Malurus Cyaneus Research Articles

Does signal deterioration compromise eavesdropping on other species' alarm calls?

Individuals gain valuable information by eavesdropping on others species' signals, but there are potentially greater constraints on eavesdropping than reception of signals from conspecifics. Eavesdroppers rely on signals addressed to others, which may come from unpredictable directions and distances. Furthermore, eavesdroppers might lack familiarity with other species' calls or perceptual adaptations to detect and recognize them, and these difficulties may be exacerbated by signal changes during transmission. We tested whether signal changes differentially affected the response to heterospecific compared with conspecific aerial (‘hawk’) alarm calls in two sympatric species that respond to each other's alarms, superb fairy-wrens, Malurus cyaneus, and white-browed scrubwrens, Sericornis frontalis. We assessed the effects of signal attenuation (reduced amplitude) and degradation (including reverberation). Attenuation caused a reduction in probability of fleeing to cover, and birds were less likely to flee to heterospecific than conspecific alarms. Signal changes did affect the response to heterospecific compared to conspecific calls, but not in the simple way expected. For conspecifics, degradation had no effect, and attenuation caused a similar reduction in fleeing for degraded and undegraded calls. By contrast, for heterospecifics, attenuation caused a reduction in fleeing for undegraded but not degraded calls, which prompted constant, low fleeing rates. Additional measures of response suggest that a lower probability of fleeing was partly a consequence of poorer detection or recognition of calls, and not merely assessment of reduced danger. Overall, the results are consistent with greater constraints on heterospecific eavesdropping than conspecific communication, perhaps because of lower familiarity or perceptual specialization.

Wild Birds Learn to Eavesdrop on Heterospecific Alarm Calls

Many vertebrates gain critical information about danger by eavesdropping on other species' alarm calls [1], providing an excellent context in which to study information flow among species in animal communities [2-4]. A fundamental but unresolved question is how individuals recognize other species' alarm calls. Although individuals respond to heterospecific calls that are acoustically similar to their own, alarms vary greatly among species, and eavesdropping probably also requires learning [1]. Surprisingly, however, we lack studies demonstrating such learning. Here, we show experimentally that individual wild superb fairy-wrens, Malurus cyaneus, can learn to recognize previously unfamiliar alarm calls. We trained individuals by broadcasting unfamiliar sounds while simultaneously presenting gliding predatory birds. Fairy-wrens in the experiment originally ignored these sounds, but most fled in response to the sounds after two days' training. The learned response was not due to increased responsiveness in general or to sensitization following repeated exposure and was independent of sound structure. Learning can therefore help explain the taxonomic diversity of eavesdropping and the refining of behavior to suit the local community. In combination with previous work on unfamiliar predator recognition (e.g., [5]), our results imply rapid spread of anti-predator behavior within wild populations and suggest methods for training captive-bred animals before release into the wild [6]. A remaining challenge is to assess the importance and consequences of direct association of unfamiliar sounds with predators, compared with social learning-such as associating unfamiliar sounds with conspecific alarms.

Contrasting effects of climate on juvenile body size in a Southern Hemisphere passerine bird.

Despite extensive research on the topic, it has been difficult to reach general conclusions as to the effects of climate change on morphology in wild animals: in particular, the effects of warming temperatures have been associated with increases, decreases or stasis in body size in different populations. Here, we use a fine-scale analysis of associations between weather and offspring body size in a long-term study of a wild passerine bird, the cooperatively breeding superb fairy-wren, in south-eastern Australia to show that such variation in the direction of associations occurs even within a population. Over the past 26years, our study population has experienced increased temperatures, increased frequency of heatwaves and reduced rainfall - but the mean body mass of chicks has not changed. Despite the apparent stasis, mass was associated with weather across the previous year, but in multiple counteracting ways. Firstly, (i) chick mass was negatively associated with extremely recent heatwaves, but there also positive associations with (ii) higher maximum temperatures and (iii) higher rainfall, both occurring in a period prior to and during the nesting period, and finally (iv) a longer-term negative association with higher maximum temperatures following the previous breeding season. Our results illustrate how a morphological trait may be affected by both short- and long-term effects of the same weather variable at multiple times of the year and that these effects may act in different directions. We also show that climate within the relevant time windows may not be changing in the same way, such that overall long-term temporal trends in body size may be minimal. Such complexity means that analytical approaches that search for a single 'best' window for one particular weather variable may miss other relevant information, and is also likely to make analyses of phenotypic plasticity and prediction of longer-term population dynamics difficult.

Superb Fairy-wrens (Malurus cyaneus) increase vigilance near their nest with the perceived risk of brood parasitism

Brood parasites typically impose costs on their hosts, which select for host defenses. However, where defenses are costly, hosts can benefit by facultative expression of defenses in relation to the risk of parasitism. The results of our model-presentation experiments show that Superb Fairy-wrens (Malurus cyaneus) mediate vigilance around their nest according to their perceived risk of brood parasitism; when the risk of parasitism is high, they increase the time they spend in the vicinity of their nests. In combination with previous studies, these data suggest that Superb Fairy-wrens have a plastic defense portfolio that can be acquired rapidly and deployed facultatively to prevent parasitism while minimizing wasteful investment in defenses in the absence of parasitism.

Animal personality and pace-of-life syndromes: do fast-exploring fairy-wrens die young?

The pace-of-life syndrome (POLS) hypothesis for animal personality proposes that variation among individuals in life-history strategies is associated with consistent differences in behavior. We tested predictions of this hypothesis in the superb fairy-wren, Malurus cyaneus, by investigating long-term individual differences in risk-related behaviors (latency to enter a novel artificial environment, exploration, activity and response to mirror image stimulation) and survival. We found consistent differences between individuals in these behaviors (adjusted repeatability of exploration of artificial novel environment = 0.37). Individual differences were consistent over several years and bi-variate analyses showed a significant among-individual correlation (‘behavioral syndrome’) between exploration behavior at two life stages (young adult and old adult). Docility at the nestling stage predicted exploration behavior of juveniles. Behavioral traits measured in a risky context were correlated with one another, forming a behavioral syndrome of coping strategies ranging from ‘proactive’ to ‘reactive’. Nestlings that were more active and exploratory in isolation were less docile during handling, while adults that entered the artificial environment fast were more exploratory, active, and aggressive in the artificial environment. Exploration behavior increased within individuals as they aged and when they were in poorer condition, consistent with expectations of more risk-prone behavior with lower residual reproductive value (reduced ‘asset protection’). Risk-related behavior predicted the probability of apparent survival: more exploratory individuals were less likely to be present in the population twelve months later. Our findings suggest that, consistent with the predictions of the POLS hypothesis, individual variation in survival is associated with consistent individual differences in risk-related behavior that are maintained long-term and span developmental boundaries.

Differential influence of urbanisation on Coccidian infection in two passerine birds.

Urbanisation has the potential to increase the risk of parasitism on wildlife. Although some ectoparasite groups appear unaffected, different responses are hypothesised for parasites with simpler life histories such as gastrointestinal parasites. Red-browed finches (RBF) and the superb fairywrens (SFW), two native passerine birds affected by urbanisation, were examined for Coccidian parasites along an urbanisation gradient in New South Wales, Australia, in order to detect if prevalence might be directly related to the degree of urbanisation. Influence of urbanisation on Coccidian infection was differential. In RBF, the prevalence of Isospora increased significantly in more urbanised areas but prevalence did not change between breeding and non-breeding seasons. In contrast, in SFW, the degree of urbanisation did not significantly change with the degree of urbanisation, and season exhibited no significant effects on the prevalence of coccidians. Diet, behaviour and habits are suspected to be the most influential factors on the variation seen between both species where granivorous and gregarious species are significantly infected. Since the dynamics of urban wildlife-pathogen interactions is largely unexplored, more studies are needed to corroborate if this pattern of Isospora infections can be extended to other passerine birds in cities from Australia and overseas.

Prenatal learning in an Australian songbird: habituation and individual discrimination in superb fairy-wren embryos.

Embryos were traditionally considered to possess limited learning abilities because of the immaturity of their developing brains. By contrast, neonates from diverse species show behaviours dependent on prior embryonic experience. Stimulus discrimination is a key component of learning and has been shown by a handful of studies in non-human embryos. Superb fairy-wren embryos (Malurus cyaneus) learn a vocal password that has been taught to them by the attending female during incubation. The fairy-wren embryos use the learned element as their begging call after hatching to solicit more parental feeding. In this study, we test whether superb fairy-wren embryos have the capacity to discriminate between acoustical stimuli and whether they show non-associative learning. We measured embryonic heart rate response using a habituation/dishabituation paradigm with eggs sourced from nests in the wild. Fairy-wren embryos lowered their heart rate in response to the broadcasts of conspecific versus heterospecific calls, and in response to the calls of novel conspecific individuals. Thus, fairy-wrens join humans as vocal-learning species with known prenatal learning and individual discrimination.

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.

The cost of teaching embryos in superb fairy-wrens

There is growing empirical support for teaching in nonhuman animals. To unravel the evolutionary dynamics of teaching, we need to understand its costs and benefits. In superb fairy-wrens (Malurus cyaneus), females teach their embryos by calling to them: embryos learn a vocal password, and hatchlings incorporate the learned vocal password into their begging calls to solicit parental feeding. The more a female teaches (higher call rate), the better the embryos learn (greater call similarity), leading to more food provisioning by parents. Given these direct benefits, we would expect all female fairy-wrens to call often to maximize embryonic learning in their genetic progeny, yet they do not. Teaching the password carries a severe cost: nest predation was higher at both natural and artificial nests that had more incubation calls. At artificial nests, predation was 8-fold higher for high incubation call rate (30 calls per hour) and 5-fold higher for low incubation call rate (15 calls per hour) compared with nests without any incubation calls. At natural nests, nests that were depredated during incubation had higher incubation call rate (18.3 calls per hour) than nests that survived (11.4 calls per hour). Mother fairy-wrens must trade-off the costs of calling and the benefits of learning to optimize fitness benefits of teaching.

Females that experience threat are better teachers.

Superb fairy-wren (Malurus cyaneus) females use an incubation call to teach their embryos a vocal password to solicit parental feeding care after hatching. We previously showed that high call rate by the female was correlated with high call similarity in fairy-wren chicks, but not in cuckoo chicks, and that parent birds more often fed chicks with high call similarity. Hosts should be selected to increase their defence behaviour when the risk of brood parasitism is highest, such as when cuckoos are present in the area. Therefore, we experimentally test whether hosts increase call rate to embryos in the presence of a singing Horsfield's bronze-cuckoo (Chalcites basalis). Female fairy-wrens increased incubation call rate when we experimentally broadcast cuckoo song near the nest. Embryos had higher call similarity when females had higher incubation call rate. We interpret the findings of increased call rate as increased teaching effort in response to a signal of threat.

When subspecies matter: resident Superb Fairy-wrens (Malurus cyaneus) distinguish the sex and subspecies of intruding birds

The widely accepted functions of complex bird song—to defend a territory or attract a mate, or both—have generally been tested in northern hemisphere species in which males produce the song and females choose the singer. In our study species, the Superb Fairy-wren (Malurus cyaneus), both males and females sing a solo song throughout the year. We compare the chatter song in males and females of two genetically distinct subspecies, and test if resident birds respond to the sex and subspecies of the intruder song. Compared with island birds (M. c. ashbyi), mainland Superb Fairy-wrens (M. c. leggei) produced songs with lower frequency and fewer elements. Compared with females, males produced longer songs with more elements. Resident birds showed acoustical discrimination for the sex and subspecies of the intruder bird. The response of resident pairs was positively correlated, but each sex showed a solo response. Resident males were the first to respond to male intruders, and resident females were the first to respond to female intruders. Fairy-wrens had the strongest response towards (1) intruders of the same subspecies and (2) male intruders. The finding of signal divergence and acoustical discrimination in males and females makes this a model system to test the mechanism of reproductive isolation when both sexes sing.

Social learning of a brood parasite by its host

Arms races between brood parasites and their hosts provide model systems for studying the evolutionary repercussions of species interactions. However, how naive hosts identify brood parasites as enemies remains poorly understood, despite its ecological and evolutionary significance. Here, we investigate whether young, cuckoo-naive superb fairy-wrens, Malurus cyaneus, can learn to recognize cuckoos as a threat through social transmission of information. Naive individuals were initially unresponsive to a cuckoo specimen, but after observing conspecifics mob a cuckoo, they made more whining and mobbing alarm calls, and spent more time physically mobbing the cuckoo. This is the first direct evidence that naive hosts can learn to identify brood parasites as enemies via social learning.

Reduced rainfall explains avian declines in an unfragmented landscape: incremental steps toward an empty forest?

Declines of formerly widespread bird species are being increasingly reported, with habitat loss, agricultural intensification and reduced rainfall frequently implicated. We report on temporal changes in the occurrence of birds over 21 years within continuous forest in the Warrumbungle Mountains to evaluate the influence of rainfall variability on changes in the abundance of birds and species occurence. During this period, six common insectivores declined significantly (Superb Fairy-wren, Malurus cyaneus; White-throated Gerygone, Gerygone albogularis; Grey Shrike-thrush, Colluricincla harmonica; Rufous Whistler, Pachycephala rufiventris; Grey Fantail, Rhipidura albiscapa; Eastern Yellow Robin, Eopsaltria australis). Rainfall significantly predicted the abundance of 13 of the 25 most common species, with the rainfall period of both July-December of the previous year and the combined effects of six years of January-June rainfall correlated with changes in the abundance of birds. Prolonged drought has likely driven food shortages (especially of litterdwelling arthropods), with changes in avian community composition reflecting changes in food availability. Thus, avian declines in southern Australia may reflect the combined effects of habitat fragmentation and other landscape-scale changes in concert with larger-scale ecological processes driven by decreased rainfall. Improved linkages between forested and agricultural landscapes at the regional scale are needed to buffer against local fluctuations in resources.

Host response to cuckoo song is predicted by the future risk of brood parasitism

IntroductionRisk assessment occurs over different temporal and spatial scales and is selected for when individuals show an adaptive response to a threat. Here, we test if birds respond to the threat of brood parasitism using the acoustical cues of brood parasites in the absence of visual stimuli. We broadcast the playback of song of three brood parasites (Chalcites cuckoo species) and a sympatric non-parasite (striated thornbill, Acanthiza lineata) in the territories of superb fairy-wrens (Malurus cyaneus) during the peak breeding period and opportunistic breeding period. The three cuckoo species differ in brood parasite prevalence and the probability of detection by the host, which we used to rank the risk of parasitism (high risk, moderate risk, low risk).ResultsHost birds showed the strongest response to the threat of cuckoo parasitism in accordance with the risk of parasitism. Resident wrens had many alarm calls and close and rapid approach to the playback speaker that was broadcasting song of the high risk brood parasite (Horsfield’s bronze-cuckoo, C. basalis) across the year (peak and opportunistic breeding period), some response to the moderate risk brood parasite (shining bronze-cuckoo, C. lucidus) during the peak breeding period, and the weakest response to the low risk brood parasite (little bronze-cuckoo, C. minutillus). Playback of the familiar control stimulus in wren territories evoked the least response.ConclusionHost response to the threat of cuckoo parasitism was assessed using vocal cues of the cuckoo and was predicted by the risk of future parasitism.

Lysozyme-associated bactericidal activity in the ejaculate of a wild passerine

Numerous antibacterial substances have been identified in the ejaculates of animals and are suggested to protect sperm from bacterial-induced damage in both the male and female reproductive tracts. Lysozymes, enzymes that exhibit bactericidal activity through their ability to break down bacterial cell walls, are likely to be particularly important for sperm defence as they are part of the constitutive innate immune system and are thus immediately available to protect sperm from bacterial attack. Birds are an ideal model for studies of ejaculate antimicrobial defences because of the dual function of the avian cloaca (i.e. waste excretion and sperm transfer), yet the antibacterial activity of avian ejaculates remains largely unexplored, and data on ejaculate lysozyme levels are only available for the domestic turkey (Meleagris gallopavo). Moreover, ejaculate lysozyme levels have not been reported for any species in the wild; which many argue is necessary to gain a comprehensive understanding of the function and dynamics of immune responses. Here, we show that lysozyme is present in the ejaculate of a wild passerine, the superb fairy-wren (Malurus cyaneus), and that the concentration of lysozyme in ejaculates varies substantially among males. This variation, however, is not associated with male condition, sperm quality or plumage coloration. Nevertheless, we suggest that lysozyme-associated antibacterial activity in ejaculates may be the target of natural and sexual selection and that these enzymes are likely to function in defending avian sperm from bacterial-induced damage. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 92–100.

Alarming features: birds use specific acoustic properties to identify heterospecific alarm calls.

Vertebrates that eavesdrop on heterospecific alarm calls must distinguish alarms from sounds that can safely be ignored, but the mechanisms for identifying heterospecific alarm calls are poorly understood. While vertebrates learn to identify heterospecific alarms through experience, some can also respond to unfamiliar alarm calls that are acoustically similar to conspecific alarm calls. We used synthetic calls to test the role of specific acoustic properties in alarm call identification by superb fairy-wrens, Malurus cyaneus. Individuals fled more often in response to synthetic calls with peak frequencies closer to those of conspecific calls, even if other acoustic features were dissimilar to that of fairy-wren calls. Further, they then spent more time in cover following calls that had both peak frequencies and frequency modulation rates closer to natural fairy-wren means. Thus, fairy-wrens use similarity in specific acoustic properties to identify alarms and adjust a two-stage antipredator response. Our study reveals how birds respond to heterospecific alarm calls without experience, and, together with previous work using playback of natural calls, shows that both acoustic similarity and learning are important for interspecific eavesdropping. More generally, this study reconciles contrasting views on the importance of alarm signal structure and learning in recognition of heterospecific alarms.

Eavesdropping on the neighbours: fledglings learn to respond to heterospecific alarm calls

Young birds and mammals suffer from a high risk of predation, and should be under strong selection for early response to cues indicating danger, including the alarm calls of other species. Despite this prediction, there has been little investigation of the development of response by young animals to heterospecific alarm calls, and none on fledgling birds. Previous studies have suggested that learning is important in the recognition of heterospecific alarm calls in adult birds, but when learning occurs is unknown. We examined the responses of fledgling white-browed scrubwrens, Sericornis frontalis, at three ages to playback of the aerial alarm calls of the sympatric superb fairy-wren, Malurus cyaneus, and New Holland honeyeater, Phylidonyris novaehollandiae. Fairy-wren and scrubwren alarm calls are acoustically similar, while honeyeater alarm calls are distinct, but adult scrubwrens respond to both. Recently fledged scrubwrens responded strongly to conspecific alarm calls, but weakly to heterospecific alarm calls. By contrast, only 2 weeks after leaving the nest most fledglings responded to fairy-wren and honeyeater alarm calls similarly to conspecific alarm calls. However, fledglings in territories without honeyeaters ignored honeyeater alarm calls. Three weeks later, fledglings on all territories responded to all heterospecific alarm calls, an identical response to that of their parents. These results demonstrate that fledglings can quickly develop appropriate responses to heterospecific alarm calls, and present strong evidence that response is learned over a microgeographical scale.

Disrupted fine-scale population processes in fragmented landscapes despite large-scale genetic connectivity for a widespread and common cooperative breeder: the superb fairy-wren (Malurus cyaneus)

Understanding how habitat fragmentation affects population processes (e.g. dispersal) at different spatial scales is of critical importance to conservation. We assessed the effects of habitat fragmentation on dispersal and regional and fine-scale population structure in a currently widespread and common cooperatively breeding bird species found across south-eastern Australia, the superb fairy-wren Malurus cyaneus. Despite its relative abundance and classification as an urban tolerant species, the superb fairy-wren has declined disproportionately from low tree-cover agricultural landscapes across the Box-Ironbark region of north-central Victoria, Australia. Loss of genetic connectivity and disruption to its complex social system may be associated with the decline of this species from apparently suitable habitat in landscapes with low levels of tree cover. To assess whether reduced structural connectivity has had negative consequences for genetic connectivity in the superb fairy-wren, we used a landscape-scale approach to compare patterns of genetic diversity and gene flow at large (landscape/regional) and fine (site-level) spatial scales. In addition, using genetic distances, for each sex, we tested landscape models of decreased dispersal through treeless areas (isolation-by-resistance) while controlling for the effect of isolation-by-distance. Landscape models indicated that larger-scale gene flow across the Box-Ironbark region was constrained by distance rather than by lack of structural connectivity. Nonetheless, a pattern of isolation-by-resistance for males (the less-dispersive sex) and lower genetic diversity and higher genetic similarity within sites in low-cover fragmented landscapes indicated disruption to fine-scale gene flow mechanisms and/or mating systems. Although loss of structural connectivity did not appear to impede gene flow at larger spatial scales, fragmentation appeared to affect fine-scale population processes (e.g. local gene flow mechanisms and/or mating systems) adversely and may contribute to the decline of superb fairy-wrens in fragmented landscapes in the Box-Ironbark region.

Embryonic Learning of Vocal Passwords in Superb Fairy-Wrens Reveals Intruder Cuckoo Nestlings

How do parents recognize their offspring when the cost of making a recognition error is high? Avian brood parasite-host systems have been used to address this question because of the high cost of parasitism to host fitness. We discovered that superb fairy-wren (Malurus cyaneus) females call to their eggs, and upon hatching, nestlings produce begging calls with key elements from their mother's "incubation call." Cross-fostering experiments showed highest similarity between foster mother and nestling calls, intermediate similarity with genetic mothers, and least similarity with parasitic Horsfield's bronze-cuckoo (Chalcites basalis) nestlings. Playback experiments showed that adults respond to the begging calls of offspring hatched in their own nest and respond less to calls of other wren or cuckoo nestlings. We conclude that wrens use a parent-specific password learned embryonically to shape call similarity with their own young and thereby detect foreign cuckoo nestlings.

Learning to listen? Nestling response to heterospecific alarm calls

Many nestling birds go silent in response to parental alarm calls, potentially lowering their risk of being overheard by predators. Parents are not always nearby, however, and so offspring could also benefit if they respond to the alarm calls of other species. Response could be innate, particularly if heterospecific alarm calls are acoustically similar to conspecific alarms, or learned through experience or association with parental behaviour. We investigated the responses of both young (5–6 days old) and older (10–11 days old, close to fledging) nestling white-browed scrubwrens, Sericornis frontalis , to the mobbing alarm calls of three heterospecifics whose nests are vulnerable to similar predators. Brown thornbills, Acanthiza pusilla , produce the most similar alarm calls to scrubwrens, while superb fairy-wren, Malurus cyaneus , and New Holland honeyeater, Phylidonyris novaehollandiae , produce alarm calls that are distinct. Heterospecific mobbing assays demonstrated that nestlings were likely to overhear the alarm calls of all three species. In support of innate response, even young nestlings suppressed calling after hearing both thornbill and parental alarms. However, young nestlings ignored or increased calling to fairy-wren and honeyeater alarms. Older nestlings continued to suppress calling to thornbill and parental alarm calls, but also suppressed calling to honeyeater and fairy-wren alarms, suggesting that they could have learnt to recognize those calls. This study thus demonstrates that nestlings can respond to the alarm calls of other species, and that these responses are likely to be enabled through both innate mechanisms and learning.