In its 2011 Revision of World Urbanization Prospects, the Population Division of the United Nations projected that the world population will increase to 9.3 billion between 2011 and 2050, of which 6.3 billion (67 %) will live in urban areas (IUCN 2012). In 1950 the world urban population was less than 500,000. The dramatic increase in size and number of cities since the Industrial Revolution has generated great interest among scientists in urbanization and its social, economic and environmental consequences (Robinson 1997; Grimm et al. 2008; Lederbogen et al. 2011). In particular, urban ecology has become an established field of research. It is now evident that the specific attributes of the urban habitat can profoundly impact and alter biogeochemical cycles, biodiversity and ultimately ecosystem functions (McKinney 2002; Eigenbrod et al.
2011).
One of the peculiar characteristics of urban areas is the presence of artificial light at night. In 1879 the first commercially produced light bulb illuminated the streets of New York City (Israel 2000). Today the use of artificial light is widespread and has lead to dramatic changes in the lifestyle of billions of people and also to a profound modification of natural environments. For instance, nowadays it is common to refer to artificial light at night as “light pollution”. But what exactly is light pollution? One of the many definitions of light pollution encompasses two different aspects of the phenomenon and is provided by Hollan (Hollan 2008): light pollution is “the alteration of light levels in the outdoor environment (from those present naturally) due to man-made sources of light.
Indoor light pollution is such alteration of light levels in the indoor environment due to
Indoor light pollution, because of its obvious implications for humans, has received great scientific interest (Rajaratnam & Arendt 2001). Light at night is now considered a public health issue (Pauley 2004), given its negative effects on cancer development (Dauchy et al. 1999; Kloog et al. 2010), psychology (Bedrosian, Weil, & Nelson 2012), and metabolism (Fonken et al. 2010). While the consequences of indoor night lighting have been extensively investigated, the understanding of the potential consequences of outdoor light pollution for wildlife has been traditionally limited to a few sparse examples, such as collision of birds with aircrafts and towers (Larkin et al. 1975), disorientation of sea-turtle hatchlings (Witherington & Bjorndal 1991), and attraction of insects by light sources (Frank 1988). However, a seminal book (Rich & Longcore 2006) has attracted new interest on this topic. In recent years, ecologists have described effects of artificial light at night on the stress physiology of tuna (Honryo et al. 2012), commuting and roosting behaviour of bats (Boldogh, Dobrosi, & Samu 2007; Stone, Jones, & Harris 2009), mating behaviour of male frogs (Baker & Richardson 2006), invertebrate community structure (Davies, Bennie, & Gaston 2012) and ecology of dispersal in salmons (Riley et al. 2013).
In birds, two of the often reported effects of urbanization are an early onset of morning activity (Stephan 1985; Fuller, Warren, & Gaston 2007; Nemeth & Brumm 2009) and an advanced timing of reproduction (Partecke, Van’t Hof, & Gwinner 2004, 2005; Schoech, Bowman, & Reynolds 2004; Chamberlain et al. 2009). Although many environmental factors could be involved in these changes, such as anthropogenic food supply, noise and warmer microclimate of urban areas, artificial light at night is also a potential candidate.
Indeed, light is probably the most important environmental cue through which the majority of organisms time their daily and seasonal activity (Foster & Kreitzmann 2004, 2009). For this reason, changes in the outdoor nighttime light may potentially cause modification of temporal niches in both diurnal and nocturnal species (Santos et al. 2010;
Rotics et al. 2011b; Dwyer et al. 2012). In songbirds, previous studies hinted at a possible effect of artificial night lighting on dawn song and seasonal reproduction (Rowan 1938; Miller 2006; Fuller et al. 2007; Kempenaers et al. 2010). However, there is a surprising lack of data on what light intensities animals are exposed to in cities.
Furthermore, most of the previous studies presented correlational data, and therefore inference on the causes and effects of light pollution is difficult to conceive.
The goals of this thesis are:
i) to find out what levels of nigh-light intensity birds are exposed to in urban environments
ii) to experimentally demonstrate the effects of artificial light at night on daily and seasonal cycles of songbirds
iii) to illuminate the physiological mechanisms underlying these effects, if they are present
I investigated these questions using the European blackbird (Turdus merula) as a model species. This species has become a reference for studying the ecological and evolutionary consequences of urbanization, given its widespread range and successful
extensively studied several aspects of the urbanization of blackbirds, including reproductive and stress physiology (Partecke et al. 2005; Partecke, Schwabl, & Gwinner 2006b), behaviour, migration (Partecke & Gwinner 2007; Fudickar et al. 2013) and genetics (Partecke, Gwinner, & Bensch 2006a). As a consequence of this extensive work, we now ample background information on two study populations, one urban and one rural, in and around the city of Munich, Germany. For my thesis I made use of this knowledge to test specific hypotheses in the context of the effects of light at night. I will now briefly list the contents of each chapter.
Chapter 2 is an extension of this general introduction and has already been published in a special edition of Proceedings of the Royal Society B, called “Biological Cycles”. It is a review about the biology of annual cycles, and how these cycles might be modified, or have already been, by anthropogenic changes of the environment. This chapter provides an insight into seasonal timing mechanisms in mammals and birds that is useful for the understanding of the other chapters. We first focus on endogenous circannual rhythms of migration, hibernation and reproduction, and then discussed how they are integrated with environmental information, namely photoperiod and temperature. We also address potential sources of environmental pressure that might modify or even impair biological timing, such as climate change and urbanization. In particular, artificial light at night is considered to be one of the most urgent issues that scientists should look at when evaluating the potential impacts of global changes on biodiversity and human health.
In Chapter 3 I present novel data on the amount of artificial light at night that European blackbirds from our urban and rural study populations are exposed to. For this purpose I used light loggers deployed on individual blackbirds in the wild. These data show that the light intensities blackbirds experience in the urban night are low, but still much higher than what rural conspecifics face. In addition, I simultaneously recorded changes in activity state (activity/rest) via a state-of-the-art automatic telemetry system. My goal was to understand if variation in timing of daily activity could be explained by variation in nightlight intensity that wild birds encounter. Furthermore, I took advantage of a natural experiment to disentangle the potentially confounding effects of light at night and noise on activity patterns in urban birds. By comparing activity, noise and light at night between weekend and weekdays I was able to show that light at night is a better predictor than noise of the variation in daily cycles observed in urban blackbirds.
The results presented in Chapter 3 show that urban and rural birds differ in their timing of the onset and the end of daily activity. But what are the physiological mechanisms underlying such changes in daily timing? I explored two alternative but not mutually exclusive hypotheses in the following two chapters. In Chapter 4, I investigated whether the variation in the onset of activity in the field is mirrored by a shift in the properties of the endogenous circadian clock. I show that wild-caught urban birds have faster and weaker circadian rhythmicity of locomotor activity than rural conspecifics when kept under constant laboratory conditions. This difference relates at the individual level with the difference observed in the time of onset of activity in the field: the shorter the period
field. Although obtained from only two populations, these results suggest that urbanization is able to modify important physiological traits of avian species. To what extent these changes are the consequence of a micro-evolutionary process, developmental effects, or phenotypic plasticity, still needs to be elucidated.
Another physiological mechanism which could be involved in shaping the extended period of daily activity of urban birds is a direct effect of light at night on the diel rhythm of melatonin, and it is discuss in Chapter 5. Melatonin is a hormone widespread in most vertebrate species, that plays a key role in the regulation of circadian rhythms and the 24 h cycles of activity and rest (Pandi-Perumal et al. 2006). Melatonin release is light-sensitive: melatonin is produced at night and suppressed by light during the day (Arendt
& Skene 2005). For this reason, I hypothesized that exposure to light at night is able to reduce the release of melatonin. To test this hypothesis, I used wild-caught blackbirds from our study populations and set up a laboratory experiment in which urban and rural individuals were equally divided into two treatments: in one group birds were exposed to 0.0001 lux at night (almost darkness), while in the other group birds were exposed to light at night of 0.3 lux. The intensity of light at night that I used in this experiment was calibrated on the data obtained with the light loggers mentioned above (Chapter 3). I obtained diel profiles of plasma melatonin concentration for all birds in winter and summer.
The same experimental set-up described in Chapter 5 was used to test for an effect of artificial light at night on seasonal organization of European blackbirds. As mentioned
above, light at night has already been suggested as a potential mechanism inducing advanced timing of reproduction in urban avian species. However, no experimental demonstration of such a link has been shown thus far, and little is known about the potential effect of light at night on other aspects of life-history, such as molt and migration. In Chapter 6 I report on the short-term effects of light at night on timing of gonadal development, plasma concentration of testosterone and onset of molt during the first annual cycle of the experiment. In this chapter I experimentally show that exposure to very low light intensities at night is able to induce an earlier development of the reproductive system, which is followed by an earlier initiation of molt.
While during the first year light at night sped up the seasonal cycles of reproduction and molt, long-term exposure to chronic night lighting (i.e. during second annual cycle) completely suppressed reproductive functions and resulted in an irregular molt sequence.
I present these results and discuss the potential explanations of such effects of light at night in Chapter 7. Although the chronic and long-term night-light stimulation used in our experiment is probably not fully representative of the natural exposure to light at night in birds living in urban areas, these results show the potential risks that an increase in light pollution could pose for wildlife. I therefore call for an urgent integration of science, policy-making and technological development to limit the impact of artificial light on the ecosystems.
Finally, in the last chapter of my thesis, I review the major findings and consider their
consequences of light pollution, and propose some experiments that will enhance our knowledge of the impact of artificial lights on reproductive success and survival.
Furthermore, I stress that a thorough understanding of the phenomenon of light pollution cannot be disregarded when considering how altered the daily and seasonal rhythmicity of individual birds will translate at the population, community and ecosystem level.