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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References
Amaya JP, Cuello PA, Valentinuzzi VS, Lacey EA (2021) Dynamic spatial overlap in a solitary subterranean rodent: the Anillaco tuco-tuco (Ctenomys sp.). J Mammal 102:826–836. https://doi.org/10.1093/jmammal/gyab011
Aschoff J (1960) Exogenous and endogenous components in circadian rhythms. Cold Spr Harb Symp Quant Biol 25:11–28. https://doi.org/10.1101/sqb.1960.025.01.004
Beale AD, Whitmore D, Moran D (2016) Life in a dark biosphere: a review of circadian physiology in ‘arrhythmic’ environments. J Comp Physiol B-Biochem Syst Environ Physiol 186:947–968. https://doi.org/10.1007/s00360-016-1000-6
Ben-Shlomo R, Ritte U, Nevo E (1995) Activity pattern and rhythm in the subterranean mole-rat superspecies Spalax ehrenbergi. Behav Genet 25:239–245. https://doi.org/10.1007/BF02197182
Buijs RM, Escobar C (2007) Corticosterone and activity: the long arms of the clock talk back. Endocrinology 148(11):5162–5164. https://doi.org/10.1210/en.2007-0926
Bünning E (1936) Die endonomen Tagesrhythmen als Grundlage der photoperiodischen Reaktion. Ber Dtsch Bot Ges 54:590–607
Calebe PM, Carreira D, Pedrosa F, Beca G, Lautenschlager L, Akkawia P, Bercê W, Ferraz KMPMB, Galetti M (2020) Landscape of human fear in Neotropical rainforest mammals. Biol Cons. https://doi.org/10.1016/j.biocon.2019.108257
Chmura HE, Duncan C, Burrell G, Barnes BM, Buck CL, Williams CT (2023) Climate change is altering the physiology and phenology of an arctic hibernator. Science 380(6647):846. https://doi.org/10.1126/science.adf5341
Daan S, Aschoff J (1975) Circadian rhythms of locomotor activity in captive birds and mammals: their variations with season and latitude. Oecologia 18:269–316. https://doi.org/10.1007/BF00345851
Daan S, Pittendrigh CS (1976a) A functional analysis of circadian pacemakers in nocturnal rodents: II. The variability of phase response curves. J Comp Physiol A 106:253–266. https://doi.org/10.1007/BF01417857
Daan S, Pittendrigh CS (1976b) A functional analysis of circadian pacemakers in nocturnal rodents: III Heavy water and constant light: homeostasis of frequency? J Comp Physiol A 106:267–290. https://doi.org/10.1007/BF01417858
Dardente H, Wood S, Ebling F, Sáenz de Miera C (2019) An integrative view of mammalian seasonal neuroendocrinology. J Neuroendocrinol 31(5):e12729. https://doi.org/10.1111/jne.12729
Dark J, Pickard GE, Zucker I (1985) Persistence of circannual rhythms in ground squirrels with lesions of the suprachiasmatic nuclei. Brain Res 322:201–207. https://doi.org/10.1016/0006-8993(85)90589-x
DeCoursey P (1986) Light sampling behaviour in photoentrainment of a rodent circadian system. J Comp Physiol A 159:161–169. https://doi.org/10.1007/BF00612299
Dominoni DM, Åkesson S, Klaassen R, Spoelstra K, Bulla M (2017) Methods in field chronobiology. Philos Trans R Soc B Biol Sci 372(1734):20160247. https://doi.org/10.1098/rstb.2016.0247
Flôres DEFL, Oda GA (2018) Novel light/dark regimens with minimum light promote circadian disruption: simulations with a model oscillator. J Biol Rhythms 34(1):105–110. https://doi.org/10.1177/0748730418820727
Flôres DEFL, Oda GA (2020) Quantitative study of dual-oscillator models under different skeleton photoperiods. J Biol Rhythms 35(3):302–316. https://doi.org/10.1177/0748730420901939
Flôres DEFL, Tomotani BM, Tachinardi P, Oda GA, Valentinuzzi VS (2013) Modeling natural photic entrainment in a subterranean rodent (Ctenomys aff. knighti), the tuco-tuco. PLoS ONE 8(7):e68243. https://doi.org/10.1371/journal.pone.0068243
Flôres DEFL, Jannetti M, Valentinuzzi VS, Oda GA (2016) Entrainment of circadian rhythms to irregular light/dark cycles: a subterranean perspective. Sci Rep 6:34264. https://doi.org/10.1038/srep34264
Flôres DEFL, Jannetti MG, Improta GC, Tachinardi P, Valentinuzzi VS, Oda GA (2021) Telling the seasons underground: the circadian clock and ambient temperature shape light exposure and photoperiodism in a subterranean rodent. Front Physiol 12:738471. https://doi.org/10.3389/fphys.2021.738471
Gaynor KM, Hojnowski CE, Carter NH, Brashares JS (2018) The influence of human disturbance on wildlife nocturnality. Science 360(6394):1232–1235. https://doi.org/10.1126/science.aar7121
Goldman BD, Goldman SL, Riccio AP, Terkel J (1997) Circadian patterns of locomotor activity and body temperature in blind mole-rats Spalax ehrenbergi. J Biol Rhythms 12(4):348–361. https://doi.org/10.1177/074873049701200407
Halle S, Stenseth NC (2000) Activity patterns in small mammals—an ecological approach. Springer, Berlin
Houben T, Deboer T, van Oosterhout F, Meijer JH (2009) Correlation with behavioral activity implies circadian regulation by SCN neuronal activity levels. J Biol Rhythms 24(6):477–487. https://doi.org/10.1177/0748730409349895
Hut RA, van Oort BEH, Daan S (1999) Natural entrainment without dawn and dusk: the case of the European ground squirrel (Spermophilus citellus). J Biol Rhythms 14:290–299. https://doi.org/10.1177/074873099129000704
Hut RA, Kronfeld-Schor N, van der Vinne V, De la Iglesia H (2012) In search of a temporal niche. Prog Brain Res 199:281–304. https://doi.org/10.1016/b978-0-444-59427-3.00017-4
Ikegami K, Yoshimura T (2012) Circadian clocks and the measurement of daylength in seasonal reproduction. Mol Cell Endocrinol 349:76–81. https://doi.org/10.1016/j.mce.2011.06.040
Improta GC, Flôres DEFL, Oda GA, Valentinuzzi VS (2022) Daylength shapes entrainment patterns to artificial photoperiods in a subterranean rodent. J Biol Rhythms. https://doi.org/10.1177/07487304221085105
Jannetti MG (2018) Sazonalidade dos padrões diários de atividade de superfície em um roedor subterrâneo, o tuco-tuco. Dissertação de Mestrado, Instituto de Biociências, Universidade de São Paulo, São Paulo
Jannetti MG, Buck CL, Valentinuzzi VS, Oda GA (2019) Day and night in the subterranean: measuring daily activity patterns of subterranean rodents (Ctenomys aff. knighti) using bio-logging. Cons Physiol 7:coz044. https://doi.org/10.1093/conphys/coz044
Jannetti MG, Tachinardi P, Oda GA, Valentinuzzi VS (2023) Temporal dissociation between activity and body temperature rhythms of a subterranean rodent (Ctenomys famosus) in field enclosures. J Biol Rhythms 38:074873042311547. https://doi.org/10.1177/07487304231154715
Kaczmarek JL, Thompson SV, Holscher HD (2017) Complex interactions of circadian rhythms, eating behaviors, and the gastrointestinal microbiota and their potential impact on health. Nutr Rev 75(9):673–682. https://doi.org/10.1093/nutrit/nux036
Kenagy GJ (1976) The periodicity of daily activity and its seasonal changes in free-ranging and captive kangaroo rats. Oecologia 24:105–140. https://doi.org/10.1007/BF00572754
Kenagy GJ, Nespolo RF, Vásquez RA, Bozinovic F (2002) Daily and seasonal limits of time and temperature on the activity of degus. Rev Chil Hist Nat 75:567–581. https://doi.org/10.4067/S0716-078X2002000300008
Kronfeld-Schor N, Bloch G, Schwartz WJ (2013) Animal clocks: when science meets nature. Proc R Soc B 280:20131354. https://doi.org/10.1098/rspb.2013.1354
Leise TL, Harrington ME, Molyneux PC, Song I, Queenan H, Zimmerman E, Lall GS, Biello SM (2013) Voluntary exercise can strengthen the circadian system in aged mice. Age 35:2137–2152. https://doi.org/10.1007/s11357-012-9502-y
Levy O, Dayan T, Kronfeld-Schor N (2007) The relationship between the golden spiny mouse circadian system and its diurnal activity: an experimental field enclosures and laboratory study. Chron Int 24:599–613. https://doi.org/10.1080/07420520701534640
Long RA, Martin TJ, Barnes BM (2005) Body temperature and activity patterns in free-living arctic ground squirrels. J Mammal 86:314–322. https://doi.org/10.1644/BRG-224.1
Nakane Y, Yoshimura T (2019) Photoperiodic regulation of reproduction in vertebrates. Annu Rev Anim Biosci 7:173–194. https://doi.org/10.1146/annurev-animal-020518-115216
Oda GA, Friesen WO (2011) Modeling two-oscillator circadian systems entrained by two environmental cycles. PLoS ONE 6(8):e23895. https://doi.org/10.1371/journal.pone.0023895
Oda GA, Menaker M, Friesen WO (2000) Modeling the dual pacemaker system of the tau mutant hamster. J Biol Rhythms 15(3):246–264. https://doi.org/10.1177/074873040001500306
Olde Engberink AH, Huisman J, Michel S, Meijer JH (2020) Brief light exposure at dawn and dusk can encode day-length in the neuronal network of the mammalian circadian pacemaker. FASEB J 34:13685–13695. https://doi.org/10.1096/fj.202001133RR
Oosthuizen MK, Bennett NC (2022) Clocks ticking in the dark: a review of biological rhythms in subterranean mole rats. Front Ecol Evol 10:878533. https://doi.org/10.3389/fevo.2022.878533
Pittendrigh CS, Daan S (1976a) A functional analysis of circadian pacemakers in nocturnal rodents. I. The stability and lability of spontaneous frequency. J Comp Physiol A 106:223–252. https://doi.org/10.1007/BF01417856
Pittendrigh CS, Daan S (1976b) A functional analysis of circadian pacemakers in nocturnal rodents: IV. Entrainment: pacemaker as clock. J Comp Physiol A 106:291–331. https://doi.org/10.1007/BF01417857
Pittendrigh CS, Daan S (1976c) A functional analysis of circadian pacemakers in nocturnal rodents: V. Pacemaker structure: a clock for all seasons. J Comp Physiol A 106:333–335. https://doi.org/10.1007/BF01417857
Pittendrigh CD, Minis DH (1964) The entrainment of circadian oscillations by light and their role as photoperiodic clocks. The Am Nat 98:261–294. https://doi.org/10.1086/282327
Reebs SG, Mrosovsky N (1989) Effects of induced wheel running on the circadian activity rhythms of Syrian hamsters: entrainment and phase response curve. J Biol Rhythms 4(1):39–48. https://doi.org/10.1177/074873048900400103
Rezende EL, Cortés A, Bacigalupe LD, Nespolo RF, Bozinovic F (2003) Ambient temperature limits above-ground activity of the subterranean rodent Spalacopus cyanus. J Arid Environ 55:63–74. https://doi.org/10.1016/S0140-1963(02)00259-8
Roenneberg T, Merrow M (2005) Circadian clocks—the fall and rise of physiology. Nat Rev Mol Cell Biol 6(12):965–971. https://doi.org/10.1038/nrm1766
Roenneberg T, Daan S, Merrow M (2003) The art of entrainment. J Biol Rhythms 18(3):183–194. https://doi.org/10.1177/0748730403018003001
Sánchez RT, Tomasco IH, Díaz MM, Bárquez RM (2023) Review of three neglected species of Ctenomys (Rodentia: Ctenomyidae) from Argentina. J Mammal. https://doi.org/10.1093/jmammal/gyad001
Schmal C, Herzel H, Myung J (2020) Clocks in the wild: entrainment to natural light. Front Physiol 11:272. https://doi.org/10.3389/fphys.2020.00272
Schwartz WJ, Helm B, Gerkema MP (2017) Wild clocks: preface and glossary. Phil Trans R Soc Lond B Biol Sci 372(1734):20170211. https://doi.org/10.1098/rstb.2017.0211
Silvério JT, Tachinardi P (2020) Chronobiology in the wild: toolkit to study daily rhythms in free-living animals. Sleep Sci 13:87–91. https://doi.org/10.5935/1984-0063.20200020
Sklíba J, Sumbera R, Chitaukali WN, Burda H (2007) Determinants of daily activity patterns in a free-living afrotropical solitary subterranean rodent. J Mammal 88:1009–1016. https://doi.org/10.1644/06-MAMM-A-235R1.1
Tachinardi P, Bicudo JEW, Oda GA, Valentinuzzi VS (2014) Rhythmic 24 h variation of core body temperature and locomotor activity in a subterranean rodent (Ctenomys aff. knighti), the tuco-tuco. PLoS ONE 9:e85674. https://doi.org/10.1371/journal.pone.0085674
Tachinardi P, Tøien Ø, Valentinuzzi VS, Buck CL, Oda GA (2015) Nocturnal to diurnal switches with spontaneous suppression of wheel-running behavior in a subterranean rodent. PLoS ONE 10:e0140500. https://doi.org/10.1371/journal.pone.0140500
Tachinardi P, Valentinuzzi VS, Oda GA, Buck CL (2017) The interplay of energy balance and daily timing of activity in a subterranean rodent: a laboratory and field approach. Physiol Biochem Zool 90(5):546–552. https://doi.org/10.1086/693003
Tackenberg MC, Hughey JJ, McMahon DG (2020) Distinct components of photoperiodic light are differentially encoded by the mammalian circadian clock. J Biol Rhythms 35:353–367. https://doi.org/10.1177/0748730420929217
Tammone MN, Torres TF, Ojeda AA, Chemisquy MA (2022) Disentangling the taxonomic status of Ctenomys (Rodentia: Ctenomyidae) populations inhabiting northern areas of La Rioja Province, Argentina. Mammalia 86:527–538. https://doi.org/10.1515/mammalia-2021-0169
Tomotani BM, Flores DEFL, Tachinardi P, Paliza JD, Oda GA, Valentinuzzi VS (2012) Field and laboratory studies provide insights into the meaning of day-time activity in a subterranean rodent (Ctenomys aff. knighti), the tuco-tuco. PLoS ONE. https://doi.org/10.1371/journal.pone.0037918
Valentinuzzi VS, Oda GA, Araújo JF, Ralph RM (2009) Circadian pattern of wheel running activity of a South American subterranean rodent (Ctenomys knighti). Chron Int 26(1):14–27. https://doi.org/10.1080/07420520802686331
Van der Vinne V, Gorter JA, Riede SJ, Hut RA (2015) Diurnality as an energy-saving strategy: energetic consequences of temporal niche switching in small mammals. J Exp Biol 218:2585–2593. https://doi.org/10.1242/jeb.119354
Vlasatá T, Sklíba J, Lovy M, Meheretu Y, Sillero-Zubiri C, Sumbera R (2017) Daily activity patterns in the giant root rat (Tachyoryctes macrocephalus), a fossorial rodent from the afro-alpine zone of the Bale Mountains, Ethiopia. J Zool 302:157–163. https://doi.org/10.1111/jzo.12441
Williams CT, Wilsterman K, Kelley AD, Breton AR, Stark H, Humphries MM et al (2014) Biologging in small mammals: light loggers reveal weather-driven changes in the daily activity patterns of arboreal and semi-fossorial rodents. J Mammal 95:1230–1239. https://doi.org/10.1644/14-MAMM-A-062
Williams CT, Barnes BM, Buck CL (2016) Integrating physiology, behavior, and energetics: biologging in a free-living arctic hibernator. Comp Biochem Physiol A 202:53–62. https://doi.org/10.1016/j.cbpa.2016.04.020
Winfree AT (2001) The geometry of biological time, vol 12. Springer, New York
Wright KP, McHill AW, Birks BR, Griffin BR, Rusterholz T, Chinoy ED (2013) Entrainment of the human circadian clock to the natural light-dark cycle. Curr Biol 23:1554–1558. https://doi.org/10.1016/j.cub.2013.06.039
Yan L, Smale L, Nunez AA (2020) Circadian and photic modulation of daily rhythms in diurnal mammals. Eur J Neurosci 51(1):551–566. https://doi.org/10.1111/ejn.14172
Yassumoto TI, Tachinardi P, Oda GA, Valentinuzzi VS (2019) Acute effects of light and darkness on the activity and temperature rhythms of a South-American subterranean rodent, the Anillaco tuco-tuco. Physiol Behav 1:112645. https://doi.org/10.1016/j.physbeh.2019.112645
Yoshikawa T, Inagaki NF, Takagi S, Kuroda S, Yamazaki M, Watanabe M, Honma S, Honma K (2017) Localization of photoperiod responsive circadian oscillators in the mouse suprachiasmatic nucleus. Sci Rep 7:1–13. https://doi.org/10.1038/s41598-017-08186-5
Zhang Y, Li Y, Sehgal A (2023) The microbiome stabilizes circadian rhythms in the gut. PNAS 120(5):e2217532120. https://doi.org/10.1073/pnas.2217532120
Zucker I, Boshes M, Dark J (1983) Suprachiasmatic nuclei influence circannual and circadian rhythms of ground squirrels. Am J Physiol 244:R472–R480. https://doi.org/10.1152/ajpregu.1983.244.4.R472
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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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