The origins of musicality in the motion of primates.

Animals communicate acoustically to report location, identity, and emotive state to conspecifics. Acoustic signals can also function as displays to potential mates and as territorial advertisement. Music and song are terms often reserved only for humans and birds, but elements of both forms of acoustic display are also found in non-human primates. While culture, bonding, and side-effects all factor into the emergence of musicality, biophysical insights into what might be signaled by specific acoustic features are less well understood. OBJECTIVES: Here we probe the origins of musicality by evaluating the links between musical features (structural complexity, rhythm, interval, and tone) and a variety of potential ecological drivers of its evolution across primate species. Alongside other hypothesized causes (e.g. territoriality, sexual selection), we evaluated the hypothesis that perilous arboreal locomotion might favor musical calling in primates as a signal of capacities underlying spatio-temporal precision in motor tasks. MATERIALS AND METHODS: We used musical features found in spectrographs of vocalizations of 58 primate species and corresponding measures of locomotion, diet, ranging, and mating. Leveraging phylogenetic information helped us impute missing data and control for relatedness of species while selecting among candidate multivariate regression models. RESULTS: Results indicated that rapid inter-substrate arboreal locomotion is highly correlated with several metrics of music-like signaling. Diet, alongside mate-choice and range size, emerged as factors that also correlated with complex calling patterns. DISCUSSION: These results support the hypothesis that musical calling may function as a signal, to neighbors or potential mates, of accuracy in landing on relatively narrow targets.

American crows that excel at tool use activate neural circuits distinct from less talented individuals.

Tools enable animals to exploit and command new resources. However, the neural circuits underpinning tool use and how neural activity varies with an animal's tool proficiency, are only known for humans and some other primates. We use 18F-fluorodeoxyglucose positron emission tomography to image the brain activity of naïve vs trained American crows (Corvus brachyrhynchos) when presented with a task requiring the use of stone tools. As in humans, talent affects the neural circuits activated by crows as they prepare to execute the task. Naïve and less proficient crows use neural circuits associated with sensory- and higher-order processing centers (the mesopallium and nidopallium), while highly proficient individuals increase activity in circuits associated with motor learning and tactile control (hippocampus, tegmentum, nucleus basorostralis, and cerebellum). Greater proficiency is found primarily in adult female crows and may reflect their need to use more cognitively complex strategies, like tool use, to obtain food.

Traffic noise inhibits inhibitory control in wild-caught songbirds.

Anthropogenic noise is ubiquitous across environments and can have negative effects on animals, ranging from physiology to community structure. Recent work with captive-bred zebra finches demonstrated that traffic noise also affects cognitive performance. We examined whether these results extend to animals that have experienced noise in the wild. We collected black-capped chickadees from areas frequently exposed to road traffic noise and tested them on a detour reaching task, a commonly used measure of inhibitory control. Those chickadees exposed to traffic noise playback had much lower performance on the task than control birds, indicating that noise negatively impacts inhibitory control. These data corroborate previous findings in lab-reared zebra finches. Furthermore, these results suggest that prior experience with traffic noise is not sufficient for animals to habituate to noise and overcome its negative effects on cognitive performance. Instead, noise-induced cognitive effects might have broad impacts on animal species living in noise-polluted habitats.

Links between personality traits and problem-solving performance in zebra finches (Taeniopygia guttata).

Consistent individual differences in behaviour across time or contexts (i.e. personality types) have been found in many species and have implications for fitness. Likewise, individual variation in cognitive abilities has been shown to impact fitness. Cognition and personality are complex, multidimensional traits. However, previous work has generally examined the connection between a single personality trait and a single cognitive ability, yielding equivocal results. Links between personality and cognitive ability suggest that behavioural traits coevolved and highlight their nuanced connections. Here we examined individuals' performance on multiple personality tests and repeated problem-solving tests (each measuring innovative performance). We assessed behavioural traits (dominance, boldness, activity, risk-taking, aggressiveness and obstinacy) in 41 captive zebra finches. Birds' scores for boldness and obstinacy were consistent over two years. We also examined whether personality correlated with problem-solving performance on repeated tests. Our results indicate that neophobia, dominance and obstinacy were related to successful solving, and less dominant, more obstinate birds solved the tasks quicker on average. Our results indicate the importance of examining multiple measures over a long period. Future work that identifies links between personality and innovation in non-model organisms may elucidate the coevolution of these two forms of individual differences.

American Crow Brain Activity in Response to Conspecific Vocalizations Changes When Food Is Present.

Social interaction among animals can occur under many contexts, such as during foraging. Our knowledge of the regions within an avian brain associated with social interaction is limited to the regions activated by a single context or sensory modality. We used 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) to examine American crow (Corvus brachyrhynchos) brain activity in response to conditions associated with communal feeding. Using a paired approach, we exposed crows to either a visual stimulus (the sight of food), an audio stimulus (the sound of conspecifics vocalizing while foraging) or both audio/visual stimuli presented simultaneously and compared to their brain activity in response to a control stimulus (an empty stage). We found two regions, the nucleus taenia of the amygdala (TnA) and a medial portion of the caudal nidopallium, that showed increased activity in response to the multimodal combination of stimuli but not in response to either stimulus when presented unimodally. We also found significantly increased activity in the lateral septum and medially within the nidopallium in response to both the audio-only and the combined audio/visual stimuli. We did not find any differences in activation in response to the visual stimulus by itself. We discuss how these regions may be involved in the processing of multimodal stimuli in the context of social interaction.

On reappearance and complexity in musical calling.

Music is especially valued in human societies, but music-like behavior in the form of song also occurs in a variety of other animal groups including primates. The calling of our primate ancestors may well have evolved into the music of modern humans via multiple selective scenarios. But efforts to uncover these influences have been hindered by the challenge of precisely defining musical behavior in a way that could be more generally applied across species. We propose an acoustic focused reconsideration of "musicality" that could help enable independent inquiry into potential ecological pressures on the evolutionary emergence of such behavior. Using published spectrographic images (n = 832 vocalizations) from the primate vocalization literature, we developed a quantitative formulation that could be used to help recognize signatures of human-like musicality in the acoustic displays of other species. We visually scored each spectrogram along six structural features from human music-tone, interval, transposition, repetition, rhythm, and syllabic variation-and reduced this multivariate assessment into a concise measure of musical patterning, as informed by principal components analysis. The resulting acoustic reappearance diversity index (ARDI) estimates the number of different reappearing syllables within a call type. ARDI is in concordance with traditional measures of bird song complexity yet more readily identifies shorter, more subtly melodic primate vocalizations. We demonstrate the potential utility of this index by using it to corroborate several origins scenarios. When comparing ARDI scores with ecological features, our data suggest that vocalizations with diversely reappearing elements have a pronounced association with both social and environmental factors. Musical calls were moderately associated with wooded habitats and arboreal foraging, providing partial support for the acoustic adaptation hypothesis. But musical calling was most strongly associated with social monogamy, suggestive of selection for constituents of small family-sized groups by neighboring conspecifics. In sum, ARDI helps construe musical behavior along a continuum, accommodates non-human musicality, and enables gradualistic co-evolutionary paths between primate taxa-ranging from the more inhibited locational calls of archaic primates to the more exhibitional displays of modern apes.

Traffic noise inhibits cognitive performance in a songbird.

Noise pollution is commonly associated with human environments and mounting evidence indicates that noise has a variety of negative effects on wildlife. Noise has also been linked to cognitive impairment in humans and because many animals use cognitively intensive processes to overcome environmental challenges, noise pollution has the potential to interfere with cognitive function in animals living in urban areas or near roads. We experimentally examined how road traffic noise impacts avian cognitive performance by testing adult zebra finches (Taeniopygia guttata) on a battery of foraging tasks in the presence or absence of traffic noise playback. Here, we show that traffic noise reduces cognitive performance, including inhibitory control, motor learning, spatial memory and social learning, but not associative colour learning. This study demonstrates a novel mechanism through which anthropogenic noise can impact animals, namely through cognitive interference, and suggests that noise pollution may have previously unconsidered consequences for animals.

Breeding season length predicts duet coordination and consistency in Neotropical wrens (Troglodytidae).

Many animals produce coordinated signals, but few are more striking than the elaborate male-female vocal duets produced by some tropical songbirds. Yet, little is known about the factors driving the extreme levels of vocal coordination between mated pairs in these taxa. We examined evolutionary patterns of duet coordination and their potential evolutionary drivers in Neotropical wrens (Troglodytidae), a songbird family well known for highly coordinated duets. Across 23 wren species, we show that the degree of coordination and precision with which pairs combine their songs into duets varies by species. This includes some species that alternate their song phrases with exceptional coordination to produce rapidly alternating duets that are highly consistent across renditions. These highly coordinated, consistent duets evolved independently in multiple wren species. Duet coordination and consistency are greatest in species with especially long breeding seasons, but neither duet coordination nor consistency are correlated with clutch size, conspecific abundance or vegetation density. These results suggest that tightly coordinated duets play an important role in mediating breeding behaviour, possibly by signalling commitment or coalition of the pair to mates and other conspecifics.

Brain activity underlying American crow processing of encounters with dead conspecifics.

Animals utilize a variety of auditory and visual cues to navigate the landscape of fear. For some species, including corvids, dead conspecifics appear to act as one such visual cue of danger, and prompt alarm calling by attending conspecifics. Which brain regions mediate responses to dead conspecifics, and how this compares to other threats, has so far only been speculative. Using 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) we contrast the metabolic response to visual and auditory cues associated with a dead conspecific among five a priori selected regions in the American crow (Corvus brachyrhynchos) brain: the hippocampus, nidopallium caudolaterale, striatum, amygdala, and the septum. Using a repeated-measures, fully balanced approach, we exposed crows to four stimuli: a dead conspecific, a dead song sparrow (Melospiza melodia), conspecific alarm calls given in response to a dead crow, and conspecific food begging calls. We find that in response to observations of a dead crow, crows show significant activity in areas associated with higher-order decision-making (NCL), but not in areas associated with social behaviors or fear learning. We do not find strong differences in activation between hearing alarm calls and food begging calls; both activate the NCL. Lastly, repeated exposures to negative stimuli had a marginal effect on later increasing the subjects' brain activity in response to control stimuli, suggesting that crows might quickly learn from negative experiences.

Nuthatches vary their alarm calls based upon the source of the eavesdropped signals.

Animal alarm calls can contain detailed information about a predator's threat, and heterospecific eavesdropping on these signals creates vast communication networks. While eavesdropping is common, this indirect public information is often less reliable than direct predator observations. Red-breasted nuthatches (Sitta canadensis) eavesdrop on chickadee mobbing calls and vary their behaviour depending on the threat encoded in those calls. Whether nuthatches propagate this indirect information in their own calls remains unknown. Here we test whether nuthatches propagate direct (high and low threat raptor vocalizations) or indirect (high and low threat chickadee mobbing calls) information about predators differently. When receiving direct information, nuthatches vary their mobbing calls to reflect the predator's threat. However, when nuthatches obtain indirect information, they produce calls with intermediate acoustic features, suggesting a more generic alarm signal. This suggests nuthatches are sensitive to the source and reliability of information and selectively propagate information in their own mobbing calls.

A duetting perspective on avian song learning.

Avian song learning has a rich history of study and has become the preeminent system for understanding the ontogeny of vocal communication in animals. Song learning in birds has many parallels with human language learning, ranging from the neural mechanisms involved to the importance of social factors in shaping signal acquisition. While much has been learned about the process of song learning, virtually all of the research done to date has focused on temperate species, where often only one sex (the male) sings. Duetting species, in which both males and females learn to sing and learn to combine their songs into temporally coordinated joint displays, could provide many insights into the processes by which vocal learning takes place. Here we highlight three key features of song learning-neuroendocrine control mechanisms, timing and life history stages of song acquisition, and the role of social factors in song selection and use-that have been elucidated from species where only males sing, and compare these with duetting species. We summarize what is known about song learning in duetting species and then provide several suggestions for fruitful directions for future research. We suggest that focusing research efforts on duetting species could significantly advance our understanding of vocal learning in birds and further cement the importance of avian species as models for understanding human conversations and the processes of vocal learning more broadly.

Mobbing.

Carlson and colleagues introduce mobbing an anti-predator behaviour found in many animals.

Stress hormones, social associations and song learning in zebra finches.

The use of information provided by others is a common short-cut adopted to inform decision-making. However, instead of indiscriminately copying others, animals are often selective in what, when and whom they copy. How do they decide which 'social learning strategy' to use? Previous research indicates that stress hormone exposure in early life may be important: while juvenile zebra finches copied their parents' behaviour when solving novel foraging tasks, those exposed to elevated levels of corticosterone (CORT) during development copied only unrelated adults. Here, we tested whether this switch in social learning strategy generalizes to vocal learning. In zebra finches, juvenile males often copy their father's song; would CORT-treated juveniles in free-flying aviaries switch to copying songs of other males? We found that CORT-treated juveniles copied their father's song less accurately as compared to control juveniles. We hypothesized that this could be due to having weaker social foraging associations with their fathers, and found that sons that spent less time foraging with their fathers produced less similar songs. Our findings are in line with a novel hypothesis linking early-life stress and social learning: early-life CORT exposure may affect social learning indirectly as a result of the way it shapes social affiliations.This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'.

Animal Communication: Learning by Listening about Danger.

A variety of animals eavesdrop and learn to use other species' alarm calls to avoid predators. Superb fairy-wrens, when hearing unfamiliar calls together with known alarm calls, can learn to associate these new calls with danger.

Early development of vocal interaction rules in a duetting songbird.

Exchange of vocal signals is an important aspect of animal communication. Although birdsong is the premier model for understanding vocal development, the development of vocal interaction rules in birds and possible parallels to humans have been little studied. Many tropical songbirds engage in complex vocal interactions in the form of duets between mated pairs. In some species, duets show precise temporal coordination and follow rules (duet codes) governing which song type one bird uses to reply to each of the song types of its mate. We determined whether these duetting rules are acquired during early development in canebrake wrens. Results show that juveniles acquire a duet code by singing with a mated pair of adults and that juveniles gradually increase their fidelity to the code over time. Additionally, we found that juveniles exhibit poorer temporal coordination than adults and improve their coordination as time progresses. Human turn-taking, an analogous rule to temporal coordination, is learned during early development. We report that the ontogeny of vocal interaction rules in songbirds is analogous to that of human conversation rules.

Sparrowhawk movement, calling, and presence of dead conspecifics differentially impact blue tit (Cyanistes caeruleus) vocal and behavioral mobbing responses.

ABSTRACT: Many animals alter their anti-predator behavior in accordance to the threat level of a predator. While much research has examined variation in mobbing responses to different predators, few studies have investigated how anti-predator behavior is affected by changes in a predator's own state or behavior. We examined the effect of sparrowhawk (Accipiter nisus) behavior on the mobbing response of wild blue tits (Cyanistes caeruleus) using robotic taxidermy sparrowhawks. We manipulated whether the simulated predator moved its head, produced vocalizations, or held a taxidermy blue tit in its talons. When any sparrowhawk model was present, blue tits decreased foraging and increased anti-predator behavior and vocalizations. Additionally, each manipulation of the model predator's state (moving, vocalizing, or the presence of a dead conspecific) impacted different types of blue tit anti-predator behavior and vocalizations. These results indicate that different components of mobbing vary according to the specific state of a given predator-beyond its presence or absence-and suggest that each might play a different role in the overall mobbing response. Last, our results indicate that using more life-like predator stimuli-those featuring simple head movements and audio playback of vocalizations-changes how prey respond to the predator; these 'robo-raptor' models provide a powerful tool to provide increased realism in simulated predator encounters without sacrificing experimental control. SIGNIFICANCE STATEMENT: Anti-predatory behavior is often modulated by the threat level posed by a particular predator. While much research has tested how different types of predators change prey behavior, few experiments have examined how predator behavior affects anti-predatory responses of prey. By experimentally manipulating robotic predators, we show that blue tits not only respond to the presence of a sparrowhawk, by decreasing feeding and increasing anti-predator behavior and vocalizations, but that they vary specific anti-predator behaviors when encountering differently behaving predators (moving, vocalizing, or those with captured prey), suggesting that prey pay attention to their predators' state and behavior.

Sex and pairing status impact how zebra finches use social information in foraging.

Many factors, including the demonstrator's sex, status, and familiarity, shape the nature and magnitude of social learning. Given the important role of pair bonds in socially-monogamous animals, we predicted that these intimate relationships would promote the use of social information, and tested this hypothesis in zebra finches (Taeniopygia guttata). Observer birds witnessed either their mate or another familiar, opposite-sex bird eat from one, but not a second novel food source, before being allowed to feed from both food sources themselves. Birds used social information to make foraging decisions, but not all individuals used this information in the same way. While most individuals copied the foraging choice of the demonstrator as predicted, paired males did not, instead avoiding the feeder demonstrated by their mate. Our findings reveal that sex and pairing status interact to influence the use of social information and suggest that paired males might use social information to avoid competing with their mate.

Traffic noise drowns out great tit alarm calls.

Anthropogenic noise is one of the fastest growing and most ubiquitous types of environmental pollution and can impair acoustic communication in a variety of animals [1]. Recent research has shown that birds can adjust acoustic parameters of their sexual signals (songs) in noisy environments [2,3], yet we know little about other types of vocalizations. Anti-predator signals contain subtle information that is critical for avoiding predation [4,5], and failure to detect these calls [6,7] as a result of anthropogenic noise pollution could have large fitness consequences by negatively impacting survival. We investigated whether traffic noise impacts both the production and perception of avian alarm calls using a combination of lab and field experiments with great tits (Parus major), a songbird that frequently inhabits noise-polluted environments. In response to experimental noise manipulation in controlled laboratory conditions, great tits increased the amplitude, but not the frequency parameters, of their mobbing alarm calls (hereafter 'alarm calls'). Playback experiments conducted in the wild indicate that current levels of road traffic noise mask alarm calls, impeding the ability of great tits to perceive these critical signals. These results show that, despite the vocal adjustments used to compensate for anthropogenic noise, great tits are not able to restore the active space of their calls in even moderately noisy environments. Consequently, birds are likely to suffer from increased predation risk under noise, with likely effects on their behaviour, populations, and community dynamics in noise-polluted areas.

Name that tune: Melodic recognition by songbirds.

Recent findings have indicated that European starlings perceive overall spectral shape and use this, rather than absolute pitch or timbre, to generalize between similar melodic progressions. This finding highlights yet another parallel between human and avian vocal communication systems and has many biological implications.

Female happy wrens select songs to cooperate with their mates rather than confront intruders.

Vocal duetting occurs in many taxa, but its function remains much-debated. Like species in which only one sex sings, duetting birds can use their song repertoires to signal aggression by singing song types that match those of territorial intruders. However, when pairs do not share specific combinations of songs (duet codes), individuals must choose to signal aggression by matching the same-sex rival, or commitment by replying appropriately to their mate. Here, we examined the song types used by female happy wrens (Pheugopedius felix) forced to make this decision in a playback experiment. We temporarily removed the male from the territory and then played songs from two loudspeakers to simulate an intruding female and the removed mate's response, using song types that the pair possessed but did not naturally combine into duets. Females were aggressive towards the female playback speaker, approaching it and overlapping the female playback songs, but nevertheless replied appropriately to their mate's songs instead of type matching the intruding female. This study indicates that females use song overlapping to signal aggression but use their vocal repertoires to create pair-specific duet codes with their mates, suggesting that duetting functions primarily to demonstrate pair commitment.