Journal Home > Volume 14 , Issue 3

Light is an essential environmental cue influencing the endogenous circadian clocks that regulate behavioral and physiological processes in animals. Despite extensive research on the circadian rhythms of avian behavior and physiology, the mechanisms by which they adapt and adjust to abnormal photoperiod conditions, such as artificial light, have yet to be fully elucidated. Here, the circadian rhythms of the body mass, activity, and core and peripheral body temperatures of the Eurasian Tree Sparrow (Passer montanus, ETS)—a diurnal passerine—were examined under three different lighting conditions: constant light (LL), constant darkness (DD), and normal light–dark cycles (LD). Our results showed that the activity, body mass, core, tarsometatarsus, and eye temperatures of the ETSs varied significantly with treatment, time, and the interaction between treatment and time; however, there was no significant change in body mass in response to the interaction between time and treatment. Under LD conditions, the ETSs exhibited significant circadian rhythms in activity and core, tarsometatarsus, and eye temperatures. Under LL conditions, only the core temperature exhibited significant rhythmicity. Under DD conditions, there were no significant circadian rhythms in activity, body mass, and eye temperature; however, the core and tarsometatarsus temperatures remained rhythmic. Our results indicate that the core body temperature rhythm of ETS is endogenous and can be maintained under abnormal photoperiods. In contrast, the activity and body surface temperature, uncoupled from the core body temperature under abnormal photoperiod conditions, strongly depend on light. These results differ from those of other diurnal avian species, suggesting a unique coping mechanism of ETS in response to an abnormal photoperiod.


menu
Abstract
Full text
Outline
About this article

Effects of constant light and dark conditions on the locomotor activity, body mass, and body temperature rhythms of Eurasian Tree Sparrows (Passer montanus)

Show Author's information Lirong Zuoa,bIbrahim M. Ahmada,bYuanyuan LiuaLimin Wanga,bShu FangaDongming Lia,b( )
Hebei Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang, 050024, Hebei Province, China
Hebei Collaborative Innovation Center for Eco-Environment, Hebei Normal University, Shijiazhuang, 050024, China

Abstract

Light is an essential environmental cue influencing the endogenous circadian clocks that regulate behavioral and physiological processes in animals. Despite extensive research on the circadian rhythms of avian behavior and physiology, the mechanisms by which they adapt and adjust to abnormal photoperiod conditions, such as artificial light, have yet to be fully elucidated. Here, the circadian rhythms of the body mass, activity, and core and peripheral body temperatures of the Eurasian Tree Sparrow (Passer montanus, ETS)—a diurnal passerine—were examined under three different lighting conditions: constant light (LL), constant darkness (DD), and normal light–dark cycles (LD). Our results showed that the activity, body mass, core, tarsometatarsus, and eye temperatures of the ETSs varied significantly with treatment, time, and the interaction between treatment and time; however, there was no significant change in body mass in response to the interaction between time and treatment. Under LD conditions, the ETSs exhibited significant circadian rhythms in activity and core, tarsometatarsus, and eye temperatures. Under LL conditions, only the core temperature exhibited significant rhythmicity. Under DD conditions, there were no significant circadian rhythms in activity, body mass, and eye temperature; however, the core and tarsometatarsus temperatures remained rhythmic. Our results indicate that the core body temperature rhythm of ETS is endogenous and can be maintained under abnormal photoperiods. In contrast, the activity and body surface temperature, uncoupled from the core body temperature under abnormal photoperiod conditions, strongly depend on light. These results differ from those of other diurnal avian species, suggesting a unique coping mechanism of ETS in response to an abnormal photoperiod.

Keywords: Circadian rhythm, Activity, Eurasian Tree Sparrow, Body mass, Body temperature

References(67)

Al-Hasani, H., Tschop, M.H., Cushman, S.W., 2003. Two birds with one stone: novel glucokinase activator stimulates glucose-induced pancreatic insulin secretion and augments hepatic glucose metabolism. Mol. Interv. 3, 367–370. https://doi.org/10.1124/mi.3.7.367.

Appenroth, D., Nord, A., Hazlerigg, D.G., Wagner, G.C., 2021. Body temperature and activity rhythms under different photoperiods in high arctic Svalbard ptarmigan (Lagopus muta hyperborea). Front. Physiol. 12, 633866. https://doi.org/10.3389/fphys.2021.633866.

Benstaali, C., Mailloux, A., Bogdan, A., Auzeby, A., Touitou, Y., 2001. Circadian rhythms of body temperature and motor activity in rodents: their relationships with the light-dark cycle. Life Sci. 68, 2645–2656. https://doi.org/10.1016/S0024-3205(01)01081-5.

Binkley, S., Kluth, E., Menaker, M., 1971. Pineal function in sparrows: circadian rhythms and body temperature. Science 174, 311–314. https://doi.org/10.1126/science.174.4006.311.

Binkley, S., Mosher, K., 1986. Photoperiod modifies circadian resetting responses in sparrows. Am. J. Physiol. 251, R1156-R1162. https://doi.org/10.1152/ajpregu.1986.251.6.R1156.

Borniger, J.C., Maurya, S.K., Periasamy, M., Nelson, R.J., 2014. Acute dim light at night increases body mass, alters metabolism, and shifts core body temperature circadian rhythms. Chronobiol. Int. 31, 917–925. https://doi.org/10.3109/07420528.2014.926911.

Boshouwers, F., Nicaise, E., 1987. Physical activity and energy expenditure of laying hens as affected by light intensity. Br. Poultry Sci. 28, 155–163. https://doi.org/10.1080/00071668708416947.

Brandstaetter, R., 2002. The circadian pacemaking system of birds. In: Kumar, V. (Ed.), Biological Rhythms. Springer, Berlin, Heidelberg, pp. 144-163. https://doi.org/10.1007/978-3-662-06085-8_13.
DOI

Bronstein, D.M., Haak, K.A., Torres, G., Lytle, L.D., 1990. Light-induced changes in pineal gland N-acetyltransferase activity: developmental aspects. Neuroendocrinology 51, 139–146. https://doi.org/10.1159/000125329.

Budki, P., Rani, S., Kumar, V., 2012. Persistence of circannual rhythms under constant periodic and aperiodic light conditions: sex differences and relationship with the external environment. J. Exp. Biol. 215, 3774–3785. https://doi.org/10.1242/jeb.065581.

Buhr, E.D., Takahashi, J.S., 2013. Molecular components of the mammalian circadian clock. In: Kramer, A., Merrow, M. (Eds.), Circadian Clocks, Handbook of Experimental Pharmacology, vol. 217. Springer, Berlin, pp. 3-27. https://doi.org/10.1007/978-3-642-25950-0_1.
DOI

Cassone, V.M., 2014. Avian circadian organization: a chorus of clocks. Front. Neuroendocrinol. 35, 76–88. https://doi.org/10.1016/j.yfrne.2013.10.002.

Cassone, V.M., Paulose, J.K., Whitfield-Rucker, M.G., Peters, J.L., 2009. Time's arrow flies like a bird: two paradoxes for avian circadian biology. Gen. Comp. Endocrinol. 163, 109–116. https://doi.org/10.1016/j.ygcen.2009.01.003.

Coomans, C.P., van den Berg, S.A., Houben, T., van Klinken, J.B., van den Berg, R., Pronk, A.C., et al., 2013. Detrimental effects of constant light exposure and high-fat diet on circadian energy metabolism and insulin sensitivity. Faseb. J. 27, 1721–1732. https://doi.org/10.1096/fj.12-210898.

Coverdill, A.J., Bentley, G.E., Ramenofsky, M., 2008. Circadian and masking control of migratory restlessness in Gambel's white-crowned sparrow (Zonotrichia leucophrys gambelii). J. Biol. Rhythm. 23, 59–68. https://doi.org/10.1177/0748730407311456.

Dawson, A., King, V.M., Bentley, G.E., Ball, G.F., 2001. Photoperiodic control of seasonality in birds. J. Biol. Rhythm. 16, 365–380. https://doi.org/10.1177/074873001129002079.

Dawson, A., Sharp, P.J., 2007. Photorefractoriness in birds-photoperiodic and non-photoperiodic control. Gen. Comp. Endocrinol. 153, 378–384. https://doi.org/10.1016/j.ygcen.2007.01.043.

Depres-Brummer, P., Levi, F., Metzger, G., Touitou, Y., 1995. Light-induced suppression of the rat circadian system. Am. J. Physiol. 268, R1111-R1116. https://doi.org/10.1152/ajpregu.1995.268.5.R1111.

Dixit, A.S., Byrsat, S., Kataki, B., 2022. Hypothalamic expression of GnRH-Ⅰ and GnIH in the Eurasian tree sparrow over a single long day. Photochem. Photobiol. Sci. 21, 147–158. https://doi.org/10.1007/s43630-021-00143-6.

Dixit, A.S., Singh, N.S., 2011. Photoperiod as a proximate factor in control of seasonality in the subtropical male Tree Sparrow, Passer montanus. Front. Zool. 8, 1. https://doi.org/10.1186/1742-9994-8-1.

Dixit, A.S., Singh, N.S., 2012. Seasonal variation in sensitivity of the photoperiodic response system in the subtropical tree sparrow (Passer montanus). J. Exp. Zool. A Ecol. Genet. Physiol. 317, 488–498. https://doi.org/10.1002/jez.1741.

Dominoni, D.M., 2015. The effects of light pollution on biological rhythms of birds: an integrated, mechanistic perspective. J. Ornithol. 156, 409–418. https://doi.org/10.1007/s10336-015-1196-3.

Ebihara, S., Kawamura, H., 1981. The role of the pineal organ and the suprachiasmatic nucleus in the control of circadian locomotor rhythms in the Java sparrow, Padda oryzivora. J. Comp. Physiol. 141, 207–214. https://doi.org/10.1007/bf01342667.

Ebihara, S., Uchiyama, K., Oshima, I., 1984. Circadian organization in the pigeon, Columba livia: the role of the pineal organ and the eye. J. Comp. Physiol. 154, 59–69. https://doi.org/10.1007/BF00605391.

Farsi, H., Harti, D., Achaaban, M.R., Piro, M., Raverot, V., Bothorel, B., et al., 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. https://doi.org/10.1111/jpi.12634.

Fonken, L.K., Nelson, R.J., 2014. The effects of light at night on circadian clocks and metabolism. Endocr. Rev. 35, 648–670. https://doi.org/10.1210/er.2013-1051.

Fonken, L.K., Workman, J.L., Walton, J.C., Weil, Z.M., Morris, J.S., Haim, A., et al., 2010. Light at night increases body mass by shifting the time of food intake. Proc. Natl. Acad. Sci. USA 107, 18664–18669. https://doi.org/10.1073/pnas.1008734107.

Gaston, S., Menaker, M., 1968. Pineal function: the biological clock in the sparrow? Science 160, 1125–1127. https://doi.org/10.1126/science.160.3832.1125.

Giloh, M., Shinder, D., Yahav, S., 2012. Skin surface temperature of broiler chickens is correlated to body core temperature and is indicative of their thermoregulatory status. Poultry Sci. 91, 175–188. https://doi.org/10.3382/ps.2011-01497.

Grunst, A.S., Grunst, M.L., Raap, T., Pinxten, R., Eens, M., 2023. Anthropogenic noise and light pollution additively affect sleep behaviour in free-living birds in sex-and season-dependent fashions. Environ. Pollut. 316, 120426. https://doi.org/10.1016/j.envpol.2022.120426.

Gwinner, E., 1978. Effects of pinealectomy on circadian locomotor activity rhythms in European starlings, Sturnus vulgaris. J. Comp. Physiol. 126, 123–129. https://doi.org/10.1007/BF00666364.

Harmening, W.M., 2017. Contrast sensitivity and visual acuity in animals. Ophthalmologe 114, 986–996. https://doi.org/10.1007/s00347-017-0561-4.

Hohtola, E., Stevens, E.D., 1986. The relationship of muscle electrical activity, tremor and heat production to shivering thermogenesis in Japanese quail. J. Exp. Biol. 125, 119–135. https://doi.org/10.1242/jeb.125.1.119.

Hughes, M.E., Hogenesch, J.B., Kornacker, K., 2010. JTK_CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J. Biol. Rhythm. 25, 372–380. https://doi.org/10.1177/0748730410379711.

Hurly, T.A., 1992. Energetic reserves of marsh tits (Parus palustris): food and fat storage in response to variable food supply. Behav. Ecol. 3, 181–188. https://doi.org/10.1093/beheco/3.2.181.

Jiang, J.X., He, Y., Kou, H.H., Ju, Z.Q., Gao, X.B., Zhao, H.F., 2020. The effects of artificial light at night on Eurasian tree sparrow (Passer montanus): behavioral rhythm disruption, melatonin suppression and intestinal microbiota alterations. Ecol. Indicat. 108. https://doi.org/10.1016/j.ecolind.2019.105702, 105702–105702.

Kontogiannis, J.E., 1967. Day and night changes in body weight of the White-throated Sparrow, Zonotrichia albicollis. Auk 84, 390–395. https://doi.org/10.2307/4083088.

Le Tallec, T., Perret, M., Théry, M., 2013. Light pollution modifies the expression of daily rhythms and behavior patterns in a nocturnal primate. PLoS One 8, e79250. https://doi.org/10.1371/journal.pone.0079250.

Li, D., Wang, G., Wingfield, J.C., Zhang, Z., Ding, C., Lei, F., 2008. Seasonal changes in adrenocortical responses to acute stress in Eurasian tree sparrow (Passer montanus) on the Tibetan Plateau: comparison with house sparrow (P. domesticus) in North America and with the migratory P. domesticus in Qinghai Province. Gen. Comp. Endocrinol. 158, 47–53. https://doi.org/10.1016/j.ygcen.2008.06.002.

Li, D., Wu, J., Zhang, X., Ma, X., Wingfield, J.C., Lei, F., et al., 2011. Comparison of adrenocortical responses to acute stress in lowland and highland Eurasian tree sparrows (Passer montanus): similar patterns during the breeding, but different during the prebasic molt. J. Exp. Zool. A Ecol. Genet. Physiol. 315, 512–519. https://doi.org/10.1002/jez.699.

Li, D., Zhang, X., Li, Y., Hao, C., Zhang, J., Wu, Y., et al., 2012. Stress responses of testosterone and corticosterone-binding globulin in a multi-brooded species, Eurasian Tree Sparrows (Passer montanus): Does CBG function as a mediator? Horm. Behav. 61, 582–589. https://doi.org/10.1016/j.yhbeh.2012.02.007.

Li, Y., Sun, Y., Krause, J.S., Li, M., Liu, X., Zhu, W., et al., 2017. Dynamic interactions between corticosterone, corticosteroid binding globulin and testosterone in response to capture stress in male breeding Eurasian tree sparrows. Comp. Biochem. Physiol. A 205, 41–47. https://doi.org/10.1016/j.cbpa.2016.12.016.

Lucia, M., Andre, J.M., Gonzalez, P., Baudrimont, M., Bernadet, M.D., Gontier, K., et al., 2010. Effect of dietary cadmium on lipid metabolism and storage of aquatic bird Cairina moschata. Ecotoxicology 19, 163–170. https://doi.org/10.1007/s10646-009-0401-7.

McMillan, J., 1972. Pinealectomy abolishes the circadian rhythm of migratory restlessness. J. Comp. Physiol. 79, 105–112. https://doi.org/10.1007/BF00697766.

Montoya, A., Lopez-Olmeda, J.F., Garayzar, A.B., Sanchez-Vazquez, F.J., 2010. Synchronization of daily rhythms of locomotor activity and plasma glucose, cortisol and thyroid hormones to feeding in Gilthead seabream (Sparus aurata) under a light-dark cycle. Physiol. Behav. 101, 101–107. https://doi.org/10.1016/j.physbeh.2010.04.019.

Mosher, J.A., White, C.M., 1978. Falcon temperature regulation. Auk 95, 80–84. https://doi.org/10.2307/4085497.

Oshima, I., Yamada, H., Goto, M., Sato, K., Ebihara, S., 1989. Pineal and retinal melatonin is involved in the control of circadian locomotor activity and body temperature rhythms in the pigeon. J. Comp. Physiol. 166, 217–226. https://doi.org/10.1007/BF00193466.

Pandey, R.K., Bhardwaj, S.K., 2011. Circadian and seasonal responses in Indian weaver bird: subjective interpretation of day and night depends upon both light intensity and contrast between illuminations. Chronobiol. Int. 28, 758–763. https://doi.org/10.3109/07420528.2011.603873.

Plano, S.A., Casiraghi, L.P., García Moro, P., Paladino, N., Golombek, D.A., Chiesa, J.J., 2017. Circadian and metabolic effects of light: implications in weight homeostasis and health. Front. Neurol. 8, 558. https://doi.org/10.3389/fneur.2017.00558.

Porcu, A., Riddle, M., Dulcis, D., Welsh, D.K., 2018. Photoperiod-induced neuroplasticity in the circadian system. Neural Plast. 2018, 5147585. https://doi.org/10.1155/2018/5147585.

Prabhat, A., Malik, I., Jha, N.A., Bhardwaj, S.K., Kumar, V., 2020. Developmental effects of constant light on circadian behaviour and gene expressions in zebra finches: Insights into mechanisms of metabolic adaptation to aperiodic environment in diurnal animals. J. Photochem. Photobiol. B 211, 111995. https://doi.org/10.1016/j.jphotobiol.2020.111995.

Ramkisoensing, A., Meijer, J., 2015. Synchronization of biological clock neurons by light and peripheral feedback systems promotes circadian rhythms and health. Front. Neurol. 6, 128. https://doi.org/10.3389/fneur.2015.00128.

Ravikumar, G., Tewary, P.D., 1990. Photo refractoriness and its termination in the subtropical house sparrow, Passer domesticus: involvement of circadian rhythm. Chronobiol. Int. 7, 187–191. https://doi.org/10.3109/07420529009056974.

Refinetti, R., Menaker, M., 1992. The circadian rhythm of body temperature. Physiol. Behav. 51, 613–637. https://doi.org/10.1016/0031-9384(92)90188-8.

Regas, P.P., 1998. Circadian rhythms of body temperature and metabolic rate in the House Sparrow (Passer domesticus). Honors Theses. St. John's University, New York. https://digitalcommons.csbsju.edu/honors_theses/653.

Spoelstra, K., Verhagen, I., Meijer, D., Visser, M.E., 2018. Artificial light at night shifts daily activity patterns but not the internal clock in the great tit (Parus major). Proc. Biol. Sci. 285, 20172751. https://doi.org/10.1098/rspb.2017.2751.

Stenvers, D.J., van Dorp, R., Foppen, E., Mendoza, J., Opperhuizen, A.L., Fliers, E., et al., 2016. Dim light at night disturbs the daily sleep-wake cycle in the rat. Sci. Rep. 6, 35662. https://doi.org/10.1038/srep35662.

Tosini, G., Menaker, M., 1995. Circadian rhythm of body temperature in an ectotherm (Iguana iguana). J. Biol. Rhythm. 10, 248–255. https://doi.org/10.1177/074873049501000307.

Trivedi, A.K., Rani, S., Kumar, V., 2005. Differential responses of the photoperiodic clock in two passerine birds possessing a strongly self-sustained circadian system. Chronobiol. Int. 22, 801–806. https://doi.org/10.1080/07420520500263151.

Underwood, H., Steele, C.T., Zivkovic, B., 1999. Effects of fasting on the circadian body temperature rhythm of Japanese quail. Physiol. Behav. 66, 137–143. https://doi.org/10.1016/S0031-9384(98)00287-X.

van Jaarsveld, B., Bennett, N.C., Hart, D.W., Oosthuizen, M.K., 2019. Locomotor activity and body temperature rhythms in the Mahali mole-rat (Cryptomys hottentotus mahali): The effect of light and ambient temperature variations. J. Therm. Biol. 79, 24–32. https://doi.org/10.1016/j.jtherbio.2018.11.013.

Wang, L., Nabi, G., Zhang, L., Liu, D., Li, M., Li, J., et al., 2022. Seasonal variations in gonad morphology and hypothalamic GnRH-Ⅰ and GnIH in Eurasian Tree Sparrow, a multi-brooded passerine. Avian Res. 13, 100037. https://doi.org/10.1016/j.avrs.2022.100037.

West, A.C., Smith, L., Ray, D.W., Loudon, A.S.I., Brown, T.M., Bechtold, D.A., 2017. Misalignment with the external light environment drives metabolic and cardiac dysfunction. Nat. Commun. 8, 417. https://doi.org/10.1038/s41467-017-00462-2.

Wideman, C.H., Murphy, H.M., 2009. Constant light induces alterations in melatonin levels, food intake, feed efficiency, visceral adiposity, and circadian rhythms in rats. Nutr. Neurosci. 12, 233–240. https://doi.org/10.1179/147683009X423436.

Wyse, C.A., Selman, C., Page, M.M., Coogan, A.N., Hazlerigg, D.G., 2011. Circadian desynchrony and metabolic dysfunction; did light pollution make us fat? Med. Hypotheses 77, 1139–1144. https://doi.org/10.1016/j.mehy.2011.09.023.

Yamada, H., Oshima, I., Sato, K., Ebihara, S., 1988. Loss of the circadian rhythms of locomotor activity, food intake, and plasma melatonin concentration induced by constant bright light in the pigeon (Columba livia). J. Comp. Physiol. 163, 459–463. https://doi.org/10.1007/BF00604900.

Zhang, X.J., Yang, W.Y., Liang, W., Wang, Y., Zhang, S.P., 2019. Intensity dependent disruptive effects of light at night on activation of the HPG axis of tree sparrows (Passer montanus). Environ. Pollut. 249, 904–909. https://doi.org/10.1016/j.envpol.2019.03.008.

Publication history
Copyright
Rights and permissions

Publication history

Received: 27 July 2023
Accepted: 01 August 2023
Published: 15 August 2023
Issue date: September 2023

Copyright

© 2023 The Authors.

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return