黑线仓鼠自身生存和繁殖输出间的权衡不受温度影响
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摘要
为阐明野生小型哺乳动物哺乳期能量收支对策,深入理解最大持续能量摄入(Sus EI)限制的因素和机理,测定了不同环境温度下(21℃、30℃和5℃)与哺育不同胎仔数(自然胎仔数Con、减少Minus和增加胎仔数Plus)的黑线仓鼠哺乳期体重、摄食量、基础代谢率(BMR)、非颤抖性产热(NST),以及褐色脂肪组织(BAT)细胞色素C氧化酶(COX)活性、血清T3、T4和催乳素水平。结果显示,哺乳期体重显著降低,摄食量显著增加,21℃和30℃组间差异不显著。最大持续摄食量约为14 g/d,Minus组分别比Con组和Plus组低20.3%和18.6%。温度对摄食量的影响显著,5℃下摄食量达16 g/d,比21℃和30℃组高14%(P<0.05)。Con组和Minus组胎仔数维持稳定,而Plus组胎仔数显著降低,断乳时Con组和Plus组胎仔数差异不显著。Minus组胎仔重显著低于Con组和Plus组。断乳时Minus组平均幼体体重比Con组和Plus组分别高17.9%和24.9%(P<0.05)。5℃下BMR、NST、COX活性、血清T3、T4和催乳素水平显著高于21℃和30℃,而21℃和30℃组间差异不显著。结果表明:黑线仓鼠Sus EI水平为5×BMR,低温下可通过增加能量摄入应对代谢产热的能量支出,在自身维持和繁殖输出之间采取了"权衡分配"的能量学策略,研究结果支持热耗散限制假说,也符合外周限制假说的预测。
The present study was aimed at examining the energy budget during lactation in small mammals,within which the factors limiting maximum sustained energy intake(Sus EI) and the physiological mechanisms underpinning the limitation would be further explored. Body mass,food intake,litter size and litter mass during lactation were determined in striped hamsters raising natural litters(Con),minus 2-3(Minus) and plus 2-3 pups(Plus) at 21℃,30℃ and 5℃. Basal metabolic rate(BMR),nonshivering thermogenesis(NST),cytochrome c oxydase(COX) activity of brown adipose tissue(BAT),serum T3,T4 and prolactin levels also were measured. Females increased food intake,but decreased body mass throughout lactation,during which the differences between 21 and 30℃ were not significant. Maximum asymptotic food intake averaged 14 g / d,and it was lower by 20. 3% and 18. 6% in Minus group than Con and Plus groups,respectively. The effect of temperature on food intake was significant. Food intake was increased to 16 g / d at 5℃,which was significantly higher than that at 21 and 30℃(by 14%,P < 0. 05). Litter size decreased significantly in Plus group,but did not change in Con and Minus groups throughout the lactation. Mean litter size was 4. 5 ± 0. 3,2. 6 ± 0. 3 and 4. 6 ± 0. 3 in Con,Minus and Plus groups,respectively,at weaning(P < 0. 01),and no difference was observed between Con and Plus groups. On weaning day,litter mass was not different between Con and Plus groups,but it was significantly lower in Minus group(33. 9 ± 3. 8) g than Con(50. 9 ± 2. 2) g and Plus groups(49. 0 ± 1. 8) g. Mean pup body mass was(13. 7 ±0. 7) g in Minus group,which was higher by 17. 9% and 24. 9% than that in Con(11. 6 ± 0. 5) g and Plus(10. 9 ± 0. 6)g groups(P < 0. 05),respectively. BMR,NST,BAT COX activity,serum T3,T4 and prolactin levels were significantly higher at 5℃ than 21℃ and 30℃,whereas no differences were observed between 21℃ and 30℃. It suggested that Sus EIwas 5 × BMR in striped hamster raising different litter size at 5℃,21℃ and 30℃. Cold-exposed hamsters were able to increase energy intake to cope with the energy expenditure for thermogenesis,showing a trade-off energetic budget between maintenance and reproductive output. The finding provided support for the"heat dissipation limitation hypothesis",but was also consistent with the prediction of the "peripheral limitation hypothesis".
The present study was aimed at examining the energy budget during lactation in small mammals,within which the factors limiting maximum sustained energy intake(Sus EI) and the physiological mechanisms underpinning the limitation would be further explored. Body mass,food intake,litter size and litter mass during lactation were determined in striped hamsters raising natural litters(Con),minus 2-3(Minus) and plus 2-3 pups(Plus) at 21℃,30℃ and 5℃. Basal metabolic rate(BMR),nonshivering thermogenesis(NST),cytochrome c oxydase(COX) activity of brown adipose tissue(BAT),serum T3,T4 and prolactin levels also were measured. Females increased food intake,but decreased body mass throughout lactation,during which the differences between 21 and 30℃ were not significant. Maximum asymptotic food intake averaged 14 g / d,and it was lower by 20. 3% and 18. 6% in Minus group than Con and Plus groups,respectively. The effect of temperature on food intake was significant. Food intake was increased to 16 g / d at 5℃,which was significantly higher than that at 21 and 30℃(by 14%,P < 0. 05). Litter size decreased significantly in Plus group,but did not change in Con and Minus groups throughout the lactation. Mean litter size was 4. 5 ± 0. 3,2. 6 ± 0. 3 and 4. 6 ± 0. 3 in Con,Minus and Plus groups,respectively,at weaning(P < 0. 01),and no difference was observed between Con and Plus groups. On weaning day,litter mass was not different between Con and Plus groups,but it was significantly lower in Minus group(33. 9 ± 3. 8) g than Con(50. 9 ± 2. 2) g and Plus groups(49. 0 ± 1. 8) g. Mean pup body mass was(13. 7 ±0. 7) g in Minus group,which was higher by 17. 9% and 24. 9% than that in Con(11. 6 ± 0. 5) g and Plus(10. 9 ± 0. 6)g groups(P < 0. 05),respectively. BMR,NST,BAT COX activity,serum T3,T4 and prolactin levels were significantly higher at 5℃ than 21℃ and 30℃,whereas no differences were observed between 21℃ and 30℃. It suggested that Sus EIwas 5 × BMR in striped hamster raising different litter size at 5℃,21℃ and 30℃. Cold-exposed hamsters were able to increase energy intake to cope with the energy expenditure for thermogenesis,showing a trade-off energetic budget between maintenance and reproductive output. The finding provided support for the"heat dissipation limitation hypothesis",but was also consistent with the prediction of the "peripheral limitation hypothesis".
引文
Bao W D,Wang D H,Wang Z W,Zhou Y L,Wang L M.2001.The comparison of reproductive traits of the striped hamster from Kubuqi Sandy-land and Hohhot Plain of Inner Mongolia.Chin J Zool,36:15-18.(in Chinese)
Bao W D,Wang D H,Wang Z W.2002.Metabolism in four rodent species from Ordos arid environment in Inner Mongolia,China.Folia Zool,51(Suppl.1):3-7.
Hammond K A,Konarzewski M,Torres R M,Diamond J.1994.Metabolic ceilings under a combination of peak energy demands.Physiol Zool,67:1479-1506.
Hammond K A,Kent Lloyd K C,Diamond J.1996.Is mammary output capacity limiting to lactational performance in mice?J Exp Biol,199:337-349.
Hammond K A,Diamond J.1997.Maximal sustained energy budgets in humans and animals.Nature,386:457-462.
Johnson M S,Thomson S C,Speakman J R.2001.Limits to sustained energy intake.III.Effects of concurrent pregnancy and lactation in Mus musculus.J Exp Biol,204:1947-1956.
Król E,Speakman J R.2003.Limits to sustained energy intake VII.Milk energy output in laboratory mice at thermoneutrality.J Exp Biol,206:4267-4281.
Li Y C,Lu H Q,Zhang X D,Xu W S.1989.Growth analysis and age indicator determination of striped hamster.Acta Theriol Sin,9(1):49-55.(in Chinese)
Liu J S,Wang D H,Sun R Y.2003.Metabolism and thermoregulation in striped hamsters(Cricetulus barabensis)from the Northeast of China.Acta Zool Sin,49:451-457.(in Chinese)
Lowry O H,Rosebrough N J,Farr A L,Randall J.1951.Protein measurement with the Folin phenol reagent.J Biol Chem,193:265-275.
Myers P,Master L L.1983.Reproduction by Peromyscus maniculatus:size and compromise.J Mammal,64:1-18.
Rogowitz G L.1996.Trade-offs in energy allocation during lactation.Am Zool,36:197-204.
Song Z G,Wang D H.2003.Metabolism and thermoregulation in the striped hamster Cricetulus barabensis.J Therm Biol,28:509-514.
Speakman J R.2000.The cost of living:field metabolic rates of small mammals.Adv Ecol Res,30:177-297.
Speakman J R.2007.The energy cost of reproduction in small rodents.Acta Theriol Sin,27:1-13.
Speakman J R,Król E.2005.Limits to sustained energy intake.IX.Areview of hypotheses.J Comp Physiol,175:B375-394.
Sundin U,Moore G,Nedergaard J,Cannon B.1978.Thermogenin amount and activity in hamster brown fat mitochondria:effect of cold acclimation.Am J Physiol,252:R822-832.
Valencak T G,Hacklnder K,Ruf T.2010.Peak energy turnover in lactating European hares:a test of the heat dissipation limitation hypothesis.J Exp Biol,213:2832-2839.
Wang J M,Wang D H.2006.Comparison of nonshivering thermogenesis induced by dosages of norepinephrine from 3 allometric equations in Brandt’s voles(Lasiopodomys brandtii).Acta Theriol Sin,26(1):84-88.(in Chinese)
Wang Y S,Wang D H,Wang Z W.2000.The progress on the theory of long-term energy budget in animals.Zool Res,21:238-244.
Weir J B de V.1949.New methods for calculating metabolic rate with special reference to protein metabolism.J Physiol Lond,109:1-9.
Wiesinger H,Heldmaier G,Buchberger A.1989.Effect of photoperiod and acclimation temperature on nonshivering thermogenesis and GDPbinding of brown fat mitochondria in the Djungarian hamster Phodopus sungorus.Pflugers Arch,413:667-672.
Wu S H,Zhang L N,Speakman J R,Wang D H.2009.Limits to sustained energy intake XI.A test of the heat dissipation limitation hypothesis in lactating Brandt’s vole(Lasiopodomys brandtii).J Exp Biol,212:3455-3465.
Yang Y P,Zhou Y L,Zhang P L,Hou X X,Dong W H.1996.A study of growth and development of striped hamster.Acta Theriol Sin,16(4):309-311.(in Chinese)
Zhang X Y,Wang D H.2007.Thermogenesis,food intake and serum leptin in cold-exposed lactating Brandt’s voles Lasiopodomys brandtii.J Exp Biol,210:512-521.
Zhao Z J,Chen J F,Wang D H.2008.Effects of photoperiod and high fat diet on energy intake and thermogenesisin Brandt’s voles Lasiopodomys brandtii.Acta Zool Sin,54(4):576-589.(in Chinese)
Zhao Z J,Cao J.2009.Effect of fur removal on the thermal conductance and energy budget in lactating Swiss mice.J Exp Biol,212:2541-2549.
Zhao Z J,Chi Q S,Cao J.2009.Limits on sustained metabolic rate in small mammals.Chin J Zool,44(4):155-160.(in Chinese)
Zhao Z J,Cao J,Meng X L,Li Y B.2010.Seasonal variations in metabolism and thermoregulation in the striped hamster(Cricetulus barabensis).J Therm Biol,35:52-57.
Zhao Z J.2011.Relationship between reproductive output and basal metabolic rate in striped hamster(Cricetulus barabensis).Acta Theriol Sin,31(1):69-78.(in Chinese)
Zhao Z J.2012.Effect of food restriction on energy metabolism and thermogenesis in striped hamster.Acta Theriol Sin,32(4):297-305.(in Chinese)
Zhao Z J,Wang D H.2005.Short photoperiod enhances thermogenic capacity in Brandt’s voles.Physiol Behav,85:143-149.
王玉山,王德华,王祖望.2000.动物长期能量收支理论及研究进展.动物学研究,21:238-244.
王建梅,王德华.2006.不同去甲肾上腺素剂量下布氏田鼠非颤抖性产热比较.兽类学报,26(1):84-88.
李玉春,卢浩泉,张学栋,徐文生.1989.黑线仓鼠的生长指标分析与年龄指标确定.兽类学报,9(1):49-55.
杨玉平,周延林,张鹏利,侯希贤,董维惠.1996.黑线仓鼠生长发育的研究.兽类学报,16(4):309-311.
赵志军,迟庆生,曹静.2009.小型哺乳动物的持续能量收支限制研究进展.动物学杂志,44(4):155-160.
赵志军,陈竞峰,王德华.2008.光周期和高脂食物对布氏田鼠能量代谢和产热的影响.动物学报,54(4):576-589.
赵志军.2011.黑线仓鼠繁殖输出与基础代谢率的关系.兽类学报,31(1):69-78.
赵志军.2012.食物限制对黑线仓鼠能量代谢和产热的影响.兽类学报,32(4):297-305.
柳劲松,王德华,孙儒泳.2003.东北地区黑线仓鼠的代谢产热特征及其体温调节.动物学报,49(4):451-457.
鲍伟东,王德华,王祖望,周延林,王利民.2001.内蒙古库布齐沙地和呼和浩特平原黑线仓鼠种群繁殖特征的比较.动物学杂志,36(1):15-18.
Bao W D,Wang D H,Wang Z W.2002.Metabolism in four rodent species from Ordos arid environment in Inner Mongolia,China.Folia Zool,51(Suppl.1):3-7.
Hammond K A,Konarzewski M,Torres R M,Diamond J.1994.Metabolic ceilings under a combination of peak energy demands.Physiol Zool,67:1479-1506.
Hammond K A,Kent Lloyd K C,Diamond J.1996.Is mammary output capacity limiting to lactational performance in mice?J Exp Biol,199:337-349.
Hammond K A,Diamond J.1997.Maximal sustained energy budgets in humans and animals.Nature,386:457-462.
Johnson M S,Thomson S C,Speakman J R.2001.Limits to sustained energy intake.III.Effects of concurrent pregnancy and lactation in Mus musculus.J Exp Biol,204:1947-1956.
Król E,Speakman J R.2003.Limits to sustained energy intake VII.Milk energy output in laboratory mice at thermoneutrality.J Exp Biol,206:4267-4281.
Li Y C,Lu H Q,Zhang X D,Xu W S.1989.Growth analysis and age indicator determination of striped hamster.Acta Theriol Sin,9(1):49-55.(in Chinese)
Liu J S,Wang D H,Sun R Y.2003.Metabolism and thermoregulation in striped hamsters(Cricetulus barabensis)from the Northeast of China.Acta Zool Sin,49:451-457.(in Chinese)
Lowry O H,Rosebrough N J,Farr A L,Randall J.1951.Protein measurement with the Folin phenol reagent.J Biol Chem,193:265-275.
Myers P,Master L L.1983.Reproduction by Peromyscus maniculatus:size and compromise.J Mammal,64:1-18.
Rogowitz G L.1996.Trade-offs in energy allocation during lactation.Am Zool,36:197-204.
Song Z G,Wang D H.2003.Metabolism and thermoregulation in the striped hamster Cricetulus barabensis.J Therm Biol,28:509-514.
Speakman J R.2000.The cost of living:field metabolic rates of small mammals.Adv Ecol Res,30:177-297.
Speakman J R.2007.The energy cost of reproduction in small rodents.Acta Theriol Sin,27:1-13.
Speakman J R,Król E.2005.Limits to sustained energy intake.IX.Areview of hypotheses.J Comp Physiol,175:B375-394.
Sundin U,Moore G,Nedergaard J,Cannon B.1978.Thermogenin amount and activity in hamster brown fat mitochondria:effect of cold acclimation.Am J Physiol,252:R822-832.
Valencak T G,Hacklnder K,Ruf T.2010.Peak energy turnover in lactating European hares:a test of the heat dissipation limitation hypothesis.J Exp Biol,213:2832-2839.
Wang J M,Wang D H.2006.Comparison of nonshivering thermogenesis induced by dosages of norepinephrine from 3 allometric equations in Brandt’s voles(Lasiopodomys brandtii).Acta Theriol Sin,26(1):84-88.(in Chinese)
Wang Y S,Wang D H,Wang Z W.2000.The progress on the theory of long-term energy budget in animals.Zool Res,21:238-244.
Weir J B de V.1949.New methods for calculating metabolic rate with special reference to protein metabolism.J Physiol Lond,109:1-9.
Wiesinger H,Heldmaier G,Buchberger A.1989.Effect of photoperiod and acclimation temperature on nonshivering thermogenesis and GDPbinding of brown fat mitochondria in the Djungarian hamster Phodopus sungorus.Pflugers Arch,413:667-672.
Wu S H,Zhang L N,Speakman J R,Wang D H.2009.Limits to sustained energy intake XI.A test of the heat dissipation limitation hypothesis in lactating Brandt’s vole(Lasiopodomys brandtii).J Exp Biol,212:3455-3465.
Yang Y P,Zhou Y L,Zhang P L,Hou X X,Dong W H.1996.A study of growth and development of striped hamster.Acta Theriol Sin,16(4):309-311.(in Chinese)
Zhang X Y,Wang D H.2007.Thermogenesis,food intake and serum leptin in cold-exposed lactating Brandt’s voles Lasiopodomys brandtii.J Exp Biol,210:512-521.
Zhao Z J,Chen J F,Wang D H.2008.Effects of photoperiod and high fat diet on energy intake and thermogenesisin Brandt’s voles Lasiopodomys brandtii.Acta Zool Sin,54(4):576-589.(in Chinese)
Zhao Z J,Cao J.2009.Effect of fur removal on the thermal conductance and energy budget in lactating Swiss mice.J Exp Biol,212:2541-2549.
Zhao Z J,Chi Q S,Cao J.2009.Limits on sustained metabolic rate in small mammals.Chin J Zool,44(4):155-160.(in Chinese)
Zhao Z J,Cao J,Meng X L,Li Y B.2010.Seasonal variations in metabolism and thermoregulation in the striped hamster(Cricetulus barabensis).J Therm Biol,35:52-57.
Zhao Z J.2011.Relationship between reproductive output and basal metabolic rate in striped hamster(Cricetulus barabensis).Acta Theriol Sin,31(1):69-78.(in Chinese)
Zhao Z J.2012.Effect of food restriction on energy metabolism and thermogenesis in striped hamster.Acta Theriol Sin,32(4):297-305.(in Chinese)
Zhao Z J,Wang D H.2005.Short photoperiod enhances thermogenic capacity in Brandt’s voles.Physiol Behav,85:143-149.
王玉山,王德华,王祖望.2000.动物长期能量收支理论及研究进展.动物学研究,21:238-244.
王建梅,王德华.2006.不同去甲肾上腺素剂量下布氏田鼠非颤抖性产热比较.兽类学报,26(1):84-88.
李玉春,卢浩泉,张学栋,徐文生.1989.黑线仓鼠的生长指标分析与年龄指标确定.兽类学报,9(1):49-55.
杨玉平,周延林,张鹏利,侯希贤,董维惠.1996.黑线仓鼠生长发育的研究.兽类学报,16(4):309-311.
赵志军,迟庆生,曹静.2009.小型哺乳动物的持续能量收支限制研究进展.动物学杂志,44(4):155-160.
赵志军,陈竞峰,王德华.2008.光周期和高脂食物对布氏田鼠能量代谢和产热的影响.动物学报,54(4):576-589.
赵志军.2011.黑线仓鼠繁殖输出与基础代谢率的关系.兽类学报,31(1):69-78.
赵志军.2012.食物限制对黑线仓鼠能量代谢和产热的影响.兽类学报,32(4):297-305.
柳劲松,王德华,孙儒泳.2003.东北地区黑线仓鼠的代谢产热特征及其体温调节.动物学报,49(4):451-457.
鲍伟东,王德华,王祖望,周延林,王利民.2001.内蒙古库布齐沙地和呼和浩特平原黑线仓鼠种群繁殖特征的比较.动物学杂志,36(1):15-18.