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Biological Rhythms and Sleep in Reindeer ($\textit{Rangifer tarandus tarandus}$) across Arctic Seasons


Meier, Sara Andrea. Biological Rhythms and Sleep in Reindeer ($\textit{Rangifer tarandus tarandus}$) across Arctic Seasons. 2024, University of Zurich, Faculty of Science.

Abstract

Biological rhythms synchronize organisms to their environment and accordingly orchestrate physiological process and behaviors. For example, the circadian clock anticipates 24-h rhythms of day and night and accordingly synchronizes behavior and physiological processes like sleep and wake and feeding and fasting. Additionally, it detects changes in day length (photoperiod) across seasons, entraining the circannual clock. The circannual clock controls physiology and behavior on an annual scale, such as filling-up energy deposits in summer or slowing down metabolic rate in winter to reduce energy expenditure. Throughout the day, ultradian rhythms regulate behavioral and physiological processes with periods shorter than 24 h. Sleep is an essential behavior for maintenance of brain function, reduction of energy expenditure and survival. Sleep behavior is regulated by a homeostatic process, tracking time spent awake and a circadian process, modulating sleep need across the day. Biological rhythms and sleep are found across almost all kingdoms of life and their disruption has severe consequences to health and survival. In humans, chronic sleep restriction or circadian disruption by jet lag, shift work or artificial light at night increase the risk for many metabolic diseases like obesity, metabolic syndrome and cancer. Arctic species experience the most drastic seasonal changes in environmental conditions, posing unique challenges to their biological timing systems. Daylength varies from constant darkness for several months in winter to constant light for several months in summer. Under these unusual photoperiods reindeer (Rangifer tarandus) lose 24-h patterns in behavioral activity, while they show normal 24-h rhythms in activity under the light-dark conditions of spring and fall, raising the question whether reindeer have a functional circadian clock. Additionally, reindeer are highly active during summer to maximize food intake during the short arctic growing season and drastically decrease their behavioral activity in winter. These observations raised two questions: First, if reindeer might not have a functional circadian clock, how do they maintain healthy metabolic control during seasons when they lack environmental entrainment of behavioral daily rhythms? Secondly, what happens to sleep across seasons when reindeer undergo these drastic changes in behavioral activity? To gain insight into these questions, ultra-high performance liquid chromatography coupled mass spectrometry was applied to explore the temporal regulation of reindeer blood metabolites and electroencephalography was used to measure reindeer sleep across season. In winter and spring, many metabolic features in reindeer blood expressed 24-h rhythms. In contrast, in summer and fall, the number of metabolic features expressing 24-h rhythms was drastically reduced. Sleep measurements revealed a homeostatic regulation of reindeer sleep in all seasons examined (winter, summer, fall) and sleep patterns paralleled behavioral activity patterns of loss of 24-h rhythms in winter and summer and entrained 24-h rhythms in fall. Interestingly, slow-wave activity decreased during rumination similarly than during NREM sleep. Additionally, sleep/activity patterns correlated with temporal metabolic changes in summer in many metabolic features which expressed 24-h rhythms in winter and spring. This suggests that 24-h rhythms in reindeer metabolism are expressed during seasons of low food availability, ensuring efficient energy usage, and a switch to ultradian, sleep-controlled metabolism in summer and fall to maximize food intake during the short growing season of the Arctic.

Abstract

Biological rhythms synchronize organisms to their environment and accordingly orchestrate physiological process and behaviors. For example, the circadian clock anticipates 24-h rhythms of day and night and accordingly synchronizes behavior and physiological processes like sleep and wake and feeding and fasting. Additionally, it detects changes in day length (photoperiod) across seasons, entraining the circannual clock. The circannual clock controls physiology and behavior on an annual scale, such as filling-up energy deposits in summer or slowing down metabolic rate in winter to reduce energy expenditure. Throughout the day, ultradian rhythms regulate behavioral and physiological processes with periods shorter than 24 h. Sleep is an essential behavior for maintenance of brain function, reduction of energy expenditure and survival. Sleep behavior is regulated by a homeostatic process, tracking time spent awake and a circadian process, modulating sleep need across the day. Biological rhythms and sleep are found across almost all kingdoms of life and their disruption has severe consequences to health and survival. In humans, chronic sleep restriction or circadian disruption by jet lag, shift work or artificial light at night increase the risk for many metabolic diseases like obesity, metabolic syndrome and cancer. Arctic species experience the most drastic seasonal changes in environmental conditions, posing unique challenges to their biological timing systems. Daylength varies from constant darkness for several months in winter to constant light for several months in summer. Under these unusual photoperiods reindeer (Rangifer tarandus) lose 24-h patterns in behavioral activity, while they show normal 24-h rhythms in activity under the light-dark conditions of spring and fall, raising the question whether reindeer have a functional circadian clock. Additionally, reindeer are highly active during summer to maximize food intake during the short arctic growing season and drastically decrease their behavioral activity in winter. These observations raised two questions: First, if reindeer might not have a functional circadian clock, how do they maintain healthy metabolic control during seasons when they lack environmental entrainment of behavioral daily rhythms? Secondly, what happens to sleep across seasons when reindeer undergo these drastic changes in behavioral activity? To gain insight into these questions, ultra-high performance liquid chromatography coupled mass spectrometry was applied to explore the temporal regulation of reindeer blood metabolites and electroencephalography was used to measure reindeer sleep across season. In winter and spring, many metabolic features in reindeer blood expressed 24-h rhythms. In contrast, in summer and fall, the number of metabolic features expressing 24-h rhythms was drastically reduced. Sleep measurements revealed a homeostatic regulation of reindeer sleep in all seasons examined (winter, summer, fall) and sleep patterns paralleled behavioral activity patterns of loss of 24-h rhythms in winter and summer and entrained 24-h rhythms in fall. Interestingly, slow-wave activity decreased during rumination similarly than during NREM sleep. Additionally, sleep/activity patterns correlated with temporal metabolic changes in summer in many metabolic features which expressed 24-h rhythms in winter and spring. This suggests that 24-h rhythms in reindeer metabolism are expressed during seasons of low food availability, ensuring efficient energy usage, and a switch to ultradian, sleep-controlled metabolism in summer and fall to maximize food intake during the short growing season of the Arctic.

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Additional indexing

Item Type:Dissertation (cumulative)
Referees:Huber Reto, Schaepman-Strub Gabriela, Wagner Gabriela, Brown Steven, Sundset Monica
Communities & Collections:04 Faculty of Medicine > Institute of Pharmacology and Toxicology
07 Faculty of Science > Institute of Pharmacology and Toxicology

07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
UZH Dissertations
Dewey Decimal Classification:570 Life sciences; biology
610 Medicine & health
590 Animals (Zoology)
Language:English
Place of Publication:Zürich
Date:21 March 2024
Deposited On:21 Mar 2024 15:24
Last Modified:21 Mar 2024 15:25
Number of Pages:98
OA Status:Closed