Thomas Raap

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.

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.

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.

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.

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.

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.

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

We quantified the effect of artificial light at night on oxalate, a potential marker of sleep debt, in free-living developing songbirds. Rather than a decrease, as was found in sleep-deprived mammals, oxalate increased in male nestlings. This research indicates a sex-specific physiological impact of ALAN that warrants further investigation.

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.

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.