Because astronomically based environmental rhythms are so predictable (Fig. 6.1), organisms have evolved a range of preparatory strategies for coping with them. A big step early in the evolution of life (Hut and Beersma 2011) was anticipation of environmental changes, when cyanobacteria progressed from simply reacting to periodical changes to predicting them in advance. Since then, organisms have evolved sophisticated behaviors that rely on precise prediction of the periodic changes in the environment. For example, many migratory bird species leave their breeding grounds before they become inhospitable, and initiate their return movements in anticipation of the upcoming spring (Numata and Helm 2014). Likewise, birds are usually not simply woken by morning twilight but will have anticipated the upcoming day well in advance (Foster and Kreitzman 2005).
The remarkable achievement of anticipation is possible, because birds, like other organisms, have internalized timekeeping. They have evolved body clocks (referred to as biological rhythms) that are innate and thereby part of their inheritance from generation to generation. These clocks tick on even if the birds are sheltered from environmental changes, for example in a continuously lit room or under the continuous light of polar summer days (Foster and Kreitzman 2005; Ashley et al. 2014; Helm and Lincoln 2017). Birds will alternate each day between activity and rest, their body temperature will rise and fall, and they may rhythmically show behaviors, for example crowing, even under constant conditions (Shimmura and Yoshimura 2013; Shimmura et al. 2015). However, these biological clocks run at their own, internal speed, which often makes them drift a bit. If a bird cannot experience environmental cycles, its biological rhythm is usually somewhat faster, or slower, than the corresponding environmental cycles (hence, it is called a “circa” rhythm). The best-known biological rhythm is that of the circadian clock which drives timing across the 24-hour day. This can be seen in Fig. 6.2 which shows the time of crowing in a rooster. While the rooster experiences changes between light (indicated by the yellow box) and darkness, it always starts crowing at a similar time of day, somewhat before dawn. But once the light is kept constant, the rooster crows a bit earlier each morning, and its rhythm drifts. This drift can be measured as the “period length” of a rooster, i.e., the time taken from one cycle (start of crowing) to the next. In Fig. 6.2, the rooster’s clock is faster than 24 hours, and hence, it has a shorter period length. In their natural environment, such fast-clocked individuals are usually particularly early risers, whereas slow-clocked individuals tend to be late risers (Dominoni et al. 2013b).
For the circadian clock, the mechanisms that drive this rhythm have been intensively studied, highlighted by the recent award of the 2017 Nobel Prize in Physiology or Medicine. We now know that rhythms are generated within cells by a loop of so-called clock genes, which switch each other on and off to measure out the period of circa 24 hours. Many other genes are involved, for example by linking clocks to metabolism. Then, the millions of cellular clocks in a bird, fly or human need to be coordinated to produce useful body time. This is achieved, for example by nerve-cell coupling in brain centers and by hormones, such as melatonin which peaks at night (Foster and Kreitzman 2005). Through various links and feedback loops, organisms thus achieve coordinated rhythms within their bodies. Because clocks are so important to the life of organisms, they are very sensitive to important cues from the environment, in particular to changes of light and darkness. Birds perceive these changes and adjust (“synchronize”) their biological rhythms so that they match the 24-hour daily cycle of the environment (Fig. 6.2).
Although only circadian rhythms are understood in detail, the same principles hold for cycles on other time scales (Numata and Helm 2014). Recent, exciting breakthroughs have shed light on circatidal clocks, which help coastal organisms anticipate the rising and falling of marine water levels (Zhang et al. 2013; Kaiser et al. 2016), and circalunar clocks, by which organisms anticipate the waxing and waning of the Moon (Zantke et al. 2013). Finally, the rhythms that relate most directly to avian reproduction are circannual rhythms (cycles repeating with a period length of circa one year; Gwinner 1986, 1996; Helm and Lincoln 2017). Circannual rhythms can regulate many processes, including preparations for breeding, molt, and migration. Most avian species breed at least to some extent seasonally (Goymann and Helm 2014). Likewise, birds generally molt at least once per year to replace their feathers, and many species carry out regular migrations which are often precisely timed (Gwinner 1996; Battley 2006; Helm et al. 2006; Newton 2008). Associated with their aerial lifestyle, birds undergo extreme annual changes: for example, they greatly reduce their reproductive organs (testes of males, ovaries and oviducts of females; Williams 2012) outside the breeding seasons. In small songbirds, testes typically grow to diameters of 0.5 cm during breeding but shrink in winter to below 10% of this size and contain no sperm (Helm 2009; Williams 2012). This makes reproduction in birds generally highly seasonal, preventing many species from spontaneously breeding, for example during warm weather in winter or after migrating to tropical areas. An example for innate circannual rhythms in reproductive condition is shown in Fig. 6.3 for Eurasian Blackcaps Sylvia atricapilla.
As described above for circadian rhythms, circannual cycles also typically continue if a bird is prevented from witnessing environmental changes (Gwinner 1996; Goymann and Helm 2014). For example, in stonechats (songbirds within the genus Saxicola), the growth and reduction of reproductive organs is driven by a circannual clock. When pairs were kept in aviaries under constant day length of 12 hours of light alternating with 12 hours of night, males and females reproduced if they came into reproductive condition at similar times (Gwinner 1996; Goymann and Helm 2014). Their sons and daughters never experienced rhythms in their environment, but nonetheless showed annual cycles of breeding condition and molt, driven by their circannual clocks. Under these conditions, breeding condition of the stonechats drifted from the annual cycle of 365 days, much like the crowing behavior of the rooster drifted from the 24-hour cycle shown in Fig. 6.2. Under natural conditions, circannual rhythms like circadian rhythms synchronize to environmental cycles (Gwinner 1986; Helm and Lincoln 2017). The most important synchronizing cue on an annual time scale is photoperiod (day length), although other cues can also play a role (Helm et al. 2006; Goymann and Helm 2014).
The precise timing of behavior and activities of birds under natural conditions is influenced by many additional factors that modify the outcome of biological timekeeping. For example, the time of song and breeding can be influenced by age, experience, dominance, body condition, and various local environmental factors (Poesel et al. 2006; Helm et al. 2006; Shimmura et al. 2015). But importantly for the subject of avian speciation, innate biological rhythms provide a powerful substrate for evolutionary change (Fig. 6.3; Helm and Visser 2010; Taylor and Friesen 2017).