Christopher N. Templeton

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.

An experimental study of duet integration in the happy wren, Pheugopedius felix

Pairs of duetting birds can sing coordinated duets with such precision that they are often mistaken for a single individual, yet little is known about how this impressive temporal synchronization is achieved. We experimentally examined duet coordination in male happy wrens, held briefly in captivity, by playing song phrases from their partner at different distances and tempos. Males were more likely to respond to songs played nearby, but did not vary their amplitude to compensate for their partners simulated distance. Males modified their song rate to match the manipulated female playback tempo, indicating that they listen and respond to each female utterance. Each happy wren has a sex-specific repertoire of about 40 different song phrases and pairs combine particular phrases according to pair-specific duet ‘codes’, creating a further challenge for coordinating duets. We found that most males produced the appropriate phrase to reply to the female playback song in the absence of any other potential cues, sometimes delivering the correct song phrase type within 0.5xa0s of the start of the very first female playback heard. These experiments demonstrate rapid decision making and vocal production, indicative of sophisticated underlying cognitive processing, and provide a novel experimental technique to investigate the mechanisms controlling vocal duets.

Does song complexity correlate with problem-solving performance in flocks of zebra finches?

The ‘cognitive capacity hypothesis’ states that song complexity could potentially be used by prospective mates to assess an individual’s overall cognitive ability. Several recent studies have provided support for the cognitive capacity hypothesis, demonstrating that individuals with more complex songs or larger song repertoires performed better on various learning tasks. These studies all measured individuals’ learning performance in social isolation. However, for gregarious species such as the zebra finch, Taeniopygia guttata, testing individuals in a group context is socially and ecologically more relevant if song complexity is to be a meaningful indicator of cognitive ability. We tested whether song complexity correlated with performance on a suite of novel foraging problems in flocks of male zebra finches, starting by replicating the lid-flipping task used by Boogert et al. (Animal Behaviour ,2 008,76, 1735e1741), who provided the first support for the cognitive capacity hypothesis in zebra finches isolated during testing. We also presented flocks with a barrier task and two types of novel food. We found that males’ song complexity scores did not correlate with their latency to solve any of these novel foraging problems in a social context. Individuals that solved the tasks likewise did not have more complex songs than nonsolvers. However, performance was positively correlated across the different foraging tasks. These results raise doubts as to whether the song complexity measures used by Boogert et al. are predictors of problem-solving performance, and perhaps cognitive ability, in a more ecologically relevant, social setting. Stress responsiveness might instead explain the association between song complexity and foraging task performance among isolated zebra finches reported by

Hoo are you? Tits do not respond to novel predators as threats

To combat the threat of predation, prey species have developed a variety of ways to recognize and respond appropriately to novel predators. While there is evidence that predator recognition does not require learning in certain species, learning appears to play an important role for other species. In systems where learning is important, it is less clear whether predator identification requires prior experience with specific predators or, whether general experience with predators provides sufficient tools for identifying similar species of novel predators. Here we test whether wild-living adult birds recognize a dangerous predator that occurs in only part of their geographical range. We presented taxidermy mounts of little owls, Athene noctua, and sparrowhawks, Accipiter nisus, to blue tits, Cyanistes caeruleus, and great tits, Parus major. All populations of both tit species co-occur with sparrowhawks, but populations differ in their prior experience with little owls. We found that tits that overlap geographically with little owls responded to little owls using the same intensity of mobbing behaviour exhibited toward sparrowhawks. In populations with no historical contact with little owls, however, both blue and great tits treated little owls as a lower threat than sparrowhawks. These results suggest that blue tits and great tits do not generalize ‘predatory features’ to novel predators and instead need prior experience with specific predators before they assign the correct level of threat.

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.

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 fathers song; would CORT-treated juveniles in free-flying aviaries switch to copying songs of other males? We found that CORT-treated juveniles copied their fathers 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’.

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

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 statementAnti-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.

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.

Presence of an audience and consistent interindividual differences affect archerfish shooting behaviour

The social environment can play an important role in shaping the foraging behaviour of animals. In this study we investigated whether archerfish, Toxotes jaculatrix, display any behavioural changes in response to the presence of an audience while using their specialized foraging tactic of shooting, spitting precisely aimed jets of water, at prey targets. As any prey items shot down are potentially available to competitors, we hypothesized that shooting fish would be sensitive to the presence of potential competitors, especially given the suggestion that, in the wild, this species shows intraspecific kleptoparasitism and faces interspecific competition. We found that in the presence of another fish, archerfish took longer to shoot, made more orientations (aiming events) per shot, and tended to be closer to the target at the time of shooting. Additionally, archerfish showed high interindividual differences in latency to shoot, and these differences were consistent across contexts, with and without an audience. Our results show that archerfish are sensitive to, and adjust their shooting behaviour in response to, the presence of an audience and highlight the importance of social context in this fish species. We also suggest that interindividual differences may play an important role in archerfish shooting behaviour. This study highlights the importance of social effects and competition on foraging behaviour and decision making. Further work in this species could explore whether differences in competitive foraging ability are linked to sensitivity to the presence of an audience.

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

Many factors, including the demonstrators 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.