Body Temperature and Activity Rhythms Under Different Photoperiods in High Arctic Svalbard ptarmigan (Lagopus muta hyperborea)

Abstract

Organisms use circadian rhythms to anticipate and exploit daily environmental oscillations. While circadian rhythms are of clear importance for inhabitants of tropic and temperate latitudes, its role for permanent residents of the polar regions is less well understood. The high Arctic Svalbard ptarmigan shows behavioral rhythmicity in presence of light-dark cycles but is arrhythmic during the polar day and polar night. This has been suggested to be an adaptation to the unique light environment of the Arctic. In this study, we examined regulatory aspects of the circadian control system in the Svalbard ptarmigan by recording core body temperature (T _b) alongside locomotor activity in captive birds under different photoperiods. We show that T _b and activity are rhythmic with a 24-h period under short (SP; L:D 6:18) and long photoperiod (LP; L:D 16:8). Under constant light and constant darkness, rhythmicity in T _b attenuates and activity shows signs of ultradian rhythmicity. Birds under SP also showed a rise in T _b preceding the light-on signal and any rise in activity, which proves that the light-on signal can be anticipated, most likely by a circadian system.

Keywords: Arctic; Svalbard ptarmigan; chronobiology; circadian rhythm; heterothermy; photoperiod; thermoregulation.

Figure 1

Svalbard ptarmigan (Lagopus muta hyperborea) and experimental design. (A) The picture shows a Svalbard ptarmigan male in white winter plumage and a female in the cryptic brown summer plumage (© Ida-Helene Sivertsen). (B) The Svalbard ptarmigan is a subspecies of the rock ptarmigan (Lagopus muta) but is geographically isolated to the high Arctic archipelago of Svalbard and Franz Josef Land. (C) The experimental birds were bred at the University of Tromsø and were separated into three groups: the short photoperiod (SP) group remained under L:D 6:18. The LP/LL-group was gradually transferred from L:D 6:18 to L:D 16:8 (LP), and subsequently into constant light (LL). The constant darkness (DD) group was directly transferred from L:D 6:18 into DD.

Figure 2

Representative double-plotted actograms for body temperature (T_b) and activity. (A-C) T_b was plotted actogram-like between 40 and 42°C for representative birds from each group (bird IDs A: SP3, B: LP/LL11, C: DD3). (D–F) Actograms for normalized activity were plotted between 0 and 1 for representative birds from each group (bird IDs D: SP6, E: LP/LL15, F: DD2). χ²-periodograms were plotted for 10 consecutive days in each light treatment (red shading in actograms) and are displayed next to the respective recordings. Values above the red line indicate that the cycle period was significant (p < 0.05). Additional actograms and periodograms can be found in Supplementary Figures S1–S3.

Figure 3

Diel variation in T_b and activity in short and long photoperiod. (A,B) Mean ± SD T_b over the course of 24 h (01:00 to midnight) in SP (based on 222 × 24-h recordings from five birds) and LP (based on 184 × 24-h recordings from eight birds). T_b was measured every hour throughout the experiment. (C,D) Mean normalized activity ± SD over the course of 24 h (midnight to midnight) in SP (61 × 24-h recordings from three birds) and LP (27 × 24-h recordings from three birds). Light gray shadowing in the panels indicate periods of darkness and dark gray indicates SD.

Figure 4

Representative time series for T_b and activity. (A–D) T_b (red) was plotted together with normalized activity (black) for 5 consecutive days for one representative bird per experimental treatment (bird IDs A: SP6, B,C: LP/LL13, D: DD2). Light gray shadings indicate periods of darkness. Additional time series can be found in Supplementary Figure S4.

Figure 5

Anticipatory rise in T_b based on segmental regression breakpoints. Hourly means of T_b (red) and activity (black) 5 h before and 1 h after the light-on signal, given in Zeitgeber time (ZT). (A) T_b in birds under SP was rising 2 h 56 min before the light-on signal while activity rises 1 h 40 min before light-on. (B) In birds under LP T_b increased 43 min before light-on, while activity rose 34 min before the light-on signal. The data correspond to the measurement in Figure 4 and Supplementary Figure S4 and are displayed as mean ± 95% CI. Dotted lines indicate segmented regression breaking points and the shading shows the corresponding SD. Light gray shadings indicate periods of darkness.