Body Temperature Patterns in Captive Barbary Striped Grass Mousse (Lemniscomysbarbarus): Influence of Photoperiod and Sex Steroids
DOI:
https://doi.org/10.14738/tmlai.54.2970Keywords:
Body Temperature, Daily Torpor, Photoperiod, Light-Dark Cycle, Diurnality, LemniscomysbarbarusAbstract
This study use miniature temperature-sensitive data loggers to record core body temperature (Tb) in Lemniscomysbarbarus, a diurnal Muridae rodent living in Africa. The work shows the existence of a strong and bimodal daily Tb rhythm in this species whose external synchronizer is the light-dark cycle; it’s also confirmed the diurnal and photoperiodic character of this animal. The highest values of Tb were registered during the light-phase in anti-phase with the nocturnal species. In the experimental conditions of this work Lemniscomysbarbarus do not express the phenomenon of diurnal torpor. Nevertheless, this characteristic mechanism of energy saving in small-sized mammals could be appearing by the association of the combined effects of short photoperiod, low ambient temperature and limited food supply.
References
(1) Benstaali C., Bogdan A., Touitou Y., 2002. Effect of a short photoperiod on circadian rhythms of body temperature and motor activity in old rats. Pflugers Arch.444(1-2):73-79.
(2) Biggar K.K., Wu C.W., Tessier S.N., Zhang J., Pifferi F., Perret M., Storey K.B., 2015. Primate Torpor: Regulation of Stress-activated Protein Kinases During Daily Torpor in the Gray Mouse Lemur, Microcebus murinus. Genomics Proteomics Bioinformatics. 13:81-90.
(3) Blank J.L., Desjardins C., 1984. Spermatogenesis is modified by food intake in mice. Biol. Reprod. 30: 410-415.
(4) Challet E., Pitrosky B., Sicard B., Malan A., Pévet P., 2002. Circadian organization in a diurnal rodent, Arvicanthis ansorgei Thomas 1910: chronotypes, responses to constant lighting conditions and photoperiodic changes. J. Biol. Rhythms. 17:52–64.
(5) Chakir I., 2014. Rôle du gène horloge Clock dans l’intégration de la photopériode par les noyaux suprachiasmatiques chez un rongeur nocturne, Mesocricetus auratus, et dans le déterminisme de la diurnalité chez un rongeur diurne, Lemniscomys barbarus. Doctoral thesis at the Abdelmalek Essaâdi University, Tétouan, Morocco.
(6) Cuesta M., Clesse D., Pévet P., Challet E., 2009. From daily behavior to hormonal and neurotransmitters rhythms: Comparison between diurnal and nocturnal rat species. Hormones and Behavior. 55: 338-347.
(7) Dardente H., Menet J.S., Challet E., Tournier B.B., Pévet P., Masson-Pévet M., 2004. Daily and circadian expression of neuropeptides in the suprachiasmatic nuclei of nocturnal and diurnal rodents. Mol. Brain. Res. 124:143–151.
(8) Dzal Y.A., Brigham R.M., 2013. The tradeoff between torpor use and reproduction in little brown bats (Myotis lucifugus). J. Comp. Physiol.B. 183 : 279-288.
(9) El Allali K., Achaâban M.R., Bothorel B., Piro M., Bouâouda
H., El Allouchi M., 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(11):R1044-52.
(10) El Ouazzani S., Janati I.A., Magoul R., Pévet P., Saboureau M., 2011. Overwinter body temperature patterns in captive jerboas (Jaculis orientalis): Influence of sex and group. J. Comp. Physiol. B. 181(2):299-309.
(11) Freeman M.E., Crissma J.K., Low G.N., Butcher R.L., Inskeep E.K., 1970. Thermogenic action of progesterone in the rat. Endocrinology. 86: 717-720.
(12) Geiser F., 2004. Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66: 239-274.
(13) Geiser F., Ruf T., 1995. Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol. Zool. 68:935–66.
(14) Geiser F., Turbill C., 2009. Hibernation and daily torpor minimize mammalian extinctions. Naturwissenschaften .96:1235-1240.
(15) Golombek D.A., Rosenstein R.E., 2010. Physiology of circadian entrainment. Physiol. Rev. 90:1063-1102.
(16) Haim A., Zizapel N., 1994. Daily rhythm of body temperature in coexisting rodents of the Genus Acomys acclimated to long-photoperiod: effects of ethanol and melatonin. Thermal Balance in Health and Disease APS. 22:191-196.
(17) Haim A., Shachaf K., Zisapel N., Reiter R.J., 1997. Daily rhythm of body temperature in Acomys russatus: Their response to photoperiod manipulations and melatonin. J. therm. Biol. 22( 3): 219-222.
(18) Heldmaier G., Steinlechner S., 1981. Seasonal pattern and energetic of short daily torpor in the Djungarian hamster, Phodopus sungorus. Oecologia .48 : 265-270.
(19) Jefimow M., Ostrowski M., Jakubowska A., Wojciechowski M.S., 2014. The effects of Dietary Cholesterol on metabolism and Daily Torpor Patterns in Siberian Hamsters. Physiological and Biochemical Zoology. 87(4): 527-538.
(20) Kirsch R., Ouarour A., Pévet P., 1991. Daily torpor in the Djungarian hamster (Phodopus sungorus): photoperiodic regulation, characteristics and circadian organization. J. Comp. Physiol. A. 168:121-128.
(21) Lahmam M., El M'rabet A., Ouarour A., Pévet P., Challet E., Vuillez P., 2008. Daily behavioral rhythmicity and organization of the suprachiasmatic nuclei in the diurnal rodent, Lemniscomys barbarus. Chronobiol Int. 25 :882-904.
(22) Lahmam M., 2008. Rythmicité comportementale journalière et organisation des noyaux suprachiasmatiques et de la rétine chez Lemniscomys barbarus, un rongeur diurne à reproduction saisonnière. Doctoral Thesis at the Abdelmalek Essaâdi University, Tétouan, Morocco.
(23) Lee T.M., Labyak S.E., 1997. Free-running rhythms and light- and dark-pulse phase response curves for diurnal Octodon degus (Rodentia). Am. J. Physiol. Regul. Integr. Comp. Physiol. 273: R278–R286.
(24) Leproult R., Van Onderbergen A., L’hermite-Baleriaux M., Van Cauter E., Copinschi G., 2005. Phase-Shifts of 24-h rhythms of hormonal release and body temperature following early evening administration of melatonin agonist agomelatine in healthy older men. Clin, Endocrinol. (Oxf) .63:298-304.
(25) Levi O., Dayan T., Kronfeld-Schor N., 2011. Adaptive thermoregulation in Golden Spiny Mice: The Influence of Season and Food Availability on Body Temperature. Physiological an Biochemical Zoology. 84(2): 175-184.
(26) Lovegrove B.G., Heldmaier G., Ruf T., 1991. Perspectives of endothermy revisited: the endothermic temperature range. J Therm Biol .16(4): 185–197.
(27) Mahoney M., Bult A., Smale L., 2001. Phase response curve and light-induced fos expression in the suprachiasmatic nucleus and adjacent hypothalamus of Arvicanthis niloticus. J. Biol. Rhythms .16: 149–162.
(28) Maillox A., Benstaali C., Bogdan A., Auzéby A., Touitou Y., 1999. Body temperature and locomotor activity as marker rhythms of aging of the circadian system in rodents. Experimental Gerontology. 34(6): 733-740.
(29) Marrone B.L., Gentry R.T., Wade G.N., 1976. Gonadal Hormones and Body Temperature in Rats: Effects of Estrous Cycles, Castration and Steroid Replacement. Physiology & Behavior. 17(3): 419-425.
(30) McDonald R.B., Day C., Carlson K., Stern J.S., Horwitz B.A. 1989. Effect of age and gender on thermoregulation. Am. J. Physiol. 257 (4 pt 2), R700-R704.
(31) McElhinny T.L., Smale L., Holeklamp K.E., 1997. Patterns of body temperature, activity, and reproductive behavior in a tropical murid rodent, Arvicanthis nioticus. Physiol. Behav. 62: 91-96.
(32) Mzilikazi, N., Lovegrove, B.G., 2002. Reproductive activity influences thermoregulation and torpor in the pouched mouse, Saccostomus campestris. J. comp. Physiol. B. 172: 7-16.
(33) Ouarour A., Kirsch R., Pévet P., 1991. Effects of temperature, steroids and castration on daily torpor in the Djungarian hamster (Phodopus sungorus). J. Comp. Physiol. A. 168:477-481.
(34) Piccione G., Caola G., Refinetti R., 2005. Temporal relationships of 21 physiological variable in horse and sheep. Com. Biochem. Physiol. A. Mol. Integr. Physiol. 142:389-396.
(35) Prendergast B.J., Tyler J. Stevenson T.J., Zucker I., 2013. Sex differences in Siberian hamster ultradian locomotor rhythms. Physiol. Behav. 0: 206–212.
(36) Refinetti R., Manaker, M., 1992. The circadian rhythm of body temperature. Physiol.Behav. 51:613-637.
(37) Refinetti R., 1996. Rhythm of body temperature and temperature selection are out of phase in a diurnal rodent, Octodon degus. Physiol. Behav. 60:959-961.
(38) Refinetti R. 1999a. Relationship between the daily rhythms of locomotor activity and body temperature in eight mammalian species. Am. J. Physiol. 277 (5pt2): R1493–R1500.
(39) Refinetti R., 1999b. Amplitude of the daily rhythm of body temperature in eleven mammalian species. J Thermal Biol. 24 (5-6): 477–481.
(40) Refinetti R., Piccione, G., 2004. Intra-and inter-individual variability in the circadian rhythm of body temperature of rats, squirrels, dogs, and horses. J. of Thermal Biology. 30:139-146.
(41) Refinetti R., 2006. Variability of diurnality in laboratory rodents.J. Comp. Physiol. A. 192(7):701-714.
(42) Refinetti, R., 2010. The circadian rhythm of body temperature. Frontiers in Bioscience. 15: 564–594.
(43) Ruf T., Geiser F., 2015. Daily torpor and hibernation in birds and mammals. Biol. Rev. 90:891-926.
(44) Ruf T., Heldmaier G., 1992. The impact of daily torpor on energy requirements in the Djungarian hamster, Phodopus sungorus. Physiol Zool65: 994–1010.
(45) Schmidt P.T., Raju, J., Danaceau M., Murphy D.L., Berlin R.E., 2002. The effects of gender and gonadal steroids on the neuroendocrine ant temperature response to m-chlorophenylpiperazine in leuropide-induced hypogonadism in women and men. Neuropsychopharmacology. 27800-27812.
(46) Smale L., Lee T., Nunez A.A., 2003. Mammalian diurnality: some facts and gaps. J. Biol. Rhythms. 18:356–366.
(47) Steinlechner S., Heldmaier G., Weber C., Ruf T., 1986. Role of photoperiod: pineal gland interaction in torpor control. In Heller H.C. et al. (Eds), Living in the cold: 301-307.
(48) Sumova A., Travnickova Z., Illnerova H., 1995. Memory on long but not on short days is stored in the rat suprachiasmatic nucleus. Neurosci. Lett. 200(3): 191-4.
(49) Tachinardi P., Bicudo J.E.W., Oda G.A., Valentinuzzi V.S, 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(1): e85674.
(50) Teresa L., McElhinny, Smale, L., Holekamp, K.E., 1997. Patterns of body temperature, Activity, and reproductive behavior in a tropical murid roden, Arvivanthis niloticus. Physiology & Behavior. 62(1): 91-96.
(51) Turbill C., Smith S., Deimel C., Ruf T., 2012. Daily torpor is associated with telomere length change over winter in Djungarian hamsters. Biol. Lett.8:304–307.
(52) Verhagen L.A., Pévet P., Saboureau M., Sicard B., Nesme B., Claustrat B., Buijs R.M., Kalsbeek A., 2004. Temporal organization of the 24-h corticosterone rhythm in the diurnal murid rodent Arvicanthis ansorgei Thomas 1910. Brain
Res.995(2):197-204.
(53) Vitale P.M., Darrow J.M., Duncan M.J., Shustak C.A., Goldman B.D., 1985. Effects of photoperiod, pinealectomy and castration on body weight and daily torpor in Djungarian hamsters (Phodopus sungorus). J. Endocrinology. 106:367-375.
(54) Vuillez P., Jacob N., Teclemariam-Mesbah R., Pévet P., 1996. In Syrian and European hamsters, the duration of sensitive phase to light of the suprachiasmatic nuclei depends on the photoperiod. Neurosci Lett.208(1):37-40.
(55) Wang L.C.H., Wolomyk M.W., 1988. Torpor in mammals and birds. Can. J. Zool. 66: 133-137.
(56) Weinert D., 2010. Circadian temperature variation and ageing. Ageing Res. Rev. 9(1): 51-60.
(57) Wollnik, F., Schimidt, B., 1995. Seasonal and rhytms of body temperature in the European hamster (Cricetus cricetus) under semi-natural conditions. J. Comp Physiol B. 165: 171-182
(58) Zhi-Jun Zhaon, Jing Cao, Zheng-Chao Liu, Gui-Ying Wang, Lu-Sheng Li, 2010. Seasonal regulations of resting metabolic rate and thermogenesis instriped hamster (Cricetulus barabensis). J. of Thermal Biology. 35: 401-405.
(59) Zuloaga D.G., McGiverna R.F., Handa R.J., 2009. Organizational influence of the postnatal testosterone surge on the circadian rhythm of core body temperature of adult male rats. Brain Research. 1268:68-75.