Pre- and postnatal noise directly impairs avian development, with fitness consequences.

Noise pollution is expanding at an unprecedented rate and is increasingly associated with impaired reproduction and development across taxa. However, whether noise sound waves are intrinsically harmful for developing young-or merely disturb parents-and the fitness consequences of early exposure remain unknown. Here, by only manipulating the offspring, we show that sole exposure to noise in early life in zebra finches has fitness consequences and causes embryonic death during exposure. Exposure to pre- and postnatal traffic noise cumulatively impaired nestling growth and physiology and aggravated telomere shortening across life stages until adulthood. Consistent with a long-term somatic impact, early life noise exposure, especially prenatally, decreased individual offspring production throughout adulthood. Our findings suggest that the effects of noise pollution are more pervasive than previously realized.

Acute exposure to high temperature affects expression of heat shock proteins in altricial avian embryos.

As the world warms, understanding the fundamental mechanisms available to organisms to protect themselves from thermal stress is becoming ever more important. Heat shock proteins are highly conserved molecular chaperones which serve to maintain cellular processes during stress, including thermal extremes. Developing animals may be particularly vulnerable to elevated temperatures, but the relevance of heat shock proteins for developing altricial birds exposed to a thermal stressor has never been investigated. Here, we sought to test whether three stress-induced genes - HSPD1, HSPA2, HSP90AA1 - and two constitutively expressed genes - HSPA8, HSP90B1 - are upregulated in response to acute thermal shock in zebra finch (Taeniopygia guttata) embryos half-way through incubation. Tested on a gradient from 37.5 °C (control) to 45 °C, we found that all genes, except HSPD1, were upregulated. However, not all genes initiated upregulation at the same temperature. For all genes, the best fitting model included a correlate of developmental stage that, although it was never significant after multiple-test correction, hints that heat shock protein upregulation might increase through embryonic development. Together, these results show that altricial avian embryos are capable of upregulating a known protective mechanism against thermal stress, and suggest that these highly conserved cellular mechanisms may be a vital component of early developmental protection under climate change.

Physiological and morphological correlates of blood parasite infection in urban and non-urban house sparrow populations.

In the last decade, house sparrow populations have shown a general decline, especially in cities. Avian malaria has been recently suggested as one of the potential causes of this decline, and its detrimental effects could be exacerbated in urban habitats. It was initially thought that avian malaria parasites would not have large negative effects on wild birds because of their long co-evolution with their hosts. However, it is now well-documented that they can have detrimental effects at both the primo- and chronical infection stages. In this study, we examined avian malaria infection and its physiological and morphological consequences in four populations of wild house sparrows (2 urban and 2 rural). We did not find any relationship between the proportions of infected individuals and the urbanisation score calculated for our populations. However, we observed that the proportion of infected individuals increased during the course of the season, and that juveniles were less infected than adults. We did not detect a strong effect of malaria infection on physiological, morphological and condition indexes. Complex parasite dynamics and the presence of confounding factors could have masked the potential effects of infection. Thus, longitudinal and experimental studies are needed to understand the evolutionary ecology of this very common, but still poorly understood, wild bird parasite.

Parent-embryo acoustic communication: a specialised heat vocalisation allowing embryonic eavesdropping.

Sound is arguably the external cue most accessible to embryos of many species, and as such may constitute an unrivalled source of early information. Recent evidence shows that prenatal sounds, similarly to maternal effects, may shape developmental trajectories. Establishing whether parental vocalisations are signals directed at embryos, or parental cues on which embryos eavesdrop, can elucidate whether parents or embryos control developmental outcomes. Prenatal exposure to a characteristic heat-related parental call was recently shown to alter zebra finch growth and fitness. Here, we test the ecological context of this behaviour in the wild, and assess the information value and specificity of this vocalisation for an embryonic audience. We show that wild zebra finches also produce this characteristic call, only at high temperatures. In addition, in the lab, we demonstrate experimentally that calling is specifically triggered by high air temperatures, can occur without an embryonic audience, and importantly, is predicted by individuals' body mass. Overall, our findings reveal a specialised heat vocalisation that enables embryonic eavesdropping, by indicating high ambient temperatures, and parents' capacity to cope with such conditions. This challenges the traditional view of embryos as passive agents of their development, and opens exciting research avenues on avian adaptation to extreme heat.

House sparrows mitigate growth effects of post-natal glucocorticoid exposure at the expense of longevity.

Acute, short-term effects of early-life stress and associated glucocorticoid upregulation on physiology and survival are widely documented across vertebrates. However, the persistence and severity of these effects are largely unknown, especially through the adult stage and for natural systems. Here, we investigate physiological, morphological, and survival effects of post-natal glucocorticoid upregulation across the nestling, juvenile, and adult life stages in house sparrows (Passer domesticus). We manipulate circulating corticosterone concentration in wild, free-living house sparrow nestlings and monitor body size, size-corrected mass, two measures of health (hematocrit and phytohemagglutinin-induced skin swelling), and survival in a captive environment until adulthood. We find that early-life corticosterone exposure depresses nestling size-corrected mass in both sexes, with no strong effect of the treatment on body size or our two measures of health. Birds are able to compensate for negative effects of high early-life corticosterone exposure in the long-term and this effect largely disappears by the juvenile and adult stages. However, treatment has a negative effect on survival through one year of age, suggesting that long-term compensation comes at a price.

Corticosterone levels in relation to trace element contamination along an urbanization gradient in the common blackbird (Turdus merula).

In a rapidly urbanizing world, trace element pollution may represent a threat to human health and wildlife, and it is therefore crucial to assess both exposition levels and associated effects of trace element contamination on urban vertebrates. In this study, we investigated the impact of urbanization on trace element contamination and stress physiology in a wild bird species, the common blackbird (Turdus merula), along an urbanization gradient (from rural to moderately urbanized areas). Specifically, we described the contamination levels of blackbirds by 4 non-essential (Ag, Cd, Hg, Pb) and 9 essential trace elements (As, Co, Cr, Cu, Fe, Mn, Ni, Se, Zn), and explored the putative disrupting effects of the non-essential element contamination on corticosterone levels (a hormonal proxy for environmental challenges). We found that non-essential trace element burden (Cd and Pb specifically) increased with increasing urbanization, indicating a significant trace element contamination even in medium sized cities and suburban areas. Interestingly, the increased feather non-essential trace element concentrations were also associated with elevated feather corticosterone levels, suggesting that urbanization probably constrains birds and that this effect may be mediated by trace element contamination. Future experimental studies are now required to disentangle the influence of multiple urban-related constraints on corticosterone levels and to specifically test the influence of each of these trace elements on corticosterone secretion.

No evidence for an effect of traffic noise on the development of the corticosterone stress response in an urban exploiter.

Anthropogenic noise can have important physiological and behavioral effects on wild animals. For example, urban noise could lead to a state of chronic stress and could alter the development of the hypothalamus-pituitary-adrenal (HPA) axis. Supporting this hypothesis, several studies have found that human disturbance is associated with increased circulating corticosterone (CORT) levels. However, it remains unclear whether increased CORT levels are the result of anthropogenic noise or other anthropogenic factors. Here, we experimentally tested the impact of urban noise on the CORT stress response in an urban exploiter (the house sparrow, Passer domesticus) by exposing chicks to a traffic noise ('disturbed chicks') or not ('control chicks'). If noise exposure has a negative impact on developing chicks, we predicted that (1) disturbed chicks will grow slower, will be in poorer condition, and will have a lower fledging probability than controls; (2) disturbed chicks will have higher baseline CORT levels than control; (3) the CORT stress response will be affected by this noise exposure. Contrary to these predictions, we found no effect of our experiment on growth, body condition, and fledging success, suggesting that house sparrow chicks were not negatively affected by this noise exposure. Moreover, we did not find any effect of noise exposure on either baseline CORT levels or the CORT stress response of chicks. This suggests not only that house sparrow chicks did not perceive this noise as stressful, but also that the development of the HPA axis was not affected by such noise exposure. Our study suggests that, contrary to urban avoiders, urban exploiters might be relatively insensitive to urban noise during their development. Further comparative studies are now needed to understand whether such insensitivity to anthropogenic noise is a consistent phenomenon in urban exploiters and whether this is a major requirement of an urban way of life.

Traffic noise exposure affects telomere length in nestling house sparrows.

In a consistently urbanizing world, anthropogenic noise has become almost omnipresent, and there are increasing evidence that high noise levels can have major impacts on wildlife. While the effects of anthropogenic noise exposure on adult animals have been widely studied, surprisingly, there has been little consideration of the effects of noise pollution on developing organisms. Yet, environmental conditions experienced in early life can have dramatic lifelong consequences for fitness. Here, we experimentally manipulated the acoustic environment of free-living house sparrows (Passer domesticus) breeding in nest boxes. We focused on the impact of such disturbance on nestlings' telomere length and fledging success, as telomeres (the protective ends of chromosomes) appear to be a promising predictor of longevity. We showed that despite the absence of any obvious immediate consequences (growth and fledging success), nestlings reared under traffic noise exposure exhibited reduced telomere lengths compared with their unexposed neighbours. Although the mechanisms responsible for this effect remain to be determined, our results provide the first experimental evidence that noise alone can affect a wild vertebrate's early-life telomere length. This suggests that noise exposure may entail important costs for developing organisms.

Influence of Urbanization on Body Size, Condition, and Physiology in an Urban Exploiter: A Multi-Component Approach.

Consistent expanding urbanization dramatically transforms natural habitats and exposes organisms to novel environmental challenges, often leading to reduced species richness and diversity in cities. However, it remains unclear how individuals are affected by the urban environment and how they can or cannot adjust to the specific characteristics of urban life (e.g. food availability). In this study, we used an integrative multi-component approach to investigate the effects of urbanization on the nutritional status of house sparrows (Passer domesticus). We assessed several morphological and physiological indices of body condition in both juveniles (early post-fledging) and breeding adults from four sites with different levels of urbanization in France, Western Europe. We found that sparrows in more urbanized habitats have reduced body size and body mass compared to their rural conspecifics. However, we did not find any consistent differences in a number of complementary indices of condition (scaled mass index, muscle score, hematocrit, baseline and stress-induced corticosterone levels) between urban and rural birds, indicating that urban sparrows may not be suffering nutritional stress. Our results suggest that the urban environment is unlikely to energetically constrain adult sparrows, although other urban-related variables may constrain them. On the other hand, we found significant difference in juvenile fat scores, suggesting that food types provided to young sparrows differed highly between habitats. In addition to the observed smaller size of urban sparrows, these results suggest that the urban environment is inadequate to satisfy early-life sparrows' nutritional requirements, growth, and development. The urban environment may therefore have life-long consequences for developing birds.

Wandering albatrosses document latitudinal variations in the transfer of persistent organic pollutants and mercury to Southern Ocean predators.

Top marine predators are effective tools to monitor bioaccumulative contaminants in remote oceanic environments. Here, we used the wide-ranging wandering albatross Diomedea exulans to investigate potential geographical variations of contaminant transfer to predators in the Southern Ocean. Blood concentrations of 19 persistent organic pollutants and 14 trace elements were measured in a large number of individuals (N = 180) of known age, sex and breeding status from the subantarctic Crozet Islands. Wandering albatrosses were exposed to a wide range of contaminants, with notably high blood mercury concentrations. Contaminant burden was markedly influenced by latitudinal foraging habitats (inferred from blood δ(13)C values), with individuals feeding in warmer subtropical waters having lower concentrations of pesticides, but higher concentrations of mercury, than those feeding in colder subantarctic waters. Sexual differences in contaminant burden seemed to be driven by gender specialization in feeding habitats, rather than physiological characteristics, with females foraging further north than males. Other individual traits, such as adult age and reproductive status, had little effect on blood contaminant concentrations. Our study provides further evidence of the critical role of global distillation on organic contaminant exposure to Southern Ocean avian predators. In addition, we document an unexpected high transfer of mercury to predators in subtropical waters, which merits further investigation.

Demographic consequences of heavy metals and persistent organic pollutants in a vulnerable long-lived bird, the wandering albatross.

Seabirds are top predators of the marine environment that accumulate contaminants over a long life-span. Chronic exposure to pollutants is thought to compromise survival rate and long-term reproductive outputs in these long-lived organisms, thus inducing population decline. However, the demographic consequences of contaminant exposure are largely theoretical because of the dearth of long-term datasets. This study aims to test whether adult survival rate, return to the colony and long-term breeding performance were related to blood mercury (Hg), cadmium (Cd) and persistent organic pollutants (POPs), by using a capture-mark-recapture dataset on the vulnerable wandering albatross Diomedea exulans. We did not find evidence for any effect of contaminants on adult survival probability. However, blood Hg and POPs negatively impacted long-term breeding probability, hatching and fledging probabilities. The proximate mechanisms underlying these deleterious effects are likely multifaceted, through physiological perturbations and interactions with reproductive costs. Using matrix population models, we projected a demographic decline in response to an increase in Hg or POPs concentrations. This decline in population growth rate could be exacerbated by other anthropogenic perturbations, such as climate change, disease and fishery bycatch. This study gives a new dimension to the overall picture of environmental threats to wildlife populations.

Oxidative stress in relation to reproduction, contaminants, gender and age in a long-lived seabird.

Reproduction is a demanding activity for animals, since they must produce, and in some cases protect and provision, their young. It is often overlooked that demands of reproduction may also be exacerbated by exposure to contaminants. In this study, we make use of an exceptional long-term dataset to perform a cross-sectional study on the long-lived wandering albatross (Diomedea exulans) in order to test the effects of reproduction, persistent organic pollutants [POPs: pesticides and polychlorinated biphenyls (PCBs)], mercury, individual age (3-47 years), and sex on the levels of plasma oxidative damage and inflammation. The results of our study support the hypothesis that oxidative damage may be a physiological cost of reproduction and that individuals carrying higher levels of organic or non-organic contaminants have higher oxidative damage. Levels of the inflammatory protein haptoglobin were similar between breeding and non-breeding birds, with the exception of breeding males which had the lowest levels of haptoglobin. Our data also show an effect of age and of organic contaminants on the plasma oxidative damage level, but not on plasma haptoglobin. In addition, plasma oxidative damage level increased with red blood cell mercury concentration in females but not in males. Hence, our study highlights that the harmful effects of contaminants may come through interaction with factors like life stage or gender, suggesting potential for high variation in susceptibility to contamination among individuals.