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.

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.

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.

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.

Exposure to soiled bedding reduces abnormal repetitive behaviors in mice.

Hygiene management protocols in laboratory mouse husbandries worldwide most commonly employ soiled bedding-exposed sentinel mice to monitor the occurrence of infections in mouse colonies. Using this approach, sentinel mice repeatedly receive a mixture of used bedding, supplied by a variety of cages of a defined hygienic unit for a period of several months. Hereby, microorganisms shed in the used bedding can infect the sentinel animals and can be detected in subsequent health monitoring procedures. However, murine excrements carry more than only microorganisms. Mouse feces and urine also contain a multitude of olfactory molecules, which the animals use to code information about social status and context. However, if and how the persistent and repeated experience with these odor cues affects the behavior of sentinel mice, has not yet been explored. To address this question, we conducted a longitudinal study for neurochemical output parameters related to an organism's responsiveness to challenging conditions, and for the exploratory assessment of a panel of home cage behaviors in soiled bedding and control female C57BL/6J mice. We found that the number of mice showing abnormal repetitive behaviors, including barbering and bar mouthing, was lower in the soiled bedding group. While neutrophil/lymphocyte ratios and fecal corticosterone metabolites did not differ between groups, the within-group variance of the neutrophil/lymphocyte ratio was reduced in the soiled bedding group. These results show that the occurrence of abnormal repetitive behaviors is lower in sentinel than in control mice and suggest a beneficial effect of soiled bedding on the welfare of laboratory mice and on outcome variability.

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.

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.

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.

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'.

From individual to population level: Temperature and snow cover modulate fledging success through breeding phenology in greylag geese (Anser anser).

Local weather conditions may be used as environmental cues by animals to optimize their breeding behaviour, and could be affected by climate change. We measured associations between climate, breeding phenology, and reproductive output in greylag geese (Anser anser) across 29 years (1990-2018). The birds are individually marked, which allows accurate long-term monitoring of life-history parameters for all pairs within the flock. We had three aims: (1) identify climate patterns at a local scale in Upper Austria, (2) measure the association between climate and greylag goose breeding phenology, and (3) measure the relationship between climate and both clutch size and fledging success. Ambient temperature increased 2 °C across the 29-years study period, and higher winter temperature was associated with earlier onset of egg-laying. Using the hatch-fledge ratio, average annual temperature was the strongest predictor for the proportion of fledged goslings per season. There is evidence for an optimum time window for egg-laying (the earliest and latest eggs laid had the lowest fledging success). These findings broaden our understanding of environmental effects and population-level shifts which could be associated with increased ambient temperature and can thus inform future research about the ecological consequences of climate changes and reproductive output in avian systems.

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.

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.

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.

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.

An inter-island comparison of Darwin's finches reveals the impact of habitat, host phylogeny, and island on the gut microbiome.

Darwin's finch species in the Galapagos Archipelago are an iconic adaptive radiation that offer a natural experiment to test for the various factors that influence gut microbiome composition. The island of Floreana has the longest history of human settlement within the archipelago and offers an opportunity to compare island and habitat effects on Darwin's finch microbiomes. In this study, we compare gut microbiomes in Darwin's finch species on Floreana Island to test for effects of host phylogeny, habitat (lowlands, highlands), and island (Floreana, Santa Cruz). We used 16S rRNA Illumina sequencing of fecal samples to assess the gut microbiome composition of Darwin's finches, complemented by analyses of stable isotope values and foraging data to provide ecological context to the patterns observed. Overall bacterial composition of the gut microbiome demonstrated co-phylogeny with Floreana hosts, recapitulated the effect of habitat and diet, and showed differences across islands. The finch phylogeny uniquely explained more variation in the microbiome than did foraging data. Finally, there were interaction effects for island × habitat, whereby the same Darwin's finch species sampled on two islands differed in microbiome for highland samples (highland finches also had different diets across islands) but not lowland samples (lowland finches across islands had comparable diet). Together, these results corroborate the influence of phylogeny, age, diet, and sampling location on microbiome composition and emphasize the necessity for comprehensive sampling given the multiple factors that influence the gut microbiome in Darwin's finches, and by extension, in animals broadly.

Host phylogeny, diet, and habitat differentiate the gut microbiomes of Darwin's finches on Santa Cruz Island.

Darwin's finches are an iconic example of an adaptive radiation with well-characterized evolutionary history, dietary preferences, and biogeography, offering an unparalleled opportunity to disentangle effects of evolutionary history on host microbiome from other factors like diet and habitat. Here, we characterize the gut microbiome in Darwin's finches, comparing nine species that occupy diverse ecological niches on Santa Cruz island. The finch phylogeny showed moderate congruence with the microbiome, which was comprised mostly of the bacterial phyla Firmicutes, Actinobacteria, and Proteobacteria. Diet, as measured with stable isotope values and foraging observations, also correlated with microbiome differentiation. Additionally, each gut microbial community could easily be classified by the habitat of origin independent of host species. Altogether, these findings are consistent with a model of microbiome assembly in which environmental filtering via diet and habitat are primary determinants of the bacterial taxa present with lesser influence from the evolutionary history between finch species.

Genetic admixture predicts parasite intensity: evidence for increased hybrid performance in Darwin's tree finches.

Hybridization can increase adaptive potential when enhanced genetic diversity or novel genetic combinations confer a fitness advantage, such as in the evolution of anti-parasitic mechanisms. Island systems are especially susceptible to invasive parasites due to the lack of defence mechanisms that usually coevolve in long-standing host-parasite relationships. We test if host genetic admixture affects parasite numbers in a novel host-parasite association on the Galápagos Islands. Specifically, we compare the number of Philornis downsi in nests with offspring sired by Darwin's small tree finch (Camarhynchus parvulus), Darwin's medium tree finch (C. pauper) and hybrids of these two species. The number of P. downsi decreased with an increasing genetic admixture of the attending male, and nests of hybrid males had approximately 50% fewer parasites than C. parvulus nests, and approximately 60% fewer parasites than C. pauper nests. This finding indicates that hybridization in this system could be favoured by selection and reveal a mechanism to combat an invasive parasite.

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.

Neural activation in response to conspecific songs in zebra finch (Taeniopygia guttata) embryos and nestlings.

Classic studies on the effects of auditory stimulation in embryonic birds have largely been limited to precocial taxa. In altricial taxa, physiological responses of embryos and, subsequently, the behavioral responses of nestlings have begun to receive increasing attention, yet it remains unclear whether and to what specificity neural responses are generated in ovo. Using in-situ hybridization for an immediate early gene, ZENK, we detected significant neural activation in both the embryos and nestlings of an altricial songbird, the zebra finch (Taeniopygia guttata) when exposed to conspecific song playbacks relative to silence. In turn, embryonic ZENK responses to heterospecific songs were intermediate in strength. These results are consistent with physiological evidence for conspecific song selectivity in embryos of other altricial songbird taxa.