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 12L:12D (period length: 24h), 13.5L:13.5D (27 h), 10.5L:10.5D (23 h) or 12D:8L:3D:1L (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.

Figure 1

Schematic of the four photoperiod schedules birds were exposed to during the experiment. (a–d) The 24-h skeleton photoperiod, the control 24-h day, the 27- and the 21-h day. The descriptions on the right-hand side indicate the number of subjective days per calendar year, as well as the number of light hours. Note that double plots over 48 h are shown.

Figure 2

Temporal (approx. bimonthly) changes in gonad (circle) and follicle (square) sizes of house sparrows exposed to the photoperiods as indicated (see explanation in figure 1). Data are means±1s.e. Sample sizes for each group are indicated in (a–d). Data for females in the 21-h day group are missing after November 2000 due to equipment failure.

Figure 3

Circannual periodicities of gonad (a) and follicle (b) sizes of house sparrows exposed to various photoperiods (explained in figure 1). Data show mean±1s.e., sample sizes are indicated in the columns. Stars denote significant differences as determined by Scheffe post hoc tests.

Figure 4

Temporal (within 24 h) changes in energy expenditure of house sparrows exposed to the photoperiods as indicated (see explanation in figure 1). Data are means±1s.e. (N=7), black bars indicate dark periods, light bars indicate light periods.

Figure 5

Summary data on energy expenditure of house sparrows exposed to various photoperiods (explained in figure 1). Data are normalized to 21-, 24- and 27-h days and show mean±s.e., sample sizes are indicated in the columns. Stars denote significant differences as determined by Scheffe post hoc tests. Note that the y-axis does not start from zero.

Figure 6

Graphs showing temporal (within 24 h) changes in plasma concentrations of the hormone melatonin, for house sparrows exposed to the photoperiods as indicated (see explanation in figure 1). Data show means±1s.e., sample sizes are N=6 except when indicated, black bars indicate dark periods, light bars indicate light periods.

Figure 7

Summary data on average melatonin concentrations of house sparrows exposed to various photoperiods (explained in figure 1). Averages are roughly approximated from data shown in figure 6 and calculated per day. Data indicate summed means±s.e., sample sizes are indicated in the columns (missing data were replaced by the population averages). We found no significant differences between the groups.