Dose-dependent responses of avian daily rhythms to artificial light at night
Introduction
Research recently started to focus on dramatically changed night-time light conditions, and our understanding of the ecological consequences of light pollution is still limited [1], [2], [3]. Artificial lighting of urban and rural areas will continue to increase worldwide [4] and can have major effects on the behaviour and fitness of wild species [5]. Besides very direct and often lethal effects, such as the well-known fatal attraction of sea turtle nestlings to coastal lights [6] and avian mortality from collisions with human-made illuminated structures [7], more subtle effects can occur due to the disruption of natural daily cycles of light and darkness as well as seasonal cycles in day length that are used to anticipate environmental changes [8].
In birds, internal circadian and circannual clocks are synchronised by light stimulation of photoreceptors [9]. This photosensitivity enables birds to align their activity and physiology to the appropriate time of the day and year. Recent studies on wild populations show that blackbirds (Turdus merula) in more light polluted areas perceive a longer subjective day than conspecifics in darker regions [10] and that they extend foraging activity into illuminated nights [11]. Great tits (Parus major) that were exposed to light inside their nest box woke up and left their nest box earlier in the morning [12]. Also, timing of dawn and dusk singing in common songbirds was altered by light at night [13]. In addition, multiple studies showed an effect of artificial light on timing of reproduction, such as in the blue tit (Cyanistes caeruleus) [14], the blackbird [15] and the great tit [16].
The presence of light at night cannot be indicated as a ‘yes or no’ event, but is a disturbance of natural habitat which continues from bright light close to the light source to very low light intensities at greater distance. Knowing the behavioural response to different light intensities and consequent effects on reproduction and survival is therefore necessary to quantify the impact of artificial light on bird populations. Gaston et al. [17] recently concluded that so far most studies have focused on light at night versus no light at night, and that one of the important research challenges is to determine the thresholds and dose–response functions for biological impacts of artificial light at night. One of the few examples of this kind of studies is on the dispersal of Atlantic salmon fry (Salmo salar) [18], in which researchers identified the intensity at which artificial light disrupted dispersal behaviour: the threshold for delaying dispersal was reached at low light intensity, with little additive effect of increasing light intensity up to 8 lx. Altered daily activity patterns have previously been found in the Indian weaver bird (Ploceus philippinus), where activity in the subjective night increased with higher light levels [19], although daytime light levels in this study were relatively low.
The hormone melatonin plays an important role in the circadian organisation of birds and other vertebrates. Melatonin is released by the pineal gland during the dark phase of the day and suppressed by (day-) light via photoreceptors [20], [21]. It accurately encodes the duration of the night and hence day length, thereby helping birds to synchronise their behaviour and physiology to the external light–dark cycle [22]. Melatonin is known to be related to locomotor activity and both are regularly measured in relation to effects of light at night [23], [24]. We expect artificial light at night to suppress melatonin levels, which was recently shown to be the case in the tammar wallaby (Macropus eugenii) [25], in the Indian weaver bird [19] and in the blackbird [23]. In fish, circadian melatonin patterns were inhibited by low intensity night light levels [26]. In contrast, a study on western scrub-jays (Aphelocoma californica) showed opposite effects of light at night: amplitude of melatonin was increased [27]. Therefore, it is still largely unknown how activity patterns and melatonin levels relate to intensity of light at night.
In our study, we determined the dose–response relationship for the effect of night light intensity on the daily rhythms of a small passerine, the great tit. In a laboratory setting, we exposed birds to five night light treatments, varying from 0.05 to 5 lx. These intensities are comparable to light levels around lamp posts in rural areas in most of Northern Europe [28], and those on the lower end have been empirically measured on European blackbirds that carried light loggers [29]. We continuously measured daily activity patterns. We sampled plasma melatonin levels at midday to obtain baseline levels, at midnight to determine suppressive effects of light, and shortly before morning light to measure possible changes in melatonin timing reported in blackbirds [23]. We hypothesise that daily activity patterns are altered under light at night and that the effects are larger with increasing light intensity. We expect secretion of melatonin to be progressively depressed at midnight with increasing intensities of light at night. To test for possible carry-over effects, we used a longitudinal design, in which we exposed each bird first to dark nights, then to artificial light at night, and then again to dark nights. In addition to information on carry-over effects, this design also accounts for possible changes in the circadian system as the season progressed [30]. We expect no differences between the treatments for behaviour as well as physiology when comparing the first and last period, without nocturnal illumination.
Section snippets
Animals
For this experiment we studied 35 male great tits. Birds were hand raised and housed at the Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands. They were between one and four years of age, and had known pedigrees. Birds were housed in individual cages (90 cm × 50 cm × 40 cm). Each cage had two separate light sources for day- and night-time illumination, and external light was completely excluded. Cages were ventilated and temperature was maintained between 10 and 14 °C, and did
Activity patterns
Actograms of five representative individuals, one from each treatment group, are shown in Fig. 1. All individuals, even those in the lowest light intensity treatment, reacted clearly to the light at night introduced at the start of experimental period 2. Birds adjusted their activity patterns, with especially a strong response in the morning (Fig. 1). During the following experimental period 3 with dark nights, activity patterns quickly reverted back to normal, with a very sharp on- and offset
Discussion
In this study, we show a strong dose–response relationship for the effect of night light intensity on activity patterns and physiology in the great tit. We found a strong response in the daily onset of activity. Birds advanced their activity more when exposed to higher light intensities at night, the part of their active period that took place during the objective night increased with higher intensities and they stayed active longer at the end of the day. Furthermore, naturally elevated
Acknowledgements
We thank Marylou Aaldering and Franca Kropman for taking good care of our experimental birds, Gilles Wijlhuizen and Jeroen Laurens for technical assistance during the study and Barbara Helm and Davide Dominoni for fruitful discussions about the set-up of the experiment and comments on the manuscript. We are grateful to the numerous NIOO colleagues and students who helped with catching birds and taking blood samples for the melatonin measurements. This research is supported by the Dutch
References (45)
- et al.
Light pollution as a biodiversity threat
Trends Ecol. Evol.
(2010) - et al.
Avian mortality at communication towers in the United States and Canada: which species, how many, and where?
Biol. Conserv.
(2013) - et al.
Artificial night lighting affects dawn song, extra-pair siring success, and lay date in songbirds
Curr. Biol.
(2010) - et al.
Functional similarity in relation to the external environment between circadian behavioral and melatonin rhythms in the subtropical Indian weaver bird
Horm. Behav.
(2012) Avian circadian organization: a chorus of clocks
Front. Neuroendocrinol.
(2014)- et al.
Melatonin: generation and modulation of avian circadian rhythms
Brain Res. Bull.
(1997) - et al.
Role of light wavelengths in synchronization of circadian physiology in songbirds
Physiol. Behav.
(2015) - et al.
Spotlight on fish: light pollution affects circadian rhythms of European perch but does not cause stress
Sci. Total Environ.
(2015) - et al.
Street lighting disturbs commuting bats
Curr. Biol.
(2009) - et al.
Bird interactions with offshore oil and gas platforms: review of impacts and monitoring techniques
J. Environ. Manag.
(2015)