Nestling Begging Calls Resemble Maternal Vocal Signatures When Mothers Call Slowly to Embryos.

AbstractVocal production learning (the capacity to learn to produce vocalizations) is a multidimensional trait that involves different learning mechanisms during different temporal and socioecological contexts. Key outstanding questions are whether vocal production learning begins during the embryonic stage and whether mothers play an active role in this through pupil-directed vocalization behaviors. We examined variation in vocal copy similarity (an indicator of learning) in eight species from the songbird family Maluridae, using comparative and experimental approaches. We found that (1) incubating females from all species vocalized inside the nest and produced call types including a signature "B element" that was structurally similar to their nestlings' begging call; (2) in a prenatal playback experiment using superb fairy wrens (Malurus cyaneus), embryos showed a stronger heart rate response to playbacks of the B element than to another call element (A); and (3) mothers that produced slower calls had offspring with greater similarity between their begging call and the mother's B element vocalization. We conclude that malurid mothers display behaviors concordant with pupil-directed vocalizations and may actively influence their offspring's early life through sound learning shaped by maternal call tempo.

Temporal and spatial variation in sex-specific abundance of the avian vampire fly (Philornis downsi).

Understanding the range and behaviour of an invasive species is critical to identify key habitat areas to focus control efforts. Patterns of range use in parasites can differ temporally, across life stages and between sexes. The invasive avian vampire fly, Philornis downsi, spends the larval stage of its life within bird nests, feeding on developing nestlings and causing high levels of mortality and deformation. However, little is known of the ecology and behaviour of the non-parasitic adult fly life stage. Here, we document sex-specific temporal and spatial patterns of abundance of adult avian vampire flies during a single Darwin's finch breeding season. We analyse fly trapping data collected across 7 weeks in the highlands (N = 405 flies) and lowlands (N = 12 flies) of Floreana Island (Galápagos). Lowland catches occurred later in the season, which supports the hypothesis that flies may migrate from the food-rich highlands to the food-poor lowlands once host breeding has commenced. Fly abundance was not correlated with host nesting density (oviposition site) but was correlated with distance to the agricultural zone (feeding site). We consistently caught more males closer to the agricultural zone and more females further away from the agricultural zone. These sex differences suggest that males may be defending or lekking at feeding sites in the agricultural zone for mating. This temporal and sex-specific habitat use of the avian vampire fly is relevant for developing targeted control methods and provides insight into the behavioural ecology of this introduced parasite on the Galápagos Archipelago.

Female in-nest attendance predicts the number of ectoparasites in Darwin's finch species.

Selection should act on parental care and favour parental investment decisions that optimize the number of offspring produced. Such predictions have been robustly tested in predation risk contexts, but less is known about alternative functions of parental care under conditions of parasitism. The avian vampire fly (Philornis downsi) is a myasis-causing ectoparasite accidentally introduced to the Galápagos Islands, and one of the major mortality causes in Darwin's finch nests. With an 11-year dataset spanning 21 years, we examine the relationship between parental care behaviours and number of fly larvae and pupae in Darwin's finch nests. We do so across three host species (Camarhynchus parvulus, C. pauper, Geospiza fuliginosa) and one hybrid Camarhynchus group. Nests with longer female brooding duration (minutes per hour spent sitting on hatchlings to provide warmth) had fewer parasites, and this effect depended on male food delivery to chicks. Neither male age nor number of nest provisioning visits were directly associated with number of parasites. While the causal mechanisms remain unknown, we provide the first empirical study showing that female brooding duration is negatively related to the number of ectoparasites in nests. We predict selection for coordinated host male and female behaviour to reduce gaps in nest attendance, especially under conditions of novel and introduced ectoparasites.

Behavioural response to songs between genetically diverged allopatric populations of Darwin's small tree finch in the Galápagos.

Empirical data that identify contemporary mechanisms of divergence shed light on how species could multiply. In this study, we measured population genetic structure, song syllable diversity and response to simulated intruder song in Darwin's small tree finch (Camarhynchus parvulus) on Santa Cruz and Floreana Islands, Galápagos archipelago. Our aim was to test whether the magnitude of contemporary behavioural response in resident birds was consistent with patterns of genetic or cultural differences between populations. We analysed genetic structure and the occurrence of song syllable types, and experimentally measured the response of resident birds to intruder bird song from different geographical origin (i.e., island) or syllable type. We discovered a weak signal of population genetic structure between Santa Cruz and Floreana Islands. Although some song syllables occurred on both islands, others were unique to each island; Santa Cruz Island males used more unique syllables than Floreana Island males. Both Santa Cruz and Floreana resident males discriminated their response towards a simulated intruder song based on the geographical origin of the intruder song, but not on the syllable type sung by the intruder. We conclude that the populations are diverging in genetic and cultural traits and identified a signal of contemporary behavioural response that could maintain divergence upon secondary contact.

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.

Prenatal environment affects embryonic response to song.

Early environmental enrichment improves postnatal cognition in animals and humans. Here, we examined the effects of the prenatal acoustic environment (parental song rate) on prenatal attention in superb fairy-wren (Malurus cyaneus) embryos, the only songbird species with evidence of prenatal discrimination of maternal calls and in ovo call learning. Because both adults also sing throughout the incubation phase, we broadcast songs to embryos and measured their heart rate response in relation to parental song rate and tutor identity (familiarity, sex). Embryos from acoustically active families (high parental song rate) had the strongest response to songs. Embryos responded (i) strongest to male songs irrespective of familiarity with the singer, and (ii) strongest if their father had a high song rate during incubation. This is the first evidence for a prenatal physiological response to particular songs (potential tutors) in the egg, in relation to the prenatal acoustic environment, and before the sensitive period for song learning.

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.

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.

Age effects in Darwin's finches: older males build more concealed nests in areas with more heterospecific singing neighbors.

Nesting success tends to increase with age in birds, in part because older birds select more concealed nest sites based on experience and/or an assessment of prevailing predation risk. In general, greater plant diversity is associated with more biodiversity and more vegetation cover. Here, we ask if older Darwin's finch males nest in areas with greater vegetation cover and if these nest sites also have greater avian species diversity assessed using song. We compared patterns in Darwin's Small Tree Finch (Camarhynchus parvulus) and Darwin's Small Ground Finch (Geospiza fuliginosa) as males build the nest in both systems. We measured vegetation cover, nesting height, and con- vs. heterospecific songs per minute at 55 nests (22 C. parvulus, 33 G. fuliginosa). As expected, in both species, older males built nests in areas with more vegetation cover and these nests had less predation. A novel finding is that nests of older males also had more heterospecific singing neighbors. Future research could test whether older males outcompete younger males for access to preferred nest sites that are more concealed and sustain a greater local biodiversity. The findings also raise questions about the ontogenetic and fitness consequences of different acoustical experiences for developing nestlings inside the nest. Supplementary Information: The online version contains supplementary material available at 10.1007/s10336-023-02093-5.

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

INTRODUCTION: Risk 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). RESULTS: Host 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. CONCLUSION: Host response to the threat of cuckoo parasitism was assessed using vocal cues of the cuckoo and was predicted by the risk of future parasitism.

Smaller Australian raptors have greater urban tolerance.

Urbanisation is occurring around the world at a rapid rate and is generally associated with negative impacts on biodiversity at local, regional, and global scales. Examining the behavioural response profiles of wildlife to urbanisation helps differentiate between species that do or do not show adaptive responses to changing landscapes and hence are more or less likely to persist in such environments. Species-specific responses to urbanisation are poorly understood in the Southern Hemisphere compared to the Northern Hemisphere, where most of the published literature is focussed. This is also true for raptors, despite their high diversity and comparably high conservation concern in the Southern Hemisphere, and their critical role within ecosystems as bioindicators of environmental health. Here, we explore this knowledge gap using community science data sourced from eBird to investigate the urban tolerance of 24 Australian raptor species at a continental scale. We integrated eBird data with a global continuous measure of urbanisation, artificial light at night (ALAN), to derive an urban tolerance index, ranking species from positive to negative responses according to their tolerance of urban environments. We then gathered trait data from the published literature to assess whether certain traits (body mass, nest substrate, habitat type, feeding guild, and migratory status) were associated with urban tolerance. Body size was negatively associated with urban tolerance, as smaller raptors had greater urban tolerance than larger raptors. Out of the 24 species analysed, 13 species showed tolerance profiles for urban environments (positive response), and 11 species showed avoidance profiles for urban environments (negative response). The results of this study provide impetus to conserve native habitat and improve urban conditions for larger-bodied raptor species to conserve Australian raptor diversity in an increasingly urbanised world.

When aggressiveness could be too risky: linking personality traits and predator response in superb fairy-wrens.

Personality syndromes in animals may have adaptive benefits for survival. For example, while engaging in predator deterrence, reactive individuals tend to prioritise their own survival, while proactive individuals engage in riskier behaviours. Studies linking animal personality measured in captivity with individual fitness or behaviours in the wild are sparse, which is a gap in knowledge this study aims to address. We used playback experiments in superb fairy-wrens (Malurus cyaneus), a common Australian songbird with a cooperative breeding system, to assess whether three personality traits measured during short-term captivity correlated with behavioural responses in the wild to a perceived nest and adult predator, the grey currawong (Strepera versicolor). We used three standard measures of personality in birds: struggle responses to human handling (boldness), exploration during a novel environment test, and aggressiveness during a mirror presentation. Superb fairy-wrens showed a significantly stronger response to the predator playback than to the control (willie wagtail, Rhipidura leucophrys) playback, suggesting that they recognised the predator playback as a threat without any accompanying visual stimulus. Birds that attacked their mirror image during the mirror presentation and those that spent a moderate amount of time close to the mirror responded more strongly to predator playback (by approaching the speaker faster and closer, spending more time near the speaker, and being more likely to alarm call) compared to those with low aggressiveness or those that spent very short or long durations close to the mirror. Neither boldness nor exploration in the novel environment test predicted playback response. Our results align with a growing number of studies across species showing the importance of animal personalities as factors for fitness and survival.

Avian vampire fly (Philornis downsi) mortality differs across Darwin's finch host species.

In invasive parasites, generalism is considered advantageous during the initial phase of introduction. Thereafter, fitness costs to parasites, such as host-specific mortality, can drive parasites towards specialism to avoid costly hosts. It is important to determine changes in host specificity of invasive populations to understand host-parasite dynamics and their effects on vulnerable host populations. We examined changes in mortality in the introduced avian vampire fly (Philornis downsi) (Diptera: Muscidae), a generalist myasis-causing ectoparasite, between 2004 and 2020 on Floreana Island (Galápagos). Mortality was measured as the proportion of immature larvae found upon host nest termination. Over the time period, the avian vampire fly was most abundant and had low mortality in nests of the critically endangered medium tree finch (Camarhynchus pauper) and had the highest mortality in nests of hybrid tree finches (Camarhynchus spp.). Low larval mortality was also found in small tree (Camarhynchus parvulus) and small ground finch (Geospiza fuliginosa) nests. Selection could favour avian vampire flies that select medium tree finch nests and/or avoid hybrid nests. Overall, the finding of differences in avian vampire fly survival across host species is parsimonious with the idea that the introduced fly may be evolving towards host specialisation.

Prenatal auditory learning in avian vocal learners and non-learners.

Understanding when learning begins is critical for identifying the factors that shape both the developmental course and the function of information acquisition. Until recently, sufficient development of the neural substrates for any sort of vocal learning to begin in songbirds was thought to be reached well after hatching. New research shows that embryonic gene activation and the outcome of vocal learning can be modulated by sound exposure in ovo. We tested whether avian embryos across lineages differ in their auditory response strength and sound learning in ovo, which we studied in vocal learning (Maluridae, Geospizidae) and vocal non-learning (Phasianidae, Spheniscidae) taxa. While measuring heart rate in ovo, we exposed embryos to (i) conspecific or heterospecific vocalizations, to determine their response strength, and (ii) conspecific vocalizations repeatedly, to quantify cardiac habituation, a form of non-associative learning. Response strength towards conspecific vocalizations was greater in two species with vocal production learning compared to two species without. Response patterns consistent with non-associative auditory learning occurred in all species. Our results demonstrate a capacity to perceive and learn to recognize sounds in ovo, as evidenced by habituation, even in species that were previously assumed to have little, if any, vocal production learning. This article is part of the theme issue 'Vocal learning in animals and humans'.

Both natural selection and isolation by distance explain phenotypic divergence in bill size and body mass between South Australian little penguin colonies.

Morphological variation between populations of the same species can arise as a response to genetic variation, local environmental conditions, or a combination of both. In this study, I examined small-scale geographic variation in bill size and body mass in little penguins (Eudyptula minor) across five breeding colonies in South Australia separated by <150 km. To help understand patterns driving the differences, I investigated these variations in relation to environmental parameters (air temperature, sea surface temperature, and water depth) and geographic distances between the colonies. I found substantial morphological variation among the colonies for body mass and bill measurements (except bill length). Colonies further located from each other showed greater morphological divergence overall than adjacent colonies. In addition, phenotypic traits were somewhat correlated to environmental parameters. Birds at colonies surrounded by hotter sea surface temperatures were heavier with longer and larger bills. Birds with larger and longer bills were also found at colonies surrounded by shallower waters. Overall, the results suggest that both environmental factors (natural selection) and interpopulation distances (isolation by distance) are causes of phenotypic differentiation between South Australian little penguin colonies.

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.