Animals regularly experience periods of food uncertainty due to seasonal changes and environmental variability. Further, the changing climate is leading to more variable weather patterns, which alter environmental conditions, and can result in resource distributions being less predictable in space and time. How animals respond to uncertain conditions, and in particular a changing distribution of food resources, remains largely unclear and is an important question in the field of movement and animal ecology. We used an experimental approach to study how Merino sheep (Ovis aries) respond to different levels of food location uncertainty in a drought-impacted region of the Australian arid zone. Sheep were unfamiliar with the experimental food locations at the start and progressively decreased their uncertainty (i.e., increased their environmental knowledge) when discovering an increasing number of foraging patches. We tracked 50 sheep with GPS collars (1 location every 15 s) and deduced their movement and space use behaviour. When food uncertainty decreased, individuals moved more directionally (greater step length, smaller turn angles) and moved greater distances per day. They also had larger daily ranges. Displacement (distance between first and last location of the day) increased once and otherwise remained similar across levels of uncertainty. Our study demonstrates how an arid zone ungulate, in a large 600 ha enclosed paddock, adjusted its movement and space use behaviour as it gained environmental information on food distribution. Our study provides important insights into how animals cope with variable environments in order to forage efficiently during periods of uncertainty. Food distributions are often unpredictable over time, with climate change exacerbating variability. Understanding how animals respond to periods of environmental uncertainty is crucial to predict animal movement in space and time. We used an experimental approach and investigated how different levels of food location uncertainty affected the movement and space-use behaviour in sheep freely moving in a large 600 ha paddock. We used the number of discovered experimental food patches as a proxy for environmental knowledge (inverse of uncertainty). Movement was faster and more directional, and daily range size increased as food uncertainty decreased and sheep gained knowledge about the food locations. Our study demonstrates how an arid zone ungulate adjusted its movement and space use behaviour as it gained environmental information about food patch distributions.
Habitat fragmentation is a key driver of reduced genetic connectivity and loss of genetic variation among populations, elevating the risk of inbreeding depression and reduced adaptive potential. The black-throated finch (Poephila cincta) is an endemic Australian finch with two recognised subspecies, a northern (P. c. atropygialis) and southern form (P. c. cincta) separated by a biogeographic barrier in northern Australia. The southern subspecies is nationally endangered and has experienced severe range contractions since the rise of pastoralism, with only two stronghold populations remaining (Townsville Coastal Plain and Desert Uplands Bioregion). Using a panel of more than 14,000 genome-wide single nucleotide polymorphisms for 107 individuals, we characterised spatial genetic structure for the Desert Uplands population. We mapped effective migration surfaces and tested for isolation by resistance to identify potential barriers to gene flow, estimated contemporary effective population sizes and reconstructed the demographic history of this population. We found evidence of restricted gene flow between localities only 16 km apart and strong isolation by geographic distance. Landscape resistance modelling identified areas of suitable woodland habitat that facilitated effective dispersal. More restricted gene flow in the southern range of this population is likely influenced by the fragmentation of suitable vegetation communities. Contemporary effective population sizes were near or below 1000, and we detected two historical population bottlenecks (> 50
Understanding sex-related differences in ecology is essential for effective conservation strategies, especially in species that exhibit subtle to no sexual dimorphism. This study examines the Desert Uplands population of the Southern Black-throated Finch (Poephila cincta cincta); an endangered species endemic to north-eastern Australia, focusing on key ecological aspects, including sex ratio, movement ecology, and diet. Although previously considered sexually monomorphic, we found subtle sexual dimorphism in throat patch size (17.1% larger in males) and wing length (7.48% larger in males), with no significant differences in other morphological traits. We found a balanced adult sex ratio (52.3% females, 47.7% males), indicating no significant sex bias; a key indicator for ensuring mating opportunities and breeding success. Despite these differences, only 67.6% of individuals could be sexed accurately based on these traits. We also examined the movement ecology of the species and found no significant sex-based differences in home range size or movement distance, consistent with the subspecies' tendency to live in mixed-sex flocks. Diet analysis, based on DNA metabarcoding of crop and faecal samples, indicated no significant sex-based dietary divergence, with both sexes consuming a similar variety of grass seeds. These findings highlight the importance of understanding the ecological dynamics of the Southern Black-throated Finch for conservation efforts, suggesting that further studies on juvenile dispersal, and advanced morphometric techniques may improve understanding of this species.
The Australian zebra finch is an arid-adapted passerine with high hygric demands, that is projected to be at risk from increasing temperature and aridity throughout its distribution by the end of the century. We examine here how individual zebra finches modify their visits to water in response to the climatic conditions of ambient temperature, relative humidity, rainfall, wind speed and day length over a two-month period during an Austral summer drought in arid central Australia. Visits to water by individual zebra finches increased with increasing ambient temperature and day length, and decreased with increasing relative humidity, wind speed and rainfall. These findings are the most comprehensive data for the pattern of visits to water by individual wild birds globally and highlight the importance of regular drinking by individual finches to maintain water balance and thermoregulation. Our data highlight the importance of water availability for birds in the arid zone in a warming climate.
Anthropogenic habitat loss and climate change threaten global biodiversity. Effective conservation management is greatly benefited by a detailed understanding of geographic structure, genetic diversity, and demography of threatened species. The black-throated finch, Poephila cincta, is an Australian songbird with two subspecies: atropygialis and cincta. The southern subspecies, cincta, has experienced an ~80% range contraction over the last century and is listed as endangered, but genetic surveys of it are incomplete. Here, we use a combination of reduced representation and whole genome sequencing to examine genetic differentiation, spatial genetic structure, and demographic history in both subspecies of this species. We find that atropygialis and cincta are geographically isolated by a biogeographic barrier known as the Einasleigh Uplands and genetically distinct despite a history of divergence with gene flow. Since they last shared a common ancestor ~360,000 years ago, the two subspecies have experienced distinct demographic trajectories over the last ~100,000 years, characterized by population expansion in atropygialis and population decline in cincta. We find that the two remnant population centers of cincta, from the Galilee Basin and the Townsville Coastal Plain, each represent genetically distinct lineages that last shared appreciable levels of gene flow ~3000 years ago. Moreover, we report striking microgeographic genetic structure from the Townsville Coastal Plain between populations < 20 km apart associated with barriers to dispersal caused by anthropogenic habitat modification over the last 50 years: namely, the construction of the Ross River Dam. Our findings highlight the urgent need for a conservation approach that prioritizes habitat restoration to re-establish population connectivity in the endangered southern black-throated finch.
The interconnecting links between individuals in an animal social network are often defined by discrete, directed behaviours, but where these are difficult to observe, a network link (edge) may instead be defined by individuals sharing a space at the same time, which can then be used to infer a social association. The method by which these associations are defined should be informed by the biological significance of edges, and therefore often vary between studies. Identifying an appropriate measure of association remains a challenge to behavioural ecologists. Here, we use automatically recorded feeder visit data from four bird systems to compare three methods to identify a social association: (1) strict time-window, (2) co-occurrence in a group, and (3) arrival-time. We tested the similarity of the resulting networks by comparing the repeatability and sensitivity of individuals’ social traits (network degree, strength, betweenness). We found that networks constructed using different methods but applying similar, ecologically relevant definitions of associations based on individuals’ spatio-temporal co-occurrence, showed similar characteristics. Our findings suggest that the different methods to construct animal social networks are comparable, but result in subtle differences driven by species biology and feeder design. We urge researchers to carefully evaluate the ecological context of their study systems when making methodological decisions. Specifically, researchers in ecology and evolution should carefully consider the biological relevance of an edge in animal social networks, and the implications of adopting different definitions.
Although variation in effect sizes and predicted values among studies of similar phenomena is inevitable, such variation far exceeds what might be produced by sampling error alone. One possible explanation for variation among results is differences among researchers in the decisions they make regarding statistical analyses. A growing array of studies has explored this analytical variability in different fields and has found substantial variability among results despite analysts having the same data and research question. Many of these studies have been in the social sciences, but one small “many analyst” study found similar variability in ecology. We expanded the scope of this prior work by implementing a large-scale empirical exploration of the variation in effect sizes and model predictions generated by the analytical decisions of different researchers in ecology and evolutionary biology. We used two unpublished datasets, one from evolutionary ecology (blue tit, Cyanistes caeruleus, to compare sibling number and nestling growth) and one from conservation ecology (Eucalyptus, to compare grass cover and tree seedling recruitment). The project leaders recruited 174 analyst teams, comprising 246 analysts, to investigate the answers to prespecified research questions. Analyses conducted by these teams yielded 141 usable effects (compatible with our meta-analyses and with all necessary information provided) for the blue tit dataset, and 85 usable effects for the Eucalyptus dataset. We found substantial heterogeneity among results for both datasets, although the patterns of variation differed between them. For the blue tit analyses, the average effect was convincingly negative, with less growth for nestlings living with more siblings, but there was near continuous variation in effect size from large negative effects to effects near zero, and even effects crossing the traditional threshold of statistical significance in the opposite direction. In contrast, the average relationship between grass cover and Eucalyptus seedling number was only slightly negative and not convincingly different from zero, and most effects ranged from weakly negative to weakly positive, with about a third of effects crossing the traditional threshold of significance in one direction or the other. However, there were also several striking outliers in the Eucalyptus dataset, with effects far from zero. For both datasets, we found substantial variation in the variable selection and random effects structures among analyses, as well as in the ratings of the analytical methods by peer reviewers, but we found no strong relationship between any of these and deviation from the meta-analytic mean. In other words, analyses with results that were far from the mean were no more or less likely to have dissimilar variable sets, use random effects in their models, or receive poor peer reviews than those analyses that found results that were close to the mean. The existence of substantial variability among analysis outcomes raises important questions about how ecologists and evolutionary biologists should interpret published results, and how they should conduct analyses in the future.
Identifying the physiological mechanisms underpinning inter-individual differences in performance and fitness remains a key challenge in organismal biology. Variation in mitochondrial aerobic metabolism has been suggested to underlie inter-individual variation in performance, but this remains seldom tested, partly because of the need to use terminal sampling for assessing mitochondrial parameters. To fill this knowledge gap, we investigated whether inter-individual variation in mitochondrial aerobic parameters measured from less-invasively taken samples (i.e. blood cells) would correlate with both anaerobic and aerobic metrics of flight performance in house sparrows (Passer domesticus). We predicted that mitochondrial aerobic metabolism should correlate with aerobic but not anaerobic metrics of flight performance. As expected, we found no evidence for a relationship between mitochondrial metabolism and the energy required to take-off (i.e. anaerobic), but flight duration to exhaustion (i.e. aerobic) correlated positively with both cellular mitochondrial respiration rates and oxidative phosphorylation efficiency, a proxy of mitochondrial efficiency to convert nutrients into ATP. Our results, therefore, support the idea that inter-individual variation in mitochondrial aerobic metabolism could underlie variation in aerobic performance and suggest that the nucleated blood cells of birds (and potentially other non-mammalian vertebrates) may be a relevant biological sample to test those links.
Understanding the responses of organisms to environmental change is critical to tackling the grand challenges of 21st century biology. Fields such as ecophysiology and ecology have embraced these challenges and “re-invented” themselves in part by shifting the scale of scientific enquiry and utilizing large-scale comparative approaches. Behavioural research has not yet realized this potential to the same extent. In this paper, we argue that adopting a trait-based approach at large spatial, temporal and taxonomic scales can advance the field of behavioral ecology and address emerging questions in biology. We surveyed the literature in relevant ecology and behavior journals between 1981 and 2020 and found that ecological journals have changed markedly over time, specifically in their focus on understanding interspecific trait variation at broad taxonomic, spatial and temporal scales. This pattern is not apparent for animal behavior, where intra-specific and often intra-population scale of scientific enquiry has mostly been the focus over the last four decades. We argue that behavioral plasticity can be a critical first response to environmental change that might buffer or even lower the risk of extinction. To estimate the capacity of populations or species to respond to change behaviorally, we propose a comparative approach- spatially, temporally or taxonomically- that systematically captures variation in key traits with broad implications for conservation and community ecology. Further, we provide guidance in the methods and resources required to apply a trait-based approach to animal behavior.
Bird genomes are among the most stable in terms of synteny and gene content across vertebrates. However, germline-restricted chromosomes (GRCs) represent a striking exception where programmed DNA elimination confines large-scale genomic changes to the germline. GRCs are known to occur in songbirds (oscines), but have been studied only in a few species of Passerides such as the zebra finch, the key model for passerine genomics. Their presence and evolutionary dynamics in most major passerine lineages remain largely unexplored, with suboscines entirely unexamined by cytogenetic or genomic methods. Here, we present the most comprehensive comparative analysis of GRCs to date, spanning 44 million years of passerine evolution. By generating the first germline reference genomes of an oscine and a suboscine, 22 novel germline draft genomes spanning nearly all major passerine lineages and a germline draft genome of a parrot outgroup, we show that the GRC is likely present in 6,700 passerine species. Our results reveal that the GRC evolves rapidly and distinctly from the standard A chromosomes (autosomes and sex chromosomes), yet retains functionally important, selectively maintained genes. We observed gene and repeat turnover occuring orders of magnitude faster than on the A chromosomes. Some GRC genes, such as cpeb1 and pim1, are widespread from an ancient duplication. In contrast, other GRC genes, like mfsd2b and bmp15, have been independently duplicated onto the GRC multiple times, suggesting adaptive constraints. The discovery of zglp1 on the zebra finch GRC, initially copied from chromosome 30 and subsequently lost from it, indicates functional replacement, where the GRC permits gene loss from the standard genome. As the GRC harbors the only zglp1 copy in most of the ~4000 Passerides species, GRC loss would compromise essential germline functions. Our findings establish the GRC as a genomic innovator driving rapid germline evolution. This fact highlights its evolutionary significance for passerine diversification and suggests that programmed DNA elimination may be an overlooked yet phylogenetically widespread mechanism in many understudied animal lineages.
The interconnecting links (edges) between individuals (nodes) in an animal social network are often defined by discrete, directed behaviours (interactions). However, where interactions are difficult to observe, a network edge is instead defined as individuals sharing space or overlapping in time (an association). Despite an increasingly accessible toolkit to assemble and analyse animal social networks, defining associations remains a challenge in behavioural ecology. While different study systems have used different ways to validate the definition of an association, an empirical comparison of how these different methods compare is lacking. Here, we apply three methods to define social associations, by 1) strict time-window, 2) co-occurrence in a group, and 3) arrival-time, in four bird systems. We first test the ability of each method to detect individually repeatable social traits. Then we describe the structure of each network using Jaccard similarity and Mantel tests, and finally, we test the sensitivity of network structure to changing parameters within the three definitions. We found that the network structure was largely robust to changing how associations were defined, with subtle differences. We suggest that these differences are the result of an inappropriate definition of association in the context of experimental design and system ecology. Researchers in ecology and evolution should carefully consider the biological relevance of association definition prior to starting research into animal social behaviour.
To survive, prey animals must correctly assess and respond to predation, by vigilantly scanning their environment for threats, assessing predation risk through gaze aversion (responding fearfully to predator gaze), and escaping efficiently. As these anti-predatory behaviours are integrated through the nervous and motor systems, they could be disrupted by neurotoxic contaminants, such as lead (Pb), which is ubiquitous in the Anthropocene. Here, we examined the effects of Pb on anti-predatory behaviours of free-living house sparrows (Passer domesticus), in the mining city of Broken Hill, Australia, where birds have been exposed to elevated Pb levels for many generations. We found that sparrows in higher-Pb contaminated areas spent more time scanning their surroundings and were more reluctant to approach a feeder under direct, experimentally introduced human gaze, than sparrows in lower-Pb contaminated areas. Higher-Pb birds had slightly worse (though not statistically different) escape flight performance than their lower-Pb counterparts. Our results suggest that greater exposure to Pb is associated with increased fear, which may or may not be linked to Pb-compromised escape performance. We highlight the importance of considering multi-faceted, integrated effects of environmental pollution on the behaviours of urban wildlife.
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.
[This corrects the article DOI: 10.1098/rsos.181269.][This corrects the article DOI: 10.1098/rsos.181269.].
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 km(2)). 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.
Many animals maintain long-term monogamous partnerships, but the extent to which partners associate varies substantially and has implications for the scope of cooperation between pair members. Zebra finches ( Taeniopygia castanosis ) are monogamously paired for life and maintain continuous partnerships, raising questions as to if and how they maintain pair cohesion despite being non-territorial and having only short-range acoustic signals. While zebra finches are the best-studied songbird in captivity, their social and spatial behaviour in the wild is poorly understood. Determining pair cohesion in songbirds to date has almost exclusively been studied at specific locations where pairs would be expected to meet, such as nesting or feeding sites, without quantifying broader movements. Here, we used solar-powered automated tracking to simultaneously monitor the movements of radio-tagged zebra finch pairs during periods of breeding activity. We reveal extremely high spatial cohesion with pairs using nearly identical home ranges and maintaining close spatial proximity across large areas. This characterization of extremely high spatio-temporal coordination of zebra finch pairs provides important insights into the operation and benefits of monogamous relationships in highly mobile taxa, such as birds.
Abstract 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.
Sperm traits are important in determining fertilisation success and are metabolically expensive to produce. There is little known about how energy acquisition and allocation affect sperm traits in avian taxa. This study assesses the impact of experimentally manipulated diet on long‐tailed finch sperm by comparing the length of sperm components (head, midpiece, flagellum and total sperm) between the treatment groups (homogenous diet and diverse diet) and across time points (before and after the experiment). Diet homogeneity was manipulated as this may impact diet quality in a species that is usually fed a diversity of seed species to thrive in captivity. Our results showed no impact of diet on the length of different sperm components. These results contrast with findings of a similar recent study of the zebra finch which found a significant level of diet‐affected plasticity in midpiece length. For both diet treatment groups in this study there was a slight but significant increase in head, flagellum and total sperm length over the treatment period. Despite this, all sperm components were highly repeatable, consistent with the finding from observational studies in passerine birds. The efficacy of our dietary manipulation was confirmed by a significant reduction in the saturation of bill colour in the long‐tailed finches as a result of the homogenous diet, and a difference in body mass across the treatment groups.
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.