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A clock for all seasons in the subterranean

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Abstract

In 1976, Pittendrigh and Daan established a theoretical framework which has coordinated research on circadian clock entrainment and photoperiodism until today. The “wild clocks” approach, which concerns studying wild species in their natural habitats, has served to test their models, add new insights, and open new directions of research. Here, we review an integrated laboratory, field and modeling work conducted with subterranean rodents (Ctenomys sp.) living under an extreme pattern of natural daily light exposure. Tracking animal movement and light exposure with biologgers across seasons and performing laboratory experiments on running-wheel cages, we uncovered the mechanisms of day/night entrainment of the clock and of photoperiodic time measurement in this subterranean organism. We confirmed most of the features of Pittendrigh and Daan’s models but highlighted the importance of integrating them with ecophysiological techniques, methodologies, and theories to get a full picture of the clock in the wild. This integration is essential to fully establish the importance of the temporal dimension in ecological studies and tackling relevant questions such as the role of the clock for all seasons in a changing planet.

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Fig. 1

(Modified from Flôres 2016)

Fig. 2

(Modified from Improta et al. 2022)

Fig. 3
Fig. 4
Fig. 5

(Modified from Valentinuzzi et al. 2009)

Fig. 6

(Modified from Flôres et al. 2021)

Fig. 7
Fig. 8

(Modified from Jannetti et al. 2023)

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Data is available upon request.

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Acknowledgements

The authors thank the invaluable contributions of all students who shared opinions and decisions throughout this study, performed field work and lab experiments, developed data analysis and computer simulations, and brought new techniques and enthusiastic collaboration: Danilo Flôres, Barbara Tomotani, Patricia Tachinardi, Milene Jannetti, Jefferson Silvério, Tamiris Yassumoto, and Giovane Improta. Technical assistance of Johanna Barros is deeply acknowledged. The authors also thank Prof. Mirian Marques for promoting the study of Pittendrigh and Daan´s works, Prof. Otto Friesen for making mathematical modeling possible and introducing the study of natural entrainment, Prof. Loren Buck for introducing biologging devices and improving field and lab methods, Prof. James Kenagy for constructive criticisms, James Fox from Migrate Company and Carlo Cattoni from Technosmart Company for the confection of biologgers and kind attention, Jose D. Paliza, Eugenio Sanchez (Charly), Carlos Herrera (Carlitos) and Juan Mulet for the construction and maintenance of the enclosures, Prof. Martin Ralph, Prof. Diego Golombek, and Prof. Juan Chiesa for all help and encouragement in the early years.

Funding

This work was supported by FONCyT—Agencia Nacional de Promoción Científica y Tecnológica, CONICET—Consejo Nacional de Investigaciones Científicas y Técnicas, FAPESP—Fundação de Amparo à Pesquisa do Estado de São Paulo, CAPES—Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, and CNPq—Conselho Nacional de Pesquisa.

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GAO and VSV wrote the main manuscript text and GAO and VSV prepared Figs. 1, 2, 3, 4, 5, 6, 7. All authors reviewed the manuscript.

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Correspondence to Gisele A. Oda or Veronica S. Valentinuzzi.

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Oda, G.A., Valentinuzzi, V.S. A clock for all seasons in the subterranean. J Comp Physiol A (2023). https://doi.org/10.1007/s00359-023-01677-z

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  • DOI: https://doi.org/10.1007/s00359-023-01677-z

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