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Chronobiology International
The Journal of Biological and Medical Rhythm Research
Volume 41, 2024 - Issue 3
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Original article

The role of ambient temperature and light as cues in the control of circadian rhythms of Damaraland mole-rat

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Pages 356-368 | Received 08 Nov 2023, Accepted 27 Feb 2024, Published online: 05 Mar 2024

References

  • Abhilash L, Shindey R, Sharma VK. 2017. To be or not to be rhythmic? A review of studies on organisms inhabiting constant environments. Biol Rhythm Res. 48:677–691. doi: 10.1080/09291016.2017.1345426.
  • Bates DM, Machler M, Bolker BM, Walker SC. 2014. Fitting linear mixed-effects models using lme4. J Stat Softw. 67:1–48.
  • Beale AD, Whitmore D, Moran D. 2016. Life in a dark biosphere: a review of circadian physiology in “arrhythmic” environments. J Comp Physiol B. 186:947–968. doi: 10.1007/s00360-016-1000-6.
  • Bennett NC, Faulkes CG. 2000. African mole-rats: ecology and eusociality. UK: Cambridge University Press.
  • Bennett NC, Hart DW, Munro S, Amor N, Mohammed OB, Alagaili AN. 2024. Hopping from the heat: the locomotory activity patterns of the lesser Egyptian Jerboa (Jaculus jaculus). J Arid Environ. 220:105116.
  • Bennett NC, Jarvis JUM. 1995. Coefficients of digestibility and nutritional values of geophytes and tubers eaten by southern African mole-rats (Rodentia: Bathyergidae). J Zool. 236:189–198. doi: 10.1111/j.1469-7998.1995.tb04487.x.
  • Bhadra U, Thakkar N, Das P, Pal-Bhadra M. 2017. Evolution of circadian rhythms: from bacteria to human. Sleep Med. 35:49–61. doi: 10.1016/j.sleep.2017.04.008.
  • Daan S, Aschoff J. 2001. The entrainment of circadian systems. In: Takahashi J, Turek F Moore R, editors. Circadian clocks. Boston, MA: Springer US. pp. 7–43.
  • El Allali K, Achaâban MR, Bothorel B, Piro M, Bouâouda H, Allouchi ME, Ouassat M, Malan A, Pévet P. 2013. Entrainment of the circadian clock by daily ambient temperature cycles in the camel (Camelus dromedarius). Am J Physiol Regul Integr Comp Physiol. 304:1044–1052.
  • Farsi H, Achaâban MR, Piro M, Bothorel B, Ouassat M, Challet E, Pévet P, El Allali K. 2020. Entrainment of circadian rhythms of locomotor activity by ambient temperature cycles in the dromedary camel. Sci Rep. 10:19515. doi: 10.1038/s41598-020-76535-y.
  • Farsi H, Harti D, Achaâban MR, Piro M, Raverot V, Bothorel B, Ouassat M, Challet E, Pévet P, El Allali K. 2020. Melatonin rhythm and other outputs of the master circadian clock in the desert goat (Capra hircus) are entrained by daily cycles of ambient temperature. J Pineal Res. 68:e12634. doi: 10.1111/jpi.12634.
  • Finn KT, Janse van Vuuren AK, Hart DW, Süess T, Zöttl M, Bennett NC. 2022. Seasonal changes in locomotor activity patterns of wild social Natal mole-rats (Cryptomys hottentotus natalensis). Front Ecol Evol. 10:62.
  • Fraker ME. 2008. The influence of the circadian rhythm of green frog (Rana clamitans) tadpoles on their antipredator behavior and the strength of the nonlethal effects of predators. Am Nat. 171:545–552. doi: 10.1086/528961.
  • Gall AJ, Shuboni-Mulligan DD. 2022. Keep your mask on: the benefits of masking for behavior and the contributions of ageing and disease on dysfunctional masking pathways. Front Neurosci. 16:911153.
  • Gander P, Mulrine HM, van den Berg MJ, Wu L, Smith A, Signal L, Mangie J. 2016. Does the circadian clock drift when pilots fly multiple transpacific flights with 1-to 2-day layovers? Chronobiol Int. 33:982–994.
  • Golombek DA, Rosenstein RE. 2010. Physiology of circadian entrainment. Physiol Rev. 90:1063–1102. doi: 10.1152/physrev.00009.2009.
  • Gravett N, Bhagwandin A, Sutcliffe R, Landen K, Chase MJ, Lyamin OI, Siegel JM, Manger PR, Vyazovskiy VE, Vyazovskiy V. 2017. Inactivity/Sleep in two wild free-roaming African elephant matriarchs – does large body size make elephants the shortest mammalian sleepers? PLoS One. 12:e0171903. doi: 10.1371/journal.pone.0171903.
  • Hart DW, Bennett NC, Best C, van Jaarsveld B, Cheng H, Ivy CM, Kirby AM, Munro D, Sprenger RJ, Storey KB, et al. 2023. The relationship between hypoxia exposure and circulating cortisol levels in social and solitary African mole-rats: an initial report. Gen Comp Endocrinol. 339:114294. doi: 10.1016/j.ygcen.2023.114294.
  • Hart DW, Bennett NC, Oosthuizen MK, Waterman JM, Hambly C, Scantlebury DM. 2022. Energetics and water flux in the subterranean rodent family bathyergidae. Front Ecol Evol. 10:867350. doi: 10.3389/fevo.2022.867350.
  • Hart DW, van Jaarsveld B, Lasch KG, Grenfell KL, Oosthuizen MK, Bennett NC. 2021. Ambient temperature as a strong zeitgeber of circadian rhythms in response to temperature sensitivity and poor heat dissipation abilities in subterranean African mole-rats. J Biol Rhythms. 36:461–469. doi: 10.1177/07487304211034287.
  • Haupt M, Bennett NC, Oosthuizen MK. 2017. Locomotor activity and body temperature patterns over a temperature gradient in the highveld mole-rat (Cryptomys hottentotus pretoriae). PLoS One. 12:e0169644. doi: 10.1371/journal.pone.0169644.
  • Hazell RWA, Bennett NC, Jarvis JUM, Griffin M. 2000. Adult dispersal in the co-operatively breeding damaraland mole-rat (Cryptomys damarensis): a case study from the Waterberg region of Namibia. J Zool. 252:19–25. doi: 10.1111/j.1469-7998.2000.tb00816.x.
  • Holtze S, Braude S, Lemma A, Koch R, Morhart M, Szafranski K, Platzer M, Alemayehu F, Goeritz F, Hildebrandt TB. 2018. The microenvironment of naked mole-rat burrows in East Africa. Afr J Ecol. 56:279–289. doi: 10.1111/aje.12448.
  • Ivy CM, Sprenger RJ, Bennett NC, van Jaarsveld B, Hart DW, Kirby AM, Yaghoubi D, Storey KB, Milsom WK, Pamenter ME. 2020. The hypoxia tolerance of eight related African mole-rat species rivals that of naked mole-rats, despite divergent ventilatory and metabolic strategies in severe hypoxia. Acta Physiol. 228:e13436. doi: 10.1111/apha.13436.
  • Jacobs PJ, Bennett NC, Oosthuizen MK. 2020. Locomotor activity in field captured crepuscular four-striped field mice, Rhabdomys dilectus and nocturnal Namaqua rock mice, Micaelamys namaquensis during a simulated heat wave. J Therm Biol. 87:102479. doi: 10.1016/j.jtherbio.2019.102479.
  • Jacobs PJ, Finn KT, van Vuuren AK J, Süess T, Hart DW, Bennett NC. 2022. Defining the link between oxidative stress, behavioural reproductive suppression and heterothermy in the natal mole-rat (Cryptomys hottentotus natalensis). Comp Biochem Physiol B Biochem Mol Biol. 261:110753. doi: 10.1016/j.cbpb.2022.110753.
  • Kott O, Šumbera R, Němec P, Iwaniuk A. 2010. Light perception in two strictly subterranean rodents: life in the dark or blue? PLoS One. 5:e11810.
  • Lenth R, Singmann H, Love J, Buerkner P, Herve M (2018). emmeans: Estimated marginal means, aka least-squares means (R package, Version 1.4) [Computer software].
  • Lövy M, Šklíba J, Šumbera R, Dornhaus A. 2013. Spatial and temporal activity patterns of the free-living giant mole-rat (fukomys mechowii), the largest social Bathyergid. PLoS One. 8:e55357. doi: 10.1371/journal.pone.0055357.
  • Luna F, Šumbera R, Okrouhlík J, Mladěnková N, Antenucci CD. 2020. Evaporative water loss in seven species of fossorial rodents: does effect of degree of fossoriality and sociality exist? J Therm Biol. 89:102564.
  • McNab BK. 1974. The energetics of endotherms. Ohio J Sci. 74:370–380.
  • Němec P, Cveková P, Benada O, Wielkopolska E, Olkowicz S, Turlejski K, Burda H, Bennett NC, Peichl L. 2008. The visual system in subterranean African mole-rats (Rodentia, Bathyergidae): retina, subcortical visual nuclei and primary visual cortex. Brain Res Bull. 75:356–364. doi: 10.1016/j.brainresbull.2007.10.055.
  • Oosthuizen MK, Bennett NC. 2015. The effect of ambient temperature on locomotor activity patterns in reproductive and non‐reproductive female Damaraland mole‐rats. J Zool. 297:1–8.
  • Oosthuizen MK, Bennett NC. 2022. Clocks ticking in the dark: a review of biological rhythms in subterranean African mole-rats. Front Ecol Evol. 10. doi: 10.3389/fevo.2022.878533.
  • Oosthuizen MK, Cooper HM, Bennett NC. 2003. Circadian rhythms of locomotor activity in solitary and social species of African mole-rats (Family: Bathyergidae). J Biol Rhythms. 18:481–490. doi: 10.1177/0748730403259109.
  • Oster H, Avivi A, Joel A, Albrecht U, Nevo E. 2002. A switch from diurnal to nocturnal activity in S. ehrenbergi is accompanied by an uncoupling of light input and the circadian clock. Curr Biol. 12:1919–1922. doi: 10.1016/S0960-9822(02)01263-0.
  • Paganelli R, Petrarca C, Di Gioacchino M. 2018. Biological clocks: their relevance to immune-allergic diseases. Clin Mol Allergy. 16:1–8. doi: 10.1186/s12948-018-0080-0.
  • Peirson SN, Thompson S, Hankins MW, Foster RG. 2005. Mammalian photoentrainment: Results, methods, and approaches. Methods Enzymol. 393:697–726.
  • Rajaratnam SMW, Redman JR. 1998. Entrainment of activity rhythms to temperature cycles in diurnal palm squirrels. Physiol Behav. 63:271–277. doi: 10.1016/S0031-9384(97)00440-X.
  • R Core Team. (2023). R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
  • Refinetti R. 2010. The circadian rhythm of body temperature. Front Biosci. 15:564–594. doi: 10.2741/3634.
  • Refinetti R. 2015. Comparison of light, food, and temperature as environmental synchronizers of the circadian rhythm of activity in mice. J Physiol Sci. 65:359–366. doi: 10.1007/s12576-015-0374-7.
  • Refinetti R, Menaker M. 1992. The circadian rhythm of body temperature. Physiol Behav. 51:613–637. doi: 10.1016/0031-9384(92)90188-8.
  • Rensing L, Ruoff P. 2002. Temperature effect on entrainment, phase shifting, and amplitude of circadian clocks and its molecular bases. Chronobiol Int. 19:807–864. doi: 10.1081/CBI-120014569.
  • Riccio AP, Goldman BD. 2000. Circadian rhythms of locomotor activity in naked mole-rats (Heterocephalus glaber). Physiol Behav. 71:1–13. doi: 10.1016/S0031-9384(00)00281-X.
  • Roper TJ, Bennett NC, Conradt L, Molteno AJ. 2001. Environmental conditions in burrows of two species of African mole-rat, Georhychus capensis and Cryptomys damarensis. J Zool. 254:101–107. doi: 10.1017/S0952836901000590.
  • Serin Y, Acar Tek N. 2019. Effect of circadian rhythm on metabolic processes and the regulation of energy balance. Ann Nutr Metab. 74:322–330. doi: 10.1159/000500071.
  • Šklíba J, Lövy M, Hrouzková E, Kott O, Okrouhlík J, Šumbera R. 2014. Social and environmental influences on daily activity pattern in free-living subterranean rodents: the case of a eusocial bathyergid. J Biol Rhythms. 29:203–214. doi: 10.1177/0748730414526358.
  • Snyman PC, Jackson CR, Bennett NC. 2006. Do dispersing non-reproductive female damaraland mole-rats, cryptomys damarensis (Rodentia: Bathyergidae) exhibit spontaneous or induced ovulation? Physiol Behav. 87:88–94. doi: 10.1016/j.physbeh.2005.09.003.
  • Speakman JR, Król E. 2010. Maximal heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. J Anim Ecol. 79:726–746. doi: 10.1111/j.1365-2656.2010.01689.x.
  • Šumbera R. 2019. Thermal biology of a strictly subterranean mammalian family, the African mole-rats (Bathyergidae, Rodentia) - a review. J Therm Biol. 79:166–189. doi: 10.1016/j.jtherbio.2018.11.003.
  • van Jaarsveld B, Bennett NC, Hart DW, Oosthuizen MK. 2019. Locomotor activity and body temperature rhythms in the mahali mole-rat (C. h. mahali): the effect of light and ambient temperature variations. J Therm Biol. 79:24–32. doi: 10.1016/j.jtherbio.2018.11.013.
  • Vasicek CA, Oosthuizen MK, Cooper HM, Bennett NC. 2005. Circadian rhythms of locomotor activity in the subterranean Mashona mole-rat, Cryptomys darlingi. Physiol Behav. 84:181–191.
  • Vleck D. 1979. The energy cost of burrowing by the pocket gopher thomomys bottae. Physiol Zool. 52:122–136. doi: 10.1086/physzool.52.2.30152558.
  • Voigt C, Medger K, Bennett NC. 2021. The oestrous cycle of the Damaraland mole-rat revisited: evidence for induced ovulation. J Zool. 314:85–95. doi: 10.1111/jzo.12860.
  • Wallace KME, Hart DW, Hagenah N, Ganswindt A, Bennett NC. 2023. A comprehensive profile of reproductive hormones in eusocial Damaraland mole-rats (Fukomys damarensis). Gen Comp Endocrinol. 333:114194. doi: 10.1016/j.ygcen.2022.114194.
  • Wallace KME, van Jaarsveld B, Bennett NC, Hart DW. 2021. The joint effect of micro- and macro-climate on the thermoregulation and heat dissipation of two African mole-rat (Bathyergidae) sub-species, Cryptomys hottentotus mahali and C. h. pretoriae. J Therm Biol. 99:103025. doi: 10.1016/j.jtherbio.2021.103025.

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