Response of bats to light with different spectra: light-shy and agile bat presence is affected by white and green, but not red light.

Artificial light at night has shown a remarkable increase over the past decades. Effects are reported for many species groups, and include changes in presence, behaviour, physiology and life-history traits. Among these, bats are strongly affected, and how bat species react to light is likely to vary with light colour. Different spectra may therefore be applied to reduce negative impacts. We used a unique set-up of eight field sites to study the response of bats to three different experimental light spectra in an otherwise dark and undisturbed natural habitat. We measured activity of three bat species groups around transects with light posts emitting white, green and red light with an intensity commonly used to illuminate countryside roads. The results reveal a strong and spectrum-dependent response for the slow-flying Myotis and Plecotus and more agile Pipistrellus species, but not for Nyctalus and Eptesicus species. Plecotus and Myotis species avoided white and green light, but were equally abundant in red light and darkness. The agile, opportunistically feeding Pipistrellus species were significantly more abundant around white and green light, most likely because of accumulation of insects, but equally abundant in red illuminated transects compared to dark control. Forest-dwelling Myotis and Plecotus species and more synanthropic Pipistrellus species are thus least disturbed by red light. Hence, in order to limit the negative impact of light at night on bats, white and green light should be avoided in or close to natural habitat, but red lights may be used if illumination is needed.

Neither artificial light at night, anthropogenic noise nor distance from roads are associated with oxidative status of nestlings in an urban population of songbirds.

Increasing urbanization is responsible for road-related pollutants and causes an unprecedented increase in light and noise pollution, with potential detrimental effects for individual animals, communities and ecosystems. These stressors rarely act in isolation but studies dissecting the effects of these multiple stressors are lacking. Moreover, studies on urban stressors have mainly focused on adults, while exposure in early-life may be detrimental but is largely ignored. To fill this important knowledge gap, we studied if artificial light at night, anthropogenic noise and road-related pollution (using distance from roads as a proxy) explain variation in oxidative status in great tit nestlings (Parus major) in an urban population. Artificial light at night, anthropogenic noise and distance from roads were not associated with variation of the nine studied metrics of oxidative status (superoxide dismutase-SOD-, glutathione peroxidase-GPX, catalase-CAT-, non-enzymatic total antioxidant capacity-TAC-, reduced glutathione-GSH-, oxidized glutathione-GSSG-, ratio GSH/GSSG, protein carbonyls and thiobarbituric acid reactive substances-TBARS). Interestingly, for all oxidative status metrics, we found that there was more variation in oxidative status among individuals of the same nest compared to between different nests. We also showed an increase in protein carbonyls and a decrease of the ratio GSH/GSSG as the day advanced, and an increase of GPX when weather conditions deteriorated. Our study suggests that anthropogenic noise, artificial light at night and road-related pollution are not the most important sources of variation in oxidative status in great tit nestlings. It also highlights the importance of considering bleeding time and weather conditions in studies with free-living animals.

Anthropogenic noise and light pollution additively affect sleep behaviour in free-living birds in sex- and season-dependent fashions.

Rapid anthropogenic transformation of environments exposes organisms to diverse disturbance factors, including anthropogenic noise pollution and artificial light at night (ALAN). These sensory pollutants interfere with acquisition of, and response to, environmental cues and can be perceived as stressors. Noise pollution and ALAN are often experienced simultaneously, and are thus likely to jointly affect organisms, either additively or interactively. Yet, combined effects of noise pollution and ALAN remain poorly elucidated. We studied combined effects of noise pollution and ALAN on the sleep behaviour of a free-living songbird, the great tit (Parus major). Sleep is widely conserved across animal taxa and fulfils essential functions, and research has demonstrated independent effects of both noise and ALAN on sleep. We measured noise and light levels at nest boxes and used infrared video-recording to assess sleep behaviour. Results did not support interactive effects of noise and ALAN. However, noise pollution and ALAN were both independently related to variation in sleep behaviour, in sex- and season-dependent fashions. Males, but not females, woke up and left the nest box ∼20 min later in the noisiest as compared to quietest environments (range: 44.2-79.4 dB), perhaps because males are more sensitive to acoustical cues that are masked by noise. Furthermore, as the season progressed from November to early March, birds woke up and left the nest box ∼35 min earlier relative to sunrise on territories with the lowest, but not the highest, light levels (range: 0.01-8.5 lux). Thus, the seasonal difference in sleep duration was dampened on light polluted territories. These effects could arise if ALAN interferes with birds' ability to sense and respond to increasing daylength, and could have fitness ramifications. Our study suggests that noise pollution and ALAN exert additive effects on sleep behaviour, and that these effects can be sex- and season-dependent.

Early-life exposure to artificial light at night elevates physiological stress in free-living songbirds☆.

Artificial light at night (ALAN) can disrupt adaptive patterns of physiology and behavior that promote high fitness, resulting in physiological stress and elevation of steroid glucocorticoids (corticosterone, CORT in birds). Elevated CORT may have particularly profound effects early in life, with the potential for enduring effects that persist into adulthood. Research on the consequences of early-life exposure to ALAN remains limited, especially outside of the laboratory, and whether light exposure affects CORT concentrations in wild nestling birds particularly remains to be elucidated. We used an experimental setup to test the hypothesis that ALAN elevates CORT concentrations in developing free-living birds, by exposing nestling great tits (Parus major) to ALAN inside nest boxes. We measured CORT in feathers grown over the timeframe of the experiment (7 nights), such that CORT concentrations represent an integrative metric of hormone release over the period of nocturnal light exposure, and of development. We also assessed the relationships between feather CORT concentrations, body condition, nestling size rank and fledging success. In addition, we evaluated the relationship between feather CORT concentrations and telomere length. Nestlings exposed to ALAN had higher feather CORT concentrations than control nestlings, and nestlings in poorer body condition and smaller brood members also had higher CORT. On the other hand, telomere length, fledging success, and recruitment rate were not significantly associated with light exposure or feather CORT concentrations. Results indicate that exposure to ALAN elevates CORT concentrations in nestlings, which may reflect physiological stress. In addition, the organizational effects of CORT are known to be substantial. Thus, despite the lack of an effect on telomere length and survivorship, elevated CORT concentrations in nestlings exposed to ALAN may have subsequent impacts on later-life fitness and stress sensitivity.

Artificial light at night does not affect telomere shortening in a developing free-living songbird: A field experiment: Artificial light at night and telomere dynamics.

Artificial light at night (ALAN) is an increasingly pervasive anthropogenic disturbance factor. ALAN can seriously disrupt physiological systems that follow circadian rhythms, and may be particularly influential early in life, when developmental trajectories are sensitive to stressful conditions. Using great tits (Parus major) as a model species, we experimentally examined how ALAN affects physiological stress in developing nestlings. We used a repeated-measure design to assess effects of ALAN on telomere shortening, body mass, tarsus length and body condition. Telomeres are repetitive nucleotide sequences that protect chromosomes from damage and malfunction. Early-life telomere shortening can be accelerated by environmental stressors, and has been linked to later-life declines in survival and reproduction. We also assayed nitric oxide, as an additional metric of physiological stress, and determined fledging success. Change in body condition between day 8 and 15 differed according to treatment. Nestlings exposed to ALAN displayed a trend towards a decline in condition, whereas control nestlings displayed a trend towards increased condition. This pattern was driven by a greater increase in tarsus length relative to mass in nestlings exposed to ALAN. Nestlings in poorer condition and nestlings that were smaller than their nest mates had shorter telomeres. However, exposure to ALAN was unrelated to telomere shortening, and also had no effect on nitric oxide concentrations or fledging success. Thus, exposure to ALAN may not have led to sufficient stress to induce telomere shortening. Indeed, plasticity in other physiological systems could allow nestlings to maintain telomere length despite moderate stress. Alternatively, the cascade of physiological and behavioral responses associated with light exposure may have no net effect on telomere dynamics.

Cavities shield birds from effects of artificial light at night on sleep.

Light pollution is an ever increasing worldwide problem disrupting animal behavior. Artificial light at night (ALAN) has been shown to affect sleep in wild birds. Even cavity-nesting bird species may be affected when sleeping inside their cavity. Correlational studies suggest that light from outside the cavity/nest box, for example from street lights, may affect sleep. We used an experimental design to study to what extent nest boxes shield animals from effects of ALAN on sleep. We recorded individual sleep behavior of free-living great tits (Parus major) that were roosting in dark nest boxes and exposed their nest box entrance to ALAN the following night (1.6 lux white LED light; a similar light intensity as was found at nest boxes near street lights). Their behavior was compared to that of control birds sleeping in dark nest boxes on both nights. Our experimental treatment did not affect sleep behavior. Sleep behavior of birds in the control group did not differ from that of individuals in the light treated group. Our results suggest that during winter cavities shield birds from some effects of ALAN. Furthermore, given that effects of ALAN and exposure to artificial light are species-, sex-, and season-dependent, it is important that studies using wild animals quantify individual exposure to light pollution, and be cautious in the interpretation and generalization of the effects, or lack thereof, from light pollution. Rigorous studies are necessary to examine individual light exposure and its consequences in cavity- and open-nesting birds.

Artificial light at night causes an unexpected increase in oxalate in developing male songbirds.

Artificial light at night (ALAN) is a widespread and increasing environmental pollutant with known negative impacts on animal physiology and development. Physiological effects could occur through sleep disruption and deprivation, but this is difficult to quantify, especially in small developing birds. Sleep loss can potentially be quantified by using oxalate, a biomarker for sleep debt in adult humans and rats. We examined the effect of ALAN on oxalate in free-living developing great tits (Parus major) as effects during early-life could have long-lasting and irreversible consequences. Nestlings' physiology was quantified at baseline (= 13 days after hatching) and again after two nights of continued darkness (control) or exposure to ALAN (treatment). We found that ALAN increased oxalate levels but only in male nestlings, rather than decreasing it as was found in sleep-deprived humans and rats. Our results using developing birds differ strongly from those obtained with adult mammals. However, we used ALAN to reduce sleep while in rats forced movement was used. Finally, we used free-living opposed to laboratory animals. Whether oxalate is a reliable marker of sleep loss in developing great tits remains to be examined. Potentially the increase of oxalate in male nestlings was unrelated to sleep debt. Nonetheless, our results substantiate physiological effects of ALAN in developing animals and may provide a foundation for future work with free-living animals.

Variation in personality traits across a metal pollution gradient in a free-living songbird.

Anthropogenic contaminants could alter traits central to animal behavioral types, or personalities, including aggressiveness, boldness and activity level. Lead and other toxic metals are persistent inorganic pollutants that affect organisms worldwide. Metal exposure can alter behavior by affecting neurology, endocrinology, and health. However, the direction and magnitude of the behavioral effects of metal exposure remain equivocal. Moreover, the degree to which metal exposure simultaneously affects suites of correlated behavioral traits (behavioral syndromes) that are controlled by common mechanisms remains unclear, with most studies focusing on single behaviors. Using a model species for personality variation, the great tit (Parus major), we explored differences in multiple behavioral traits across a pollution gradient where levels of metals, especially lead and cadmium, are elevated close to a smelter. We employed the novel environment exploration test, a proxy for variation in personality type, and also measured territorial aggressiveness and nest defense behavior. At polluted sites birds of both sexes displayed slower exploration behavior, which could reflect impaired neurological or physiological function. Territorial aggression and nest defense behavior were individually consistent, but did not vary with proximity to the smelter, suggesting that metal exposure does not concurrently affect exploration and aggression. Rather, exploration behavior appears more sensitive to metal pollution. Effects of metal pollution on exploration behavior, a key animal personality trait, could have critical effects on fitness.

Personality and artificial light at night in a semi-urban songbird population: No evidence for personality-dependent sampling bias, avoidance or disruptive effects on sleep behaviour.

Light pollution or artificial light at night (ALAN) is an increasing, worldwide challenge that affects many aspects of animal behaviour. Interestingly, the response to ALAN varies widely among individuals within a population and variation in personality (consistent individual differences in behaviour) may be an important factor explaining this variation. Consistent individual differences in exploration behaviour in particular may relate to the response to ALAN, as increasing evidence indicates its relation with how individuals respond to novelty and how they cope with anthropogenic modifications of the environment. Here, we assayed exploration behaviour in a novel environment as a proxy for personality variation in great tits (Parus major). We observed individual sleep behaviour over two consecutive nights, with birds sleeping under natural dark conditions the first night and confronted with ALAN inside the nest box on the second night, representing a modified and novel roosting environment. We examined whether roosting decisions when confronted with a camera (novel object), and subsequently with ALAN, were personality-dependent, as this could potentially create sampling bias. Finally, we assessed whether experimentally challenging individuals with ALAN induced personality-dependent changes in sleep behaviour. Slow and fast explorers were equally likely to roost in a nest box when confronted with either a camera or artificial light inside, indicating the absence of personality-dependent sampling bias or avoidance of exposure to ALAN. Moreover, slow and fast explorers were equally disrupted in their sleep behaviour when challenged with ALAN. Whether other behavioural and physiological effects of ALAN are personality-dependent remains to be determined. Moreover, the sensitivity to disturbance of different behavioural types might depend on the behavioural context and the specific type of challenge in question. In our increasingly urbanized world, determining whether the effects of anthropogenic stressors depend on personality type will be of paramount importance as it may affect population dynamics.

Disruptive effects of light pollution on sleep in free-living birds: Season and/or light intensity-dependent?

Light pollution or artificial light at night (ALAN) is an increasing anthropogenic environmental pollutant posing an important potential threat for wildlife. Evidence of its effects on animal physiology and behaviour is accumulating. However, in order to effectively mitigate light pollution it is important to determine which factors contribute to the severity of effects of ALAN. In this experimental study we explored whether there are seasonal-dependent effects of ALAN on sleep in free-living great tits (Parus major), an important model species. Additionally, we looked at whether light intensity determined the severity of effects of ALAN on sleep. We therefore exposed animals to artificial light inside the nest box (3lx) in December (winter) and February (pre-breeding season). Results from February were compared with the results from a previous study in February, using a lower light intensity (1.6lx). We found little evidence for a season-dependent response. Effects of ALAN hardly differed between high and low light intensity. ALAN disrupted sleep with as main effect a decrease in sleep duration (≈-40min) as animals woke up earlier (≈-24min). However, compared to a natural dark situation sleep onset was delayed by high but not by low light intensity of ALAN. Our study underlines earlier found disruptive effects of ALAN on sleep of free-living animals. While we found no conclusive evidence for seasonal or light intensity-dependent effects of ALAN, additional experimental work using lower light intensities might show such differences. Examining potential management options is crucial in mitigating disruptive effects of light pollution, which will be an important focus for future studies.

Artificial light at night affects sleep behaviour differently in two closely related songbird species.

Artificial light at night (ALAN) or light pollution is an increasing and worldwide problem. There is growing concern that because of the disruption of natural light cycles, ALAN may pose serious risks for wildlife. While ALAN has been shown to affect many aspects of animal behaviour and physiology, few studies have experimentally studied whether individuals of different species in the wild respond differently to ALAN. Here, we investigated the effect of ALAN on sleep behaviour in two closely related songbird species inhabiting the same study area and roosting/breeding in similar nest boxes. We experimentally exposed free-living great tits (Parus major) and blue tits (Cyanistes caeruleus) to artificial light inside their nest boxes and observed changes in their sleep behaviour compared to the previous night when the nest boxes were dark. In line with previous studies, sleep behaviour of both species did not differ under dark conditions. ALAN disrupted sleep in both great and blue tits. However, compared to blue tits, great tits showed more pronounced effects and more aspects of sleep were affected. Light exposed great tits entered the nest boxes and fell asleep later, woke up and exited the nest boxes earlier, and the total sleep amount and sleep percentage were reduced. By contrast, these changes in sleep behaviour were not found in light exposed blue tits. Our field experiment, using exactly the same light manipulation in both species, provides direct evidence that two closely related species respond differently to ALAN, while their sleep behaviour under dark conditions was similar. Our research suggests that findings for one species cannot necessarily be generalised to other species, even closely-related species. Furthermore, species-specific effects could have implications for community dynamics.

Ambient anthropogenic noise but not light is associated with the ecophysiology of free-living songbird nestlings.

Urbanization is associated with dramatic increases in noise and light pollution, which affect animal behaviour, physiology and fitness. However, few studies have examined these stressors simultaneously. Moreover, effects of urbanization during early-life may be detrimental but are largely unknown. In developing great tits (Parus major), a frequently-used model species, we determined important indicators of immunity and physiological condition: plasma haptoglobin (Hp) and nitric oxide (NOx) concentration. We also determined fledging mass, an indicator for current health and survival. Associations of ambient noise and light exposure with these indicators were studied. Anthropogenic noise, light and their interaction were unrelated to fledging mass. Nestlings exposed to more noise showed higher plasma levels of Hp but not of NOx. Light was unrelated to Hp and NOx and did not interact with the effect of noise on nestlings' physiology. Increasing levels of Hp are potentially energy demanding and trade-offs could occur with life-history traits, such as survival. Effects of light pollution on nestlings of a cavity-nesting species appear to be limited. Nonetheless, our results suggest that the urban environment, through noise exposure, may entail important physiological costs for developing organisms.

The Female Perspective of Personality in a Wild Songbird: Repeatable Aggressiveness Relates to Exploration Behaviour.

Males often express traits that improve competitive ability, such as aggressiveness. Females also express such traits but our understanding about why is limited. Intraspecific aggression between females might be used to gain access to reproductive resources but simultaneously incurs costs in terms of energy and time available for reproductive activities, resulting in a trade-off. Although consistent individual differences in female behaviour (i.e. personality) like aggressiveness are likely to influence these reproductive trade-offs, little is known about the consistency of aggressiveness in females. To quantify aggression we presented a female decoy to free-living female great tits (Parus major) during the egg-laying period, and assessed whether they were consistent in their response towards this decoy. Moreover, we assessed whether female aggression related to consistent individual differences in exploration behaviour in a novel environment. We found that females consistently differed in aggressiveness, although first-year females were on average more aggressive than older females. Moreover, conform life history theory predictions, 'fast' exploring females were more aggressive towards the decoy than 'slow' exploring females. Given that personality traits are often heritable, and correlations between behaviours can constrain short term adaptive evolution, our findings highlight the importance of studying female aggression within a multivariate behavioural framework.

Artificial light at night disrupts sleep in female great tits (Parus major) during the nestling period, and is followed by a sleep rebound.

Artificial light at night has been linked to a wide variety of physiological and behavioural consequences in humans and animals. Given that little is known about the impact of light pollution on sleep in wild animals, we tested how experimentally elevated light levels affected sleep behaviour of female songbirds rearing 10 day old chicks. Using a within-subject design, individual sleep behaviour was observed over three consecutive nights in great tits (Parus major), with females sleeping in a natural dark situation on the first and third night, whereas on the second night they were exposed to a light-emitting diode (1.6 lux). Artificial light in the nest box dramatically and significantly affected sleep behaviour, causing females to fall asleep later (95 min; while entry time was unaffected), wake up earlier (74 min) and sleep less (56%). Females spent a greater proportion of the night awake and the frequency of their sleep bouts decreased, while the length of their sleep bouts remained equal. Artificial light also increased begging of chicks at night, which may have contributed to the sleep disruption in females or vice versa. The night following the light treatment, females slept 25% more compared to the first night, which was mainly achieved by increasing the frequency of sleep bouts. Although there was a consistent pattern in how artificial light affected sleep, there was also large among-individual variation in how strongly females were affected. When comparing current results with a similar experiment during winter, our results highlight differences in effects between seasons and underscore the importance of studying light pollution during different seasons. Our study shows that light pollution may have a significant impact on sleep behaviour in free-living animals during the reproductive season, which may provide a potential mechanism by which artificial light affects fitness.

Early life exposure to artificial light at night affects the physiological condition: An experimental study on the ecophysiology of free-living nestling songbirds.

Light pollution or artificial light at night (ALAN) is increasingly recognised to be an important anthropogenic environmental pressure on wildlife, affecting animal behaviour and physiology. Early life experiences are extremely important for the development, physiological status and health of organisms, and as such, early exposure to artificial light may have detrimental consequences for organism fitness. We experimentally manipulated the light environment of free-living great tit nestlings (Parus major), an important model species in evolutionary and environmental research. Haptoglobin (Hp) and nitric oxide (NOx), as important indicators of immunity, health, and physiological condition, were quantified in nestlings at baseline (13 days after hatching) and after a two night exposure to ALAN. We found that ALAN increased Hp and decreased NOx. ALAN may increase stress and oxidative stress and reduce melatonin which could subsequently lead to increased Hp and decreased NOx. Haptoglobin is part of the immune response and mounting an immune response is costly in energy and resources and, trade-offs are likely to occur with other energetically demanding tasks, such as survival or reproduction. Acute inhibition of NOx may have a cascading effect as it also affects other physiological aspects and may negatively affect immunocompetence. The consequences of the observed effects on Hp and NOx remain to be examined. Our study provides experimental field evidence that ALAN affects nestlings' physiology during development and early life exposure to ALAN could therefore have long lasting effects throughout adulthood.

Artificial light at night affects body mass but not oxidative status in free-living nestling songbirds: an experimental study.

Artificial light at night (ALAN), termed light pollution, is an increasingly important anthropogenic environmental pressure on wildlife. Exposure to unnatural lighting environments may have profound effects on animal physiology, particularly during early life. Here, we experimentally investigated for the first time the impact of ALAN on body mass and oxidative status during development, using nestlings of a free-living songbird, the great tit (Parus major), an important model species. Body mass and blood oxidative status were determined at baseline (=13 days after hatching) and again after a two night exposure to ALAN. Because it is very difficult to generalise the oxidative status from one or two measures we relied on a multi-biomarker approach. We determined multiple metrics of both antioxidant defences and oxidative damage: molecular antioxidants GSH, GSSG; antioxidant enzymes GPX, SOD, CAT; total non-enzymatic antioxidant capacity and damage markers protein carbonyls and TBARS. Light exposed nestlings showed no increase in body mass, in contrast to unexposed individuals. None of the metrics of oxidative status were affected. Nonetheless, our study provides experimental field evidence that ALAN may negatively affect free-living nestlings' development and hence may have adverse consequences lasting throughout adulthood.

Light pollution disrupts sleep in free-living animals.

Artificial lighting can alter individual behaviour, with often drastic and potentially negative effects on biological rhythms, daily activity and reproduction. Whether this is caused by a disruption of sleep, an important widespread behaviour enabling animals to recover from daily stress, is unclear. We tested the hypothesis that light pollution disrupts sleep by recording individual sleep behaviour of great tits, Parus major, that were roosting in dark nest-boxes and were exposed to light-emitting diode light the following night. Their behaviour was compared to that of control birds sleeping in dark nest-boxes on both nights. Artificial lighting caused experimental birds to wake up earlier, sleep less (-5%) and spent less time in the nest-box as they left their nest-box earlier in the morning. Experimental birds did not enter the nest-box or fall asleep later than controls. Although individuals in lit nest-boxes did not wake up more often nor decreased the length of their sleep bouts, females spent a greater proportion of the night awake. Our study provides the first direct proof that light pollution has a significant impact on sleep in free-living animals, in particular in the morning, and highlights a mechanism for potential effects of light pollution on fitness.