Entrainment of circadian rhythms of locomotor activity by ambient temperature cycles in the dromedary camel
1.
Aschoff, J. Circadian activity pattern with two peaks. Ecology 47, 657–662 (1966).
Article Google Scholar
2.
Daan, S. & Aschoff, J. Circadian rhythms of locomotor activity in captive birds and mammals: Their variations with season and latitude. Oecologia 18, 269–316 (1975).
ADS Article PubMed PubMed Central Google Scholar
3.
Katandukila, J. V., Bennett, N. C., Chimimba, C. T., Faulkes, C. G. & Oosthuizen, M. K. Locomotor activity patterns of captive East African root rats, Tachyoryctes splendens (Rodentia: Spalacidae), from Tanzania, East Africa. J. Mamm. 94, 1393–1400 (2013).
Article Google Scholar
4.
Bennie, J. J., Duffy, J. P., Inger, R. & Gaston, K. J. Biogeography of time partitioning in mammals. Proc. Natl. Acad. Sci. U.S.A. 111, 13727–13732 (2014).
ADS CAS Article PubMed PubMed Central Google Scholar
5.
Cloudsley-Thompson, J. L. Rhythmic Activity in Animal Physiology and Behaviour (Academic Press, Cambridge, 1961).
Google Scholar
6.
Aschoff, J., Gercke, H., Pohl, P., Rieger, P. V. & Wever, S. P. U. R. Interdependent parameters of circadian activity rhythms in birds and man. In Biochronometry (ed. Menaker, M.) 3–29 (National Academy of Science, Washington, DC, 1971).
Google Scholar
7.
Risenhoover, K. L. Winter activity patterns of moose in interior Alaska. J. Wildl. Manage. 50, 727–734 (1986).
Article Google Scholar
8.
Castillo-Ruiz, A., Paul, M. J. & Schwartz, W. J. In search of a temporal niche: Social interactions. Prog. Brain Res. 199, 267–280 (2012).
Article PubMed PubMed Central Google Scholar
9.
Kronfeld-Schor, N., Visser, M. E., Salis, L. & van Gils, J. A. Chronobiology of interspecific interactions in a changing world. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. https://doi.org/10.1098/rstb.2016.0248 (2017).
Article Google Scholar
10.
Farsi, H. et al. Validation of locomotion scoring as a new and inexpensive technique to record circadian locomotor activity in large mammals. Heliyon 4, e00980–e00980 (2018).
CAS Article PubMed PubMed Central Google Scholar
11.
El Allali, K. et al. Smartphone and a freely available application as a new tool to record locomotor activity rhythm in large mammals and humans. Chronobiol. Int. 36, 1047–1057 (2019).
Article PubMed Google Scholar
12.
Schmidt-Nielsen, K., Schmidt-Nielsen, B., Jarnum, S. A. & Houpt, T. R. Body temperature of the camel and its relation to water economy. Am. J. Physiol. 188, 103–112 (1957).
CAS Article PubMed Google Scholar
13.
Bouâouda, H. et al. Daily regulation of body temperature rhythm in the camel (Camelus dromedarius) exposed to experimental desert conditions. Physiol. Rep. 2, e12151 (2014).
Article PubMed PubMed Central Google Scholar
14.
El Allali, K. et al. Entrainment of the circadian clock by daily ambient temperature cycles in the camel (Camelus dromedarius). Am. J. Physiol. Regul. Integr. Comp. Physiol. 304, R1044–R1052 (2013).
Article CAS PubMed Google Scholar
15.
Farsi, H. et al. 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 (2020).
CAS Article PubMed Google Scholar
16.
Ebling, F. J., Lincoln, G. A., Wollnik, F. & Anderson, N. Effects of constant darkness and constant light on circadian organization and reproductive responses in the ram. J. Biol. Rhythms 3, 365–384 (1988).
CAS Article PubMed Google Scholar
17.
Johnson, R. F., Randall, S. & Randall, W. Freerunning and entrained circadian rhythms in activity, eating and drinking in the cat. J. Interdiscipl. Cycle Res. 14, 315–327 (1983).
Article Google Scholar
18.
Jilge, B., Hörnicke, H. & Stähle, H. Circadian rhythms of rabbits during restrictive feeding. Am. J. Physiol. 253, R46–R54 (1987).
CAS PubMed Google Scholar
19.
Decoursey, G. & Decoursey, P. J. Adaptive aspects of activity rhythms in bats. Biol. Bull. 126, 14–27 (1964).
Article Google Scholar
20.
Erkert, H. G., Nagel, B. & Stephani, I. Light and social effects on the free-running circadian activity rhythm in common marmosets (Callithrix jacchus; Primates): Social masking, pseudo-splitting, and relative coordination. Behav. Ecol. Sociobiol. 18, 443–452 (1986).
Article Google Scholar
21.
O’Reilly, H., Armstrong, S. M. & Coleman, G. J. Restricted feeding and circadian activity rhythms of a predatory marsupial, Dasyuroides byrnei. Physiol. Behav. 38, 471–476 (1986).
CAS Article PubMed Google Scholar
22.
Boulos, Z., Frim, D. M., Dewey, L. K. & Moore-Ede, M. C. Effects of restricted feeding schedules on circadian organization in squirrel monkeys. Physiol. Behav. 45, 507–515 (1989).
CAS Article PubMed Google Scholar
23.
Mahoney, M., Bult, A. & Smale, L. Phase response curve and light-induced fos expression in the suprachiasmatic nucleus and adjacent hypothalamus of Arvicanthis niloticus. J. Biol. Rhythms 16, 149–162 (2001).
CAS Article PubMed Google Scholar
24.
Alagaili, A. N., Bennett, N. C., Amor, N. M. & Hart, D. W. The locomotory activity patterns of the arid-dwelling desert hedgehog, Paraechinus aethiopicus, from Saudi Arabia. J. Arid Environ. 177, 104141 (2020).
ADS Article Google Scholar
25.
Verwey, M., Robinson, B. & Amir, S. Recording and analysis of circadian rhythms in running-wheel activity in rodents. J. Vis. Exp. https://doi.org/10.3791/50186 (2013).
Article PubMed PubMed Central Google Scholar
26.
Refinetti, R. Early research on circadian rhythms. In Circadian Physiology 2nd edn (ed. Refinetti, R.) 1–667 (CRC Taylor and Frabcis Group, Boca Raton, 2006).
Google Scholar
27.
Goldman, B. D., Goldman, S. L., Riccio, A. P. & Terkel, J. Circadian patterns of locomotor activity and body temperature in blind mole-rats, Spalax ehrenbergi. J. Biol. Rhythms 12, 348–361 (1997).
CAS Article PubMed Google Scholar
28.
Kopp, C. et al. Effects of a daylight cycle reversal on locomotor activity in several inbred strains of mice. Physiol. Behav. 63, 577–585 (1998).
CAS Article PubMed Google Scholar
29.
Giannetto, C., Casella, S., Caola, G. & Piccione, G. Photic and non-photic entrainment on daily rhythm of locomotor activity in goats. Anim. Sci. J. 81, 122–128 (2010).
Article PubMed Google Scholar
30.
Piccione, G., Giannetto, C., Casella, S. & Caola, G. Daily locomotor activity in five domestic animals. Anim. Biol. 60, 15–24 (2010).
Article Google Scholar
31.
Challet, E. Minireview: Entrainment of the suprachiasmatic clockwork in diurnal and nocturnal mammals. Endocrinology 148, 5648–5655 (2007).
CAS Article PubMed PubMed Central Google Scholar
32.
Dibner, C., Schibler, U. & Albrecht, U. The mammalian circadian timing system: Organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 72, 517–549 (2010).
CAS Article PubMed PubMed Central Google Scholar
33.
Tanaka, M., Ichitani, Y., Okamura, H., Tanaka, Y. & Ibata, Y. The direct retinal projection to VIP neuronal elements in the rat SCN. Brain Res. Bull. 31, 637–640 (1993).
CAS Article PubMed PubMed Central Google Scholar
34.
Jacomy, H., Burlet, A. & Bosler, O. Vasoactive intestinal peptide neurons as synaptic targets for vasopressin neurons in the suprachiasmatic nucleus. Double-label immunocytochemical demonstration in the rat. Neuroscience 88, 859–870 (1999).
CAS Article PubMed PubMed Central Google Scholar
35.
Aton, S. J., Colwell, C. S., Harmar, A. J., Waschek, J. & Herzog, E. D. Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat. Neurosci. 8, 476–483 (2005).
CAS Article PubMed PubMed Central Google Scholar
36.
Reppert, S. M. & Weaver, D. R. Comparing clockworks: Mouse versus fly. J. Biol. Rhythms 15, 357–364 (2000).
CAS Article PubMed PubMed Central Google Scholar
37.
Reppert, S. M. & Weaver, D. R. Molecular analysis of mammalian circadian rhythms. Annu. Rev. Physiol. 63, 647–676 (2001).
CAS Article PubMed PubMed Central Google Scholar
38.
Shearman, L. P. et al. Interacting molecular loops in the mammalian circadian clock. Science 288, 1013–1019 (2000).
ADS CAS Article PubMed PubMed Central Google Scholar
39.
Okamura, H., Yamaguchi, S. & Yagita, K. Molecular machinery of the circadian clock in mammals. Cell Tissue Res. 309, 47–56 (2002).
CAS Article Google Scholar
40.
Takahashi, J. S., Hong, H. K., Ko, C. H. & McDearmon, E. L. The genetics of mammalian circadian order and disorder: Implications for physiology and disease. Nat. Rev. Genet. 9, 764–775 (2008).
CAS Article PubMed PubMed Central Google Scholar
41.
Mohawk, J. A., Green, C. B. & Takahashi, J. S. Central and peripheral circadian clocks in mammals. Annu. Rev. Neurosci. 35, 445–462 (2012).
CAS Article PubMed PubMed Central Google Scholar
42.
Rensing, L. & Ruoff, P. Temperature effect on entrainment, phase shifting, and amplitude of circadian clocks and its molecular bases. Chronobiol. Int. 19, 807–864 (2002).
CAS Article PubMed Google Scholar
43.
Aschoff, J. & Tokura, H. Circadian activity rhythms in squirrel monkeys: Entrainment by temperature cycles 1. J. Biol. Rhythms 1, 91–99 (1986).
CAS Article PubMed Google Scholar
44.
Pálková, M., Sigmund, L. & Erkert, H. G. Effect of ambient temperature on the circadian activity rhythm in common marmosets, Callithrix j jacchus (primates). Chronobiol. Int. 16, 149–161 (1999).
Article PubMed Google Scholar
45.
Rajaratnam, S. M. W. & Redman, J. R. Entrainment of activity rhythms to temperature cycles in diurnal palm squirrels. Physiol. Behav. 63, 271–277 (1998).
CAS Article PubMed Google Scholar
46.
Refinetti, R. Entrainment of circadian rhythm by ambient temperature cycles in mice. J. Biol. Rhythms 25, 247–256 (2010).
Article Google Scholar
47.
van Jaarsveld, B., Bennett, N. C., Hart, D. W. & Oosthuizen, M. K. 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 (2019).
Article Google Scholar
48.
Schmidt-Nielsen, K. The physiology of the camel. Sci. Am. 201, 140–151 (1959).
CAS Article PubMed PubMed Central Google Scholar
49.
Wu, H. et al. Camelid genomes reveal evolution and adaptation to desert environments. Nat. Commun. 5, 5188 (2014).
ADS CAS Article PubMed PubMed Central Google Scholar
50.
Samara, E. M. Unraveling the relationship between the topographic distribution patterns of skin temperature and perspiration response in dromedary camels. J. Therm. Biol 84, 311–315 (2019).
Article PubMed Google Scholar
51.
Tibary, A. & El Allali, K. Dromedary camel: A model of heat resistant livestock animal. Theriogenology 154, 203–211 (2020).
Article PubMed Google Scholar
52.
Lindberg, R. G. & Hayden, P. Thermoperiodic entrainment of arousal from torpor in the little pocket mouse, Perognathus longimembris. Chronobiologia 1, 356–361 (1974).
CAS PubMed Google Scholar
53.
Erkert, H. G. & Rothmund, E. Differences in temperature sensitivity of the circadian systems of homoeothermic and heterothermic neotropical bats. Comp. Biochem. Physiol. 68A, 383–390 (1980).
Google Scholar
54.
Pohl, H. Temperature cycles as zeitgeber for the circadian clock of two burrowing rodents, the normothermic antelope ground squirrel and the heterothermic Syrian Hamster. Biol. Rhythm Res. 29, 311–325 (1998).
Article Google Scholar
55.
Cain, J. W., Krausman, P. R., Rosenstock, S. S. & Turner, J. C. Mechanisms of thermoregulation and water balance in Desert Ungulates. Wildl. Soc. Bull. 1973–2006(34), 570–581 (2006).
Article Google Scholar
56.
Mengistu, U., Dahlborn, K. & Olsson, K. Mechanisms of water economy in lactating Ethiopian Somali goats during repeated cycles of intermittent watering. Anim. Int. J. Anim. Biosci. 1, 1009–1017 (2007).
CAS Article Google Scholar
57.
Gauthier-Pilters, H. Aspects of dromedary ecology and ethology. In The Camelid (ed. Cockrill, W. R.) (Scandinavian Institute of African Studies, Uppsala, 1984).
Google Scholar
58.
Miller, G. D., Cochran, M. H. & Smith, E. L. Nighttime activity of desert bighorn sheep. Desert Bighorn Council Trans. 28, 23–25 (1984).
Google Scholar
59.
Hayes, C. L. & Krausman, P. R. Nocturnal activity of female desert mule deer. J. Wildl. Manage. 57, 897–904 (1993).
Article Google Scholar
60.
Davimes, J. G. et al. Temporal niche switching in Arabian oryx (Oryx leucoryx): Seasonal plasticity of 24h activity patterns in a large desert mammal. Physiol. Behav. 177, 148–154 (2017).
CAS Article PubMed Google Scholar
61.
Davimes, J. G. et al. Seasonal variations in sleep of free-ranging Arabian oryx (Oryx leucoryx) under natural hyperarid conditions. Sleep https://doi.org/10.1093/sleep/zsy038 (2018).
Article PubMed Google Scholar
62.
El Allali, K. et al. Seasonal variations in the nycthemeral rhythm of plasma melatonin in the camel (Camelus dromedarius). J. Pineal Res. 39, 121–128 (2005).
Article CAS PubMed Google Scholar
63.
Mrosovsky, N. Circannual cycles in golden-mantled ground squirrels: Phase shift produced by low temperature. J. Comp. Physiol. 136, 349–353 (1980).
Article Google Scholar
64.
Mrosovsky, N. Circannual cycles in golden-mantled ground squirrels: Experiments with food deprivation and effects of temperature on periodicity. J. Comp. Physiol. 136, 355–360 (1980).
Article Google Scholar
65.
Mrosovsky, N. Thermal effects on the periodicity, phasing and peristance of circannual cycles. In Living in the Cold (eds Heller, H. C. et al.) 403–410 (Elsevier, New York, 1986).
Google Scholar
66.
Mrosovsky, N. Circannual cycles in golden-mantled ground squirrels: fall and spring cold pulses. J. Comp. Physiol. 167, 683–689 (1990).
Article Google Scholar
67.
Canguilhem, B., Schieber, J. P. & Koch, A. Circannual weight rhythm of the European hamster (Cricetus cricetus). Respective influence of the photoperiod and external temperature during its course. Arch. Sci. Physiol. 27, 67–90 (1973).
CAS Google Scholar
68.
Jallageas, M. & Assenmacher, I. External factors controlling annual testosterone and thyroxine cycles in the edible dormouse Glis glis. Comp. Biochem. Physiol. A Physiol. 77, 161–167 (1984).
CAS Article Google Scholar
69.
Touitou, Y., Smolensky, M. H. & Portaluppi, F. Ethics, standards, and procedures of animal and human chronobiology research. Chronobiol. Int. 23, 1083–1096 (2006).
Article PubMed Google Scholar More