Influence of photoperiod on cold-adapted thermogenesis and endocrine aspects in the tree shrew (Tupaia belangeri)

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Environmental factors play an important role in the regulation of a mammal’s physiology and behavior. Consequently, particular species may provide valuable models for understanding the regulation of energy balance. In the present study, tree shrews (Tupaia belangeri) were transferred from a short to a long day photoperiod in cold conditions, in order to test our prediction that short photoperiod may stimulate an increase in thermogenic capacity and energy intake in tree shrews. During the first four weeks of acclimation to short days, T. belangeri increased body mass, whereas during the second four weeks of acclimation to long days, the body mass of tree shrews decreased compared with the short day group. The increase in body mass reflected a significant increase in absolute amounts of body components, such as carcass mass. During long photoperiod associated with cold exposure, livers, kidney, and small intestine mass decreased. T. belangeri decreased resting metabolic rate and energy intake after exposure to long days while during the exposure to short days the shrews started to maintain a stable level after 28 days. Serum leptin levels were positively correlated with body mass, as well as resting metabolic rate and energy intake. The results show that T. belangeri may provide an attractive novel model system for investigation of the regulation of body mass and energy balance at individual levels. Leptin is potentially stimulated by the photoperiod and cold exposure and is responsible for body mass regulation and thermogenesis in T. belangeri.

Influence of photoperiod on cold-adapted thermogenesis and endocrine aspects in the tree shrew (Tupaia belangeri)

in Animal Biology



AbelendaM.LedesmaA.RialE.PuertaM. (2003) Leptin administration to cold-acclimated rats reduces both food intake and brown adipose tissue thermogenesis. J. Therm. Biol.28525-530.

ArnoldW.RufT.Frey-RoosF.BrunsU. (2011) Diet-independent remodeling of cellular membranes precedes seasonally changing body temperature in a hibernator. PLoS ONE6(4) e18641.

BartnessT.J.SongC.K. (2005) Innervation of brown adipose tissue and its role in thermogenesis. Can. J. Diabetes29(4) 420-428.

BozinovicF. (1992) Rate of basal metabolism of grazing rodents from different habitats. J. Mammal.73379-384.

BozinovicF.RosenmannM. (1989) Maximum metabolic rate of rodents: physiological and ecological consequences on distributional limits. Funct. Ecol.3173-181.

CannonB.LindbergO. (1979) Mitochondria from brown adipose tissue: isolation and properties. Methods Enzymol.5565-78.

CannonB.NedergaardJ. (2004) Brown adipose tissue: function and physiological significance. Physiol. Rev.84277-359.

CaoX. (1989) Seasonal changes in spermatogenesis of tree shrew (Tupaia belangeri chinensis). Zool. Res.1015-21.

ConcannonP.LevacK.RawsonR.TennantB.BensadounA. (2001) Seasonal changes in serum leptin, food intake, and body weight in photoentrained woodchucks. Am. J. Physiol.281R951-R959.

DemasG.E.BowersR.R.BartnessT.J.GettysT.W. (2002) Photoperiodic regulation of gene expression in brown and white adipose tissue of Siberian hamsters (Phodopus sungorus). Am. J. Physiol.282R114-R121.

EblingF.J.P. (1994) Photoperiodic differences during development in the dwarf hamsters Phodopus sungorus and Phodopus campbelli. Gen. Comp. Endocr.95475-482.

ErnestS.K.M. (2005) Body size, energy use, and community structure of small mammals. Ecology861407-1413.

EstabrookR.W. (1967) Mitochondrial respiratory control and the polarographic measurement of adp: O ratios. Methods Enzymol101-47.

FlierJ.S. (1998) What’s in a name? In search of leptin’s physiologic role. J. Clin. Endocr. Metab.831407-1413.

GettingerR.D.RalphC.L. (1985) Thermoregulatory responses to photoperiod by kangaroo rats (Dipodomys ordii): influence of night lighting on nonshivering thermogenesis and resting metabolism. J. Exp. Zool.234335-340.

HaimA. (1996) Food and energy intake, non-shivering thermogenesis and daily rhythm of body temperature in the bushy-tailed gerbil sekeetamys calurus: the role of photoperiod manipulations. J. Therm. Biol.2137-42.

HaimA.ShabtayA.AradZ. (1999) The thermoregulatory and metabolic responses to photoperiod manipulations of the macedonian mouse (Mus macedonicus), a post-fire invader. J. Therm. Biol.24279-286.

HaimA.ZisapelN. (1995) Oxygen consumption and body temperature rhythms in the golden spiny mouse: responses to changes in day length. Physiol. Behav.58775-778.

HallK.D.HeymsfieldS.B.KemnitzJ.W.KleinS.SchoellerD.A.SpeakmanJ.R. (2012) Energy balance and its components: implications for body weight regulation. Am. J. Clin. Nutr.95989-994.

HeldmaierG. (1971) Nonshivering thermogenesis and body size in mammals. J. Comp. Physiol.73222-248.

HeldmaierG.SteinlechnerS. (1981) Seasonal control of energy requirements for thermoregulation in the Djungarian hamster (Phodopus sungorus), living in natural photoperiod. J. Comp. Physiol. B142429-437.

HeldmaierG.SteinlechnerS.RafaelJ. (1982) Nonshivering thermogenesis and cold resistance during seasonal acclimatization in the Djungarian hamster. J. Comp. Physiol. B1491-9.

HeldmaierG.SteinlechnerS.RufT.WiesingerH.KlingensporM. (1989) Photoperiod and thermoregulation in vertebrates: body temperature rhythms and thermogenic acclimation. J. Biol. Rhyth.4139.

HillR.W. (1972) Determination of oxygen consumption by use of the paramagnetic oxygen analyzer. J. Appl. Physiol.33261-263.

Himms-HagenJ. (1990) Brown adipose tissue thermogenesis: interdisciplinary studies. FASEB. J.42890-2898.

HunterH.L.NagyT.R. (2002) Body composition in a seasonal model of obesity: longitudinal measures and validation of DXA. Obesity101180-1187.

JanskýL. (1973) Nonshivering thermogenesis and its thermoregulatory significance. Biol. Rev.4885-132.

KadenbachB.HüttemannM.ArnoldS.LeeI.BenderE. (2000) Mitochondrial energy metabolism is regulated via nuclear-coded subunits of cytochrome c oxidase. Free. Radical. Bio. Med.29211-221.

KhaniA.RainerG. (2012) Recognition memory in tree shrew (Tupaia belangeri) after repeated familiarization sessions. Behav. Process.90364-371.

KlausS.HeldmaierG.RicquierD. (1988) Seasonal acclimation of bank voles and wood mice: nonshivering thermogenesis and thermogenic properties of brown adipose tissue mitochondria. J. Comp. Physiol. B158157-164.

KlingensporM.NiggemannH.HeldmaierG. (2000) Modulation of leptin sensitivity by short photoperiod acclimation in the Djungarian hamster, Phodopus sungorus. J. Comp. Physiol. B17037-43.

KlokM.D.JakobsdottirS.DrentM.L. (2007) The role of leptin and ghrelin in the regulation of food intake and body weight in humans: a review. Obes. Rev.8(1) 21-34.

KnopperL.D.BoilyP. (2000) The energy budget of captive Siberian hamsters, phodopus sungorus, exposed to photoperiod changes: mass loss is caused by a voluntary decrease in food intake. Physiol. Biochem. Zool.73517-522.

KristanD.M.HammondK.A. (2006) Effects of three simultaneous demands on glucose transport, resting metabolism and morphology of laboratory mice. J. Comp. Physiol. B176139-151.

KrólE.DuncanJ.RedmanP.MorganP.MercerJ.SpeakmanJ. (2006) Photoperiod regulates leptin sensitivity in field voles, Microtus agrestis. J. Comp. Physiol. B176153-163.

KrólE.RedmanP.ThomsonP.WilliamsR.MayerC.MercerJ.SpeakmanJ. (2005) Effect of photoperiod on body mass, food intake and body composition in the field vole, Microtus agrestis. J. Exp. Biol.208571-584.

Kronfeld-SchorN.HaimA.DayanT.ZisapelN.KlingensporM.HeldmaierG. (2000) Seasonal thermogenic acclimation of diurnally and nocturnally active desert spiny mice. Physiol. Biochem. Zool.7337-44.

KsiażekA.CzernieckiJ.KonarzewskiM. (2009) Phenotypic flexibility of traits related to energy acquisition in mice divergently selected for basal metabolic rate (BMR). J. Exp. Biol.212808-814.

LanniA.MorenoM.LombardiA.GogliaF. (2003) Thyroid hormone and uncoupling proteins. FEBS. Lett.5435-10.

LeonardJ.L.MellenS.A.LarsenR.P. (1983) Thyroxine 5′-deiodinase activity in brown adipose tissue. Endocrinology1121153-1155.

LiQ.SunR.HuangC.WangZ.LiuX.HouJ.LiuJ.CaiL.LiN.ZhangS. (2001) Cold adaptive thermogenesis in small mammals from different geographical zones of China. Comp. Biochem. Physiol. A129949-961.

LiX.S.WangD.H. (2005) Regulation of body weight and thermogenesis in seasonally acclimatized Brandt’s voles (Microtus brandti). Horm. Behav.48321-328.

LiX.S.WangD.H. (2007) Photoperiod and temperature can regulate body mass, serum leptin concentration, and uncoupling protein 1 in Brandt’s voles (Lasiopodomys brandtii) and Mongolian gerbils (Meriones unguiculatus). Physiol. Biochem. Zool.80326-334.

LiuJ.S.SunR.Y.WangD.H. (2006) Thermogenic properties in three rodent species from northeastern China in summer. J. Therm. Biol.31172-176.

LiuQ.S.WangD.H. (2007) Effects of diet quality on phenotypic flexibility of organ size and digestive function in Mongolian gerbils (Meriones unguiculatus). J. Comp. Physiol. B177509-518.

LowryO.H.RosebroughN.J.FarrA.L.RandallR.J. (1951) Protein measurement with the folin phenol reagent. J. Biol. Chem.193265-275.

MercerJ.G.SpeakmanJ.R. (2001) Hypothalamic neuropeptide mechanisms for regulating energy balance: from rodent models to human obesity. Neurosci. Biobehav. R.25101-116.

NayaD.E.EbenspergerL.A.SabatP.BozinovicF. (2008) Digestive and metabolic flexibility allows female degus to cope with lactation costs. Physiol. Biochem. Zool.81186-194.

PowellC.S.BlaylockM.L.WangR.HnnterH.TohanningG.L.NagyT.R. (2002) Effects of energy expenditure and ucpi on photoperiod induced weight gain in collared lemmings. Obes. Res.6541-550.

PrendergastB.J.KayL.M. (2008) Affective and adrenocorticotrophic responses to photoperiod in Wistar rats. J. Neuroendocrinol.20261-267.

SabatP.BozinovicF. (2000) Digestive plasticity and the cost of acclimation to dietary chemistry in the omnivorous leaf-eared mouse Phyllotis darwini. J. Comp. Physiol. B170411-417.

ScarpaceP.J.MathenyM. (1998) Leptin induction of ucp1 gene expression is dependent on sympathetic innervation. Am. J. Physiol.275E259-E264.

SchneiderJ.E.BlumR.M.WadeG.N. (2000) Metabolic control of food intake and estrous cycles in syrian hamsters. I. Plasma insulin and leptin. Am. J. Physiol.278R476-R485.

SpeakmanJ.HamblyC.MitchellS.KrólE. (2007) Animal models of obesity. Obes. Rev.855-61.

SteffenJ.M.RobertsJ.C. (1977) Temperature acclimation in the Mongolian gerbil (Meriones unguiculatus): biochemical and organ weight changes. Comp. Biochem. Physiol. B58237-242.

SundinU.MooreG.NedergaardJ.CannonB. (1987) Thermogenin amount and activity in hamster brown fat mitochondria: effect of cold acclimation. Am. J. Physiol.52R822-R832.

van SantM.J.HammondK.A. (2008) Contribution of shivering and nonshivering thermogenesis to thermogenic capacity for the deer mouse (Peromyscus maniculatus). Physiol. Biochem. Zool.81605-611.

VillarinJ.J.SchaefferP.J.MarkleR.A.LindstedtS.L. (2003) Chronic cold exposure increases liver oxidative capacity in the marsupial monodelphis domestica. Comp. Biochem. Physiol. A136621-630.

WangZ.K.LiQ.F.SunR.Y. (1995) The characteristics of nonshivering thermogenesis and cellular respiration in the tree shrews. Zool. Res.16239-246.

WangZ.K.SunR.Y.LiQ.F. (1994) Characteristics of the resting metabolic rate of the treeshrews. J. Beijing Normal University (Natural Science)30408-414.

ZhangL.WangR.ZhuW.LiuP.CaiJ.WangZ.SivasakthivelS.LianX. (2011) Adaptive thermogenesis of the liver in tree shrew (Tupaia belangeri) during cold acclimation. Anim. Biol.61385-401.

ZhangL.LiuP.ZhuW.CaiJ.WangZ. (2012a) Variations in thermal physiology and energetics of the tree shrew (Tupaia belangeri) in response to cold acclimation. J. Comp. Physiol. B182167-176.

ZhangL.ZhangH.ZhuW.LiX.WangZ. (2012b) Energy metabolism, thermogenesis and body mass regulation in tree shrew (Tupaia belangeri) during subsequent cold and warm acclimation. Comp. Biochem. Physiol. A162437-442.

ZhangL.ZhuW.WangZ. (2012c) Role of photoperiod on hormone concentrations and adaptive capacity in tree shrews, Tupaia belangeri. Comp. Biochem. Physiol. A163253-259.

ZhangX.Y.WangD.H. (2006) Energy metabolism, thermogenesis and body mass regulation in Brandt’s voles (Lasiopodomys brandtii) during cold acclimation and rewarming. Horm. Behav.5061-69.

ZhangY.ProencaR.MaffeiM.BaroneM.LeopoldL.FriedmanJ.M. (1994) Positional cloning of the mouse obese gene and its human homologue. Nature372425-432.

ZhaoZ.J.WangD.H. (2005) Short photoperiod enhances thermogenic capacity in Brandt’s voles. Physiol. Behav.85143-149.

ZhaoZ.J.WangD.H. (2006) Effects of photoperiod on energy budgets and thermogenesis in Mongolian gerbils (Meriones unguiculatus). J. Therm. Biol.31323-331.

ZhuW.JiaT.LianX.WangZ. (2010) Effects of cold acclimation on body mass, serum leptin level, energy metabolism and thermognesis in Eothenomys miletus in Hengduan Mountains region. J. Therm. Biol.3541-46.

ZhuW.CaiJ.XiaoL.WangZ. (2011a) Effects of photoperiod on energy intake, thermogenesis and body mass in Eothenomys miletus in Hengduan Mountain region. J. Therm. Biol.36380-385.

ZhuW.WangB.CaiJ.LianX.WangZ. (2011b) Thermogenesis, energy intake and serum leptin in Apodemus chevrieri in Hengduan Mountains region during cold acclimation. J. Therm. Biol.36181-186.

ZhuW.YangS.CaiJ.MengL.WangZ. (2012a) Effects of photoperiod on body mass, thermogenesis and body composition in Eothenomys miletus during cold exposure. J. Stre. Physiol. Biochem.839-50.

ZhuW.ZhangH.WangZ. (2012b) Seasonal changes in body mass and thermogenesis in tree shrews (Tupaia belangeri): the roles of photoperiod and cold. J. Therm. Biol.37479-484.

ZouR.JiW.YanH.LuJ. (1991) The captivities and reproductions of tree shrews. In: PengY.YeZ.ZouR.WangY.X.TianB.P.MaY.Y.ShiL.M. (Eds.) Biology of chinese tree shrews (Tupaia belangeri chinensis). Yunnan Scientic and Technological PressKunming.


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    Photoperiodic response of body mass (A), EI (B), RMR (C) and NST (D) in tree shrews (N=23).

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    Correlation between serum leptin and BM (A), EI (B), RMR (C) and NST (D) in tree shrews (N=23).


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