Effects of artificial light at night on daily and seasonal organization of European blackbirds (Turdus merula)

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Effects of artificial light at night on daily and seasonal organization of European blackbirds (Turdus merula)

Dissertation zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften (Dr. rer nat.)

vorgelegt von

Davide Michelangelo Dominoni

an der Universität Konstanz,

Mathematisch-Naturwissenschaftliche Sektion, Fachbereich Biologie

Tag der mündlichen Prüfung: 13.09.2013 1. Referent: Prof. Dr. Martin Wikelski 2. Referentin: Prof. Dr. Michaela Hau 3. Referent: Prof. Dr. Mark van Kleunen

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Effects of artificial light at night on daily and seasonal organization of European blackbirds (Turdus merula)

Dissertation zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften (Dr. rer nat.)

vorgelegt von

Davide Michelangelo Dominoni

an der Universität Konstanz,

Mathematisch-Naturwissenschaftliche Sektion, Fachbereich Biologie

Tag der mündlichen Prüfung: 13.09.2013 1. Referent: Prof. Dr. Martin Wikelski

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The only constant in life is change Heraclitus

I wanna be your dog

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Summary

Urban areas are growing faster than any other land cover types. Associated with increasing urbanization, artificial light at night is now recognized as a public health issue and in recent years new interest has risen around the ecological effects of light pollution.

Given that light through its diel and seasonal (daylength) changes is one of most important factors regulating daily and annual cycles of virtually all organisms, I hypothesized that modifications of the environment by means of artificial light at night could strongly affect important biological cycles of wild animals. In my doctoral dissertation I experimentally demonstrate the effects of light at night on the daily and seasonal cycles of an urbanized songbird, the European blackbird (Turdus merula), and describe the physiological mechanisms that may underlie such effects.

I used a combination of radio-telemetry and light loggers to first record the light intensity to which free-ranging urban and rural blackbirds are exposed to during the night, and then to relate this information to the timing of onset and end of daily activity. Urban birds were exposed to higher intensities of light at night than rural birds. In addition, birds exposed to higher light at night started their activity earlier in the morning and ceased it later in the evening. However, a considerable amount of within-individual variation was present. Temperature, cloud cover and precipitation did not explain this source of variation, but other environmental factors such as noise, food availability and social

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light at night through a natural experiment. Indeed, while both nocturnal and diurnal noise varied considerably between weekend and weekdays, light at night intensity and time of onset of morning activity did not, further proposing light at night as a major driver of altered timing of daily activity in urbanized avian species.

The variation in the time of morning activity between urban and rural blackbirds was mirrored by the properties of their endogenous circadian rhythm. Urban birds showed faster and weaker circadian rhythms than rural individuals when kept under constant laboratory conditions. The relationship at the individual level between circadian traits and activity in the field was found to be significant, suggesting that urbanization may have shaped both the circadian clock and the behavioral phenotype of European blackbirds.

Whether this is a consequence of micro-evolution, developmental (maternal/epigenetic) effects or phenotypic plasticity in response to different environmental characteristics is still unknown. However, I suggest that a plausible scenario could be selection for early birds in urban environments, and that the presence of artificial light at night may be the underlying environmental factor promoting such micro-evolutionary process.

I then used a long-term laboratory experiment to test specific hypotheses about the effects of light at night on daily and seasonal cycles of blackbirds. Wild caught urban and rural birds were exposed for two consecutive years to either dark nights or very low light intensity at night (0.3 lux), calibrated on the data previously recorded on individual blackbirds in their natural urban environment.

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I first predicted that light at night was able to reduce plasma melatonin concentration.

Indeed, birds exposed to light at night, irrespective of their origin, had lower melatonin concentration in the late evening and in the early morning, during both winter and summer. In addition, the lower the melatonin concentration was in the early morning, the higher the amount of activity was at this time of day. I therefore suggest that light at night is able to decrease melatonin release at night, and that this could be one potential physiological mechanism underlying the link between artificial lights in urban areas and alternative temporal activity tactics of urban birds.

Using the same experimental set-up, I also monitored testicular size and plasma concentration of testosterone over two consecutive reproductive cycles. In the first year of experiment birds exposed to light at night grew their testes almost a month earlier, and also showed earlier increase in testosterone, than birds exposed to dark nights. At the end of the reproductive cycle birds exposed to light at night started to moult earlier. However, moult lasted longer in the light at night group, among which some individuals did not even finish to moult. In the second year, birds exposed to light at night did not grow the reproductive system at all and moult sequence was highly irregular, possibly because birds were stuck in a photorefractory state. Conversely, birds exposed to dark nights showed normal cycles of testicular development, testosterone and moult. The results of this experiment suggest that short-term exposure to light at night can significantly advanced important annual cycles such as reproduction and moult, but that long-term effects can dramatically impair the maintenance of seasonal functions. Although the

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chronic, constant exposure to light at night is unlikely in nature, my results call for an urgent understanding of the fitness consequences of light pollution.

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Zusammenfassung

In heutiger Zeit wachsen Städte schneller als alle anderen Landschaftstypen. Eine direkte Folge dieser globalen Verstädterung ist die sogenannte Lichtverschutzung, welche seit längerem schon als bedeutendes Thema des öffentlichen Gesundheitswesen von uns Menschen erkannt wird. Welchen ökologischen Einfluss die Lichtverschmutzung auf andere Lebenwesen hat, erfährt seit kurzem zunehmendes Interesse in der Wissenschaft.

Aufgrund der Tatsache, dass Licht und seine tages- und jahreszeitlichen Veränderungen eines der wichtigsten Faktoren ist, welche Tages- und Jahreszyklen von fast allen Organismen reguliert, nahm ich an, dass Veränderungen durch nächtlichem Kunstlicht biologisch wichtige Zyklen von Wildtieren beeinflussen könnte. In meiner Doktorarbeit zeige ich in einer kombinierten Feld/Laborstudie wie nächtliches Kunstlicht tages- und jahreszeitliche Organisation von in Städten lebenden Amseln (Turdus merula) verändert und beschreibe welche physiologischen Mechanismen hierfür verantwortlich sein könnten.

Ich verwendete eine Kombination aus Radiotelemetrie- und Lichtlogger-Technik, um zu allererst die Lichtintensität zu messen, die freilebende Stadt- und Waldamseln während der Nacht ausgesetzt sind. Diese Lichtintensitäten korrelierte ich hierauf mit den Aktivitätsmustern (Tagesbeginn und –ende) der gleichen Individuen. Stadtamseln waren deutlich höheren Lichtintensitäten während der Nacht ausgesetzt als Waldamseln. Die

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am Tag aktiv und begannen ihre Nachtruhe später am Tag. Hierzu kam aber eine beträchtliche intra-individuelle Variation. Temperatur, Bewölkung und Niederschlagsmenge konnten als potentiell erklärende Faktoren ausgeschlossen werden, wohingegen andere Umweltparameter wie Lärm, Futterverfügbarkeit udn soziale Stimuli mit verantwortlich für die vorhandene Variation sein könnten. I testete den relativen Beitrag von Stadtlärm und Nachtlicht durch ein natürliches Experiment. Während Lärm während der Nacht und am Tag zwischen den Wochentagen und dem Wochenende beträchtlich variierten, gab es keine Unterschiede im Nachtlicht und in den Aktivitätsmustern. Dieser Vergleich unterstreicht zusätzlich, dass Nachtlicht einer der bedeutenden Faktoren ist, der die tageszeitliche Organisation von Vögeln in der Stadt verändert.

Die Variation der Morgenaktivität zwischen Stadt- und Waldamseln spiegelte sich in bestimmen Eigenschaften der endogene circadianen Rhythmen wider. Stadtamseln zeigten einen schnelleren und schwächeren circadianen Rhythmus als Waldamseln, wenn die Tiere unter konstanten Laborbedingungen gehalten wurden. Die beobachteten circadianen Merkmale unter Laborbedingungen korrelierten auch mit den im Freiland gemessenen Aktivitätsmustern. Dieses Ergebnis lässt vermuten, dass die Verstädterung sowohl die circadiane Uhr als auch die Aktivitätsmuster der Amsel verändert. Ob Mikro- Evolution, Entwicklungsprozesse (z.B. materale Effekte) oder allgemein die phänotypische Plastizität die Ursache für die Veränderungen in der Rhythmik und Verhaltensmuster sind, ist bis jetzt unklar. Ein plausible Erklärung könnte sein, dass in Städten früh-aktive Vögeln bevorzugt werden, und das nächtliche Kunstlicht könnte der Faktor sein, der solche mikroevolutionären Prozesse auslöst.

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In weiteren Laborexperimenten testete ich spezifische Hypothesen über die Auswirkungen von nächtlichem Stadtlicht auf die tages- und jahreszeitliche Organisation von Amseln. Hierfür wurden gefangene Stadt- und Waldamseln über zwei Jahre entweder dunklen Nächten oder Nächten mit niedrigen Lichtintensitäten von 0.3 Lux ausgesetzt.

Diese niedrige Lichtintensität wurde vorher im Freiland an freilebenden Stadtamseln bestimmt.

In dem ersten Experiment testete ich, ob niedrige Lichtintensitäten in der Nacht die Plasma Melatonin Konzentrationen reduzieren könnten. In der Tat, beide Stadt und Waldamseln, die niedrigem Nachtlicht ausgesetzt waren, schütteten am späten Abend und am frühen Morgen sowohl im Sommer wie auch im Winter niedrigere Melatonin Konzentrationen aus als Vögel mit dunklen Nächten. Je niedirger die Melatonin Konzentration am frühen Morgen war, desto höher war die Aktivität der Vögel zu diesem Zeitpunkt. Dieses Ergebnis lässt vermuten, dass nächtliches Licht in der Lage ist die Melatoninausschüttung zu verringern und dies einer der potentiellen physiologischen Mechanismen sein könnte, warum die Aktivitätsmuster von Stadtamseln verändert sind.

In dem gleichen experimentellen Setup bestimmte ich über einen Zeitraum von zwei Jahren die Hodengröße und die Plasma Konzentration vom Testosteron. Im ersten Jahr wuchsen die Hoden der Vögel, die nächtlichem Kunstlicht ausgelöst waren, fast einen Monat früher als die Kontrollvögel. Ebenso zeigten diese Vögel einen früheren Testosteroneanstieg. Gegen Ende des Reproduktionszykluses mauserten die Vögel mit nächtlichem Kunstlich früher und länder, wobei manche der Vögel deren Mauser gar nicht vollendeten. Im zweiten Jahr zeigten die Vögel mit nächtlichem Kunstlicht

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hierfür wäre, dass die Vögel durch das Kunstlicht ständig eine Langtag erlebten und dadurch in der Photorefraktärphase stecken geblieben sind. In Gegensatz dazu zeigten die Kontrollvögel einen normalen Jahreszyklus in der Hodenentwicklung, der Testosteronausschüttung und Mauser. Die Ergebnisse dieser Studie lassen vermuten, dass niedrige Lichtintensitäten während der Nacht wichtige Jahreszyklen wie Reproduktion und Mauser, verändern können. Zudem zeigen diese Ergebnisse, dass langanhaltendes Ausgesetztsein von nächtlichem Kunstlicht saisonale Funktionen dramatisch beeinträchtigen kann. Auch wenn die chronisch konstante Exposition von Kunstlicht unter natürlichen Bedingungen vermutlich sehr unwarhscheinlich ist, zeigen meine Ergebnisse, dass Fitnesskonsequenzen, die mit der Lichtverschmutzung einhergehen, untersucht werden sollten.

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Chapter 1

General introduction

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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

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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.

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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

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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.

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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

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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

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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

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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.

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Chapter 2 Annual rhythms that underlie phenology:

biological time-keeping meets environmental

change

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Helm, B., Ben Shlomo, R., Sheriff, M.J., Hut, R., Foster, R., Barnes, B., Dominoni, D. Annual rhythms that underlie phenology: biological time-keeping meets environmental change. Proc. Roy. Soc. London B, in press

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ABSTRACT

Phenological research addresses changing inter-relationships between seasonality and environment but largely overlooks contributions of internal time-keeping mechanisms to organisms’ responsiveness to environmental conditions. We emphasize the value of chronobiology for understanding phenology by this overview of time-keeping processes and their interaction with environmental input, focussing 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 urgent examples of anthropogenic influences that put biological timing systems under pressure. We propose that consideration of Homo sapiens as principally a

“seasonal animal” can inspire new perspectives for understanding medical and psychological problems.

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MECHANISMS OF ANNUAL TIMING

In a seasonal world, precise timing of annual processes is essential for survival and reproductive success. Accordingly, organisms have adapted to align with the predictable, periodic changes that are caused by geophysical cycles (Bradshaw & Holzapfel 2007;

Foster & Kreitzmann 2009). Phenology, the seasonal timing of recurring biological processes, is the result of these complex, and species-specific, timing processes (Visser et al. 2010). The importance of understanding phenology is particularly evident in the context of global warming. Organisms show wide-ranging variation in the mechanisms that underlie nature’s calendar, but generally combine internal time-keeping with information from external cues to prepare for predictable, annual change in their environment. Then annual cycles are fine-tuned in response to current, local conditions (Dawson 2008; Wingfield 2012). Some species use cues directly to time annual cycles, while in other species internal time-keeping plays a major role, from short-term interval timers to sustained rhythms that continue even under constant experimental conditions. In some long-lived animal and plant species, internal time-keeping regulates annual cycles to such extent that they recur with periodicities that are close to, but not identical to one year (“circannual” rhythms) (Gwinner 1986; Andersen & Keafer 1987). Under natural conditions, environmental cues provide temporal information and synchronize circannual rhythms. The most reliable cue (Zeitgeber) is the annual change in daylength or

“photoperiod” (Bradshaw & Holzapfel 2007; Foster & Kreitzmann 2009). Other fluctuations also provide information for the timing of annual processes, for example ambient temperature, rain, or food availability, but the relative importance of these differs

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environments with high environmental unpredictability, temperature and rainfall cues may increase in importance (Hau 2001), while in the Arctic the timing of snowmelt initiates the growing season and can influence timing of animal reproduction (Sheriff et al. 2011).

Species vary in their reliance on external cues versus internal time-keeping. Those living in environments where daylength information is limited seasonally (eg, at the equator, during Polar solstices or in deep ocean) or have lifestyles that make daylength unreliable or temporarily inaccessible (e.g., during migration and hibernation) typically rely greatly on internal time-keeping (Gwinner 1986; Anderson & Keafer 1987). Species at mid- latitude locations use photoperiod as the dominant source of temporal information. These examples were thought to fundamentally differ, but now are increasingly seen as based on common mechanisms that are modified in species-specific ways (Bradshaw &

Holzapfel 2007; Paul, Zucker, & Schwartz 2008; Hazlerigg & Lincoln 2011). Here we present an overview of the mechanisms by which animals keep track of time to create annual phenologies, with an emphasis on birds and mammals and a focus on the still largely enigmatic circannual clocks.

Circannual rhythms – Circannual cycles persist in absence of any external time cues across a wide range of taxa (Gwinner 1986). For example, when kept under constant daylength and temperature conditions, pupation of larvae of carpet beetles Anthrenus verbasci and germination in the marine dinoflagellate Gonyaulax tamarensis recur approximately once per year (Anderson & Keafer 1987). Most endogenous circannual cycles measured so far have periods shorter than 365 days (Gwinner 1986), but some are

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longer (Piersma et al. 2008). Thus, under experimental conditions phases of circannual cycles drift progressively towards either earlier or later dates.

Circannual studies have focused on birds and mammals, whose annual cycle comprises several phases, including reproduction, moult, migration or hibernation (Gwinner 1986;

Lincoln et al. 2006) These phases involve substantial modifications of morphology, physiology and behaviour that must be precisely orchestrated and occur at the correct time of year. Hibernating mammals maintain robust circannual cycles of seasonal weight gain, due to increases in food intake, fattening and anabolism, and profound thermoregulatory changes. Subsequently species may hibernate for 5-8 months, during which core body temperature can fall to as low as -3°C. Hibernation is followed by an active season characterized by a brief spring breeding period of 2-3 weeks followed by a weight gain of 2-3 times their emergence weight. While under constant experimental conditions circannual rhythms of hibernators drift, in the wild they are synchronized with the external year. Thus, although hibernators remain sequestered within a hibernaculum for much of their life, an environmental Zeitgeber sets their clock.

Circannual rhythms are also particularly evident in long-distance migratory birds, whose amazing mobility implies a need to keep track of time of year (Gwinner 1986; Piersma et al. 2008). Because the photoperiodic conditions that the birds experience depend on the latitude where they are flying, daylength provides only ambiguous calendar information.

For example, trans-equatorial migrants experience long days during both summer and winter (Gwinner 1986), and local cues like temperature and rain are usually unrelated to conditions in far-away target areas. Migrants that winter in tropical regions nonetheless

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first to demonstrate that some species, like the willow warbler (Phylloscopus trochilus), show persistent, circannual rhythms of migratory restlessness (a captivity proxy for migration) and other annual processes for several years when kept under constant environmental conditions (Gwinner 1967). In various migrants, cycles of fattening, moult and reproductive competence also persist under circannual conditions (Gwinner 1986).

A third group of animals with well-described circannual rhythms are species living near the equator where the photoperiod is almost constant and annual Zeitgeber information has low amplitude. A well-documented example is that of African stonechats (Saxicola torquata axillaris), that under constant conditions express circannual rhythms of reproductive capacity and moult for up to 10 years. These cycles persisted even in hand- raised birds that never experienced photoperiodic change (Gwinner 1996). Although the cues that entrain circannual rhythms in tropical animals are still elusive, subtle changes in photic conditions may be useful. For example, Hau et al. (Hau, Wikelski, & Wingfield 2009) have shown that spotted antbirds (Hylophylax naevioides) respond to changes in photoperiod of as little as 17 minutes. Goymann et al. (Goymann et al. 2012) recently suggested that stonechats might use the equatorial drift in sunrise and sunset time (“equation of time”) to synchronize the circannual rhythm of moult. However, tropical species may also respond directly to favourable environmental conditions, especially in regions where seasonality has poor predictability. For example, rainfall is considered to be a strong predictor of food abundance in some arid regions. In Galapagos finches the reproductive system remains quiescent for most of the year without being fully regressed and can develop rapidly once favourable conditions arise (Hau et al. 2004).

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Photoperiodism – Photoperiodism, “the ability of organisms to assess and use the daylength as an anticipatory cue to time seasonal events” (Bradshaw & Holzapfel 2007), is pervasive among plants and animals. While daylength provides timing information around the year, its effects on annual cycles are particularly well-studied for reproduction. The daylengths that activate reproduction differ between species and reflect the times of year when crucial preparations occur. In resident birds at mid-latitudes, the vernal increase in daylength times a cascade of physiological events along the hypothalamus-pituitary-gonads axis (Dawson et al. 2001). In birds and similarly in mammals, these involve thyroid hormone metabolism in the Pars tuberalis (PT) and stimulation of GnRH neurons to release gonadotropins (Hut 2011). Gonadotropins promote the development of the reproductive organs, whose recrudescence increases release of steroid hormones. These stimulate brain receptors promoting reproductive behaviours like song, territorial aggression and courtship displays (Sharp 2005; Cassone et al. 2009).

Photoperiodism differs between birds and mammals in the input pathways to the hypothalamus. Mammals have a single pathway to the PT, in which plasma melatonin plays an essential signalling role (Lincoln et al. 2006). The PT is rich with melatonin receptors (Hut 2011). Melatonin codes for daylength because it is excreted at night by the pineal gland, which in mammals seems to be solely driven by the circadian pacemaker in the hypothalamic suprachiasmatic nucleus (SCN). In birds, the PT also expresses a melatonin receptor, but melatonin is not critical for the response although it may modify it (Greives et al. 2012). Pinealectomized birds still show a photoperiodic response, which

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contrast to mammals, the avian pineal is itself a self-sustained circadian oscillator that entrains to light (Cassone 2009). The hypothalamic photoperiodic response of birds and mammals converges in the involvement of local thyroid hormone metabolism, triggered by thyroid stimulating hormone (thyrotrophinsubunit β; Tsh β) (Dardente et al. 2010).

Along these pathways, photoperiodism activates reproductive function either directly or by synchronization of an underlying circannual rhythm.

Photoperiodic response mechanisms of circannual clocks – Circannual clocks need to be synchronized by an environmental Zeitgeber, which usually is photoperiod. Circannual rhythms of some birds and mammals respond so strongly to photoperiod that by accelerated change of daylength, several annual cycles can be forced to occur within one year (Gwinner 1986). However, effects of photoperiod on circannual rhythms depend on Zeitgeber strength and on species. In sheep, a strong photoperiodic stimulus (8 weeks of short photoperiod) resets the internal circannual clock to a spring state irrespective of the timing of its application (Lincoln et al. 2006). In contrast, in other species the response to calendar information depends on the phase of the underlying circannual rhythm (Helm, Schwabl, & Gwinner 2009). In birds, reproductive activation is usually stimulated by increasing daylength, but most species do not retain breeding condition indefinitely under long daylength (Helm et al. 2009). The phenomenon, whereby reproductive condition is terminated on long photoperiods and often initially not even re-stimulated by constant light (MacDougall-Shackleton & Hahn 2007), has been termed "photo-refractoriness", although birds certainly remain responsive to photoperiod and shortening days accelerate post-breeding processes like moult. As indicated by their sustained circannual rhythms,

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some species regain reproductive competence spontaneously, while others restore a subsequent responsiveness to long photoperiods only after exposure to short days. This requirement for short days has been termed the breaking of refractoriness, but could also be seen as an advance of the underlying circannual system which in some species is obligatory (Gwinner 1986; Sharp 2005). Hence, it is not excluded that photorefractoriness, in birds and in mammals, could depend on a similar circannual timing mechanism (Paul et al. 2008; Bradshaw & Holzapfel 2007).

In some mammals circannual rhythms are so robust that resynchronization after photoperiodic shifts may take several years (Concannon et al. 1997). Most hibernators overwinter in closed or snow-covered underground burrows where daylight does not penetrate. Thus, timing of when to end hibernation and begin reproduction relies on signals from the circannual clock with no acute influence of photoperiod in spring. Lee and Zucker (Lee & Zucker 1991) demonstrated a role of daylength changes experienced by animals during summer in the annual entrainment of circannual rhythms of golden- mantled ground squirrels (Citellus lateralis). Ground squirrels that were held on naturally changing photoperiods were more synchronized within groups and had longer cycle lengths between body weight peaks and estrus (closer to 365 days) than conspecifics kept under constant conditions. This effect was lessened when circadian systems were impaired by SCN-lesions. Sensitivity to changing daylength must be acute for photoperiod to entrain circannual rhythms of some hibernators, such as arctic ground squirrels, Urocitellus parryii, which are active above ground from only early May to late July, but are nonetheless entrained by the Zeitgeber (Sheriff et al. 2011).

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Temperature and other factors - Other environmental factors can either modulate the interpretation of photoperiod or directly affect seasonal transitions (Visser et al. 2010).

These include food (Schoech et al. 2004), weather conditions (Dawson 2008) and especially ambient temperature (Schaper et al. 2012). In hibernating mammals, changes in temperature can advance phases within circannual rhythms. For example, transferring hibernating male golden-mantled ground squirrels from 4 to 30°C in mid-winter terminated torpor and advanced reproductive maturation. However, in the subsequent year timing was not advanced in warmed compared to control animals, suggesting that the underlying circannual pacemaker was not affected (Barnes & York 1990). Field and captive studies that compared timing between locations and years showed that high spring temperatures advanced the end of hibernation and the onset of reproduction in ground squirrels. Because prolonged cold temperatures in spring delayed the autumn body mass peak, the circannual rhythm appeared to be phase-delayed by cold temperature (Joy & Mrosovsky 1985). Therefore, high spring temperatures probably have direct causal effects on the phenology of hibernating mammals, while involvement of the underlying circannual rhythm remains unclear.

Several studies of birds (Schaper et al. 2012) and mammals suggest that environmental temperature can affect photoperiodic synchronization of annual rhythms. For example, cold exposure at short photoperiods facilitates testicular regression in hamsters (Larkin et al. 2002) and prairie voles (Microtus ochrogaster; (Kriegsfeld et al. 2000)), and winter pelage change in Djungarian hamsters (Phodopus sungorus) (Ruf et al. 1993). Critical photoperiod for the autumn regression of testes size in Djungarian hamsters was reduced by about 7 min per degree of increased ambient temperature (Steinlechner, Heldmaier, &

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Becker 1983). Under natural photoperiod this may translate to a one-week delay of testicular regression when temperature is 4 degrees higher. Temperature effects in small mammals are thought to be mediated through melatonin (Stieglitz et al. 1991; Ruf et al.

1993; Larkin, Jones, & Zucker 2002), and would thereby take place through modulation of the essential input signal to the annual hypothalamic timing mechanism. Based on neuro-anatomical evidence in the prairie vole, Kriegsfeld (Kriegsfeld et al. 2000) suggested that lower temperatures may inhibit the release of GnRH by neurons located in a brain area that also contains temperature sensitive neurons. Together, these results suggest that environmental temperature may act on both the input signal and the target neurons of the photoperiodic timing mechanism.

Molecular mechanisms - The molecular mechanisms underlying variation in animal phenology are still unknown. Because photoperiodism involves the measuring of daylength, the circadian system is likely to be implicated. The molecular mechanism underlying the circadian clock in eukaryotes involves periodic gene expression, with RNA and protein products from these ‘cycling’ genes defining the clock by operating within molecular feedback loops to generate their own rhythms. An appealing candidate for phenological variation is the circadian gene clock. Recently, Liedvogel et al.

(Liedvogel et al. 2009) and Caprioli et al. (Caprioli et al. 2012) reported an association between polymorphism between clock and breeding phenology in birds.

Clock and other circadian genes could function through interaction with melatonin.

Melatonin affects the expression of circadian genes, at least in mammalian peripheral

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responsive to the circadian transcription factors CLOCK and BMAL1. Melatonin was found to affect the expression of several E-box controlled genes. Two additional transcription factors: eyes absent 3 (eya3) and six homeobox (six) participate in mammalian responses to daylength by forming a transcriptional co-activator complex that may contribute to inducing TSHβ. Eya3 promoter presents three E-box elements, and its expression is directly controlled by melatonin (Dardente et al. 2010). However, a general relationship between photoperiodic timers and the circadian pacemaker is still controversial.

The processes of modulating reproductive transitions probably involve epigenetic molecular regulation that alters temporal and spatial patterns of gene expression.

Epigenetic imprinting, resulted from genome - environment interactions, also can affect the following generations. Although direct effects of epigenetic modulation on phenology are unknown, prenatal exposure to various photoperiods or temperatures influenced circadian or thermoregulatory adaptations, for example by persistent changes in individual SCN neurons of mice (Ciarleglio et al. 2011). This suggests urgent need for further study.

ANNUAL TIMING IN A CHANGING WORLD

The current, rapid global changes in climate and land-use are likely to impair the functionality of time-keeping that had been fine-tuned over evolutionary history. Changes in phenology have been among the earliest observed “footprints” of global change (Visser et al. 1998; Peñuelas & Filella 2001), and are particularly evident in association with climate change and urbanization.

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Climate change - Clear shifts in phenology have been related to warming (Peñuelas &

Filella 2001; Fitter & Fitter 2002; Cotton 2003), but also to other changes in climate, for example, to changes in snow-cover (Høye et al. 2007), or, in tropical and arid habitats, to patterns of rainfall (Hulme, Doherty, & Ngara 2001). However, species differ in the rate at which they adjust their timing to altered conditions (Sherry et al. 2007; Visser et al.

2010). In particular, organisms at different trophic levels are modifying their seasonal processes at different rates, which can lead to progressively mismatched seasonal timing between interacting species.

A classic example is mistimed reproduction of great tits (Parus major) in The Netherlands. Peak availability of caterpillars, the main food for great tit nestlings, is advancing rapidly in response to increasing spring temperature and earlier oak bud burst (Visser & Holleman 2001). Great tits show phenotypic plasticity in the timing of egg- laying, which allows them to adjust to warmer springs. However, this plasticity is limited by the complex mechanisms of avian reproduction, so that their breeding season is progressively delayed with respect to the food peak (Visser et al. 1998). Although evidence for large effects on recruitment rates and population density is still scarce, mismatched timing of reproduction has imposed energetic and fitness consequences, including reduced fledging rate, fledging mass and adult survival (Thomas et al. 2001;

Lof et al. 2012) Compared to sedentary species like great tits, long-distant migratory birds might be additionally constrained in their response to changing phenology (Both et al. 2010). Pied flycatchers (Ficedula hypoleuca) in a Dutch oak tree forest laid their eggs earlier in response to warming spring temperatures, but did not advance reproduction

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Such inadequate responses to changing weather patterns were associated with local population declines of European flycatcher populations (Both et al. 2006). For these migrants, annual migration appeared to have slowed the advance of breeding phenology.

Pied flycatchers winter in West Africa, where they cannot access information about phenology on the breeding grounds and rely on circannual rhythms and daylength to initiate spring migration. Their endogenous timing program appears to prevent birds from returning in time to advance breeding in a warming climate and from taking advantage of extended breeding seasons (Both & Visser 2001). New techniques for tracking migrants support this proposition by revealing remarkable constancy of individual timing (Altshuler, Cockle, & Boyle 2013).

In the Arctic, hibernating mammals may incur particular difficulties because the timing of spring events is largely set through circannual mechanisms in the previous summer or autumn. Nonetheless, in some hibernators the timing of annual events responded to climate differences due to altitude (Bronson 1979), latitude (Barnes 1996), and local differences in seasonality. Sheriff et al. (Sheriff et al. 2011) report on a 6-year study of two populations (Atigun and Toolik) of free-living arctic ground squirrels that live only 20km apart. However, due to differences in winter precipitation and wind, Atigun becomes snow free approximately 26 days earlier than Toolik. Ground squirrels differed consistently in the timing of spring emergence, parturition and re-entry into hibernation between the two sites. These differences were not correlated with differences in soil temperatures, but instead, were presumably related to snow-cover (Sheriff et al. 2011;

Williams et al. 2012).

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In addition to mismatches between interacting species, climate change may also disrupt the interactions of individuals within a species. In the ground squirrel example above, recent evidence suggests that the response of males and females to earlier snowmelt differs (MJ Sheriff, pers. comm). Similarly, males of many migratory bird species have advanced spring arrival more substantially than females (Spottiswoode, Tøttrup, &

Coppack 2006), and in geese, adults may moult at progressively different times than their young (Van Der Jeugd et al. 2009). Clearly, we need to understand mismatches on the level of individuals and populations to fully appreciate effects of global warming and climate-induced disruptions between interacting trophic levels.

Urbanization - Another important anthropogenic process that promotes phenological change is the rapid increase of urban sprawl. Urbanization entails the commonly reported effect of “urban heat island” (Arnfield 2003), i.e., an air temperature excess over that of surrounding rural areas. A well-studied feature is the buffering of cold winters and reduction of temperature variation between seasons (Santamouris 2001). Although its consequences are still poorly understood, it might be the major cause for the generally advanced plant phenology in cities, at least at temperate latitudes (Neil & Wu 2006).

However, changes in plant phenology depend on functional type: early spring bloomers and insect-pollinated plants seem to advance their phenology more in response to warmer springs than late spring bloomers or wind-dispersed species do (Fitter & Fitter 2002).

In animals, evidence that urbanization can alter seasonal timing is mostly based on bird studies. Avian city-dwellers in temperate areas show earlier development of the

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breeding season (Chamberlain 2009). It is possible that these changes are due to the warmer micro-climate in urban areas since temperature can directly affect the time of egg-laying (Yom-Tov & Wright 1993; Schaper et al. 2012). However, urbanization could also alter phenology by changed photic conditions due to artificial lights at night. Light pollution could modify perceived daylength through increased ambient illumination and/or shifts in spectral properties of light (Rich & Longcore 2006). Recent experimental work demonstrated that light at night can speed up the reproductive physiology of European blackbirds (Turdus merula) (Dominoni, Quetting, & Partecke 2013). However, the possible fitness consequences of phenological change in cities are still poorly understood.

Urbanization should be a rewarding model system for understanding phenological change. Two research directions could exploit the potential of an integration of urban ecology and chronobiology. The first is possible differences in cue sensitivity between urban and rural species, and in the response of internal systems of the circadian and circannual clock to urbanization pressure. The second direction is elucidation of the fitness consequences of modified phenology. For example, do birds and insects modify their phenology in cities at similar rates? And what are the consequences of potential mistiming on urban ecosystem function? Modification of seasonal rhythms might allow wild organisms to succeed in human cities, but for some species, it might equally be a lost race around the annual clock.

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ANNUAL CYCLES IN A CHANGING WORLD – OF HUMAN CONCERN?

Two key processes of global change, climate change and urbanization, rapidly modify phenology and may impose substantial challenges on wild organisms. However, because the observed patterns differ so widely across organisms, it is difficult to interpret and predict their responses. In this review we have summarized the diversity and complexity of the mechanisms that underlie phenology. The control and expression of annual cycles vary in the degree of flexibility depending on the species, on the environment where they live, and on the temporal cues that affect their physiological systems (Forrest & Miller- Rushing 2010; Visser et al. 2010). The difficulties in explaining organismal responses may be largely due to our limited understanding of the diverse mechanisms of nature’s calendar, and specifically to a neglect of contributions by biological clocks. These difficulties can be jointly addressed by ecologists and chronobiologists (Foster &

Kreitzmann 2009; Bradshaw & Holzapfel 2010; Visser et al. 2010).

In addition, seasonality and the changes it currently undergoes may also affect humans in ways that are still more direct. We have a very limited understanding of the extent to which our own species is affected by and responds to seasonality (Foster & Roenneberg 2008; Foster & Kreitzmann 2009). Until the recent past the changing seasons had markedly influenced human biology, with indication of annual cycles of reproduction, immune function, disease and death. Since then, humans have become progressively isolated from seasonal changes in temperature, food and photoperiod in the industrialised nations. Nevertheless, the seasons continue to have effects on our lives. An individual’s birth, susceptibility to disease, and death are not randomly distributed across the year in

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Kreitzmann 2009; Disanto et al. 2011) is difficult to explain why this seasonality still exists, in particular as food availability is largely constant and seasonal changes in temperature are masked by central heating and air-conditioning (Foster & Roenneberg 2008). A possible explanation is that these cycles are residuals of responses that had evolved originally in our ancestors, who - like other tropical species - may have timed physiological processes by circannual clocks and environmental cues. Perhaps we have retained a circannual timer that can be synchronised by photoperiod or metabolic status (Wehr 2001; Wikelski et al. 2008). Alternatively, as our ancestors moved from Africa to the higher latitudes and encountered progressively greater variation in food availability, they could have evolved a strongly photoperiodic response, for example based upon a daylength-dependent melatonin signal (Paul et al. 2008).

Recent studies provide increasing support for the idea of humans as a “seasonal species”

that responds to photoperiod. Human daily activity patterns are influenced by the solar day (Roenneberg, Kumar, & Merrow 2007), and the specific timing of activity (“chronotype”) differs between populations along latitudinal gradients (Roenneberg &

Allebrandt 2013). Humans, along with other primates, have the basic biological machinery that would drive a response to seasonally changing light exposure (Wehr 2001). Hence, some aspects of human seasonality may be explained by its effects, either directly or via effects of maternal light exposure on offspring health. A recent meta- analysis looked at the occurrence of anorexia nervosa in British cohort studies (Disanto et al. 2011). Patients who suffered of anorexia were much more likely to have been born in spring and much less likely to have been born in autumn than the general population.

Such patterns, and increasingly more examples of seasonality in epidemiology, are still

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poorly understood. Possible contributions of circannual rhythms also cannot be excluded.

These are difficult to test in humans but have been documented in other primates (Wehr 2001). A case study of seasonal affective disorder reports suggestive data of a possible circannual rhythm from a single patient (Wirz-Justice, Kräuchi, & Graw 2001), which, if confirmed, could open new prospects for treatment. Regardless of the specific, underlying timing mechanism, an increasing number of studies indicates that a closer look at seasonal patterns in our own species could contribute to health and well-being.

OUTLOOK

Seasonal variation shapes the life-cycles of animals and plants, and their adaptations to such change play a large part in determining their survival and reproductive success. The same is true for humans. The difference is that we have developed and adapted in such a way that we survive environmental change by modifying the environment. But in modifying the world we have lost contact with nature and its timing, and feel ourselves immune from such changes. An understanding of phenology and the internal timing mechanisms in which we and other organisms have adapted to environmental change will help us both mitigate and manage some of the broad effects of seasonal change, including the impact of global climate change. It will provide evidence-based approaches for the development of new therapeutic, agricultural and horticultural practices, the means to protect human health from attacks by both old and resurgent pathogens, and strategies for the conservation of other species (Foster & Kreitzmann 2009).

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Chapter 3 The nightlife of city birds: artificial light at night affects daily activity patterns of European

blackbirds (Turdus merula)

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In review as:

Dominoni, D. Carmona-Wagner, E., Hofmann, M., Kranstauber, B., Partecke, J. The nightlife of city birds: artificial light at night affects daily activity patterns of European blackbirds (Turdus merula). J.

Anim. Ecol.

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ABSTRACT

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. 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. 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 daily activity patterns through an automated telemetry system.

We first analyzed the relationship between light at night, weather conditions and date with daily activity onset, end, and duration of inactivity at night. We then compared activity, light at night exposure and noise levels between weekdays and weekends. We found that birds exposed to higher amounts of light at night showed earlier onset of activity in the morning and ceased activity later in the evening, and thus were inactive for a shorter period at night. Light exposure at night and activity patterns did not vary between weekdays and weekends, but noise did. In addition, a strong seasonal effect was detected in both populations, such as birds tended to be active earlier in the morning and later in 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 temporal niche shifting.

Future research should focus on the costs and benefits of altered daily rhythmicity in

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INTRODUCTION

Urbanization is one of the most extreme man-made habitat changes. In the last two centuries urban sprawl has proceeded at an unprecedented rate, and the proportion of human population living in urban agglomerates recently exceeded that living in rural areas (IUCN 2012). The most conspicuous effect of urbanization is the spatial modification of habitats which can dramatically alter species distribution and abundance and ultimately ecosystem functions and services (Grimm et al. 2008; Shochat et al. 2010;

Eigenbrod et al. 2011). In addition, it is known that animal species thriving in urban habitats show differences in morphology, physiology and behaviour (Riley et al. 2003;

Chace & Walsh 2006; Ibáñez-álamo & Soler 2010; Dominoni et al. 2013). In particular, species in urban areas exhibit altered daily activity patterns (Chace et al. 2003; Riley et al. 2003; Longcore & Rich 2004). These data suggest that urbanization has the potential to alter not only spatial aspects of habitat use, but also temporal niches. Since an accurate timing of daily activities is crucial for fitness (Foster & Kreitzmann 2004; Lyon, Chaine,

& Winkler 2008), it is relevant to understand the causes and consequences of altered biological cycles in species living in a rapidly urbanizing world.

In birds the most reported shift in daily timing in urban species is the advanced onset of dawn activity (Miller 2006; Nemeth & Brumm 2009; Kempenaers et al. 2010). Previous studies have highlighted that birds that are active earlier during the day are preferred by females: These birds have higher rates of extra-pair paternity (Poesel et al. 2006;

Kempenaers et al. 2010) and are in better body condition (Murphy et al. 2008) than birds displaying later in the morning. Several environmental factors are known to affect daily

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Grava, & Otter 2009; Saggese et al. 2011) and weather conditions (Dunnett & Hinde 1953; Slagsvold 1977). In recent years two alternative (but not mutually exclusive) hypotheses have received attention. Fuller et al. (Fuller et al. 2007) showed that European robins (Erithacus rubecola) which occupied territories with high levels of noise during the day tended to sing more during the night than birds in quieter areas. The authors interpreted this result as a mechanism to avoid masking of vocal communication by daytime noise. Another hypothesis involves artificial light at night. The potential effect of light pollution in inducing nocturnal behaviour of songbirds was first suggested from observations of London starlings in 1937 (Rowan 1938). In recent years, new interest has grown around this topic. Correlational results from field studies hint at an effect of light at night on dawn song (Miller 2006; Kempenaers et al. 2010). A more recent study found no effect of small lights placed outside nest boxes on start, end or duration of daily activity in great tits Parus major (Titulaer et al. 2012), although the light intensity provided was perhaps not sufficient to illuminate the forest around the nest box. A potential drawback of these studies is that light exposure was never directly measured on birds, therefore information about what light intensities the animals can really perceive at night is still lacking.

The goal of this study was to elucidate the relationship between light exposure at night and activity patterns in songbirds by measuring light intensity on individual animals. For this purpose we conducted a field study in and around the city of Munich, Germany, attempting at sampling different areas within the city to include a range of sites with different intensities of artificial lights. We recorded daily activity patterns of adult male European blackbirds (Turdus merula) through an automated telemetry system, and

Effects of artificial light at night on daily and seasonal organization of European blackbirds (Turdus merula)

Effects of artificial light at night on daily and seasonal organization of European blackbirds (Turdus merula)

Effects of artificial light at night on daily and seasonal organization of European blackbirds (Turdus merula)

Table of contents

Summary

Zusammenfassung

Chapter 1

General introduction

Chapter 2

Annual rhythms that underlie phenology:

biological time-keeping meets environmental

change

Chapter 3

The nightlife of city birds: artificial light at night affects daily activity patterns of European

blackbirds (Turdus merula)