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Traits that exhibit differences between the sexes have been of special interest in the study of phenotypic evolution. Classic hypotheses explain sexually dimorphic traits via intra-sexual competition and mate selection, yet natural selection may also act differentially on the sexes to produce dimorphism. Natural selection can act either through physiological and ecological constraints on one of the sexes, or by modulating the strength of sexual/social selection. This predicts an association between the degree of dimorphism and variation in ecological environments. Here, we characterize the variation in hummingbird dimorphism across ecological gradients using rich databases of morphology, colouration and song. We show that morphological dimorphism decreases with elevation in the understorey and increases with elevation in mixed habitats, that dichromatism increases at high altitudes in open and mixed habitats, and that song is less complex in mixed habitats. Our results are consistent with flight constraints, lower predation pressure at high elevations and with habitat effects on song transmission. We also show that dichromatism and song complexity are positively associated, while tail dimorphism and song complexity are negatively associated. Our results suggest that key ecological factors shape sexually dimorphic traits, and that different communication modalities do not always evolve in tandem.

The ability of an animal to detect environmental cues is crucial for its survival and fitness. In bats, sound certainly plays a significant role in the search for food, spatial navigation, and social communication. Yet, the efficiency of bat’s echolocation could be limited by atmospheric attenuation and background clutter. In this context, sound can be complemented by other sensory modalities, like smell or vision. Spix’s disc-winged bat (Thyroptera tricolor) uses acoustic cues from other group members to locate the roost (tubular unfurled leaves of plants in the order Zingiberales). Our research focused on how individuals find a roost that has not been yet occupied, considering the urge to find a suitable leaf approximately every day, during nighttime or in daylight. We observed the process of roost finding in T. tricolor in a flight cage, manipulating the audio/visual sensory input available for each trial. A broadband noise was broadcast in order to mask echolocation, while experiments conducted at night reduced significantly the amount of light. We measured the time needed to locate the roost under these different conditions. Results show that with limited visual and acoustic cues, search time increases significantly. In contrast bats seemed capable of using acoustic and visual cues in a similarly efficient manner, since roost search showed no strong differences in duration when bats could use only sound, only vision, or both senses at the same time. Our results show that non-acoustic inputs can still be an important source of information for finding critical resources in bats.

Despite longstanding interest in the evolutionary origins and maintenance of vocal learning, we know relatively little about how social dynamics influence vocal learning processes in natural populations. The “signaling group membership” hypothesis proposes that socially learned calls evolved and are maintained as signals of group membership. However, in fission–fusion societies, individuals can interact in social groups across various social scales. For learned calls to signal group membership over multiple social scales, they must contain information about group membership over each of these scales, a concept termed “hierarchical mapping.” Monk parakeets (Myiopsitta monachus), small parrots native to South America, exhibit vocal mimicry in captivity and fission–fusion social dynamics in the wild. We examined patterns of contact call acoustic similarity in Uruguay to test the hierarchical mapping assumption of the signaling group membership hypothesis. We also asked whether geographic variation patterns matched regional dialects or geographic clines that have been documented in other vocal learning species. We used visual inspection, spectrographic cross-correlation and random forests, a machine learning approach, to evaluate contact call similarity. We compared acoustic similarity across social scales and geographic distance using Mantel tests and spatial autocorrelation. We found high similarity within individuals, and low, albeit significant, similarity within groups at the pair, flock and site social scales. Patterns of acoustic similarity over geographic distance did not match mosaic or graded patterns expected in dialectal or clinal variation. Our findings suggest that monk parakeet social interactions rely more heavily upon individual recognition than group membership at higher social scales.

1. Assessing diversity of discretely varying behavior is a classical ethological problem. In particular, the challenge of calculating an individuals' or species' vocal repertoire size is often an important step in ecological and behavioral studies, but a reproducible and broadly applicable method for accomplishing this task is not currently available. 2. We offer a generalizable method to automate the calculation and quantification of acoustic diversity using an unsupervised random forest framework. We tested our method using natural and synthetic datasets of known repertoire sizes that exhibit standardized variation in common acoustic features as well as in recording quality. We tested two approaches to estimate acoustic diversity using the output from unsupervised random forest analyses: (i) cluster analysis to estimate the number of discrete acoustic signals (e.g., repertoire size) and (ii) an estimation of acoustic area in acoustic feature space, as a proxy for repertoire size. 3. We find that our unsupervised analyses classify acoustic structure with high accuracy. Specifically, both approaches accurately estimate element diversity when repertoire size is small to intermediate (5-20 unique elements). However, for larger datasets (20-100 unique elements), we find that calculating the size of the area occupied in acoustic space is a more reliable proxy for estimating repertoire size. 4. We conclude that our implementation of unsupervised random forest analysis offers a generalizable tool that researchers can apply to classify acoustic structure of diverse datasets. Additionally, output from these analyses can be used to compare the distribution and diversity of signals in acoustic space, creating opportunities to quantify and compare the amount of acoustic variation among individuals, populations, or species in a standardized way. We provide R code and examples to aid researchers interested in using these techniques.

Animals produce a wide array of sounds with highly variable acoustic structures. It is possible to understand the causes and consequences of this variation across taxa with phylogenetic comparative analyses. Acoustic and evolutionary analyses are rapidly increasing in sophistication such that choosing appropriate acoustic and evolutionary approaches is increasingly difficult. However, the correct choice of analysis can have profound effects on output and evolutionary inferences. Here, we identify and address some of the challenges for this growing field by providing a roadmap for quantifying and comparing sound in a phylogenetic context for researchers with a broad range of scientific backgrounds. Sound, as a continuous, multidimensional trait can be particularly challenging to measure because it can be hard to identify variables that can be compared across taxa and it is also no small feat to process and analyse the resulting high-dimensional acoustic data using approaches that are appropriate for subsequent evolutionary analysis. Additionally, terminological inconsistencies and the role of learning in the development of acoustic traits need to be considered. Phylogenetic comparative analyses also have their own sets of caveats to consider. We provide a set of recommendations for delimiting acoustic signals into discrete, comparable acoustic units. We also present a three-stage workflow for extracting relevant acoustic data, including options for multivariate analyses and dimensionality reduction that is compatible with phylogenetic comparative analysis. We then summarize available phylogenetic comparative approaches and how they have been used in comparative bioacoustics, and address the limitations of comparative analyses with behavioural data. Lastly, we recommend how to apply these methods to acoustic data across a range of study systems. In this way, we provide an integrated framework to aid in quantitative analysis of cross-taxa variation in animal sounds for comparative phylogenetic analysis. In addition, we advocate the standardization of acoustic terminology across disciplines and taxa, adoption of automated methods for acoustic feature extraction, and establishment of strong data archival practices for acoustic recordings and data analyses. Combining such practices with our proposed workflow will greatly advance the reproducibility, biological interpretation, and longevity of comparative bioacoustic studies.

Historically, bird song complexity was thought to evolve primarily through sexual selection on males; yet, in many species, both sexes sing and selection pressure on both sexes may be broader. Previous research suggests competition for mates and resources during short, synchronous breeding seasons leads to more elaborate male songs at high, temperate latitudes. Furthermore, we expect male–female song structure and elaboration to be more similar at lower, tropical latitudes, where longer breeding seasons and year‐round territoriality yield similar social selection pressures in both sexes. However, studies seldom take both types of selective pressures and sexes into account. We examined song in both sexes in 15 populations of nine‐fairy‐wren species (Maluridae), a Southern Hemisphere clade with female song. We compared song elaboration (in both sexes) and sexual song dimorphism to latitude and life‐history variables tied to sexual and social selection pressures and sex roles. Our results suggest that song elaboration evolved in part due to sexual competition in males: male songs were longer than female songs in populations with low male survival and less male provisioning. Also, female songs evolved independently of male songs: female songs were slower paced than male songs, although only in less synchronously breeding populations. We also found male and female songs were more similar when parental care was more equal and when male survival was high, which provides strong evidence that sex role similarity correlates with male–female song similarity. Contrary to Northern Hemisphere latitudinal patterns, male and female songs were more similar at higher, temperate latitudes. These results suggest that selection on song can be sex specific, with male song elaboration favored in contexts with stronger sexual selection. At the same time, selection pressures associated with sex role similarity appear to favor sex role similarity in song structure., Birdsong is often studied as a sexually selected male trait; yet, in many species, both sexes sing. Here, we examined selection pressures responsible for song elaboration and sexual dimorphism in 15 populations of 9 fairy‐wren species (Maluridae), an Australasian lineage with female song. We provide evidence that sex role similarity and sexual selection contribute to male–female song similarity and dimorphism in this group. These results suggest that selection on song can be sex specific, with male song elaboration favored in contexts coincident with sexual selection, while selection pressures associated with sex role similarity also appear to constrain sex‐specific song evolution and song dimorphism.

Vocal learning, in which animals modify their vocalizations based on social experience, has evolved in several lineages of mammals and birds, including humans. Despite much attention, the question of how this key cognitive trait has evolved remains unanswered. The motor theory for the origin of vocal learning posits that neural centres specialized for vocal learning arose from adjacent areas in the brain devoted to general motor learning. One prediction of this hypothesis is that visual displays that rely on complex motor patterns may also be learned in taxa with vocal learning. While learning of both spoken and gestural languages is well documented in humans, the occurrence of learned visual displays has rarely been examined in non-human animals. We tested for geographical variation consistent with learning of visual displays in long-billed hermits ( Phaethornis longirostris ), a lek-mating hummingbird that, like humans, has both learned vocalizations and elaborate visual displays. We found lek-level signatures in both vocal parameters and visual display features, including display element proportions, sequence syntax and fine-scale parameters of elements. This variation was not associated with genetic differentiation between leks. In the absence of genetic differences, geographical variation in vocal signals at small scales is most parsimoniously attributed to learning, suggesting a significant role of social learning in visual display ontogeny. The co-occurrence of learning in vocal and visual displays would be consistent with a parallel evolution of these two signal modalities in this species.

Summary Animal acoustic communication is one of the most fruitful research areas in behavioural and evolutionary biology. Work in this area depends largely on quantifying the structure of acoustic signals, which has often depended upon closed-source or graphical user interface (GUI)-based software. Here, we describe the r package warbleR, a new package for the analysis of animal acoustic signal structure. The package offers functions for downloading avian vocalizations from the open-access online repository Xeno-Canto, displaying the geographic extent of the recordings, manipulating sound files, detecting acoustic signals or importing detected signals from other software, assessing performance of methods that measure acoustic similarity, conducting cross-correlations, measuring acoustic parameters and analysing interactive vocal signals, among others. Functions working iteratively allow parallelization to improve computational efficiency. We present a case study showing how warbleR functions can be used in a workflow to evaluate the structure of acoustic signals. We analyse geographic variation in long-billed hermit hummingbirds (Phaethornis longirostris) songs obtained from Xeno-Canto. The code in warbleR can be executed by less experienced r users, but has also been thoroughly commented, which will facilitate further customization by advanced users. The combination of the tools described here with other acoustic analysis packages in r should significantly expand the range of analytical approaches available.

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.

We present an interdisciplinary effort to record feeding behaviors and control the diet of a hummingbird species (Phaethornis longirostris, the long-billed hermit or LBH) by developing a Radio Frequency Identification (RFID) based smart feeder. The system contains an RFID reader, a microcontroller, and a servo-controlled hummingbird feeder opener, the system is presented as a tool for studying the cognitive ability of the LBH species. When equipped with glass capsule RFID tags (which are mounted on the hummingbird), the smart feeder can provide specific diets for predetermined sets of hummingbirds at the discretion of biologists. This is done by reading the unique RFID tag on the hummingbirds and comparing the ID number with the pre-programmed ID numbers stored in the smart feeder. The smart feeder records the time and ID of each hummingbird visit. The system data is stored in a readily available SD card and is powered by two 9 V batteries. The detection range of the system is approximately 9–11 cm. Using this system, biologists can assign the wild hummingbirds to different experimental groups and monitor their diets to determine if they develop a preference to any of the available nectars. During field testing, the smart feeder system has demonstrated consistent detection (when compared to detections observed by video-recordings) of RFID tags on hummingbirds and provides pre-designed nectars varying water and sugar concentrations to target individuals. The smart feeder can be applied to other biological and environmental studies in the future.

Pair collaborative behavior may play an important role in avian reproduction. However, evidence for this mainly comes from certain ecological groups (e.g. passerines). We studied the coordination of parents in foraging and its effect on food provisioning rate and chick growth in a small seabird, the Dovekie (Little auk, Alle alle). The species exhibits a dual foraging strategy, where provisioning adults make foraging trips of short (mean ~2 h; to provide food for the chick) and long duration (mean ~ 13 h; mainly for adults self-maintenance, although the food is also brought to the chick). We expected that offspring would benefit if parents coordinate their foraging patterns: one making short trips in the time when the other performing the long one. We examined this hypothesis using Monte Carlo randomization tests on field data collected during observations of individually marked birds. We found that parents did indeed adjust provisioning, making their long and short trips in an alternating pattern with respect to each other. Furthermore, we found that a higher level of coordination is associated with a lower variability in the duration of inter-feeding intervals, although this does not affect chick growth. Nevertheless, our results provide compelling evidence on the coordinated behavior of breeding partners.

One way in which secondary sexual traits can influence differential reproductive success is by playing a key role in the outcome of direct physical contests for mates. Here we describe an undocumented trait in a species of hummingbird with a lek mating system, the Long-billed hermit (LBH, Phaethornis longirostris). The trait under consideration is a dagger-like structure at the bill tip, which we hypothesize is a secondary sexual trait that functions as a sexually dimorphic weapon. We tested our hypothesis by examining 5 leks during 4 consecutive years, and by employing morphological analyses, performance experiments, and behavioral observations. We found that 1) adult male bill tips were longer and pointier than their counterparts in females and juvenile males, 2) juvenile males acquired dagger-like tips during their transition to adulthood, 3) variation in bill tip morphology reflected puncture capability, and 4) males with larger and pointier bill tips were more successful in achieving lek territory tenure. Our study provides the first evidence of sexually dimorphic weapons in bird bills and stands as one of the few examples of male weaponry in birds. Our results suggest a role of sexual selection on the evolution of overall bill morphology, an alternative hypothesis to the prevailing "ecological causation" explanation for bill sexual dimorphism in hummingbirds.

We use allometric analysis to explore how acoustic signals scale on individual body size and to test hypotheses about the factors shaping relationships between signals and body size. Across case studies spanning birds, crickets, tree crickets, and tree frogs, we find that most signal traits had low coefficients of variation, shallow allometric scalings, and little dispersion around the allometric function. We relate variation in these measures to the shape of mate preferences and the level of condition dependence of signal traits. We find 3 major patterns: 1) signal traits associated with closed mate preferences had lower coefficients of variation and shallower allometries than signal traits with open preferences, 2) signal traits with higher levels of condition dependence had higher coefficients of variation and steeper allometries, and 3) the relationship between condition dependence and allometry varied with preference shape. We find no difference in coefficient of variation or allometry between advertisement and aggressive acoustic signals. Together, our findings suggest 2 main conclusions: 1) most acoustic signals do not appear to have been selected to function as indicators of body size and 2) an interplay between the form of selection and body size–related cost/benefit relationships of trait expression has great potential to explain variation in sexual allometries.

Predator-prey interactions occur regularly in nature; however, predation events are difficult to observe in the canopy of tropical rain forests. We describe a successful capture of a Chestnut-mandibled Toucan (Ramphastos swainsonii) by a Collared Forest-Falcon (Micrastur semitorquatus) in Carara National Park, Costa Rica. The predator-prey interaction lasted for ∼30 min from the moment of the first wounding strike in the canopy to the killing of the toucan on the ground. During the predation process, the falcon engaged in multiple attacks from different directions at the sub-canopy level. We video recorded a total of 323.3 sec tracks during the predation event to produce a detailed description of the behavior of both species. In addition, we analyzed the structure of the call of the toucan while being attacked and compared that with a regular call of another individual recorded at a different time in the same area. The toucan produced a distress call with strong harmonics and a broad-band rattlin...

When using signals to attract mates or defend resources, animals often overlap the voices of other individuals in close proximity. In such contexts signal masking is likely and animals would benefit by adopting behavioural strategies that modify the timing of signals to minimize the negative effects of masking or take advantage of its signalling value. Indeed, temporal coordination has been commonly described in a wide variety of taxa, but compelling evidence demonstrating that it arises as an active process is scarce. Here we investigate the degree of coordinated singing by lekking long-billed hermit hummingbirds, Phaethornis longirostris, in the Neotropics, using randomization tests to study the timing of vocal signals. We first demonstrate that a randomization statistical approach is robust at detecting coordinated singing in simulated data. Then, we show that long-billed hermits engage in vocal interactions in which either song alternation or song overlap is used. Furthermore, we show that singing behaviour varies with the distance between singers: hermits alternate their songs when they are in close proximity, and they overlap songs at farther distances. Birds achieve these two behaviours by modifying the time intervals between signals. The association between pattern of coordination and distance is not fully explained by any of the current hypotheses for song overlap and suggests that multiple context-dependent singing strategies could be involved. Our findings provide compelling evidence on vocal coordination as an active process in this species and validate an analytical approach that could be extended to investigate similar patterns in other taxa. © 2016 The Association for the Study of Animal Behaviour

Although song development in songbirds has been much studied as an analogue of language development in humans, the development of vocal interaction rules has been relatively neglected in both groups. Duetting avian species provide an ideal model to address the acquisition of interaction rules as duet structure involves time and pattern-specific relationships among the vocalizations from different individuals. In this study, we address the development of the most striking properties of duets: the specific answering rules that individuals use to link their own phrase types to those of their partners (duet codes) and precise temporal coordination. By performing two removal experiments in canebrake wrens ( Cantorchilus zeledoni ), we show that individuals use a fixed phrase repertoire to create new phrase pairings when they acquire a new partner. Furthermore, immediately after pairing, individuals perform duets with poor coordination and poor duet code adherence, but both aspects improve with time. These results indicate that individuals need a learning period to be able to perform well-coordinated duets that follow a consistent duet code. We conclude that both duet coordination and duet code adherence are honest indicators of pair-bond duration.

The nightingale, the lark ascending; the cuckoo, the dawn chorus; since ancient times man has found beauty in birdsong. It appeals to our senses. It inspires composers. But is it music? Marcelo Araya-Salas listens to the nightingale wren and tries to find out if it is singing in tune.

In the context of global change the possible loss of biodiversity has been identified as a major concern. Biodiversity could be seriously threatened as a direct consequence of changes in availability of food, changing thermal conditions, and loss and fragmentation of habitat. Considering the magnitude of global change, an understanding of the mechanisms involved in coping with a changing environment is urgent. We explore the hypothesis that species and individuals experiencing highly variable environments are more likely to develop a wider range of responses to handle the different and unpredictable conditions imposed by global change. In the case of vertebrates, the responses to the challenges imposed by unpredictable perturbations ultimately are linked to cognitive abilities allowing the solving of problems, and the maximization of energy intake. Our models were hummingbirds, which offer a particularly compelling group in which to examine the functional and mechanistic links between behavioral and energetic strategies in individuals experiencing different degrees of social and environmental heterogeneity.

Learning has been traditionally thought to accelerate the evolutionary change of behavioural traits. We evaluated the evolutionary rate of learned vocalizations and the interplay of morphology and ecology in the evolution of these signals. We examined contact calls of 51 species of Neotropical parrots from the tribe Arini. Parrots are ideal subjects due to their wide range of body sizes and habitats, and their open-ended vocal learning that allows them to modify their calls throughout life. We estimated the evolutionary rate of acoustic parameters of parrot contact calls and compared them to those of morphological traits and habitat. We also evaluated the effect of body mass, bill length, vegetation density and species interactions on acoustic parameters of contact calls while controlling for phylogeny. Evolutionary rates of acoustic parameters did not differ from those of our predictor variables except for spectral entropy, which had a significantly slower rate of evolution. We found support for correlated evolution of call duration, and fundamental and peak frequencies with body mass, and of fundamental frequency with bill length. The degree of sympatry between species did not have a significant effect on acoustic parameters. Our results suggest that parrot contact calls, which are learned acoustic signals, show evolutionary rates similar to those of morphological traits. This is the first study to our knowledge to provide evidence that change through cultural evolution does not necessarily accelerate the evolutionary rate of traits acquired through life-long vocal learning.

Vocal learning is a complex trait that is expressed differently across different taxa. While many of the best-studied species exhibit close-ended learning, in which vocal signals are learned from adult tutors during juvenile critical learning periods, other species have open-ended learning in which new signals are learned throughout life. Budgerigars (Melopsittacus undulatus) are an extreme example of an open-ended learner, in which both sexes have a repertoire of multiple contact calls types that continually change through adulthood to match the call types of social associates. We discuss the analytical challenges posed by the rapid plasticity of the budgerigar vocal repertoire and compare results from several different approaches to characterizing call variation. We then consider the social implications and benefits of contact call matching in fission–fusion groups. Finally, we examine the mechanisms underlying this plasticity, with a special focus on the role of the gene FoxP2. We find downregulation of FoxP2 mRNA and protein in the primary parrot vocal learning center, MMSt, across a variety of social conditions in which birds also show vocal plasticity. The results support the hypothesis that FoxP2 is a key gene regulating the neural plasticity that underlies the persistent vocal plasticity exhibited by budgerigars.

Vocal learning in birds is typically restricted to a sensitive period early in life, with the few exceptions reported in songbirds and parrots. Here, we present evidence of open-ended vocal learning in a hummingbird, the third avian group with vocal learning. We studied vocalizations at four leks of the long-billed hermit Phaethornis longirostris during a four-year period. Individuals produce a single song repertoire, although several song-types can coexist at a single lek. We found that nine of 49 birds recorded on multiple days (18%) changed their song-type between consecutive recordings. Three of these birds replaced song-types twice. Moreover, the earliest estimated age when song replacement occurred ranged from 186 to 547 days (mean = 307 days) and all nine birds who replaced song-types produced a crystallized song before replacement. The findings indicate that song-type replacement is distinct from an initial early learning sensitive period. As half of lekking males do not survive past the first year of life in this species, song learning may well extend throughout the lifespan. This behaviour would be convergent to vocal learning programmes found in parrots and songbirds.