds contribute to anti-predator vigilance behaviour and because social isolation often causes behavioural inhibition in social species. We found that exploratory behaviour of focal individuals was significantly reduced in the presence of conspecific companions, irrespective of the companion's sex. Moreover, we found a weak trend towards females being more exploratory than males, irrespective of the social context. These results demonstrate the importance of considering the social context in animal personality studies and of exploring sex differences in personalities.     

Winter dialects in the bronzed cowbird and their relationship to breeding-season dialects

Studies of geographical variation in animal signals generally focus on breeding-season behaviour but, in many species, signalling persists throughout the year. In passerine birds, patterns of variation in the nonbreeding season might provide opportunities for vocal learning that have been neglected by a historic focus on breeding-season behaviour. This study provides the first example of dialect variation outside of the breeding season. Quantitative analysis of acoustic similarity showed discrete differences between the songs of bronzed cowbirds, Molothrus aeneus, in four winter flocks. Most songs produced by members of a given flock were classified as belonging to the same dialect. Songs from one of the four winter dialects were indistinguishable from songs recorded in the breeding season in the same region. Depending on migratory patterns, dialects in one season may be a consequence of dialects in the other season, or the two seasonal patterns may be the result of independent social or evolutionary forces. Because the nonbreeding season is an important period of vocal learning in some bird species, winter dialects might limit the range of signals available for individuals to learn to produce. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Contrast versus colour in aposematic signals

Conspicuousness is an important feature of warning coloration. One hypothesis for its function is that it increases signal efficacy by facilitating avoidance learning. An alternative, based on the handicap hypothesis, suggests that the degree of conspicuousness holds information directly about the quality of the prey, and that predators associate and learn about the conspicuousness of the coloration, and not the actual colour pattern. We studied the relative importance of signal contrast and the colours of signals for predator attention during discrimination. We used young chicks, Gallus gallus domesticus, as predators and small blue or red paper cones on either matching or contrasting paper backgrounds as stimuli associated with palatable or unpalatable chick crumbs. In four treatment groups, birds could use either cone and/or background colour, cone colour only, background colour only or cone-to-background contrast as cues for discrimination. Only birds in the contrast treatment failed to learn their discrimination task. Birds that had a choice between cone and background colour as cues used the cone colour and they learned the task faster than did birds that had to use background colour as a cue. The results suggest that birds primarily attend to the colours of signals and disregard contrast in discrimination tasks; they thus fail to support a handicap function of conspicuous aposematic coloration. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Auditory Same/Different Concept Learning and Generalization in Black-Capped Chickadees (Poecile atricapillus)

Abstract concept learning was thought to be uniquely human, but has since been observed in many other species. Discriminating same from different is one abstract relation that has been studied frequently. In the current experiment, using operant conditioning, we tested whether black-capped chickadees (Poecile atricapillus) could discriminate sets of auditory stimuli based on whether all the sounds within a sequence were the same or different from one another. The chickadees were successful at solving this same/different relational task, and transferred their learning to same/different sequences involving novel combinations of training notes and novel notes within the range of pitches experienced during training. The chickadees showed limited transfer to pitches that was not used in training, suggesting that the processing of absolute pitch may constrain their relational performance. Our results indicate, for the first time, that black-capped chickadees readily form relational auditory same and different categories, adding to the list of perceptual, behavioural, and cognitive abilities that make this species an important comparative model for human language and cognition.     

Categorization and discrimination of "chick-a-dee" calls by wild-caught and hand-reared chickadees

Bloomfield and Sturdy [Bloomfield, L.L., Sturdy, C.B. All chick-a-dee calls are not created equally. Part I. Open-ended categorization by sympatric and allopatric chickadees. Behav. Proc., in press] previously reported that black-capped chickadees (Poecile atricapillus) discriminate conspecific from heterospecific (mountain chickadee, P. gambeli) 'chick-a-dee' calls, and their ability to accurately discriminate and classify the calls as belonging to separate species' defined categories was largely unaffected by their prior experience with mountain chickadees and their calls. To further examine the potential influence of experience on discrimination and categorization, we compare wild-caught black-capped chickadees, wild-caught mountain chickadees, and black-capped chickadees hand-reared among either adult laboratory-housed black-capped chickadees or adult laboratory-housed mountain chickadees on a true category/pseudo category chick-a-dee call discrimination task. Irrespective of group assignment, hand-reared birds performed as well as wild-caught birds and did not show a conspecific- or rearing-specific advantage in discrimination, categorization or memorization of chick-a-dee calls. While vocal learning is under the influence of ontogenetic experience, the results derived from the current methods suggest that experience (or a lack thereof) does not affect categorization and memorization abilities.     

Innovative foraging behaviour in birds: what characterizes an innovator?

Innovative foraging behaviour has been observed in many species, but little is known about how novel behaviour emerges or why individuals differ in their propensity to innovate. Here, we investigate these questions by presenting 36 wild-caught adult male Carib grackles (Quiscalus lugubris) with a novel problem-solving task. Twenty birds solved the task (“innovators”) while 16 did not (“non-innovators”). We compared innovators to non-innovators and explored variation in latency to innovate to determine the characteristics of an innovative bird. Innovativeness was not predicted by any morphological trait, but innovators had higher exploration scores and lower object neophobia scores than non-innovators. Within the innovators, latency to innovate was positively correlated with learning speed. Video analysis also revealed a marked difference in the way individuals interacted with the novel apparatus: when innovators contacted the correct part of the apparatus, they continued to do so until they solved the problem. Non-innovators often contacted the correct part of the apparatus, but did not persist in doing so. The importance of obstacle movement cues was confirmed by an experiment where they were manipulated.     

Environmental transmission of a personality trait: foster parent exploration behaviour predicts offspring exploration behaviour in zebra finches

Consistent behavioural differences among individuals are common in many species and can have important effects on offspring fitness. To understand such ‘personality’ variation, it is important to determine the mode of inheritance, but this has been quantified for only a few species. Here, we report results from a breeding experiment in captive zebra finches, Taeniopygia guttata, in which we cross-fostered offspring to disentangle the importance of genetic and non-genetic transmission of behaviour. Genetic and foster-parents’ exploratory type was measured in a novel environment pre-breeding and offspring exploratory type was assessed at adulthood. Offspring exploratory type was predicted by the exploratory behaviour of the foster but not the genetic parents, whereas offspring size was predicted by genetic but not foster-parents’ size. Other aspects of the social environment, such as rearing regime (uni- versus biparental), hatching position, brood size or an individual''s sex did not influence offspring exploration. Our results therefore indicate that non-genetic transmission of behaviour can play an important role in shaping animal personality variation.     

Prosody Discrimination by Songbirds (Padda oryzivora)

In human verbal communication, not only lexical information, but also paralinguistic information plays an important role in transmitting the speakers’ mental state. Paralinguistic information is conveyed mainly through acoustic features like pitch, rhythm, tempo and so on. These acoustic features are generally known as prosody. It is known that some species of birds can discriminate certain aspects of human speech. However, there have not been any studies on the discrimination of prosody in human language which convey different paralinguistic meanings by birds. In the present study, we have shown that the Java sparrow (Padda oryzivora) can discriminate different prosodic patterns of Japanese sentences. These birds could generalize prosodic discrimination to novel sentences, but could not generalize sentence discrimination to those with novel prosody. Moreover, unlike Japanese speakers, Java sparrows used the first part of the utterance as the discrimination cue.     

An evolved spatial memory bias in a nectar-feeding bird?

Studies have shown that nectar-feeding birds more easily learn to avoid a previously rewarding location (to win-shift) than to return to such a location (to win-stay). This pattern has been interpreted as evidence of an evolved adaptation to the fact that nectar is a depleting resource; however, such a conclusion requires ruling out the possibility that this tendency is a consequence of the experience of individual birds, and is more compelling if performance in the memory task reveals sensitivity to detailed features of the spatiotemporal distribution of nectar in the environment. We tested the tendency of captive-reared Regent honeyeaters, Xanthomyza phrygia, a species of nectar-feeding bird, to win-shift or win-stay at different intervisit intervals. The birds generally avoided rewarding locations after a short retention interval (10 min), but returned to these locations after a long retention interval (3 h). This behaviour tracks the replenishment rate of the flowers exploited by this species in the wild, even though the subjects were born and reared in captivity. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Personality drives physiological adjustments and is not related to survival

The evolutionary function and maintenance of variation in animal personality is still under debate. Variation in the size of metabolic organs has recently been suggested to cause and maintain variation in personality. Here, we examine two main underlying notions: (i) that organ sizes vary consistently between individuals and cause consistent behavioural patterns, and (ii) that a more exploratory personality is associated with reduced survival. Exploratory behaviour of captive red knots (Calidris canutus, a migrant shorebird) was negatively rather than positively correlated with digestive organ (gizzard) mass, as well as with body mass. In an experiment, we reciprocally reduced and increased individual gizzard masses and found that exploration scores were unaffected. Whether or not these birds were resighted locally over the 19 months after release was negatively correlated with their exploration scores. Moreover, a long-term mark–recapture effort on free-living red knots with known gizzard masses at capture confirmed that local resighting probability (an inverse measure of exploratory behaviour) was correlated with gizzard mass without detrimental effects on survival. We conclude that personality drives physiological adjustments, rather than the other way around, and suggest that physiological adjustments mitigate the survival costs of exploratory behaviour. Our results show that we need to reconsider hypotheses explaining personality variation based on organ sizes and differential survival.     

Seasonal variability in habitat structure may have shaped acoustic signals and repertoires in the black-capped and boreal chickadees

Many songbird species have evolved multiple vocalizations, or repertoires, that function to communicate various biological signals. More diverse repertoires may have evolved in response to the effects of seasonal variation in habitat structure on signal transmission. Such changes in habitat necessarily occur for migrating species, but they also occur for resident species that occupy deciduous forests. The black-capped chickadee (Poecile atricapillus) possesses a chick-a-dee call and a fee-bee song, but the closely related boreal chickadee (P. borealis) lacks a song. Consistent with the habitat variability hypothesis, the black-capped chickadee possesses a larger repertoire and primarily occupies deciduous forests, whereas the songless boreal chickadee occurs more often in coniferous forests. We explored the ecological basis of this hypothesis by recording audio playbacks of two species in two habitat types during two seasons. Specifically, we played both songs and calls of the black-capped chickadee and calls of the boreal chickadee in deciduous and coniferous habitats, prior to and after leaf-out. We measured attenuation and degradation in re-recorded vocalizations. For black-capped chickadees, the song was less degraded than the call in post-leaf, deciduous forests. The boreal chickadee call attenuated more quickly in all treatments, but maintained its acoustic structure better than both black-capped chickadee vocalizations in coniferous forests. Our results support the hypothesis that variable habitats provided a seasonal transmission benefit for both song and call in the black-capped chickadee, but that the transmission benefit of song is lost in the less variant coniferous forests, which may underlie the absence of a song in the boreal chickadee.     

All "chick-a-dee" calls are not created equally. Part I. Open-ended categorization of chick-a-dee calls by sympatric and allopatric chickadees

Researchers trained 24 black-capped (Poecile atricapillus) and 12 mountain (P. gambeli) chickadees in an operant conditioning task to determine if they use open-ended categorization to classify "chick-a-dee" calls, and whether black-capped chickadees that had experience with mountain chick-a-dee calls (sympatric group) would perform this task differently than inexperienced black-capped chickadees (allopatric group). All experimental birds learned to discriminate between species' call categories faster than within a category (Experiment 1), and subsequently classified novel and original between-category chick-a-dee calls in Experiments 2 and 3 following a change in the category contingency. These results suggest that regardless of previous experience, black-capped and mountain chickadees classify their own and the other species' calls into two distinct, yet open-ended, species-level categories.     

Does reduced social contact affect discrimination of distance cues and individual vocalizations?

For songbirds, experience with conspecific vocalizations during development is important for the ontogeny of both production of vocalizations and perceptual abilities in young oscines. We examined the effects of reduced experience with conspecific vocalizations during development on two auditory perceptual tasks: discrimination of distance cues and discrimination between individual vocalizations in black-capped chickadees, Poecile atricapillus. Discrimination of distance cues was nearly identical in field- and isolate-reared chickadees, but the capacity for memorization of numbers of individual vocalizations was lower in isolate-reared chickadees. We conclude that discrimination of distance cues, and thus distance perception, is probably not learned through experience but is an innate skill. We also conclude that discrimination between many individual vocalizations, a task demanding memorization, is aided by early experience with conspecific vocalizations.Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Call Learning in Black-capped Chickadees (Parus atricapillus): The Role of Experience in the Development of ‘Chick-A-Dee’ Calls

The role of learning in the development of bird vocalizations other than territorial song is not well studied. The well-known role of direct imitation in the development of territorial song potentially masks the effects of other processes in the development of vocal behaviour. The ‘chick-a-dee’ call of black-capped chickadees is a good system in which to investigate more subtle developmental processes because this call is composed of a small number of distinctive note types. These note types may be classified objectively based on a simple set of acoustic variables, allowing for a quantitative assessment of vocal learning. We raised four groups of black-capped chickadees under different degrees of social and acoustic isolation. We then used a multivariate analysis of the acoustic structure of the introductory call notes (‘A-’ ‘B-’ and ‘C-notes’) to determine how similar the notes produced by these hand-reared birds were to the notes of wild birds. Hand-reared chickadees with greater exposure to normal phonology produced notes of all three note types that were more similar to those of wild birds. Regardless of experience, however, all birds produced A-notes that fell within the normal range of those produced by wild birds. By contrast, the development of normal B- and C-notes appears to be more dependent upon experience. These data suggest that learning may play a different role in the development of different phonological units within one vocalization. Our results also illustrate the importance of considering processes other than simple imitation in the development of avian vocalizations.     

Photoperiodic regulation of food storing and hippocampus volume in black-capped chickadees, Poecile atricapillus

In seasonal environments animals organize their behaviour around annual cycles of resource availability. Wild black-capped chickadees are most likely to hoard food in autumn. At this time of year chickadees are also reported to have a larger hippocampus, a brain area important for spatial memory. This study examined how photoperiodic condition affects these seasonal changes. Captive chickadees were exposed to one of three treatments. Photorefractory birds were held on long days (19:5 h light:dark) and had small gonads. Photosensitive birds were held on short days (LD 9:15 h) and also had small gonads. Photostimulated birds were switched from short to long days and quickly entered breeding condition with large gonads. Photosensitive birds (on short days) stored more seeds than photorefractory birds (on long days). Photostimulated birds stored seeds at a high rate when on short days, but reduced storing when transferred to long days. These results indicate that long days inhibit storing regardless of gonadal condition. There were no differences between groups in hippocampal volume, indicating that photoperiod can produce changes in food-storing behaviour without affecting hippocampal size. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.     

Olfactory kin recognition in a songbird

The ability to recognize close relatives in order to cooperate or to avoid inbreeding is widespread across all taxa. One accepted mechanism for kin recognition in birds is associative learning of visual or acoustic cues. However, how could individuals ever learn to recognize unfamiliar kin? Here, we provide the first evidence for a novel mechanism of kin recognition in birds. Zebra finch (Taeniopygia guttata) fledglings are able to distinguish between kin and non-kin based on olfactory cues alone. Since olfactory cues are likely to be genetically based, this finding establishes a neglected mechanism of kin recognition in birds, particularly in songbirds, with potentially far-reaching consequences for both kin selection and inbreeding avoidance.     

Response of Black-Capped Chickadees to House Finch Mycoplasma gallisepticum

Tests for the presence of pathogen DNA or antibodies are routinely used to survey for current or past infections. In diseases that emerge following a host jump estimates of infection rate might be under- or overestimated. We here examine whether observed rates of infection are biased for a non-focal host species in a model system. The bacterium Mycoplasma gallisepticum is a widespread pathogen in house finches (Haemorhous mexicanus), a fringillid finch, but an unknown proportion of individuals of other songbird species are also infected. Our goal is to determine the extent to which detection of M. gallisepticum DNA or antibodies against the bacteria in a non-fringillid bird species is over- or underestimated using black-capped chickadees Poecile atricapillus, a species in which antibodies against M. gallisepticum are frequently detected in free-living individuals. After keeping black-capped chickadees in captivity for 12 weeks, during which period the birds remained negative for M. gallisepticum, four were inoculated with M. gallisepticum and four were sham inoculated in both eyes to serve as negative controls. Simultaneously we inoculated six house finches with the same isolate of M. gallisepticum as a positive control. All inoculated birds of both species developed infections detectable by qPCR in the conjunctiva. For the 6 weeks following inoculation we detected antibodies in all M. gallisepticum-inoculated house finches but in only three of the four M. gallisepticum-inoculated black-capped chickadees. All house finches developed severe eye lesions but none of the black-capped chickadees did. Modeling the Rapid Plate Agglutination test results of black-capped chickadees shows that the rate of false-positive tests would be not more than 3.2%, while the estimated rate of false negatives is 55%. We conclude that the proportion of wild-caught individuals in which we detect M. gallisepticum-specific antibodies using Rapid Plate Agglutination is, if anything, substantially underestimated.     

All "chick-a-dee" calls are not created equally. Part II. Mechanisms for discrimination by sympatric and allopatric chickadees

The 'chick-a-dee' call, common to all members of the genus Poecile, is used by both sexes throughout the year to putatively co-ordinate flock movements and register alarm. In some regions, two or more chickadee species occupy overlapping territories, and therefore it is essential that these sympatric species learn to discriminate between the acoustically similar calls of the species. Previous work from our laboratory has shown that black-capped (P. atricapillus) and mountain chickadees (P. gambeli) discriminate between the species' calls and treat each species' calls as belonging to separate open-ended categories. In the current set of experiments we use an operant conditioning paradigm to gain an understanding of (1) how the birds perform this discrimination and (2) whether birds with different levels of experience with heterospecific calls perform this task differently. We use natural recordings of chick-a-dee calls and perform several manipulations to test the importance of the introductory 'chick-a' portion and the terminal 'dee' portion for discriminating among the calls of the two species. Evidence suggests that birds mainly use the terminal 'dee' portion, as all groups of birds responded similarly to these probe stimuli and control chick-a-dee calls. We propose that the terminal 'dee' portion, consisting of lower frequency notes, is more likely to be resistant to degradation, and therefore a more reliable species-specific marker.