Circadian rhythmicity persists through the Polar night and midnight sun in Svalbard reindeer

Abstract

Studies of locomotor activity in Svalbard reindeer reported the temporary absence of diel rhythms under Arctic photic conditions. However, using Lomb-Scargle periodogram analyses with high statistical power we found diel or circadian rhythmicity throughout the entire year in measures of behaviour, temperature in the rumen and heart rate in free-living Svalbard reindeer. Significant diel rhythmicity was only lacking during some of the 15-day intervals analysed in the less frequently measured heart rate. During Polar Night these rhythms were free-running and attenuated. During continual daylight in summer, rhythms where entrained to 24 hours corresponding with the daily variation in the intensity of solar radiation, but attenuated when continuous daylight coincided with the period of growing forage. Diel rhythmicity was reduced during this short period of peak foraging activity, which coincided with peak heart rate and temperature in the rumen, most likely to facilitate fattening when food is abundant. For the rest of the year, heart rate and temperature showed the most pronounced and long-lasting suppression ever found in ungulates. The profound seasonal changes in foraging, metabolic activity, and power of diel and circadian rhythmicity of Svalbard reindeer can be viewed as adaptations to the extreme living conditions in the High Arctic.

Figure 1

Course of analysed measurements during the study period. Plotted are daily means of telemetrically measured variables of three study individuals represented by differently coloured dots (pregnancy status for each individual in each year is given in Table 1), and 16-day mean NDVI values from three parts of the study area, depicted by variants of green.

Figure 2

Duration, timing, and height of annual peaks of telemetrically measured variables and NDVI. Sections separated by vertical lines indicate periods with different light and vegetation conditions, i.e. the period when the sun was continuously below the horizon (Polar Night, DD), the periods with daylight and night (LD), the period of continual light (Midnight Sun, LL) before the onset of the vegetation period with NDVI values <0 (LL low), and the period of continual light with above-ground new vascular plant growth (NDVI >0, LL high). Plotted are baseline cosine fits to empirical data shown in Fig. 1, and their 95% confidence intervals (for details see Methods).

Figure 3

Annual course of circadian rhythmicity and potential zeitgebers. (a) Average normalized power of significant rhythms (p < 0.05) with period lengths between 21 and 27 hours, calculated with Lomb-Scargle periodogram analyses for 15-day intervals from Nov 15, 2012 to Nov 15, 2013, for ‘stationary’ heart rate (red), rumen temperature (orange), activity (blue), and head position changes (black; means and 95% confidence intervals reflecting variation between individuals, open symbols are single values). Note that more significant rhythms are found here compared to the analyses depicted in third panels of Supplementary Figs S4–S14. This is because the probability of detecting significant peaks depends on the number of periods scanned, i.e., it is higher when searching for periods between 21 to 27 hours than between 0.5 to 30 hours, as done for Supplementary Figs S4–S14. (b) 16-day averages of NDVI values from the three major parts of the study site for 2013 (see Fig. 1) and a baseline cosine fit to this data. (c) Ambient temperature measured in the collar (15-day means of daily variation and 95% confidence intervals, reflecting variation between individuals). (d) Daily variance of direct maximum solar radiation at the study site (disregarding weather effects). Horizontal bars and dotted vertical lines in each plot indicate periods of continual darkness (black), daylight/night changes (hatched), and continual daylight (open). Note that periods of daylight/night changes begin before and end after the sun firstly and lastly arises above the horizon. This difference results from using civil twilight for calculating beginning and end of daylight.

Figure 4

Comparison of rhythms of activity with period lengths between 21 and 27 hours of study animals #2, #3, and #4 between Nov 15, 2012 and Nov 15, 2013. Plotted are normalized powers of rhythms of activity. Each row of panels represents the different time periods: Polar Night (DD), daylight and night (LD), continual light (Midnight Sun, LL) before the onset of new vegetation growth with NDVI values <0 (LL low), and continual light with above-ground new vascular plant growth (NDVI >0, LL high). Horizontal red lines indicate the significance threshold of p = 0.001.

Figure 5

Daily patterns of activity of individual #4 between Nov 15, 2012 and Nov 15, 2013 as a representative example. Leftmost panel: Actogram of activity showing black bars for each 3 minute interval, with a height proportional to activity, one horizontal line for each day. Yellow lines indicate beginning and end of civil twilight (i.e. the geometric centre of the Sun’s disk is ≤6° below the horizon), a luminance that is sufficient to cause photic responses, e.g., suppression of melatonin production. Second panel: Normalized power of rhythms with period lengths between 30 minutes and 30 hours identified by Lomb-Scargle periodogram analysis. Horizontal red lines indicate the significance threshold of p = 0.001. Lines and arrows to the left indicate the intervals analysed, i.e. the period when the sun is continuously below the horizon during winter (Polar Night, DD), the periods with daylight and night (LD), the period of continual light (Midnight Sun, LL) before the onset of the vegetation period with NDVI values <0 (LL low), and the period of continual light with above-ground live vascular plants (NDVI >0, LL high). Third panel: as second panel but with periodograms of 15-day intervals. Rightmost panel: 16-day mean NDVI values from the three major parts of the study site for 2013 (see Fig. 1) and a baseline cosine fit to this data.

Figure 6

Comparison of the annual cycles of three species of ungulates dwelling in seasonal environments. Left, stationary heart rates; right, rumen temperatures of the study animals (white symbols), red deer (red symbols) redrawn from, and Alpine ibex (orange symbols) redrawn from. Points are means over periods of 5 days. Error bars are 95% confidence intervals of means and reflect variation between individuals.