Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control

Abstract

Endogenous circannual clocks are found in many long-lived organisms, but are best studied in mammal and bird species. Circannual clocks are synchronized with the environment by changes in photoperiod, light intensity and possibly temperature and seasonal rainfall patterns. Annual timing mechanisms are presumed to have important ultimate functions in seasonally regulating reproduction, moult, hibernation, migration, body weight and fat deposition/stores. Birds that live in habitats where environmental cues such as photoperiod are poor predictors of seasons (e.g. equatorial residents, migrants to equatorial/tropical latitudes) rely more on their endogenous clocks than birds living in environments that show a tight correlation between photoperiod and seasonal events. Such population-specific/interspecific variation in reliance on endogenous clocks may indicate that annual timing mechanisms are adaptive. However, despite the apparent adaptive importance of circannual clocks, (i) what specific adaptive value they have in the wild and (ii) how they function are still largely untested. Whereas circadian clocks are hypothesized to be generated by molecular feedback loops, it has been suggested that circannual clocks are either based upon (i) a de-multiplication ('counting') of circadian days, (ii) a sequence of interdependent physiological states, or (iii) one or more endogenous oscillators, similar to circadian rhythms. We tested the de-multiplication of days (i) versus endogenous regulation hypotheses (ii) and (iii) in captive male and female house sparrows (Passer domesticus). We assessed the period of reproductive (testicular and follicular) cycles in four groups of birds kept either under photoperiods of LD 12 L : 12 D (period length: 24 h), 13.5 L : 13.5 D (27 h), 10.5 L : 10.5 D (23 h) or 12 D : 8 L : 3 D : 1 L (24-h skeleton photoperiod), respectively, for 15 months. Contrary to predictions from the de-multiplication hypothesis, individuals experiencing 27-h days did not differ (i.e. did not have longer) annual reproductive rhythms than individuals from the 21-or 24-h day groups. However, in line with predictions from endogenous regulation, birds in the skeleton group had significantly longer circannual period lengths than all other groups. Birds exposed to skeleton photoperiods experienced fewer light hours per year than all other groups (3285 versus 4380) and had a lower daily energy expenditure, as tested during one point of the annual cycle using respirometry. Although our results are tantalizing, they are still preliminary as birds were only studied over a period of 15 months. Nevertheless, the present data fail to support a 'counting of circadian days' and instead support hypotheses proposing whole-organism processes as the mechanistic basis for circannual rhythms. We propose a novel energy turnover hypothesis which predicts a dependence of the speed of the circannual clock on the overall energy expenditure of an organism.

Annual rhythms that underlie phenology: biological time-keeping meets environmental change

“…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 synchronized by photoperiod or metabolic status [15,111,112]. Alternatively, as our ancestors moved from Africa to the higher latitudes and encountered progressively greater variation in food availability and temperature, they could have evolved a strong photoperiodic response [7,24].…”

The effects of light pollution on biological rhythms of birds: an integrated, mechanistic perspective

“…Early pioneering studies have demonstrated persisting rhythms of annual events in birds kept under constant light conditions for years (Gwinner 1986 understand very little about the physiological and molecular mechanisms that underlie avian circannual rhythmicity (but see Wikelski et al 2008 ). On top of this uncertainty, the regulation of annual cycles has also been quite a mystery, at least until the end of the last century.…”

Optimal annual routines: behaviour in the context of physiology and ecology

“…There are complex interactions between the reproductive system and the environment that involve state variables other than the state of reproductive system (see Hahn & MacDougall-Shackleton 2008;Paul et al 2008;Wikelski et al 2008). Many studies of behaviour over the annual cycle have shown that cues such as short days trigger a particular phase of the life cycle (e.g.…”