Persistent vocal learning in an aging open-ended learner reflected in neural FoxP2 expression.

BACKGROUND: Most vocal learning species exhibit an early critical period during which their vocal control neural circuitry facilitates the acquisition of new vocalizations. Some taxa, most notably humans and parrots, retain some degree of neurobehavioral plasticity throughout adulthood, but both the extent of this plasticity and the neurogenetic mechanisms underlying it remain unclear. Differential expression of the transcription factor FoxP2 in both songbird and parrot vocal control nuclei has been identified previously as a key pattern facilitating vocal learning. We hypothesize that the resilience of vocal learning to cognitive decline in open-ended learners will be reflected in an absence of age-related changes in neural FoxP2 expression. We tested this hypothesis in the budgerigar (Melopsittacus undulatus), a small gregarious parrot in which adults converge on shared call types in response to shifts in group membership. We formed novel flocks of 4 previously unfamiliar males belonging to the same age class, either "young adult" (6 mo - 1 year) or "older adult" (≥ 3 year), and then collected audio-recordings over a 20-day learning period to assess vocal learning ability. Following behavioral recording, immunohistochemistry was performed on collected neural tissue to measure FoxP2 protein expression in a parrot vocal learning center, the magnocellular nucleus of the medial striatum (MMSt), and its adjacent striatum. RESULTS: Although older adults show lower vocal diversity (i.e. repertoire size) and higher absolute levels of FoxP2 in the MMSt than young adults, we find similarly persistent downregulation of FoxP2 and equivalent vocal plasticity and vocal convergence in the two age cohorts. No relationship between individual variation in vocal learning measures and FoxP2 expression was detected. CONCLUSIONS: We find neural evidence to support persistent vocal learning in the budgerigar, suggesting resilience to aging in the open-ended learning program of this species. The lack of a significant relationship between FoxP2 expression and individual variability in vocal learning performance suggests that other neurogenetic mechanisms could also regulate this complex behavior.

Calling to the collective: contact calling rates within groups of disc-winged bats do not vary by kinship or association.

Many group-living animals coordinate social behaviours using contact calls, which can be produced for all group members or targeted at specific individuals. In the disc-winged bat, Thyroptera tricolor, group members use 'inquiry' and 'response' calls to coordinate daily movements into new roosts (furled leaves). Rates of both calls show consistent among-individual variation, but causes of within-individual variation remain unknown. Here, we tested whether disc-winged bats produce more contact calls towards group members with higher kinship or association. In 446 experimental trials, we recorded 139 random within-group pairs of one flying bat (producing inquiry calls for roost searching) and one roosting bat (producing response calls for roost advertising). Using generalized linear mixed-effect models (GLMM), we assessed how response and inquiry calling rates varied by sender, receiver, genetic kinship and co-roosting association rate. Calling rates varied consistently across senders but not by receiver. Response calling was influenced by inquiry calling rates, but neither calling rate was higher when the interacting pair had higher kinship or association. Rather than dyadic calling rates indicating within-group relationships, our findings are consistent with the hypothesis that bats produce contact calls to maintain contact with any or all individuals within a group while collectively searching for a new roost site. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Evidence for maintenance of key components of vocal learning in ageing budgerigars despite diminished affiliative social interaction.

In some species, the ability to acquire new vocalizations persists into adulthood and may be an important mediator of social interactions. While it is generally assumed that vocal learning persists undiminished throughout the lifespan of these open-ended learners, the stability of this trait remains largely unexplored. We hypothesize that vocal learning exhibits senescence, as is typical of complex cognitive traits, and that this decline relates to age-dependent changes in social behaviour. The budgerigar (Melopsittacus undulatus), an open-ended learner that develops new contact call types that are shared with social associates upon joining new flocks, provides a robust assay for measuring the effects of ageing on vocal learning ability. We formed captive flocks of 4 previously unfamiliar adult males of the same age class, either 'young adults' (6 mo-1 y) or 'older adults' (≥ 3 y), and concurrently tracked changes in contact call structure and social interactions over time. Older adults exhibited decreased vocal diversity, which may be related to sparser and weaker affiliative bonds observed in older adults. Older adults, however, displayed equivalent levels of vocal plasticity and vocal convergence compared to young adults, suggesting that many components of vocal learning are largely maintained into later adulthood in an open-ended learner.

Foraging, Fear and Behavioral Variation in a Traplining Hummingbird.

Traditionally, foraging behavior has been explained as the response to a trade-off between energetic gain from feeding resources and potential costs from concomitant risks. However, an increasing number of studies has shown that this view fails to explain an important fraction of the variation in foraging across a variety of taxa. One potential mechanism that may account for this variation is that various behavioral traits associated with foraging may have different fitness consequences, which may depend on the environmental context. Here, we explored this mechanism by evaluating the foraging efficiency of long-billed hermit hummingbirds (Phaethornis longirostris) with regard to three behavioral traits: (a) exploration (number of feeders used during the foraging visit), (b) risk avoidance (latency to start feeding) and (c) arousal (amount of movements during the foraging visit) in conditions at two different levels of perceived risk (low-control and high-experimental, with a threatening bullet ant model). Foraging efficiency decreased in response to threatening conditions. However, behavioral traits explained additional variation in foraging efficiency in a condition-dependent manner. More exploration was associated with a higher foraging efficiency under control conditions, but this was reversed when exposed to a threat. Regardless of the conditions, arousal was positively associated with foraging efficiency, while risk avoidance was negatively related. Importantly, exploratory behavior and risk avoidance were quite repeatable behaviors, suggesting that they may be related to the intrinsic traits of individuals. Our findings highlight the importance of taking into account additional behavioral dimensions to better understand the foraging strategies of individuals.

The evolution of sexually dimorphic traits in ecological gradients: an interplay between natural and sexual selection in hummingbirds.

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.

Landing manoeuvres predict roost-site preferences in bats.

Roosts are vital for the survival of many species, and how individuals choose one site over another is affected by various factors. In bats, for example, species may use stiff roosts such as caves or compliant ones such as leaves; each type requires not only specific morphological adaptations but also different landing manoeuvres. Selecting a suitable roost within those broad categories may increase landing performance, reducing accidents and decreasing exposure time to predators. We addressed whether bats select specific roost sites based on the availability of a suitable landing surface, which could increase landing performance. Our study focused on Spix's disc-winged bats (Thyroptera tricolor), a species known to roost within developing tubular leaves. As previous studies show that this species relies on the leaves' apex for safe landing and rapid post-landing settlement, we predicted that bats would prefer to roost in tubular structures with a longer apex and that landing would be consistently more effective on those leaves. Field observations showed that T. tricolor predominantly used two species for roosting, Heliconia imbricata and Calathea lutea, but they preferred roosting in the former. The main difference between these two plant species was the length of the leaf's apex (longer in H. imbricata). Experiments in a flight cage also showed that bats used more consistent approach and landing tactics when accessing leaves with a longer apex. Our results suggest that landing mechanics may strongly influence resource selection, especially when complex manoeuvres are needed to acquire those resources.

A machine learning approach for classifying and quantifying acoustic diversity.

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.

Comparative bioacoustics: a roadmap for quantifying and comparing animal sounds across diverse taxa.

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.

Sex role similarity and sexual selection predict male and female song elaboration and dimorphism in fairy-wrens.

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.

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.

Social group signatures in hummingbird displays provide evidence of co-occurrence of vocal and visual learning.

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.

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.

Spatial memory is as important as weapon and body size for territorial ownership in a lekking hummingbird.

Advanced cognitive abilities have long been hypothesized to be important in mating. Yet, most work on sexual selection has focused on morphological traits and its relevance for cognitive evolution is poorly understood. We studied the spatial memory of lekking long-billed hermits (Phaethornis longirostris) and evaluated its role in lek territory ownership, the magnitude of its effect compared to phenotypic traits expected to influence sexual selection, and whether its variation is indicated in the structure of mating vocal signal. Spatial memory (the ability to recall the position of a rewarding feeder) was compared between "territorial" and "floater" males. Interestingly, although spatial memory and body size both positively affected the probability of lek territory ownership, our results suggest a stronger effect of spatial memory. Bill tip length (used as weapon in agonistic interactions) also showed a positive but smaller effect. Load lifting during vertical flight, a measure of physical performance relevant to agonistic interactions, had no effect on territory ownership. Finally, both body size and spatial memory were indicated in the structure of male song: body size negatively correlated with song lowest frequency, while spatial memory positively predicted song consistency. Together, our findings lend support for cognition as a sexual selection target.

Seabird parents provision their chick in a coordinated manner.

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.

Neotropical wrens learn new duet rules as adults.

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.

An RFID Based Smart Feeder for Hummingbirds.

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.

Does Environmental Heterogeneity Promote Cognitive Abilities?

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.

Open-ended song learning in a hummingbird.

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.