A limit to sustained performance constrains trill length in birdsong.

In birds, song performance determines the outcome of contests over crucial resources. We hypothesized that 1) sustained performance is limited within song, resulting in a performance decline towards the end and 2) the impact of song length is compromised if performance declines. To test these hypotheses, we analyzed the songs of 597 bird species (26 families) and conducted a playback experiment on blue tits (Cyanistes caeruleus). Our multi-species analysis showed that song performance declines after sustained singing, supporting our hypothesis. If the performance decline is determined by individual attributes (i.e., physical condition), our results explain how trill length can honestly signal quality. Our experiment showed that longer trills of high performance elicited a stronger response during territorial interactions. However, long trills that declined in performance elicited a weaker response than short, high-performance trills. A trade-off between the duration and performance quality of a motor display can be an important aspect in communication across taxa.

Sound properties affect measurement of vocal consistency in birdsong: Validation of the spectrogram cross correlation method (SPCC).

In songbirds, singing with precision (vocal consistency) has been proposed to reflect whole-organism performance. Vocal consistency is measured using spectrogram cross correlation (SPCC) to assess the acoustic similarity between subsequent renditions of the same note. To quantify how SPCC is sensitive to the acoustic discrepancies found in birdsong, we created a set of 40 000 synthetic sounds that were designed based on the songs of 345 species. This set included 10 000 reference sounds and 30 000 inexact variants with quantified differences in frequency, bandwidth, or duration with respect to the reference sounds. We found that SPCC is sensitive to acoustic discrepancies within the natural range of vocal consistency, supporting the use of this method as a tool to assess vocal consistency in songbirds. Importantly, the sensitivity of SPCC was significantly affected by the bandwidth of sounds. The predictions derived from the analysis of synthetic sounds were then validated using 954 song recordings from 345 species (20 families). Based on psychoacoustic studies from birds and humans, we propose that the sensitivity of SPCC to acoustic discrepancies mirrors a perceptual bias in sound discrimination. Nevertheless, we suggest the tool be used with care, since sound bandwidth varies considerably between singing styles and therefore, SPCC scores may not be comparable.

Sexual selection for both diversity and repetition in birdsong.

From fiddler crabs to humans, animals perform repetitive displays showing neuromotor skill and vigour. Consistent repetition of identical notes (vocal consistency) facilitates the assessment of neuromotor skills and is important in communication in birds. Most birdsong research has focused on song diversity as a signal of individual quality, which seems contradictory as repetition is extremely common in most species. Here we show that consistent repetition within songs is positively correlated with reproductive success in male blue tits (Cyanistes caeruleus). A playback experiment shows that females are sexually aroused by male songs with high levels of vocal consistency, which also peaks seasonally during the fertile period of the female, supporting the role of vocal consistency in mate choice. Male vocal consistency also increases with subsequent repetitions of the same song type (a warm-up effect) which conflicts with the fact that females habituate to repeated song, showing decreased arousal. Importantly, we find that switching song types elicits significant dishabituation within the playback, supporting the habituation hypothesis as an evolutionary mechanism driving song diversity in birds. An optimal balance between repetition and diversity may explain the singing style of many bird species and displays of other animals.

Female blue tits sing frequently: a sex comparison of occurrence, context, and structure of song.

In species with mutual mate choice, we should expect adaptive signaling in both sexes. However, the role of female sexual signals is generally understudied. A case in point is female birdsong that has received considerably less attention than male song. This holds even for well-studied species such as the blue tit (Cyanistes caeruleus), an important model in evolutionary ecology. Although there have been anecdotal reports of female song from three populations, there are no quantitative studies on female song in this species. Here, we report systematic sampling from a population of individually marked blue tits over 3 years, revealing that females sang frequently throughout the sampling period. Notably, daytime singing of females occurred in functionally similar contexts as in males (agonistic, solo song, and alarm contexts) but females had lower song output than males and were not observed singing dawn song, while males showed long singing displays at dawn before copulations take place. Female and male song overlapped substantially in acoustic structure (i.e., same song types or peak frequency) but females had smaller individual song-type repertoires, shorter trills, and lower vocal consistency. Differential selection pressures related to functional differences in male and female song might explain the observed variation in acoustic structure. With the first quantitative study of female song in such a well-studied species, we hope to stimulate further investigations into the functions of female singing, especially in the Northern temperate zones where female song may have been overlooked, not only in this but perhaps in other monomorphic species.

Leafcutter ants adjust foraging behaviours when exposed to noise disturbance.

We investigate the impact of anthropogenic noise on the foraging efficiency of leafcutter ants (Acromyrmex octospinosus) in a controlled laboratory experiment. Anthropogenic noise is a widespread, pervasive and increasing environmental pollutant and its negative impacts on animal fitness and behaviour have been well documented. Much of this evidence has come from studies concerning vertebrate species with very little evidence for terrestrial invertebrates, especially social living invertebrates. We compare movement speed, forage fragment size, and colony activity levels of ants exposed to intermittent elevated noise and in ambient noise conditions. We use intermittent and temporally unpredictable bursts of white noise produced from a vibration speaker to create the elevated noise profile. Ant movement speed increased under elevated noise conditions when travelling to collect forage material and when returning to the colony nest. The size of individually measured foraged material was significantly reduced under elevated noise conditions. Colony activity, the number of ants moving along the forage route, was not affected by elevated noise and was consistent throughout the foraging events. Increased foraging speed and smaller forage fragments suggests that the ants had to make more foraging trips over an extended period, which is likely to affect energy expenditure and increases exposure to predators. This is likely to have significant fitness impacts for the colony over time.

Like Father Like Son: Cultural and Genetic Contributions to Song Inheritance in an Estrildid Finch.

Social learning of vocalizations is integral to song inheritance in oscine passerines. However, other factors, such as genetic inheritance and the developmental environment, can also influence song phenotype. The relative contributions of these factors can have a strong influence on song evolution and may affect important evolutionary processes such as speciation. However, relative contributions are well-described only for a few species and are likely to vary with taxonomy. Using archived song data, we examined patterns of song inheritance in a domestic population of Java sparrows (Lonchura oryzivora), some of which had been cross-fostered. Six-hundred and seventy-six songs from 73 birds were segmented and classified into notes and note subtypes (N = 22,972), for which a range of acoustic features were measured. Overall, we found strong evidence for cultural inheritance of song structure and of the acoustic characteristics of notes; sons' song syntax and note composition were similar to that of their social fathers and were not influenced by genetic relatedness. For vocal consistency of note subtypes, a measure of vocal performance, there was no apparent evidence of social or genetic inheritance, but both age and developmental environment influenced consistency. These findings suggest that high learning fidelity of song material, i.e., song structure and note characteristics, could allow novel variants to be preserved and accumulate over generations, with implications for evolution and conservation. However, differences in vocal performance do not show strong links to cultural inheritance, instead potentially serving as condition dependent signals.

Vocal Repertoire and Intraspecific Variation within Two Loud Calls of the Small-Eared Greater Galago (Otolemur garnettii) in Tanzania and Kenya.

Vocal repertoires and call structure can provide insights into the behaviour and evolution of species, as well as aid in taxonomic classification. Nocturnal primates have large vocal repertoires. This suggests that acoustic communication plays an important role in their life histories. Little is known about the behavioural context or the intraspecific variation of their vocalisations. We used autonomous recording units and manual recorders to investigate the vocal behaviour and structure of loud calls of the small-eared greater galago (Otolemur garnettii)in Kenya and Tanzania. We describe the vocal repertoire, temporal calling patterns and structure of 2 loud calls of 2 subspecies: O. g. panganiensis and O. g. kikuyuensis. We found considerable intraspecific structural differences in both loud calls. These are congruent with the current subspecies classification. Differences in vocalisations among populations are not consistent with the "acoustic adaptation hypothesis," rather they are likely a result of geographic variation due to isolation caused by vegetational barriers in southern Kenya.

Aircraft sound exposure leads to song frequency decline and elevated aggression in wild chiffchaffs.

The ubiquitous anthropogenic low-frequency noise impedes communication by masking animal signals. To overcome this communication barrier, animals may increase the frequency, amplitude and delivery rate of their acoustic signals, making them more easily heard. However, a direct impact of intermittent, high-level aircraft noise on birds' behaviour living close to a runway has not been studied in detail. We recorded common chiffchaffs Phylloscopus collybita songs near two airports and nearby control areas, and we measured sound levels in their territories at Manchester Airport. The song recordings were made in between aircraft movements, when ambient sound levels were similar between airport and control populations. We also conducted playback experiments at the airport and a control population to test the salience of airport, and control population specific songs. In contrast to the general pattern of increased song frequency in noisy areas, we show that common chiffchaffs at airports show a negative relationship between noise exposure level and song frequency. Experimental data show that chiffchaffs living near airports also respond more aggressively to song playback. Since the decrease in song frequency results in increased overlap with aircraft noise, these findings cannot be explained as an adaptation to improve communication. The increased levels of aggression suggest that chiffchaffs, like humans, might be affected behaviourally by extreme noise pollution. These findings should influence environmental impact assessments for airport expansions globally.

Multi-individual microsatellite identification: A multiple genome approach to microsatellite design (MiMi).

Bespoke microsatellite marker panels are increasingly affordable and tractable to researchers and conservationists. The rate of microsatellite discovery is very high within a shotgun genomic data set, but extensive laboratory testing of markers is required for confirmation of amplification and polymorphism. By incorporating shotgun next-generation sequencing data sets from multiple individuals of the same species, we have developed a new method for the optimal design of microsatellite markers. This new tool allows us to increase the rate at which suitable candidate markers are selected by 58% in direct comparisons and facilitate an estimated 16% reduction in costs associated with producing a novel microsatellite panel. Our method enables the visualisation of each microsatellite locus in a multiple sequence alignment allowing several important quality checks to be made. Polymorphic loci can be identified and prioritised. Loci containing fragment-length-altering mutations in the flanking regions, which may invalidate assumptions regarding the model of evolution underlying variation at the microsatellite, can be avoided. Priming regions containing point mutations can be detected and avoided, helping to reduce sample-site-marker specificity arising from genetic isolation, and the likelihood of null alleles occurring. We demonstrate the utility of this new approach in two species: an echinoderm and a bird. Our method makes a valuable contribution towards minimising genotyping errors and reducing costs associated with developing a novel marker panel. The Python script to perform our method of multi-individual microsatellite identification (MiMi) is freely available from GitHub (https://github.com/graemefox/mimi).

Using the relational event model (REM) to investigate the temporal dynamics of animal social networks.

Social dynamics are of fundamental importance in animal societies. Studies on nonhuman animal social systems often aggregate social interaction event data into a single network within a particular time frame. Analysis of the resulting network can provide a useful insight into the overall extent of interaction. However, through aggregation, information is lost about the order in which interactions occurred, and hence the sequences of actions over time. Many research hypotheses relate directly to the sequence of actions, such as the recency or rate of action, rather than to their overall volume or presence. Here, we demonstrate how the temporal structure of social interaction sequences can be quantified from disaggregated event data using the relational event model (REM). We first outline the REM, explaining why it is different from other models for longitudinal data, and how it can be used to model sequences of events unfolding in a network. We then discuss a case study on the European jackdaw, Corvus monedula, in which temporal patterns of persistence and reciprocity of action are of interest, and present and discuss the results of a REM analysis of these data. One of the strengths of a REM analysis is its ability to take into account different ways in which data are collected. Having explained how to take into account the way in which the data were collected for the jackdaw study, we briefly discuss the application of the model to other studies. We provide details of how the models may be fitted in the R statistical software environment and outline some recent extensions to the REM framework.

Predicting bird song from space.

Environmentally imposed selection pressures are well known to shape animal signals. Changes in these signals can result in recognition mismatches between individuals living in different habitats, leading to reproductive divergence and speciation. For example, numerous studies have shown that differences in avian song may be a potent prezygotic isolating mechanism. Typically, however, detailed studies of environmental pressures on variation in animal behavior have been conducted only at small spatial scales. Here, we use remote-sensing data to predict animal behavior, in this case, bird song, across vast spatial scales. We use remotely sensed data to predict the song characteristics of the little greenbul (Andropadus virens), a widely distributed African passerine, found across secondary and mature rainforest habitats and the rainforest-savanna ecotone. Satellite data that captured ecosystem structure and function explained up to 66% of the variation in song characteristics. Song differences observed across habitats, including those between human-altered and mature rainforest, have the potential to lead to reproductive divergence, and highlight the impacts that both natural and anthropogenic change may have on natural populations. Our approach offers a novel means to examine the ecological correlates of animal behavior across large geographic areas with potential applications to both evolutionary and conservation biology.

Testing alternative hypotheses for evolutionary diversification in an African songbird: rainforest refugia versus ecological gradients.

Geographic isolation in rainforest refugia and local adaptation to ecological gradients may both be important drivers of evolutionary diversification. However, their relative importance and the underlying mechanisms of these processes remain poorly understood because few empirical studies address both putative processes in a single system. A key question is to what extent is divergence in signals that are important in mate and species recognition driven by isolation in rainforest refugia or by divergent selection across ecological gradients? We studied the little greenbul, Andropadus virens, an African songbird, in Cameroon and Uganda, to determine whether refugial isolation or ecological gradients better explain existing song variation. We then tested whether song variation attributable to refugial or ecological divergence was biologically meaningful using reciprocal playback experiments to territorial males. We found that much of the existing song variation can be explained by both geographic isolation and ecological gradients, but that divergence across the gradient, and not geographic isolation, affects male response levels. These data suggest that ecologically divergent traits, independent of historical isolation during glacial cycles, can promote reproductive isolation. Our study provides further support for the importance of ecology in explaining patterns of evolutionary diversification in ecologically diverse regions of the planet.

The deterrent effect of bird song in territory defense.

Using the responses of territory owners to playback to infer the territorial function of acoustic signals is common practice. However, difficulties with interpreting the results of such experiments have obscured our understanding of territorial signalling. For instance, a stronger response to playback is often interpreted as more aggressive, but there is no consensus as to whether this should be in response to the least or most threatening simulated intruder. Rather than following a gradual increase or decrease, the relationship between signal intensity and response strength may instead describe a peaked curve. We manipulated banded wren (Thryophilus pleurostictus) songs to simulate low-, median-, and high-performance singers and used these songs as stimuli in playback experiments. Banded wrens were less likely to approach the high-performance stimulus compared with the low- and median-performance stimuli. However, the birds that did approach the high-performance stimulus sang more than those that approached the low-performance stimulus. In addition, birds were more likely to match the songs when exposed to the median- and high-performance stimuli compared with the low-performance stimuli, and song matching predicted approach behavior. These results are in accordance with theoretical models of aggressive encounters in which low-performance opponents are challenged without further assessment. Median- and high-performance opponents, however, may require further assessment, and the latter may be perceived as too intimidating for approach.

Trill consistency is an age-related assessment signal in banded wrens.

Older males tend to have a competitive advantage over younger males in sexual selection. Therefore, it is expected that signals used in sexual selection change with age. Although song repertoire size in songbirds is often mentioned as an age-related trait, many species, including the banded wren (Thryothorus pleurostictus), do not increase their repertoires after the first year. Here, we show that banded wrens reproduce the trill notes in their songs with less variability between them (i.e. more consistently) when they grow older. In a playback experiment, we also show that banded wrens discriminate between younger and older birds based on structural aspects of their song. In a second experiment, banded wrens also respond differentially to natural songs versus songs with artificially enhanced consistency. We argue that consistency in trill note reproduction may be achieved through practice. Sexual selection in the form of male-male competition may therefore operate on a phenotypic trait, the expression of which is enhanced by practice.

Migration strategy and divergent sexual selection on bird song.

Migratory birds are assumed to be under stronger sexual selection pressure than sedentary populations, and the fact that their song is more complex has been taken as confirmation of this fact. However, this assumes that sexual selection pressure due to both male competition and female choice increase together. A further issue is that, in many species, songs become less complex during competitive encounters; in contrast, female choice selects for more complex song, so the two selection pressures may drive song evolution in different directions. We analysed song in two sedentary and two migratory populations of blackcaps (Sylvia atricapilla), a species in which different song parts are directed to males and females. We found that migratory populations produce longer, female-directed warbles, indicating sexual selection through female choice is the strongest in these populations. However, the part of the song directed towards males is shorter and more repetitive (as observed in individual competitive encounters between males) in non-migratory populations, indicating sedentary populations, are under stronger selection due to male competition. We show for the first time that the intensity of selection pressure from male competition and female choice varies independently between populations with different migratory behaviours. Rapid alterations in the migration patterns of species are thus likely to lead to unexpected consequences for the costs and benefits of sexual signals.

Syllable Type Consistency is Related to Age, Social Status, and Reproductive Success in the Tropical Mockingbird.

Many animals repeat standardized displays multiple times while attracting a mate or deterring a rival. In such contexts it is possible that the ability to perform each display or signal type in a consistent fashion is under direct selection. Studies on sexual selection on song learning in birds have focused on differences in repertoire size with less attention to the potential importance of being able to perform each song/syllable type with high consistency. We present evidence that tropical mockingbirds decrease the variation between renditions of each syllable type as they grow older (i.e., become more consistent) and that more consistent males in this species tend to have higher dominance status and reproductive success. These findings stress the importance of consistency in the performance of sexual displays and suggest that this parameter may be very relevant even in species that are selected for high vocal diversity (i.e., large repertoires). In addition to signalling dominance status and age, we hypothesize that syllable type consistency may also be an indicator of the integrity of brain function in birds analogous to the tests used for neuropsychological assessment in humans.

The control of food-caching behavior by Western scrub-jays (Aphelocoma californica).

Western scrub-jays (Aphelocoma californica) did not show extinction when caching behavior was never rewarded and they had no choice of where to cache the food. However, when the jays had the choice of caching items in 2 different locations or during 2 successive episodes, and only 1 of each was always rewarded at recovery, they rapidly learned to cache in the rewarded location or episode. When the jays had learned during training trials that their caches were always moved to 1 of 2 locations they did not cache in, then on the test trial they cached in the location that had been previously rewarded. To test whether these jays avoided the location in which their caches had been pilfered or chose the rewarded location, the procedure was repeated to include a 3rd location that was never rewarded. The jays avoided the pilfered location but cached equally in the rewarded and nonrewarded locations.

Habitat-dependent call divergence in the common cuckoo: is it a potential signal for assortative mating?

The common cuckoo (Cuculus canorus) is an obligate brood parasite that mimics the eggs of its hosts. The host-specific egg pattern is thought to be inherited matrilinearly, creating female-only host-specific races. Males are thought not to be adapted to their host and they maintain the species by mating arbitrarily with respect to host specialization of females. However, recent results suggest that male cuckoos may also show host-specific adaptations and these may require assortative mating with respect to host. The calls males produce on the breeding grounds could provide a potential mechanism for assortative mating. We tested whether male cuckoo calls differ more between nearby populations that parasitize different hosts than between distant populations that parasitize the same host. We recorded the calls of geographically distant pairs of populations in Hungary, with each pair consisting of a forest population and a nearby reed bed population. Each habitat is characterized by one main host species for the common cuckoo. Our results show that calls of distant cuckoo populations from the same habitat type are more similar to each other than they are to those of nearby populations from a different habitat. These results suggest that cuckoo calls differ sufficiently to allow recognition of habitat-specific individuals.

An evolutionary perspective on caching by corvids.

A principal finding in the food-caching literature is that species differences in hoarding propensity are positively correlated with species differences in degree of adaptations to caching behaviour, such as performance on spatial memory tasks and hippocampal volume. However, there are examples that do not fit this pattern. We argue that these examples can be better understood by considering the phylogenetic relatedness between species. We reconstruct the ancestral state for caching behaviour in corvids and assess when transitions in caching behaviour occurred within the corvid phylogeny. Our analysis shows that the common ancestor of all corvids was a moderate cacher. This result suggests that corvids followed a bi-directional evolutionary trajectory in which caching was secondarily lost twice and there were at least two independent transitions from moderate to specialized caching. The independent evolution of specialized cachers in the two groups must, therefore, be a case of convergent evolution. This is exemplified by the fact that specialized cachers show structurally different adaptations serving the same function to intense caching, such as different pouches to transport food. Finally, we argue that convergent evolution may have led to adaptations in memory and hippocampus that serve the same function but differ in design, and that these different adaptations may explain the examples that do not fit the pattern predicted by the adaptive specialization hypothesis.

Is the western scrub-jay (Aphelocoma californica) really an underdog among food-caching corvids when it comes to hippocampal volume and food caching propensity?

Food caching has been linked to better performance on spatial memory tasks and enlarged hippocampal volume in both birds and mammals. Within food-caching birds, it has also been predicted that species less reliant on stored food should have inferior spatial memory and a smaller hippocampus compared to species that depend heavily on food caches. Several comparisons suggest that North American corvids have a significantly smaller hippocampus and overall brain volume compared to the Eurasian corvid species and that western scrub-jays (Aphelocoma californica) have a smaller hippocampus compared to the more specialized Clark's nutcracker. Here we present the largest data set of scrub-jay brains and, in contrast to previous reports, show that relative to body mass western scrub-jays have a brain size similar to the largest brain size of Eurasian corvids. The relative hippocampal volume of scrub-jays is also among the largest of all investigated corvids. These findings may not be surprising considering that scrub-jays have been reported to have remarkable cognitive capacities such as episodic-like memory and experience projection. Our data suggest that many previously made assumptions about western scrub-jays as less specialized food hoarders might be an oversimplification and that simple categorization of species into specialized and non-specialized hoarders might not provide useful insights into the evolution of memory and the hippocampus.