House Sparrows as Sentinels of Childhood Lead Exposure.

Our understanding of connections between human and animal health has advanced substantially since the canary was introduced as a sentinel of toxic conditions in coal mines. Nonetheless, the development of wildlife sentinels for monitoring human exposure to toxins has been limited. Here, we capitalized on a three-decade long child blood lead monitoring program to demonstrate that the globally ubiquitous and human commensal house sparrow (Passer domesticus) can be used as a sentinel of human health risks in urban environments impacted by lead mining. We showed that sparrows are a viable proxy for the measurement of blood lead levels in children at a neighborhood scale (0.28 km2). In support of the generalizability of this approach, the blood lead relationship established in our focal mining city enabled us to accurately predict elevated blood lead levels in children from another mining city using only sparrows from the second location. Using lead concentrations and lead isotopic compositions from environmental and biological matrices, we identified shared sources and pathways of lead exposure in sparrows and children, with strong links to contamination from local mining emissions. Our findings showed how human commensal species can be used to identify and predict human health risks over time and space.

Mitonuclear interactions impact aerobic metabolism in hybrids and may explain mitonuclear discordance in young, naturally hybridizing bird lineages.

Understanding genetic incompatibilities and genetic introgression between incipient species are major goals in evolutionary biology. Mitochondrial genes evolve rapidly and exist in dense gene networks with coevolved nuclear genes, suggesting that mitochondrial respiration may be particularly susceptible to disruption in hybrid organisms. Mitonuclear interactions have been demonstrated to contribute to hybrid dysfunction between deeply divergent taxa crossed in the laboratory, but there are few empirical examples of mitonuclear interactions between younger lineages that naturally hybridize. Here, we use controlled hybrid crosses and high-resolution respirometry to provide the first experimental evidence in a bird that inter-lineage mitonuclear interactions impact mitochondrial aerobic metabolism. Specifically, respiration capacity of the two mitodiscordant backcrosses (with mismatched mitonuclear combinations) differs from one another, although they do not differ significantly from the parental groups or mitoconcordant backcrosses as we would expect of mitonuclear disruptions. In the wild hybrid zone between these subspecies, the mitochondrial cline centre is shifted west of the nuclear cline centre, which is consistent with the direction of our experimental results. Our results therefore demonstrate asymmetric mitonuclear interactions that impact the capacity of cellular mitochondrial respiration and may help to explain the geographic discordance between mitochondrial and nuclear genomes observed in the wild.

Blood lead increases and haemoglobin decreases in urban birds along a soil contamination gradient in a mining city.

Lead contaminated soil is a persistent global threat to the health of animal populations. Nevertheless, links between soil lead and its adverse effects on exposed wildlife remain poorly understood. Here, we explore local geographic patterns of exposure in urban birds along a gradient of lead contamination in Broken Hill, an Australian mining city. Soil lead concentrations are linked to co-located blood lead measurements in rock pigeons (Columba livia), house sparrows (Passer domesticus), crested pigeons (Ocyphaps lophotes) and white-plumed honeyeaters (Lichenostomus ornatus). Median blood lead levels were highest in crested pigeons (59.6 µg/dL), followed by house sparrows (35.2 µg/dL), rock pigeons (35.1 µg/dL), and white-plumed honeyeaters (27.4 µg/dL). Blood lead levels in all species declined away from mining areas, the primary source of lead contamination in Broken Hill. Blood lead increased significantly and at the greatest rate relative to soil lead in the three ground foraging species (crested pigeons, house sparrows, rock pigeons). For these species, soil lead concentrations below 200 mg/kg and 900 mg/kg were needed to maintain a median blood lead concentration under the lower threshold of the subtoxic (20-50 µg/dL) and toxic (≥50 µg/dL) effect ranges previously identified for some bird species. We also investigated the effects of lead exposure on blood haemoglobin levels as a general measure of physiological condition in birds exposed to different levels of soil lead contamination. Overall, for every 1 µg/dL increase in blood lead, haemoglobin decreased by 0.11 g/L. The rate of this decrease was not significantly different between species, which supports the measurement of haemoglobin as a consistent though insensitive measure of physiological condition in chronically lead exposed birds. Our findings reflect the importance of lead contaminated soil as a widespread source of elevated blood lead and supressed haemoglobin levels in birds inhabiting urbanised and mining impacted environments.

The ecology of zebra finch song and its implications for vocal communication in multi-level societies.

Acoustic signalling is crucial in affecting movements and in social interactions. In species with dynamic social structures, such as multi-level societies, acoustic signals can provide a key mechanism allowing individuals to identify and find or avoid each other and to exchange information. Yet, if the spacing between individuals regularly exceeds the maximum signalling range, the relation between movements and signals becomes more complex. As the best-studied songbird in captivity, the zebra finch (Taeniopygia castanotis) is a species with individually distinct songs that are audible over just a few metres and a widely ranging dynamic multi-level social organization in the wild, raising questions on the actual role of its song in social cohesion and coordination. Here, we provide an overview of birdsong in social organizations (networks) and use the ecology of the zebra finch and male song to discuss how singing can facilitate social cohesion and coordination in species where the signal range is very short. We raise the question of the extent to which zebra finches are a representative species to understand the function of song in communication, and we broaden current views on the function of birdsong and its individual signature. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

High nest failure in a zebra finch population and persistent nest predation by a monitor lizard.

Predation is well known to have substantial effects on behaviour and fitness in many animals. In songbirds, nest predation is rarely observed directly, so that research focusses primarily on the consequences of predation and less on the behaviour of the predator. Here, we report predation data in a zebra finch (Taeniopygia catanosis) nest box population, highlighting a 22-min-long sequence, captured on video, of a sand goanna (Varanus gouldii) predating a zebra finch nest in the wild. This monitor lizard appeared to be extremely persistent with climbing and jumping up to the next box nine times, including three successive unsuccessful attempts that lead to a change in approach strategy. It removed all six nestlings from the nest box during those repeated approaches and consumed them. In combination with overall high predation rates in the study population we document here, the findings highlight the role that a single predator species can have on nest success and, thus potentially also breeding decisions and social organisation of the prey population. Specifically so in a species like the zebra finch which synchronises reproductive attempts through the use of social information acquired through nest inspections and which uses social hotspots where they could gather information on changes in local social composition due to the individualised signals they use.

Exposure to Sublethal Concentrations of Lead (Pb) Affects Ecologically Relevant Behaviors in House Sparrows (Passer domesticus).

Global contamination of environments with lead (Pb) poses threats to many ecosystems and populations. While exposure to Pb is toxic at high concentrations, recent literature has shown that lower concentrations can also cause sublethal, deleterious effects. However, there remains relatively little causal investigation of how exposure to lower concentrations of environmental Pb affects ecologically important behaviors. Behaviors often represent first-line responses of an organism and its internal physiological, molecular, and genetic responses to a changing environment. Hence, better understanding how behaviors are influenced by pollutants such as Pb generates crucial information on how species are coping with the effects of pollution more broadly. To better understand the effects of sublethal Pb on behavior, we chronically exposed adult wild-caught, captive house sparrows (Passer domesticus) to Pb-exposed drinking water and quantified a suite of behavioral outcomes: takeoff flight performance, activity in a novel environment, and in-hand struggling and breathing rate while being handled by an experimenter. Compared to controls (un-exposed drinking water), sparrows exposed to environmentally relevant concentrations of Pb exhibited decreases in takeoff flight performance and reduced movements in a novel environment following 9-10 weeks of exposure. We interpret this suite of results to be consistent with Pb influencing fundamental neuro-muscular abilities, making it more difficult for exposed birds to mount faster movements and activities. It is likely that suppression of takeoff flight and reduced movements would increase the predation risk of similar birds in the wild; hence, we also conclude that the effects we observed could influence fitness outcomes for individuals and populations altering ecological interactions within more naturalistic settings.

Heat stress conditions affect the social network structure of free-ranging sheep.

Extreme weather conditions, like heatwave events, are becoming more frequent with climate change. Animals often modify their behaviour to cope with environmental changes and extremes. During heat stress conditions, individuals change their spatial behaviour and increase the use of shaded areas to assist with thermoregulation. Here, we suggest that for social species, these behavioural changes and ambient conditions have the potential to influence an individual's position in its social network, and the social network structure as a whole. We investigated whether heat stress conditions (quantified through the temperature humidity index) and the resulting use of shaded areas, influence the social network structure and an individual's connectivity in it. We studied this in free-ranging sheep in the arid zone of Australia, GPS-tracking all 48 individuals in a flock. When heat stress conditions worsened, individuals spent more time in the shade and the network was more connected (higher density) and less structured (lower modularity). Furthermore, we then identified the behavioural change that drove the altered network structure and showed that an individual's shade use behaviour affected its social connectivity. Interestingly, individuals with intermediate shade use were most strongly connected (degree, strength, betweenness), indicating their importance for the connectivity of the social network during heat stress conditions. Heat stress conditions, which are predicted to increase in severity and frequency due to climate change, influence resource use within the ecological environment. Importantly, our study shows that these heat stress conditions also affect the animal's social environment through the changed social network structure. Ultimately, this could have further flow on effects for social foraging and individual health since social structure drives information and disease transmission.

Correction to: 'Fission-fusion dynamics in sheep: the influence of resource distribution and temporal activity patterns' (2023) by Della Libera et al.

[This corrects the article DOI: 10.1098/10.1098/rsos.230402.][This corrects the article DOI: 10.1098/rspb.2021.1115.].

Effects of heat waves on telomere dynamics and parental brooding effort in nestlings of the zebra finch (Taeniopygia castanotis) transitioning from ectothermy to endothermy.

Heat waves are predicted to be detrimental for organismal physiology with costs for survival that could be reflected in markers of biological state such as telomeres. Changes in early life telomere dynamics driven by thermal stress are of particular interest during the early post-natal stages of altricial birds because nestlings quickly shift from being ectothermic to endothermic after hatching. Telomeres of ectothermic and endothermic organisms respond differently to environmental temperature, but few investigations within species that transition from ectothermy to endothermy are available. Also, ambient temperature influences parental brooding behaviour, which will alter the temperature experienced by offspring and thereby, potentially, their telomeres. We exposed zebra finch nestlings to experimental heat waves and compared their telomere dynamics to that of a control group at 5, 12 and 80 days of age that encapsulate the transition from the ectothermic to the endothermic thermoregulatory stage; we also recorded parental brooding, offspring sex, mass, growth rates, brood size and hatch order. Nestling mass showed an inverse relationship with telomere length, and nestlings exposed to heat waves showed lower telomere attrition during their first 12 days of life (ectothermic stage) compared to controls. Additionally, parents of heated broods reduced the time they spent brooding offspring (at 5 days old) compared to controls. Our results indicate that the effect of heat waves on telomere dynamics likely varies depending on age and thermoregulatory stage of the offspring in combination with parental brooding behaviour during growth.

Fission-fusion dynamics in sheep: the influence of resource distribution and temporal activity patterns.

Fission-fusion events, i.e. changes to the size and composition of animal social groups, are a mechanism to adjust the social environment in response to short-term changes in the cost-benefit ratio of group living. Furthermore, the time and location of fission-fusion events provide insight into the underlying drivers of these dynamics. Here, we describe a method for identifying group membership over time and for extracting fission-fusion events from animal tracking data. We applied this method to high-resolution GPS data of free-ranging sheep (Ovis aries). Group size was highest during times when sheep typically rest (midday and at night), and when anti-predator benefits of grouping are high while costs of competition are low. Consistent with this, fission and fusion frequencies were highest during early morning and late evening, suggesting that social restructuring occurs during periods of high activity. However, fission and fusion events were not more frequent near food patches and water resources when adjusted for overall space use. This suggests a limited role of resource competition. Our results elucidate the dynamics of grouping in response to social and ecological drivers, and we provide a tool for investigating these dynamics in other species.

Longitudinal covariation of testosterone and sperm quality across reproductive stages in the zebra finch.

Birds that breed opportunistically maintain partial activation of reproductive systems to rapidly exploit environmental conditions when they become suitable for breeding. Maintaining reproductive systems outside of a breeding context is costly. For males, these costs are thought to include continual exposure to testosterone. Males of seasonally breeding birds minimise these costs by downregulating testosterone production outside of a breeding context. Opportunistically breeding birds trade off the need to rapidly initiate reproduction with the costs of elevated testosterone production. One way opportunistically breeding males could minimise these costs is through fine scale changes in testosterone production across discrete reproductive stages which have a greater or lesser requirement for active sperm production. Although spermatogenesis broadly depends on testosterone production, whether changes in testosterone levels across the reproductive stages affect sperm quality and production is unknown. Here, we measured testosterone, sperm quality, and body condition in male zebra finches at discrete stages within reproductive bouts (egg laying, incubation, nestling provisioning, and fledging) and across two consecutive reproductive events in captive male zebra finches (Taeniopygia castanotis). We also examined associations between male testosterone, sperm quality/production, body condition, and nestling body condition. We found that testosterone levels varied across discrete reproductive stages with the lowest levels during incubation and the highest following chick fledging. Testosterone levels were positively associated with sperm velocity and the proportion of motile sperm but were not associated with male body condition. We found no associations between paternal body condition, testosterone levels, or sperm traits with nestling body condition (a proxy for the reproductive quality of a male and his partner). This study is the first to show that opportunistically breeding males vary testosterone synthesis and sperm traits at discrete stages within a reproductive event.

Short- and long-term consequences of heat exposure on mitochondrial metabolism in zebra finches (Taeniopygia castanotis).

Understanding the consequences of heat exposure on mitochondrial function is crucial as mitochondria lie at the core of metabolic processes, also affecting population dynamics. In adults, mitochondrial metabolism varies with temperature but can also depend on thermal conditions experienced during development. We exposed zebra finches to two alternative heat treatments during early development: "constant", maintained birds at ambient 35 °C from parental pair formation to fledglings' independence, while "periodic" heated broods at 40 °C, 6 h daily at nestling stage. Two years later, we acclimated birds from both experiments at 25 °C for 21 days, before exposing them to artificial heat (40 °C, 5 h daily for 10 days). After both conditions, we measured red blood cells' mitochondrial metabolism using a high-resolution respirometer. We found significantly decreased mitochondrial metabolism for Routine, Oxidative Phosphorylation (OxPhos) and Electron Transport System maximum capacity (ETS) after the heat treatments. In addition, the birds exposed to "constant" heat in early life showed lower oxygen consumption at the Proton Leak (Leak) stage after the heat treatment as adults. Females showed higher mitochondrial respiration for Routine, ETS and Leak independent of the treatments, while this pattern was reversed for OxPhos coupling efficiency (OxCE). Our results show that short-term acclimation involved reduced mitochondrial respiration, and that the reaction of adult birds to heat depends on the intensity, pattern and duration of temperature conditions experienced at early-life stages. Our study provides insight into the complexity underlying variation in mitochondrial metabolism and raises questions on the adaptive value of long-lasting physiological adjustments triggered by the early-life thermal environment.

Experimentally testing mate preference in an avian system with unidirectional bill color introgression.

Mating behavior can play a key role in speciation by inhibiting or facilitating gene flow between closely related taxa. Hybrid zones facilitate a direct examination of mating behavior and the traits involved in establishing species barriers. The long-tailed finch (Poephila acuticauda) has two hybridizing subspecies that differ in bill color (red and yellow), and the yellow bill phenotype appears to have introgressed ~350 km eastward following secondary contact. To examine the role of mate choice on bill color introgression, we performed behavioral assays using natural and manipulated bill colors. We found an assortative female mating preference for males of their own subspecies when bill color was not manipulated. However, we did not find this assortative preference in trials based on artificially manipulated bill color. This could suggest that assortative preference is not fixed entirely on bill color and instead may be based on a different trait (e.g., song) or a combination of traits, or alternatively may be due to lower statistical power alongside the bill manipulations being unconvincing to the female choosers. Intriguingly, we find a bias in the inheritance of bill color in captive bred F1 hybrid females. Previous modeling suggests that assortative mate preference and this kind of partial dominance in the underlying genes may together contribute to introgression, making the genetic architecture of bill color in this system a priority for future research.

The social role of song in wild zebra finches.

Male songbirds sing to establish territories and to attract mates.1,2 However, increasing reports of singing in non-reproductive contexts3 and by females4,5 show that song use is more diverse than previously considered. Therefore, alternative functions of song, such as social cohesion3 and synchronization of breeding, by and large, were overlooked even in such well-studied species such as the zebra finch (Taeniopygia guttata). In these social songbirds, only the males sing, and pairs breed synchronously in loose colonies,6,7 following aseasonal rain events in their arid habitat.8,9 As males are not territorial, and pairs form long-term monogamous bonds early in life, conventional theory predicts that zebra finches should not sing much at all; however, they do and their song is the focus of hundreds of lab-based studies.10,11,12,13,14,15,16,17,18,19,20,21,22 We hypothesize that zebra finch song functions to maintain social cohesion and to synchronize breeding. Here, we test this idea using data from 5 years of field studies, including observational transects, focal and year-round audio recordings, and a large-scale playback experiment. We show that zebra finches frequently sing while in groups, that breeding status influences song output at the nest and at aggregations, that they sing year round, and that they predominantly sing when with their partner, suggesting that the song remains important after pair formation. Our playback reveals that song actively features in social aggregations as it attracts conspecifics. Together, these results demonstrate that birdsong has important functions beyond territoriality and mate choice, illustrating its importance in coordination and cohesion of social units within larger societies.

AnimalTraits - a curated animal trait database for body mass, metabolic rate and brain size.

Trait databases have become important resources for large-scale comparative studies in ecology and evolution. Here we introduce the AnimalTraits database, a curated database of body mass, metabolic rate and brain size, in standardised units, for terrestrial animals. The database has broad taxonomic breadth, including tetrapods, arthropods, molluscs and annelids from almost 2000 species and 1000 genera. All data recorded in the database are sourced from their original empirical publication, and the original metrics and measurements are included with each record. This allows for subsequent data transformations as required. We have included rich metadata to allow users to filter the dataset. The additional R scripts we provide will assist researchers with aggregating standardised observations into species-level trait values. Our goals are to provide this resource without restrictions, to keep the AnimalTraits database current, and to grow the number of relevant traits in the future.

Re-evaluating model assumptions suggests that Australian birds are more tolerant of heat and aridity than predicted: a response to Conradie et al. (2020).

Conradie et al. (2020) recently modelled the vulnerability of Australian arid birds to a changing climate. While the approach used by Conradie et al. (2020) is valuable, we argue that key assumptions in their study are poorly supported and the risks of a changing climate to arid zone avifauna are consequently overstated.

The impact of diet quality on the velocity, morphology and normality of sperm in the zebra finch Taeniopygia guttata.

Sperm traits can influence fertilisation success, but there is still much we do not understand about sperm condition dependence, that is, how much sperm traits depend on the male's energy acquisition and allocation. This is especially pronounced in avian taxa, despite extensive observational studies and sampling in wild populations. In this study, we collected sperm samples before and after experimentally reducing diet quality of wild-derived captive zebra finches in small mixed-sex groups, which we compared with individuals on a control diet. We measured the length of sperm components (head, midpiece, flagellum and total sperm length), the proportion of sperm with normal morphology, the proportion of sperm that were progressively motile and sperm swimming velocity (curvilinear velocity; VCL). The only sperm trait we found to be impacted by reduced diet quality was a significant decrease in sperm midpiece length. This is consistent with emerging evidence in other non-model systems, as well the fact that diet can alter mitochondrial density and structure in other tissue types. There was also a significant decrease in sperm velocity and the proportion of motile sperm over the course of the experiment for both experimental groups (i.e. unrelated to diet). This decrease in sperm velocity with largely unchanged sperm morphology emphasizes that there are other important determinants of sperm velocity, likely including seminal fluid composition.

Zebra finch song is a very short-range signal in the wild: evidence from an integrated approach.

Birdsong is typically seen as a long-range signal functioning in mate attraction and territory defense. Among birds, the zebra finch is the prime model organism in bioacoustics, yet almost exclusively studied in the lab. In the wild, however, zebra finch song differs strikingly from songbirds commonly studied in the wild as zebra finch males sing most after mating and in the absence of territoriality. Using data from the wild, we here provide an ecological context for a wealth of laboratory studies. By integrating calibrated sound recordings, sound transmission experiments and social ecology of zebra finches in the wild with insights from hearing physiology we show that wild zebra finch song is a very short-range signal with an audible range of about nine meters and that even the louder distance calls do not carry much farther (up to about fourteen meters). These integrated findings provide an ecological context for the interpretation of laboratory studies of this species and indicate that the vocal communication distance of the main laboratory species for avian acoustics contrasts strikingly with songbirds that use their song as a long-range advertisement signal.

Associations between DNA methylation and telomere length during early life: Insight from wild zebra finches (Taeniopygia guttata).

Telomere length and DNA methylation (DNAm) are two promising biomarkers of biological age. Environmental factors and life history traits are known to affect variation in both these biomarkers, especially during early life, yet surprisingly little is known about their reciprocal association, especially in natural populations. Here, we explore how variation in DNAm, growth rate, and early-life conditions are associated with telomere length changes during development. We tested these associations by collecting data from wild, nestling zebra finches in the Australian desert. We found that increases in the level of DNAm were negatively correlated with telomere length changes across early life. We also confirm previously documented effects of post hatch growth rate and clutch size on telomere length in a natural ecological context for a species that has been extensively studied in the laboratory. However, we did not detect any effect of ambient temperature during developmental on telomere length dynamics. We also found that the absolute telomere length of wild zebra finches, measured using the in-gel TRF method, was similar to that of captive birds. Our findings highlight exciting new opportunities to link and disentangle potential relationships between DNA based biomarkers of ageing, and of physiological reactions to environmental change.

The evolution of egg colour and patterning in Australian songbirds.

To understand why avian eggs are so variable in colour and patterning, we investigated the characteristics of extant bird species that provide insight into the evolutionary transitions that occurred during the early radiation of the songbirds. We quantified egg colour and patterning from museum collections of 269 species of Australian passerine and collated it to nest type data (cup- or dome-nesting species). Using phylogenetically reconstructed trait data, we showed that the ancestral passerine egg was likely to be white, and to have been laid inside a domed nest. Egg colouration and nest type were both phylogenetically clustered, and there was evidence of correlated evolution between the two traits. As nests transitioned from domes to cups, there was an increase in the range of egg colours observed, presumably as a response to additional stressors. Finally, we found that egg colour changes occurred more than twice as frequently in cup-nesting species than in dome-nesting species. This suggests that colour may be an adaptive trait that compensates for the loss of the protective nest roof in cup-nesting species.