Vocal convergence and social proximity shape the calls of the most basal Passeriformes, New Zealand Wrens.

Despite extensive research on avian vocal learning, we still lack a general understanding of how and when this ability evolved in birds. As the closest living relatives of the earliest Passeriformes, the New Zealand wrens (Acanthisitti) hold a key phylogenetic position for furthering our understanding of the evolution of vocal learning because they share a common ancestor with two vocal learners: oscines and parrots. However, the vocal learning abilities of New Zealand wrens remain unexplored. Here, we test for the presence of prerequisite behaviors for vocal learning in one of the two extant species of New Zealand wrens, the rifleman (Acanthisitta chloris). We detect the presence of unique individual vocal signatures and show how these signatures are shaped by social proximity, as demonstrated by group vocal signatures and strong acoustic similarities among distantly related individuals in close social proximity. Further, we reveal that rifleman calls share similar phenotypic variance ratios to those previously reported in the learned vocalizations of the zebra finch, Taeniopygia guttata. Together these findings provide strong evidence that riflemen vocally converge, and though the mechanism still remains to be determined, they may also suggest that this vocal convergence is the result of rudimentary vocal learning abilities.

Hot and dry conditions predict shorter nestling telomeres in an endangered songbird: Implications for population persistence.

Climate warming is increasingly exposing wildlife to sublethal high temperatures, which may lead to chronic impacts and reduced fitness. Telomere length (TL) may link heat exposure to fitness, particularly at early-life stages, because developing organisms are especially vulnerable to adverse conditions, adversity can shorten telomeres, and TL predicts fitness. Here, we quantify how climatic and environmental conditions during early life are associated with TL in nestlings of wild purple-crowned fairy-wrens (Malurus coronatus), endangered songbirds of the monsoonal tropics. We found that higher average maximum air temperature (range 31 to 45 °C) during the nestling period was associated with shorter early-life TL. This effect was mitigated by water availability (i.e., during the wet season, with rainfall), but independent of other pertinent environmental conditions, implicating a direct effect of heat exposure. Models incorporating existing information that shorter early-life TL predicts shorter lifespan and reduced fitness showed that shorter TL under projected warming scenarios could lead to population decline across plausible future water availability scenarios. However, if TL is assumed to be an adaptive trait, population viability could be maintained through evolution. These results are concerning because the capacity to change breeding phenology to coincide with increased water availability appears limited, and the evolutionary potential of TL is unknown. Thus, sublethal climate warming effects early in life may have repercussions beyond individual fitness, extending to population persistence. Incorporating the delayed reproductive costs associated with sublethal heat exposure early in life is necessary for understanding future population dynamics with climate change.

The effect of natural and artificial light at night on nocturnal song in the diurnal willie wagtail.

Artificial light at night (ALAN) has rapidly and drastically changed the global nocturnal environment. Evidence for the effect of ALAN on animal behaviour is mounting and animals are exposed to both point sources of light (street and other surrounding light sources) and broadscale illuminance in the form of skyglow. Research has typically taken a simplified approach to assessing the presence of ALAN, yet to fully understand the ecological impact requires consideration of the different scales and sources of light concurrently. Bird song has previously been well studied for its relationship with light, offering an opportunity to examine the relative impact of different sources of light on behaviour. In this study, we combine correlational and experimental approaches to examine how light at night affects the nocturnal song behaviour of the largely diurnal willie wagtail (Rhipidura leucophrys). Observations of willie wagtails across urban and rural locations in southeastern Australia demonstrated that nocturnal song behaviour increased with the intensity of moonlight in darker rural areas but decreased in areas with high sky glow. In addition, willie wagtails were half as likely to sing at night in the presence of localized light sources such as streetlights in urban and rural areas. Experimental introduction of streetlights to a previously dark area confirmed this relationship: willie wagtail song rates declined when lights were turned on and returned to their original rates following streetlight removal. Our findings show that scale, as well as intensity, are important when considering the impact of light at night as moonlight, sky glow, and localized sources of artificial light have different effects on nocturnal song behaviour.

Variability, heritability and condition-dependence of the multidimensional male colour phenotype in a passerine bird.

Elaborate ornamental traits are commonly assumed to be honest signals of individual quality, owing to the presumed costs involved in their production and/or maintenance. Such traits are often highly variable, possibly because of condition-dependence and/or high underlying genetic variation, and it has been suggested that their expression should be more sensitive to condition and/or more heritable than non-ornamental traits. Many bird species display colourful plumage with multiple distinct patches of different developmental origins, forming complex colour phenotypes. Despite this complexity, colourful ornaments are often studied in isolation, without comparison to suitable non-ornamental controls. Based on plumage reflectance data collected over 8 years, we assessed the signalling potential of the multidimensional male colour phenotype in a tropical bird: the purple-crowned fairy-wren Malurus coronatus. Specifically, we tested the predictions that the expression of putative ornamental colours (purple and black - the breeding colours - and blue) is (1) more variable, (2) more heritable and (3) more condition-dependent compared to year-round non-ornamental colours (buff-white and brown). Our results show that ornamental colours exhibit greater levels of variability, and some chromatic components of purple and blue colouration appear slightly heritable (h² = 0.19-0.30). However, contrary to predictions of heightened condition-dependence in ornaments, only brightness of the buff-white and brown colouration increased with male body condition, although brightness of the purple colouration was related to male age as expected. Despite partial support for predictions, the lack of consistent patterns illustrates the complexity of visual signals and highlights the need to study colour phenotypes in their entirety.

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.

Urban noise restricts, fragments, and lightens sleep in Australian magpies.

Urban areas are inherently noisy, and this noise can disrupt biological processes as diverse as communication, migration, and reproduction. We investigated how exposure to urban noise affects sleep, a process critical to optimal biological functioning, in Australian magpies (Cracticus tibicen). Eight magpies experimentally exposed to noise in captivity for 24-h spent more time awake, and less time in non-rapid eye movement (non-REM) and REM sleep at night than under quiet conditions. Sleep was also fragmented, with more frequent interruptions by wakefulness, shorter sleep episode durations, and less intense non-REM sleep. REM sleep was particularly sensitive to urban noise. Following exposure to noise, magpies recovered lost sleep by engaging in more, and more intense, non-REM sleep. In contrast, REM sleep showed no rebound. This might indicate a long-term cost to REM sleep loss mediated by noise, or contest hypotheses regarding the functional value of this state. Overall, urban noise has extensive, disruptive impacts on sleep composition, architecture, and intensity in magpies. Future work should consider whether noise-induced sleep restriction and fragmentation have long-term consequences.

White and Amber Light at Night Disrupt Sleep Physiology in Birds.

Artificial light at night can disrupt sleep in humans [1-4] and other animals [5-10]. A key mechanism for light to affect sleep is via non-visual photoreceptors that are most sensitive to short-wavelength (blue) light [11]. To minimize effects of artificial light on sleep, many electronic devices shift from white (blue-rich) to amber (blue-reduced) light in the evening. Switching outdoor lighting from white to amber might also benefit wildlife [12]. However, whether these two colors of light affect sleep similarly in different animals remains poorly understood. Here we show, by measuring brain activity, that both white and amber lighting disrupt sleep in birds but that the magnitude of these effects differs between species. When experimentally exposed to light at night at intensities typical of urban areas, domestic pigeons (Columba livia) and wild-caught Australian magpies (Cracticus tibicen tyrannica) slept less, favored non-rapid eye movement (NREM) sleep over REM sleep, slept less intensely, and had more fragmented sleep compared to when lights were switched off. In pigeons, these disruptive effects on sleep were similar for white and amber lighting. For magpies, however, amber light had less impact on sleep. Our results demonstrate that amber lighting can minimize sleep disruption in some birds but that this benefit may not be universal. VIDEO ABSTRACT.

Rapid plastic breeding response to rain matches peak prey abundance in a tropical savanna bird.

Changes in climate are shifting the timing of life cycle events in the natural world. Compared to northern temperate areas, these effects are relatively poorly understood in tropical and southern regions, where there is limited information on how timing of breeding and food availability are affected by climatic factors, and where patterns of breeding activity are more unpredictable within and between years. Combining a new statistical modelling approach with 5 years of continuous individual-based monitoring of a monsoonal tropical insectivorous bird, we quantified (a) the proximate climatic drivers at two trophic levels: timing of breeding and abundance of arthropod prey; (b) the effect of climate variation on reproductive output and (c) the role of individual plasticity. Rainfall was identified as the main determinant of phenology at both trophic levels. Throughout the year, likelihood of egg laying increased very rapidly in response to even small amounts of rain during the preceding 0-3 weeks. Adult body mass and male sperm storage also increased rapidly after rain, suggesting high breeding preparedness. Additionally, females were flexible, since they were more likely to nest whether their previous attempt was longer ago and unsuccessful. Arthropod abundance also increased after rainfall, but more slowly, with a peak around 10 weeks. Therefore, the peak food availability coincided with the presence of dependent fledglings. Fitness benefits of nesting after more rain appeared to be linked to offspring quantity rather than quality: nest attempts following higher rainfall produced larger clutches, but showed no improvement in nestling mass or relative fledging success. The response of clutch size to rainfall was plastic, since repeated sampling showed that individual females laid larger clutches after more rain, possibly mediated by improved body mass. Rapid, individually flexible breeding in response to rainfall and slower increase in arthropod abundance also as a response to rainfall, might buffer insectivorous species living in tropical seasonal environments from climate change-induced phenological trophic mismatches.

New insights from female bird song: towards an integrated approach to studying male and female communication roles.

Historically, bird song has been regarded as a sex-specific signalling trait; males sing to attract females and females drive the evolution of signal exaggeration by preferring males with ever more complex songs. This view provides no functional role for female song. Historic geographical research biases generalized pronounced sex differences of phylogenetically derived northern temperate zone songbirds to all songbirds. However, we now know that female song is common and that both sexes probably sang in the ancestor of modern songbirds. This calls for research on adaptive explanations and mechanisms regulating female song, and a reassessment of questions and approaches to identify selection pressures driving song elaboration in both sexes and subsequent loss of female song in some clades. In this short review and perspective we highlight newly emerging questions and propose a research framework to investigate female song and song sex differences across species. We encourage experimental tests of mechanism, ontogeny, and function integrated with comparative evolutionary analyses. Moreover, we discuss the wider implications of female bird song research for our understanding of male and female communication roles.

Conspicuous Plumage Does Not Increase Predation Risk: A Continent-Wide Test Using Model Songbirds.

The forces shaping female plumage color have long been debated but remain unresolved. Females may benefit from conspicuous colors but are also expected to suffer costs. Predation is one potential cost, but few studies have explicitly investigated the relationship between predation risk and coloration. The fairy-wrens show pronounced variation in female coloration and reside in a wide variety of habitats across Australasia. Species with more conspicuous females are found in denser habitats, suggesting that conspicuousness in open habitat increases vulnerability to predators. To test this, we measured attack rates on 3-D-printed models mimicking conspicuously colored males and females and dull females in eight different fairy-wren habitats across Australia. Attack rates were higher in open habitats and at higher latitudes. Contrary to our predictions, dull female models were attacked at similar rates to the conspicuous models. Further, the probability of attack in open habitats increased more for both types of female models than for the conspicuous male model. Across models, the degree of contrast (chromatic and achromatic) to environmental backgrounds was unrelated to predation rate. These findings do not support the long-standing hypothesis that conspicuous plumage, in isolation, is costly due to increased attraction of predators. Our results indicate that conspicuousness interacts with other factors in driving the evolution of plumage coloration.

Persistent low avian malaria in a tropical species despite high community prevalence.

Malarial and other haemosporidian parasites are widespread; however, their temporal dynamics are ill-understood. Longitudinal sampling of a threatened riparian bird revealed a consistently very low prevalence over 13 years (∼5%) despite infections persisting and prevalence increasing with age. In contrast, three key species within this tropical community were highly infected (∼20-75% prevalence) and these differences were stable. Although we found novel lineages and phylogenetic structure at the local level, there was little geographic structuring within Australasia. This study suggests that malarial parasite susceptibility is determined by host factors and that species can maintain low levels despite high community prevalence.

Early-life telomere length predicts lifespan and lifetime reproductive success in a wild bird.

Poor conditions during early development can initiate trade-offs that favour current survival at the expense of somatic maintenance and subsequently, future reproduction. However, the mechanisms that link early and late life-history are largely unknown. Recently it has been suggested that telomeres, the nucleoprotein structures at the terminal end of chromosomes, could link early-life conditions to lifespan and fitness. In wild purple-crowned fairy-wrens, we combined measurements of nestling telomere length (TL) with detailed life-history data to investigate whether early-life TL predicts fitness prospects. Our study differs from previous studies in the completeness of our fitness estimates in a highly philopatric population. The association between TL and survival was age-dependent with early-life TL having a positive effect on lifespan only among individuals that survived their first year. Early-life TL was not associated with the probability or age of gaining a breeding position. Interestingly, early-life TL was positively related to breeding duration, contribution to population growth and lifetime reproductive success because of their association with lifespan. Thus, early-life TL, which reflects growth, accumulated early-life stress and inherited TL, predicted fitness in birds that reached adulthood but not noticeably among fledglings. These findings suggest that a lack of investment in somatic maintenance during development particularly affects late life performance. This study demonstrates that factors in early-life are related to fitness prospects through lifespan, and suggests that the study of telomeres may provide insight into the underlying physiological mechanisms linking early- and late-life performance and trade-offs across a lifetime.

From ornament to armament or loss of function? Breeding plumage acquisition in a genetically monogamous bird.

The evolution of conspicuous male traits is thought to be driven by female mate choice or male-male competition. These two mechanisms are often viewed as distinct processes, with most studies focusing on female choice. However, both mechanisms of sexual selection can act simultaneously on the same trait (i.e., dual function) and/or interact in a synergistic or conflicting way. Dual-function traits are commonly assumed to originate through male-male competition before being used in female choice; yet, most studies focusing on such traits could not determine the direction of change, lacking phylogenetic information. We investigated the role of conspicuous male seasonal plumage in male-male competitive interactions in the purple-crowned fairy-wren Malurus coronatus, a cooperatively breeding bird. Male breeding plumage in most Malurus species is selected by female choice through extra-pair mate choice, but unlike its congeners, M. coronatus is genetically monogamous, and females do not seem to choose males based on breeding plumage acquisition. Our study shows that, within groups, subordinate males that were older, and therefore higher-ranked in the queue for breeder position inheritance, produced a more complete breeding plumage. In line with this, subordinate males that were older and/or displayed a more complete breeding plumage were more successful in competitively acquiring a breeder position. A role as a signal of competitive ability was experimentally confirmed by presenting models of males: in breeding colours, these received more aggression from resident breeder males than in nonbreeding colours, but elicited limited response from females, consistent with competitors in breeding plumage being perceived as a bigger threat to the breeder male. The role of the conspicuous breeding plumage in mediating male-male interactions might account for its presence in this genetically monogamous species. As phylogenetic reconstructions suggest a past female choice function in M. coronatus, this could represent a sexual trait that shifted functions, or a dual-function trait that lost one function. These evolutionary scenarios imply that intra- and intersexual functions of ornaments may be gained or lost independently and offer new perspectives in understanding the complex dynamics of sexual selection.

Multiple hypotheses explain variation in extra-pair paternity at different levels in a single bird family.

Extra-pair paternity (EPP), where offspring are sired by a male other than the social male, varies enormously both within and among species. Trying to explain this variation has proved difficult because the majority of the interspecific variation is phylogenetically based. Ideally, variation in EPP should be investigated in closely related species, but clades with sufficient variation are rare. We present a comprehensive multifactorial test to explain variation in EPP among individuals in 20 populations of nine species over 89 years from a single bird family (Maluridae). Females had higher EPP in the presence of more helpers, more neighbours or if paired incestuously. Furthermore, higher EPP occurred in years with many incestuous pairs, populations with many helpers and species with high male density or in which males provide less care. Altogether, these variables accounted for 48% of the total and 89% of the interspecific and interpopulation variation in EPP. These findings indicate why consistent patterns in EPP have been so challenging to detect and suggest that a single predictor is unlikely to account for the enormous variation in EPP across levels of analysis. Nevertheless, it also shows that existing hypotheses can explain the variation in EPP well and that the density of males in particular is a good predictor to explain variation in EPP among species when a large part of the confounding effect of phylogeny is excluded.

Habitat structure is linked to the evolution of plumage colour in female, but not male, fairy-wrens.

BACKGROUND: Both natural and sexual selection may drive the evolution of plumage colouration in birds. This can lead to great variation in plumage not only across species, but also between sexes within species. Australasian fairy-wrens are famous for their brightly coloured males, which exhibit colours ranging from bright blue to red and black. Female plumage in fairy wrens (and in general) has been rarely studied, but it can also be highly variable, including both bright and cryptic plumages. We use a comparative framework to explore the basis for this variation, and test the possibility that female fairy-wrens experience selection for cryptic plumage when they occupy more exposed habitats that offer little concealment from predators. We use spectral measurements of plumage for species and subspecies of Australasian fairy-wrens. RESULTS: We show that female colouration (contrast against background) is strongly correlated with vegetation cover: females in open habitats show less contrast to background colours than females in closed habitats, while male colouration is not associated with habitat type. CONCLUSIONS: Female plumage appears to be under stronger natural selection than male plumage in fairy-wrens, providing an example of how selection may act differently on males and females of the same species.

Personality and innate immune defenses in a wild bird: Evidence for the pace-of-life hypothesis.

We tested the two main evolutionary hypotheses for an association between immunity and personality. The risk-of-parasitism hypothesis predicts that more proactive (bold, exploratory, risk-taking) individuals have more vigorous immune defenses because of increased risk of parasite exposure. In contrast, the pace-of-life hypothesis argues that proactive behavioral styles are associated with shorter lifespans and reduced investment in immune function. Mechanistically, associations between immunity and personality can arise because personality differences are often associated with differences in condition and stress responsiveness, both of which are intricately linked with immunity. Here we investigate the association between personality (measured as proactive exploration of a novel environment) and three indices of innate immune function (the non-specific first line of defense against parasites) in wild superb fairy-wrens Malurus cyaneus. We also quantified body condition, hemoparasites (none detected), chronic stress (heterophil:lymphocyte ratio) and circulating corticosterone levels at the end of the behavioral test (CORT, in a subset of birds). We found that fast explorers had lower titers of natural antibodies. This result is consistent with the pace-of-life hypothesis, and with the previously documented higher mortality of fast explorers in this species. There was no interactive effect of exploration score and duration in captivity on immune indices. This suggests that personality-related differences in stress responsiveness did not underlie differences in immunity, even though behavioral style did modulate the effect of captivity on CORT. Taken together these results suggest reduced constitutive investment in innate immune function in more proactive individuals.

Territory configuration moderates the frequency of extra-group mating in superb fairy-wrens.

The frequency of extra-pair paternity (EPP) in socially monogamous birds varies substantially between and within species, but ecological drivers of this variation remain poorly understood. Habitat configuration could influence EPP by moderating access to extra-pair mates, because species occupying territories in a clustered 'honeycomb' configuration have a larger pool of potential extra-group mates in their immediate neighbourhood than those living in linearly arranged territories (e.g. along narrow strips of riparian or fragmented habitat). We exploited variation in the spatial arrangement of territories due to anthropogenic modification of habitat of the cooperatively breeding superb fairy-wren Malurus cyaneus to test whether habitat configuration influenced the frequency of EPP. In this species, most paternity is obtained by males outside the social group [extra-group paternity (EGP)]. We found that the frequency of EGP among groups living in linear strips of roadside vegetation (41% of 44 offspring) was lower than it was for groups living in clustered territories within continuous habitat (59% of 70 offspring). Differences in group size and pair relatedness did not explain differences in EGP associated with territory configuration, although the frequency of EGP was negatively correlated with pair relatedness. Our finding suggests that territory configuration can influence rates of EGP and that anthropogenic habitat fragmentation has the potential to limit access to extra-pair mates, affecting mating systems and ultimately fitness.

Migration and the evolution of duetting in songbirds.

Many groups of animals defend shared resources with coordinated signals. The best-studied of these signals are the vocal duets produced by mated pairs of birds. Duets are believed to be more common among tropical-breeding species, but a comprehensive test of this hypothesis is lacking, and the mechanisms that generate latitudinal patterns in duetting are not known. We used a stratified sample of 372 songbird species to conduct the first broad-scale, phylogenetically explicit analysis of duet evolution. We found that duetting evolves in association with the absence of migration, but not with sexual monochromatism or tropical breeding. We conclude that the evolution of migration exerts a major influence on the evolution of duetting. The perceived association between tropical breeding and duetting may be a by-product of the migration-duetting relationship. Migration reduces the average duration of partnerships, potentially reducing the benefits of cooperative behaviour, including duetting. Ultimately, the evolution of coordinated resource-defence signals in songbirds may be driven by ecological conditions that favour sedentary lifestyles and social stability.

Female song is widespread and ancestral in songbirds.

Bird song has historically been considered an almost exclusively male trait, an observation fundamental to the formulation of Darwin's theory of sexual selection. Like other male ornaments, song is used by male songbirds to attract females and compete with rivals. Thus, bird song has become a textbook example of the power of sexual selection to lead to extreme neurological and behavioural sex differences. Here we present an extensive survey and ancestral state reconstruction of female song across songbirds showing that female song is present in 71% of surveyed species including 32 families, and that females sang in the common ancestor of modern songbirds. Our results reverse classical assumptions about the evolution of song and sex differences in birds. The challenge now is to identify whether sexual selection alone or broader processes, such as social or natural selection, best explain the evolution of elaborate traits in both sexes.

Animal behaviour: a song and dance about lyrebirds.

Coordinating movements to music is often considered a uniquely human skill. A new study dispels this notion by showing that male Australian lyrebirds also perform 'dance' moves which are predictably matched with specific songs in their display routines.