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.

Reduced ectoparasite load, body mass and blood haemolysis in Eurasian kestrels (Falco tinnunculus) along an urban-rural gradient.

Urbanisation is proceeding at an alarming rate which forces wildlife to either retreat from urban areas or cope with novel stressors linked to human presence and activities. For example, urban stressors like anthropogenic noise, artificial light at night and chemical pollution can have severe impacts on the physiology of wildlife (and humans), in particular the immune system and antioxidant defences. These physiological systems are important to combat and reduce the severity of parasitic infections, which are common among wild animals. One question that then arises is whether urban-dwelling animals, whose immune and antioxidant system are already challenged by the urban stressors, are more susceptible to parasitic infections. To assess this, we studied nestlings of Eurasian kestrels (Falco tinnunculus) in Vienna, Austria, during 2015 and 2017. We measured biomarkers of innate immune function, oxidative stress and body mass index and ectoparasite infection intensity in 143 nestlings (from 56 nests) along an urban gradient. Nestlings in more urbanised areas had overall fewer ectoparasites, lower haemolysis (complement activity) and lower body mass index compared to nestlings in less urbanised areas. None of the other immune or oxidative stress markers were associated with the urban gradient. Despite some non-significant results, our data still suggest that kestrel nestlings experience some level of reduced physiological health, perhaps as a consequence of exposure to more urban stressors or altered prey availability in inner-city districts even though they had an overall lower ectoparasite burden in these heavily urbanised areas.

Evidence for rapid downward fecundity selection in an ectoparasite (Philornis downsi) with earlier host mortality in Darwin's finches.

Fecundity selection is a critical component of fitness and a major driver of adaptive evolution. Trade-offs between parasite mortality and host resources are likely to impose a selection pressure on parasite fecundity, but this is little studied in natural systems. The 'fecundity advantage hypothesis' predicts female-biased sexual size dimorphism whereby larger females produce more offspring. Parasitic insects are useful for exploring the interplay between host resource availability and parasite fecundity, because female body size is a reliable proxy for fecundity in insects. Here we explore temporal changes in body size in the myiasis-causing parasite Philornis downsi (Diptera: Muscidae) on the Galápagos Islands under conditions of earlier in-nest host mortality. We aim to investigate the effects of decreasing host resources on parasite body size and fecundity. Across a 12-year period, we observed a mean of c. 17% P. downsi mortality in host nests with 55 ± 6.2% host mortality and a trend of c. 66% higher host mortality throughout the study period. Using specimens from 116 Darwin's finch nests (Passeriformes: Thraupidae) and 114 traps, we found that over time, P. downsi pupae mass decreased by c. 32%, and male (c. 6%) and female adult size (c. 11%) decreased. Notably, females had c. 26% smaller abdomens in later years, and female abdomen size was correlated with number of eggs. Our findings imply natural selection for faster P. downsi pupation and consequently smaller body size and lower parasite fecundity in this newly evolving host-parasite system.

Introduced parasite changes host phenotype, mating signal and hybridization risk: Philornis downsi effects on Darwin's finch song.

Introduced parasites that alter their host's mating signal can change the evolutionary trajectory of a species through sexual selection. Darwin's Camarhynchus finches are threatened by the introduced fly Philornis downsi that is thought to have accidentally arrived on the Galapagos Islands during the 1960s. The P. downsi larvae feed on the blood and tissue of developing finches, causing on average approximately 55% in-nest mortality and enlarged naris size in survivors. Here we test if enlarged naris size is associated with song characteristics and vocal deviation in the small tree finch ( Camarhynchus parvulus), the critically endangered medium tree finch ( C. pauper) and the recently observed hybrid tree finch group ( Camarhynchus hybrids). Male C. parvulus and C. pauper with enlarged naris size produced song with lower maximum frequency and greater vocal deviation, but there was no significant association in hybrids. Less vocal deviation predicted faster pairing success in both parental species. Finally, C. pauper males with normal naris size produced species-specific song, but male C. pauper with enlarged naris size had song that was indistinguishable from other tree finches. When parasites disrupt host mating signal, they may also facilitate hybridization. Here we show how parasite-induced naris enlargement affects vocal quality, resulting in blurred species mating signals.

Baseline and stress-induced blood properties of male and female Darwin's small ground finch (Geospiza fuliginosa) of the Galapagos Islands.

Birds are renowned for exhibiting marked sex-specific differences in activity levels and reproductive investment during the breeding season, potentially impacting circulating blood parameters associated with stress and energetics. Males of many passerines often do not incubate, but they experience direct exposure to intruder threat and exhibit aggressive behaviour during the nesting phase in order to defend territories against competing males and predators. Nesting females often have long bouts of inactivity during incubation, but they must remain vigilant of the risks posed by predators and conspecific intruders approaching the nest. Here, we use 33 free-living male (n = 16) and female (n = 17) Darwin's small ground finches (Geospiza fuliginosa) on Floreana Island (Galapagos Archipelago) to better understand how sex-specific roles during the reproductive period impact baseline and stress-induced levels of plasma corticosterone (CORT), blood glucose and haematocrit. Specifically, we hypothesise that males are characterised by higher baseline values given their direct and relatively frequent exposure to intruder threat, but that a standardised stress event (capture and holding) overrides any sex-specific differences. In contrast with expectations, baseline levels of all blood parameters were similar between sexes (13.4 ±â€¯1.9 ng ml-1 for CORT, 13.7 ±â€¯0.4 mmol l-1 for glucose, 58.3 ±â€¯0.8% for haematocrit). Interestingly, females with higher body condition had lower baseline haematocrit. All blood parameters changed with time since capture (range 1.2-41.3 min) in both sexes, whereby CORT increased linearly, haematocrit decreased linearly, and glucose increased to a peak at ∼20 min post-capture and declined to baseline levels thereafter. Our results do not support the hypothesis that sex-specific roles during the reproductive period translate to differences in blood parameters associated with stress and energetics, but we found some evidence that blood oxygen transport capacity may decline as finches increase in body condition.

Host-specific associations affect the microbiome of Philornis downsi, an introduced parasite to the Galápagos Islands.

The composition and diversity of bacteria forming the microbiome of parasitic organisms have implications for differential host pathogenicity and host-parasite co-evolutionary interactions. The microbiome of pathogens can therefore have consequences that are relevant for managing disease prevalence and impact on affected hosts. Here, we investigate the microbiome of an invasive parasitic fly Philornis downsi, recently introduced to the Galápagos Islands, where it poses extinction threat to Darwin's finches and other land birds. Larvae infest nests of Darwin's finches and consume blood and tissue of developing nestlings, and have severe mortality impacts. Using 16s rRNA sequencing data, we characterize the bacterial microbiota associated with P. downsi adults and larvae sourced from four finch host species, inhabiting two islands and representing two ecologically distinct groups. We show that larval and adult microbiomes are dominated by the phyla Proteobacteria and Firmicutes, which significantly differ between life stages in their distributions. Additionally, bacterial community structure significantly differed between larvae retrieved from strictly insectivorous warbler finches (Certhidea olivacea) and those parasitizing hosts with broader dietary preferences (ground and tree finches, Geospiza and Camarhynchus spp., respectively). Finally, we found no spatial effects on the larval microbiome, as larvae feeding on the same host (ground finches) harboured similar microbiomes across islands. Our results suggest that the microbiome of P. downsi changes during its development, according to dietary composition or nutritional needs, and is significantly affected by host-related factors during the larval stage. Unravelling the ecological significance of bacteria for this parasite will contribute to the development of novel, effective control strategies.

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.

Female in-nest chatter song increases predation.

Female song is an ancestral trait in songbirds, yet extant females generally sing less than males. Here, we examine sex differences in the predation cost of singing behaviour. The superb fairy-wren (Malurus cyaneus) is a Southern Hemisphere songbird; males and females provision the brood and produce solo song year-round. Both sexes had higher song rate during the fertile period and lower song rate during incubation and chick feeding. Females were more likely than males to sing close to or inside the nest. For this reason, female but not male song rate predicted egg and nestling predation. This study identifies a high fitness cost of song when a parent bird attends offspring inside a nest and explains gender differences in singing when there are gender differences in parental care.

Species collapse via hybridization in Darwin's tree finches.

Species hybridization can lead to fitness costs, species collapse, and novel evolutionary trajectories in changing environments. Hybridization is predicted to be more common when environmental conditions change rapidly. Here, we test patterns of hybridization in three sympatric tree finch species (small tree finch Camarhynchus parvulus, medium tree finch Camarhynchus pauper, and large tree finch: Camarhynchus psittacula) that are currently recognized on Floreana Island, Galápagos Archipelago. Genetic analysis of microsatellite data from contemporary samples showed two genetic populations and one hybrid cluster in both 2005 and 2010; hybrid individuals were derived from genetic population 1 (small morph) and genetic population 2 (large morph). Females of the large and rare species were more likely to pair with males of the small common species. Finch populations differed in morphology in 1852-1906 compared with 2005/2010. An unsupervised clustering method showed (a) support for three morphological clusters in the historical tree finch sample (1852-1906), which is consistent with current species recognition; (b) support for two or three morphological clusters in 2005 with some (19%) hybridization; and (c) support for just two morphological clusters in 2010 with frequent (41%) hybridization. We discuss these findings in relation to species demarcations of Camarhynchus tree finches on Floreana Island.

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.

Aggressiveness predicts dominance rank in greylag geese: mirror tests and agonistic interactions.

Individual differences in aggressiveness, if consistent across time and contexts, may contribute to the long-term maintenance of social hierarchies in complex animal societies. Although agonistic interactions have previously been used to calculate individuals' positions within a dominance hierarchy, to date the repeatability of agonistic behaviour has not been tested when calculating social rank. Here, we examined the consistency and social relevance of aggressiveness as a personality trait in a free-flying population of greylag geese (Anser anser). For each individual, we quantified (i) aggressiveness using a standardized mirror stimulation test and (ii) dominance ranking based on the number of agonistic interactions won and lost in a feeding context. We found that individual differences in aggressiveness were significantly repeatable and that individuals' aggressiveness predicted their dominance rank position. The flock showed a robust and intermediately steep dominance hierarchy. Social rank was higher in paired birds, males and older birds, and most agonistic interactions occurred between individuals with moderate rank differences. We suggest that selection favours aggressiveness as a personality trait associated with resource acquisition and social rank, whereby a dominance hierarchy may increase the benefits of group living and reduce costs over conflict within dyads.

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.

Panmixia supports divergence with gene flow in Darwin's small ground finch, Geospiza fuliginosa, on Santa Cruz, Galápagos Islands.

The divergence-with-gene-flow model of speciation has a strong theoretical basis with a growing number of plausible examples in nature, but remains hotly debated. Darwin's finches of the Galápagos Archipelago have played an important role in our understanding of speciation processes. Recent studies suggest that this group may also provide insights into speciation via divergence with gene flow. On the island of Santa Cruz, recent studies found evidence for adaptive divergence in Darwin's small ground finch, Geospiza fuliginosa, between ecologically contrasting arid and humid zones. Despite the short geographical distance between these zones, strong disruptive selection during low rainfall periods is expected to generate and maintain adaptive divergence. Conversely, during high rainfall periods, when disruptive selection is predicted to be weakened, population divergence in adaptive traits is expected to break down. Because periods of low and high rainfall irregularly alternate, the geographical pattern of adaptive divergence can be assumed to break down and, importantly, regenerate in situ. Here, we use microsatellite allele frequency data to assess the genetic population structure of G. fuliginosa on Santa Cruz. We sample 21 sites and four ecological zones across the island. We reject hypotheses of population substructure linked to ecological and geographical differences among sites in favour of a single panmictic population. Panmixia implies high levels of gene flow within Santa Cruz, which favours selection over genetic drift as a valid process generating phenotypic divergence in G. fuliginosa on Santa Cruz. We discuss how our findings may support classic adaptation, phenotypic plasticity, matching habitat choice or any combination of these three processes.