The impact of urbanization on health depends on the health metric, life stage and level of urbanization: a global meta-analysis on avian species.

Stressors associated with urban habitats have been linked to poor wildlife health but whether a general negative relationship between urbanization and animal health can be affirmed is unclear. We conducted a meta-analysis of avian literature to test whether health biomarkers differed on average between urban and non-urban environments, and whether there are systematic differences across species, biomarkers, life stages and species traits. Our dataset included 644 effect sizes derived from 112 articles published between 1989 and 2022, on 51 bird species. First, we showed that there was no clear impact of urbanization on health when we categorized the sampling locations as urban or non-urban. However, we did find a small negative effect of urbanization on health when this dichotomous variable was replaced by a quantitative variable representing the degree of urbanization at each location. Second, we showed that the effect of urbanization on avian health was dependent on the type of health biomarker measured as well as the individual life stage, with young individuals being more negatively affected. Our comprehensive analysis calls for future studies to disentangle specific urban-related drivers of health that might be obscured in categorical urban versus non-urban comparisons.

Experimental light at night explains differences in activity onset between urban and forest great tits.

Artificial light at night (ALAN) is rapidly increasing and so is scientific interest in its ecological and evolutionary consequences. In wild species, ALAN can modify and disrupt biological rhythms. However, experimental proof of such effects of ALAN in the wild is still scarce. Here, we compared diel rhythms of incubation behaviour, inferred from temperature sensors, of female great tits (Parus major) breeding in urban and forest sites. In parallel, we simulated ALAN by mounting LED lights (1.8 lx) inside forest nest-boxes, to determine the potentially causal role of ALAN affecting diel patterns of incubation. Urban females had an earlier onset of activity compared to forest females. Experimentally ALAN-exposed forest females were similar to urban females in their advanced onset of activity, compared to unexposed forest birds. However, forest females exposed to experimental ALAN, but not urban females, were more restless at night than forest control females. Our findings demonstrate that ALAN can explain the early activity timing in incubating urban great tits, but its effects on sleep disturbance in the forest are not reflected in urban females. Consequently, future research needs to address potential effects of ALAN-induced timing on individual health, fitness and population dynamics, in particular in populations that were not previously affected by light pollution.

A global meta-analysis reveals higher variation in breeding phenology in urban birds than in their non-urban neighbours.

Cities pose a major ecological challenge for wildlife worldwide. Phenotypic variation, which can result from underlying genetic variation or plasticity, is an important metric to understand eco-evolutionary responses to environmental change. Recent work suggests that urban populations might have higher levels of phenotypic variation than non-urban counterparts. This prediction, however, has never been tested across species nor over a broad geographical range. Here, we conducted a meta-analysis of the avian literature to compare urban versus non-urban means and variation in phenology (i.e. lay date) and reproductive effort (i.e. clutch size, number of fledglings). First, we show that urban populations reproduce earlier and have smaller broods than non-urban conspecifics. Second, we show that urban populations have higher phenotypic variation in laying date than non-urban populations. This result arises from differences between populations within breeding seasons, conceivably due to higher landscape heterogeneity in urban habitats. These findings reveal a novel effect of urbanisation on animal life histories with potential implications for species adaptation to urban environments (which will require further investigation). The higher variation in phenology in birds subjected to urban disturbance could result from plastic responses to a heterogeneous environment, or from higher genetic variation in phenology, possibly linked to higher evolutionary potential.

Experimental warming during incubation improves cold tolerance of blue tit (Cyanistes caeruleus) chicks.

Climate change and increasing air temperature may alter environmental conditions for developing birds, with a range of phenotypic consequences for offspring. The thermal environment during incubation may affect the trade-off between growth and thermoregulation, but the effects of temperature on the ontogeny of endothermy are not fully understood. Therefore, we experimentally tested whether heating the nest cup of Eurasian blue tits (Cyanistes caeruleus) during incubation would influence cold tolerance of the chicks after hatching. Chicks from both heated and control nests showed a decrease in cooling rate with age as they became increasingly endothermic and homeothermic. However, chicks from previously heated nests cooled at a lower rate per unit surface area and from across the whole body. These chicks also had a greater body mass during the first 12 days of life compared with chicks from control nests. Lower cooling rates in heated chicks may reflect greater thermogenic capacity or a reduced surface area to volume ratio owing to a greater body mass. Future projections for climate change predict rising air temperature and increased likelihood of heatwaves, even in temperate regions. Our results indicate that nest microclimate can affect thermoregulation in offspring, and thus may be used to predict some of the future physiological responses of birds to climate change during breeding.

Wavelength-dependent effects of artificial light at night on phytoplankton growth and community structure.

Artificial light at night (ALAN) is a disruptive form of pollution, impacting physiological and behavioural processes that may scale up to population and community levels. Evidence from terrestrial habitats show that the severity and type of impact depend on the wavelength and intensity of ALAN; however, research on marine organisms is still limited. Here, we experimentally investigated the effect of different ALAN colours on marine primary producers. We tested the effect of green (525 nm), red (624 nm) and broad-spectrum white LED ALAN, compared to a dark control, on the green microalgae Tetraselmis suesica and a diatom assemblage. We show that green ALAN boosted chlorophyll production and abundance in T. suesica. All ALAN wavelengths affected assemblage biomass and diversity, with red and green ALAN having the strongest effects, leading to higher overall abundance and selective dominance of specific diatom species, some known to cause harmful algal blooms. Our findings show that green and red ALAN should be used with caution as alternative LED colours in coastal areas, where there might be a need to strike a balance between the effects of green and red light on marine primary producers with the benefit they appear to bring to other organisms.

Connecting the data landscape of long-term ecological studies: The SPI-Birds data hub.

The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long-term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and ecological processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad-scale global issues (e.g. climate change). To solve data integration issues and enable a new scale of ecological and evolutionary research based on long-term studies of birds, we have created the SPI-Birds Network and Database (www.spibirds.org)-a large-scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI-Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting. SPI-Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collaboration and synthesis. We provide community-derived data and meta-data standards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata languages (e.g. ecological meta-data language). The encouraging community involvement stems from SPI-Bird's decentralized approach: research groups retain full control over data use and their way of data management, while SPI-Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community-specific hubs (such as ours, COMADRE for animal demography, etc.) will aid much-needed large-scale ecological data integration.

Artificial light at night, in interaction with spring temperature, modulates timing of reproduction in a passerine bird.

The ecological impact of artificial light at night (ALAN) on phenological events such as reproductive timing is increasingly recognized. In birds, previous experiments under controlled conditions showed that ALAN strongly advances gonadal growth, but effects on egg-laying date are less clear. In particular, effects of ALAN on timing of egg laying are found to be year-dependent, suggesting an interaction with climatic conditions such as spring temperature, which is known have strong effects on the phenology of avian breeding. Thus, we hypothesized that ALAN and temperature interact to regulate timing of reproduction in wild birds. Field studies have suggested that sources of ALAN rich in short wavelengths can lead to stronger advances in egg-laying date. We therefore tested this hypothesis in the Great Tit (Parus major), using a replicated experimental set-up where eight previously unlit forest transects were illuminated with either white, green, or red LED light, or left dark as controls. We measured timing of egg laying for 619 breeding events spread over six consecutive years and obtained temperature data for all sites and years. We detected overall significantly earlier egg-laying dates in the white and green light vs. the dark treatment, and similar trends for red light. However, there was a strong interannual variability in mean egg-laying dates in all treatments, which was explained by spring temperature. We did not detect any fitness consequence of the changed timing of egg laying due to ALAN, which suggests that advancing reproduction in response to ALAN might be adaptive.

The preference and costs of sleeping under light at night in forest and urban great tits.

Artificial light at night (ALAN) is an increasing phenomenon associated with worldwide urbanization. In birds, broad-spectrum white ALAN can have disruptive effects on activity patterns, metabolism, stress response and immune function. There has been growing research on whether the use of alternative light spectra can reduce these negative effects, but surprisingly, there has been no study to determine which light spectrum birds prefer. To test such a preference, we gave urban and forest great tits (Parus major) the choice where to roost using pairwise combinations of darkness, white light or green dim light at night (1.5 lux). Birds preferred to sleep under artificial light instead of darkness, and green was preferred over white light. In a subsequent experiment, we investigated the consequence of sleeping under a particular light condition, and measured birds' daily activity levels, daily energy expenditure (DEE), oxalic acid as a biomarker for sleep debt and cognitive abilities. White light affected activity patterns more than green light. Moreover, there was an origin-dependent response to spectral composition: in urban birds, the total daily activity and night activity did not differ between white and green light, while forest birds were more active under white than green light. We also found that individuals who slept under white and green light had higher DEE. However, there were no differences in oxalic acid levels or cognitive abilities between light treatments. Thus, we argue that in naive birds that had never encountered light at night, white light might disrupt circadian rhythms more than green light. However, it is possible that the negative effects of ALAN on sleep and cognition might be observed only under intensities higher than 1.5 lux. These results suggest that reducing the intensity of light pollution as well as tuning the spectrum towards long wavelengths may considerably reduce its impact.

Hormonally mediated effects of artificial light at night on behavior and fitness: linking endocrine mechanisms with function.

Alternation between day and night is a predictable environmental fluctuation that organisms use to time their activities. Since the invention of artificial lighting, this predictability has been disrupted and continues to change in a unidirectional fashion with increasing urbanization. As hormones mediate individual responses to changing environments, endocrine systems might be one of the first systems affected, as well as being the first line of defense to ameliorate any negative health impacts. In this Review, we first highlight how light can influence endocrine function in vertebrates. We then focus on four endocrine axes that might be affected by artificial light at night (ALAN): pineal, reproductive, adrenal and thyroid. Throughout, we highlight key findings, rather than performing an exhaustive review, in order to emphasize knowledge gaps that are hindering progress on proposing impactful and concrete plans to ameliorate the negative effects of ALAN. We discuss these findings with respect to impacts on human and animal health, with a focus on the consequences of anthropogenic modification of the night-time environment for non-human organisms. Lastly, we stress the need for the integration of field and lab experiments as well as the need for long-term integrative eco-physiological studies in the rapidly expanding field of light pollution.

Light at night, clocks and health: from humans to wild organisms.

The increasing use of electric lights has modified the natural light environment dramatically, posing novel challenges to both humans and wildlife. Indeed, several biomedical studies have linked artificial light at night to the disruption of circadian rhythms, with important consequences for human health, such as the increasing occurrence of metabolic syndromes, cancer and reduced immunity. In wild animals, light pollution is associated with changes in circadian behaviour, reproduction and predator-prey interactions, but we know little about the underlying physiological mechanisms and whether wild species suffer the same health problems as humans. In order to fill this gap, we advocate the need for integrating ecological studies in the field, with chronobiological approaches to identify and characterize pathways that may link temporal disruption caused by light at night and potential health and fitness consequences.

Individual-based measurements of light intensity provide new insights into the effects of artificial light at night on daily rhythms of urban-dwelling songbirds.

The growing interest in the effects of light pollution on daily and seasonal cycles of animals has led to a boost of research in recent years. In birds, it has been hypothesized that artificial light at night can affect daily aspects of behaviour, but one caveat is the lack of knowledge about the light intensity that wild animals, such as birds, are exposed to during the night. Organisms have naturally evolved daily rhythms to adapt to the 24-h cycle of day and night, thus, it is important to investigate the potential shifts in daily cycles due to global anthropogenic processes such as urbanization. We captured adult male European blackbirds (Turdus merula) in one rural forest and two urban sites differing in the degree of anthropogenic disturbance. We tagged these birds with light loggers and simultaneously recorded changes in activity status (active/non-active) through an automated telemetry system. We first analysed the relationship between light at night, weather conditions and date with daily activity onset and end. We then compared activity, light at night exposure and noise levels between weekdays and weekends. Onset of daily activity was significantly advanced in both urban sites compared to the rural population, while end of daily activity did not vary either among sites. Birds exposed to higher amounts of light in the late night showed earlier onset of activity in the morning, but light at night did not influence end of daily activity. Light exposure at night and onset/end of daily activity timing was not different between weekdays and weekends, but all noise variables were. A strong seasonal effect was detected in both urban and rural populations, such as birds tended to be active earlier in the morning and later in the evening (relative to civil twilight) in the early breeding season than at later stages. Our results point at artificial light at night as a major driver of change in timing of daily activity. Future research should focus on the costs and benefits of altered daily rhythmicity in birds thriving in urban areas.

Investigating the impacts of artificial light via blackouts.

Natural experiments provide remarkable opportunities to test the large-scale effects of human activities. Widespread energy blackouts offer such an 'experiment' to test the impacts of artificial light at night (ALAN) on wildlife. We use the situation in South Africa, where regular scheduled blackouts are being implemented, to highlight this opportunity.

Artificial light at night advances avian reproductive physiology.

Artificial light at night is a rapidly increasing phenomenon and it is presumed to have global implications. Light at night has been associated with health problems in humans as a consequence of altered biological rhythms. Effects on wild animals have been less investigated, but light at night has often been assumed to affect seasonal cycles of urban dwellers. Using light loggers attached to free-living European blackbirds (Turdus merula), we first measured light intensity at night which forest and city birds are subjected to in the wild. Then we used these measurements to test for the effect of light at night on timing of reproductive physiology. Captive city and forest blackbirds were exposed to either dark nights or very low light intensities at night (0.3 lux). Birds exposed to light at night developed their reproductive system up to one month earlier, and also moulted earlier, than birds kept under dark nights. Furthermore, city birds responded differently than forest individuals to the light at night treatment, suggesting that urbanization can alter the physiological phenotype of songbirds. Our results emphasize the impact of human-induced lighting on the ecology of millions of animals living in cities and call for an understanding of the fitness consequences of light pollution.

Chronobiology by moonlight.

Most studies in chronobiology focus on solar cycles (daily and annual). Moonlight and the lunar cycle received considerably less attention by chronobiologists. An exception are rhythms in intertidal species. Terrestrial ecologists long ago acknowledged the effects of moonlight on predation success, and consequently on predation risk, foraging behaviour and habitat use, while marine biologists have focused more on the behaviour and mainly on reproduction synchronization with relation to the Moon phase. Lately, several studies in different animal taxa addressed the role of moonlight in determining activity and studied the underlying mechanisms. In this paper, we review the ecological and behavioural evidence showing the effect of moonlight on activity, discuss the adaptive value of these changes, and describe possible mechanisms underlying this effect. We will also refer to other sources of night-time light ('light pollution') and highlight open questions that demand further studies.

Annual rhythms that underlie phenology: biological time-keeping meets environmental change.

Seasonal recurrence of biological processes (phenology) and its relationship to environmental change is recognized as being of key scientific and public concern, but its current study largely overlooks the extent to which phenology is based on biological time-keeping mechanisms. We highlight the relevance of physiological and neurobiological regulation for organisms' responsiveness to environmental conditions. Focusing on avian and mammalian examples, we describe circannual rhythmicity of reproduction, migration and hibernation, and address responses of animals to photic and thermal conditions. Climate change and urbanization are used as urgent examples of anthropogenic influences that put biological timing systems under pressure. We furthermore propose that consideration of Homo sapiens as principally a 'seasonal animal' can inspire new perspectives for understanding medical and psychological problems.

Urban-like night illumination reduces melatonin release in European blackbirds (Turdus merula): implications of city life for biological time-keeping of songbirds.

INTRODUCTION: Artificial light-at-night is known to affect a broad array of behaviours and physiological processes. In urbanized bird species, light-at-night advances important biological rhythms such as daily cycles of activity/rest and timing of reproduction, but our knowledge of the underlying physiological mechanisms is limited. Given its role as chronobiological signal, melatonin is a strong candidate for mediating the effects of light-at-night. RESULTS: We exposed urban and rural European blackbirds (Turdus merula) to two light treatments equal in photoperiod but with different light intensities at night. The control group was exposed to 0.0001 lux (almost darkness), while the experimental group was exposed to 0.3 lux at night, simulating conditions recorded previously on free-living urban blackbirds. We obtained diel profiles of plasma melatonin for all birds in summer (July) and winter (January), while simultaneously recording locomotor activity. Daily patterns of melatonin concentrations were clearly affected by light-at-night in both seasons. In winter, melatonin concentrations of light-at-night birds were lower in the early and late night than in those of birds kept in darkness. In summer, melatonin concentrations of the light-at-night birds were lower through all night compared to birds kept in darkness. Locomotor activity in light-at-night birds was overall higher than in control individuals, both during the day and at night, and it increased sharply before dawn. In winter, the amount of activity before dawn in the light-at-night group correlated with changes in melatonin from midnight to late night: the greater the decrease in melatonin, the greater the amount of pre-dawn activity. Urban and rural birds responded similarly to light-at-night with respect to melatonin, but differed in their behaviour, with rural birds showing more locomotor activity than urban counterparts. CONCLUSIONS: This study points to reduced melatonin release at night as a potential physiological mechanism underlying the advanced onset of morning activity of urbanized birds. Based on the pattern of melatonin secretion, we suggest that birds responded to light-at-night as if they were exposed to a longer day than birds kept under dark nights.

The effects of artificial light at night (ALAN) on the gaping activity and feeding of mussels.

Artificial Light at Night (ALAN) is a common environmental pollutant which affects >22 % of the world's coastlines. However, the impact of ALAN wavelengths on coastal organisms is under-investigated. Here, we tested the impact of red, green, and white ALAN on the gaping activity and phytoplankton consumption of Mytilus edulis mussels and compared these to dark night. Mussels exhibited a semi-diel activity pattern. Although ALAN did not significantly affect the time open nor the phytoplankton consumption, it did have a colour-specific effect on the gaping frequency with red and white ALAN resulting in lower activity compared to the dark night. Green ALAN caused higher gaping frequency and a negative relationship between consumption and proportion of time open compared to the other treatments. Our findings suggest colour-specific ALAN effects on mussels and call for further investigation on the associated physiological mechanisms and potential ecological consequences.

Part-night exposure to artificial light at night has more detrimental effects on aphid colonies than fully lit nights.

Artificial light at night (ALAN) threatens natural ecosystems globally. While ALAN research is increasing, little is known about how ALAN affects plants and interactions with other organisms. We explored the effects of ALAN on plant defence and plant-insect interactions using barley (Hordeum vulgare) and the English grain aphid (Sitobion avenae). Plants were exposed to 'full' or 'part' nights of 15-20 lux ALAN, or no ALAN 'control' nights, to test the effects of ALAN on plant growth and defence. Although plant growth was only minimally affected by ALAN, aphid colony growth and aphid maturation were reduced significantly by ALAN treatments. Importantly, we found strong differences between full-night and part-night ALAN treatments. Contrary to our expectations, part ALAN had stronger negative effects on aphid colony growth than full ALAN. Defence-associated gene expression was affected in some cases by ALAN, but also positively correlated with aphid colony size, suggesting that the effects of ALAN on plant defences are indirect, and regulated via direct disruption of aphid colonies rather than via ALAN-induced upregulation of defences. Mitigating ecological side effects of ALAN is a complex problem, as reducing exposure to ALAN increased its negative impact on insect herbivores. This article is part of the theme issue 'Light pollution in complex ecological systems'.

Widespread extinction debts and colonization credits in United States breeding bird communities.

Species extinctions and colonizations in response to land cover change often occur with time lags rather than instantaneously, leading to extinction debts and colonization credits. These debts and credits can lead to erroneous predictions of future biodiversity. Recent attempts to measure debts and credits have been limited to small geographical areas and have not considered multiple land cover types, or the directionality of land cover change. Here we quantify the relative contribution of past and current landscapes on the current effective number of species of 2,880 US bird communities, explicitly measuring the response of biodiversity to increases and decreases in five land cover types. We find that the current effective number of species is still largely explained by the past landscape composition (legacy effect), depending on the type, magnitude and directionality of recent land cover change. This legacy effect leads to widespread extinction debts and colonization credits. Specifically, we reveal debts across 52% of the United States, particularly in recently urbanized areas, and colonization credits in the remaining 48%, which are primarily associated with grassland decrease. We conclude that biodiversity policy targets risk becoming rapidly obsolete unless past landscapes are considered and debts and credits accounted for.