环境温度对东北林蛙不同地理种群繁殖期体温和胚胎发育的影响
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摘要
全球气候变暖对两栖类的影响是生态学关注的热点问题。作为变温动物,两栖类能够从外界获取热量,并具有一定的体温调节能力。以东北林蛙(Rana dybowskii)作为实验对象,测量不同环境温度下伊春种群、白山种群和尚志种群繁殖期的体温和胚胎发育速度。结果表明:东北林蛙的体温和胚胎发育速度均与环境温度正相关;不同地理种群的选择体温、体温调节能力不同,由高到低依次为尚志种群、白山种群和伊春种群;尚志种群、白山种群和伊春种群完成胚胎发育的时间依次延长,且三者的差距随着胚胎发育的进行越来越明显;环境温度升高后,不同发育阶段完成的时间并不是等比例的减少,胚胎发育的第2阶段和第3阶段以及第4阶段的第21期(开口期)经历的时间显著缩短;与成体相比,胚胎发育过程更容易受到温度的影响,从而导致东北林蛙某些器官形态结构和功能的改变。
How global warming affects amphibians is a current hot topic because temperature is the most important and variable climatic factor that affects many biological processes and is strongly related with temporal variation. Amphibians are ectotherms,which means that they receive heat from external sources and can control their temperature through their bodies or behavior. The Dybowski's frog( Rana dybowskii) is a cold-resistant species found in Northeast Asia with an extensive geographic variation in life-history traits. In this paper,the specimens were taken from Yichun,Baishan,and Shangzhi to measure body temperature and embryonic development speed. The results showed that body temperature was positively correlated with environmental temperature,and that heat increased the rate of growth,while cold temperature slowed it. The species showed higher selected body temperature,stronger temperature regulation ability,and faster embryo development speed in the hot environment than in the cold environment. There were significant differences among the three geographic populations of R. dybowskii in the selected body temperature. The crossing point temperature at which the linear regression equation intersects with isothermal line( y = x) was the lowest in the Yichun population( 18.51℃ for males and 21.74℃for females),and was the highest in the Shangzhi population( 20. 00℃ for males and 23. 06℃ for females). The bodytemperature of the Yichun population was the lowest,while that of the Shangzhi population was the highest among the three populations under the low temperature conditions( 8—22℃ for males and 8—26℃ for females). In contrast,body temperature of the Yichun population was the highest,while that of the Shangzhi population was the lowest under high temperature conditions( 24—30℃ for males and 28—30℃ for females). Thermoregulation ability of the Shangzhi population was the strongest,followed by the Baishan population,and the Yichun population was the weakest among the three populations. The embryonic development time of the Shangzhi, Baishan, and Yichun populations increased successively and the gaps among the three populations were becoming increasingly obvious with the development of embryos.The development completion time of different stages was not reduced in proportion with the increasing of ambient temperature. The second and third stage of embryonic development,and the 21 stphase( mouth open stage) of the fourth stage were significantly shortened. This indicates that different embryo development stages have different sensitivity to temperature,and that heating can accelerate the developmental rate during certain developmental periods of this species.Thus,tadpoles and developing frogs are more susceptible to temperature than adults. This may lead to changes in morphological structure and functions in some organs. In summary,body temperature and embryonic development are different among the three geographic populations of R. dybowskii,which is a type of adaptive evolution to the environment.The temperature rise has an effect on all populations under the background of global warming. We conclude that different geographic populations have different adaptation strategies to cope with the change of environmental temperature. This study provides a basis for the artificial breeding of amphibians and the adaptation mechanism to climate change in the future.
How global warming affects amphibians is a current hot topic because temperature is the most important and variable climatic factor that affects many biological processes and is strongly related with temporal variation. Amphibians are ectotherms,which means that they receive heat from external sources and can control their temperature through their bodies or behavior. The Dybowski's frog( Rana dybowskii) is a cold-resistant species found in Northeast Asia with an extensive geographic variation in life-history traits. In this paper,the specimens were taken from Yichun,Baishan,and Shangzhi to measure body temperature and embryonic development speed. The results showed that body temperature was positively correlated with environmental temperature,and that heat increased the rate of growth,while cold temperature slowed it. The species showed higher selected body temperature,stronger temperature regulation ability,and faster embryo development speed in the hot environment than in the cold environment. There were significant differences among the three geographic populations of R. dybowskii in the selected body temperature. The crossing point temperature at which the linear regression equation intersects with isothermal line( y = x) was the lowest in the Yichun population( 18.51℃ for males and 21.74℃for females),and was the highest in the Shangzhi population( 20. 00℃ for males and 23. 06℃ for females). The bodytemperature of the Yichun population was the lowest,while that of the Shangzhi population was the highest among the three populations under the low temperature conditions( 8—22℃ for males and 8—26℃ for females). In contrast,body temperature of the Yichun population was the highest,while that of the Shangzhi population was the lowest under high temperature conditions( 24—30℃ for males and 28—30℃ for females). Thermoregulation ability of the Shangzhi population was the strongest,followed by the Baishan population,and the Yichun population was the weakest among the three populations. The embryonic development time of the Shangzhi, Baishan, and Yichun populations increased successively and the gaps among the three populations were becoming increasingly obvious with the development of embryos.The development completion time of different stages was not reduced in proportion with the increasing of ambient temperature. The second and third stage of embryonic development,and the 21 stphase( mouth open stage) of the fourth stage were significantly shortened. This indicates that different embryo development stages have different sensitivity to temperature,and that heating can accelerate the developmental rate during certain developmental periods of this species.Thus,tadpoles and developing frogs are more susceptible to temperature than adults. This may lead to changes in morphological structure and functions in some organs. In summary,body temperature and embryonic development are different among the three geographic populations of R. dybowskii,which is a type of adaptive evolution to the environment.The temperature rise has an effect on all populations under the background of global warming. We conclude that different geographic populations have different adaptation strategies to cope with the change of environmental temperature. This study provides a basis for the artificial breeding of amphibians and the adaptation mechanism to climate change in the future.
引文
[1]Tekalign W,Balakrishinan M.Effects of global climate change on wildlife:a review.Civil and Environmental Research,2016,8(6):1-13.
[2]马瑞俊,蒋志刚.全球气候变化对野生动物的影响.生态学报,2005,25(11):3061-3066.
[3]Beebee T J C.Amphibian breeding and climate.Nature,1995,374(6519):219-220.
[4]Li Y M,Cohen J M,Rohr J R.Review and synthesis of the effects of climate change on amphibians.Integrative Zoology,2013,8(2):145-161.
[5]王刚,冯学运.气候变化对两栖动物的影响.大自然,2013,(3):7-9.
[6]Ruiz-Aravena M,Gonzalez-Mendez A,Estay S A,Gaitán-Espitia J D,Barria-Oyarzo I,Bartheld J L,Bacigalupe L D.Impact of global warming at the range margins:phenotypic plasticity and behavioral thermoregulation will buffer an endemic amphibian.Ecology and Evolution,2014,4(23):4467-4475.
[7]Muir A P,Biek R,Mable B K.Behavioural and physiological adaptations to low-temperature environments in the common frog,Rana temporaria.BMC Evolutionary Biology,2014,14:110.
[8]马爽,谢惠春,李晓晨.两栖类和爬行类体温调节的神经生物学研究进展.四川动物,2008,27(3):464-467,477-477.
[9]孙清琳,徐骁骁,刘鹏,赵文阁.环境温度对东北林蛙(Rana dybowskii)体温的影响.野生动物学报,2016,37(3):266-270.
[10]Gerick A A,Munshaw R G,Palen W J,Combes S A,O'Regan S M.Thermal physiology and species distribution models reveal climate vulnerability of temperate amphibians.Journal of Biogeography,2014,41(4):713-723.
[11]Deutsch C A,Tewksbury J J,Huey R B,Sheldon K S,Ghalambor C K,Haak D C,Martin P R.Impacts of climate warming on terrestrial ectotherms across latitude.Proceedings of the National Academy of Sciences of the United States of America,2008,105(18):6668-6672.
[12]Wheeler C A,Bettaso J B,Ashton D T,Welsh Jr H H.Effects of water temperature on breeding phenology,growth,and metamorphosis of foothill yellow-legged frogs(Rana Boylii):a case study of the regulated mainstem and unregulated tributaries of California's trinity river.River Research and Applications,2015,31(10):1276-1286.
[13]陈雯,俞宝根,郑荣泉,俞丹娜.温度对棘胸蛙胚胎发育及蝌蚪表型特征的影响.贵州农业科学,2010,38(1):108-110.
[14]Oromi N,Camarasa S,Sanuy I,Sanuy D.Variation of growth rate and survival in embryos and larvae of Rana temporaria populations from the pyrenees.Acta Herpetologica,2015,10(2):85-91.
[15]赵文阁,刘鹏,陈辉.黑龙江省两栖爬行动物志.北京:科学出版社,2008.
[16]赵文阁,曹良,田秀华.东北林蛙养殖实用技术.哈尔滨:东北林业大学出版社,2009.
[17]陶娟,杨杰,陈晓虹.太行隆肛蛙的早期胚胎发育及生态适应性.动物学杂志,2010,45(5):39-46.
[18]Gosner K L.A simplified table for staging anuran embryos and larvae with notes on identification.Herpetologica,1960,16(3):183-190.
[19]K9hler A,Sadowska J,Olszewska J,Trzeciak P,Berger-Tal O,Tracy C R.Staying warm or moist?Operative temperature and thermal preferences of common frogs(Rana temporaria),and effects on locomotion.Herpetological Journal,2011,21(1):17-26.
[20]Navas C A,Gomes F R,Carvalho J E.Thermal relationships and exercise physiology in anuran amphibians:integration and evolutionary implications.Comparative Biochemistry and Physiology Part A:Molecular&Integrative Physiology,2008,151(3):344-362.
[21]Vences M,Galán P,Vieites D R,Puente M,Oetter K,Wanke S.Field body temperatures and heating rates in a montane frog population:the importance of black dorsal pattern for thermoregulation.Annales Zoologici Fennici,2002,39(3):209-220.
[22]Pollister A W,Moore J A.Tables for the normal development of Rana sylvatica.The Anatomical Record,1937,68(4):489-496.
[23]Tracy C R,Christian K A,Tracy C R.Not just small,wet,and cold:effects of body size and skin resistance on thermoregulation and arboreality of frogs.Ecology,2010,91(5):1477-1484.
[24]Zheng R Q,Liu C T.Giant spiny-frog(Paa spinosa)from different populations differ in thermal preference but not in thermal tolerance.Aquatic Ecology,2010,44(4):723-729.
[25]王丽文.环境温度对东北小鲵体温及热能代谢的影响.辽宁大学学报:自然科学版,1994,21(2):80-84.
[26]王丽文,梁传成,黄薇,彭霞.环境温度对爪鲵体温及能量代谢的影响.动物学报,2008,54(4):640-644.
[27]赵文阁,于小龙,翟小彤.温度对哈士蟆胚胎发育的影响.野生动物学报,1990,(3):31-33.
[28]夏玉国,王念民,赵文阁.中国林蛙与黑龙江林蛙温度生态比较研究//周开亚,计翔.中国动物学会两栖爬行动物学分会2005年学术研讨会暨会员代表大会论文集.长春:吉林人民出版社,2005:171-176.
[29]樊晓丽,雷焕宗,林植华.虎纹蛙选择体温和热耐受性在个体发育过程中的变化.生态学报,2012,32(17):5574-5580.
[30]施林强,赵丽华,马小浩,马小梅.泽陆蛙和饰纹姬蛙蝌蚪不同热驯化下选择体温和热耐受性.生态学报,2012,32(2):465-471.
[31]Reading C J,Clarke R T.Impacts of climate and density on the duration of the tadpole stage of the common toad Bufo bufo.Oecologia,1999,121(3):310-315.
[32]李新红,赵文阁,郭玉民,薛建华.中国林蛙性腺的发育及温度对其性别分化的影响.动物学研究,2001,22(5):351-356.
[33]田秀华,赵文阁,柏永明,段玉宝.东北林蛙人工养殖存在问题及发展对策.野生动物杂志,2009,30(4):214-216.
[34]MerilJ,Laurila A,Laugen A T,Rsnen K.Heads or tails?Variation in tadpole body proportions in response to temperature and food stress.Evolutionary Ecology Research,2004,6(5):727-738.
[2]马瑞俊,蒋志刚.全球气候变化对野生动物的影响.生态学报,2005,25(11):3061-3066.
[3]Beebee T J C.Amphibian breeding and climate.Nature,1995,374(6519):219-220.
[4]Li Y M,Cohen J M,Rohr J R.Review and synthesis of the effects of climate change on amphibians.Integrative Zoology,2013,8(2):145-161.
[5]王刚,冯学运.气候变化对两栖动物的影响.大自然,2013,(3):7-9.
[6]Ruiz-Aravena M,Gonzalez-Mendez A,Estay S A,Gaitán-Espitia J D,Barria-Oyarzo I,Bartheld J L,Bacigalupe L D.Impact of global warming at the range margins:phenotypic plasticity and behavioral thermoregulation will buffer an endemic amphibian.Ecology and Evolution,2014,4(23):4467-4475.
[7]Muir A P,Biek R,Mable B K.Behavioural and physiological adaptations to low-temperature environments in the common frog,Rana temporaria.BMC Evolutionary Biology,2014,14:110.
[8]马爽,谢惠春,李晓晨.两栖类和爬行类体温调节的神经生物学研究进展.四川动物,2008,27(3):464-467,477-477.
[9]孙清琳,徐骁骁,刘鹏,赵文阁.环境温度对东北林蛙(Rana dybowskii)体温的影响.野生动物学报,2016,37(3):266-270.
[10]Gerick A A,Munshaw R G,Palen W J,Combes S A,O'Regan S M.Thermal physiology and species distribution models reveal climate vulnerability of temperate amphibians.Journal of Biogeography,2014,41(4):713-723.
[11]Deutsch C A,Tewksbury J J,Huey R B,Sheldon K S,Ghalambor C K,Haak D C,Martin P R.Impacts of climate warming on terrestrial ectotherms across latitude.Proceedings of the National Academy of Sciences of the United States of America,2008,105(18):6668-6672.
[12]Wheeler C A,Bettaso J B,Ashton D T,Welsh Jr H H.Effects of water temperature on breeding phenology,growth,and metamorphosis of foothill yellow-legged frogs(Rana Boylii):a case study of the regulated mainstem and unregulated tributaries of California's trinity river.River Research and Applications,2015,31(10):1276-1286.
[13]陈雯,俞宝根,郑荣泉,俞丹娜.温度对棘胸蛙胚胎发育及蝌蚪表型特征的影响.贵州农业科学,2010,38(1):108-110.
[14]Oromi N,Camarasa S,Sanuy I,Sanuy D.Variation of growth rate and survival in embryos and larvae of Rana temporaria populations from the pyrenees.Acta Herpetologica,2015,10(2):85-91.
[15]赵文阁,刘鹏,陈辉.黑龙江省两栖爬行动物志.北京:科学出版社,2008.
[16]赵文阁,曹良,田秀华.东北林蛙养殖实用技术.哈尔滨:东北林业大学出版社,2009.
[17]陶娟,杨杰,陈晓虹.太行隆肛蛙的早期胚胎发育及生态适应性.动物学杂志,2010,45(5):39-46.
[18]Gosner K L.A simplified table for staging anuran embryos and larvae with notes on identification.Herpetologica,1960,16(3):183-190.
[19]K9hler A,Sadowska J,Olszewska J,Trzeciak P,Berger-Tal O,Tracy C R.Staying warm or moist?Operative temperature and thermal preferences of common frogs(Rana temporaria),and effects on locomotion.Herpetological Journal,2011,21(1):17-26.
[20]Navas C A,Gomes F R,Carvalho J E.Thermal relationships and exercise physiology in anuran amphibians:integration and evolutionary implications.Comparative Biochemistry and Physiology Part A:Molecular&Integrative Physiology,2008,151(3):344-362.
[21]Vences M,Galán P,Vieites D R,Puente M,Oetter K,Wanke S.Field body temperatures and heating rates in a montane frog population:the importance of black dorsal pattern for thermoregulation.Annales Zoologici Fennici,2002,39(3):209-220.
[22]Pollister A W,Moore J A.Tables for the normal development of Rana sylvatica.The Anatomical Record,1937,68(4):489-496.
[23]Tracy C R,Christian K A,Tracy C R.Not just small,wet,and cold:effects of body size and skin resistance on thermoregulation and arboreality of frogs.Ecology,2010,91(5):1477-1484.
[24]Zheng R Q,Liu C T.Giant spiny-frog(Paa spinosa)from different populations differ in thermal preference but not in thermal tolerance.Aquatic Ecology,2010,44(4):723-729.
[25]王丽文.环境温度对东北小鲵体温及热能代谢的影响.辽宁大学学报:自然科学版,1994,21(2):80-84.
[26]王丽文,梁传成,黄薇,彭霞.环境温度对爪鲵体温及能量代谢的影响.动物学报,2008,54(4):640-644.
[27]赵文阁,于小龙,翟小彤.温度对哈士蟆胚胎发育的影响.野生动物学报,1990,(3):31-33.
[28]夏玉国,王念民,赵文阁.中国林蛙与黑龙江林蛙温度生态比较研究//周开亚,计翔.中国动物学会两栖爬行动物学分会2005年学术研讨会暨会员代表大会论文集.长春:吉林人民出版社,2005:171-176.
[29]樊晓丽,雷焕宗,林植华.虎纹蛙选择体温和热耐受性在个体发育过程中的变化.生态学报,2012,32(17):5574-5580.
[30]施林强,赵丽华,马小浩,马小梅.泽陆蛙和饰纹姬蛙蝌蚪不同热驯化下选择体温和热耐受性.生态学报,2012,32(2):465-471.
[31]Reading C J,Clarke R T.Impacts of climate and density on the duration of the tadpole stage of the common toad Bufo bufo.Oecologia,1999,121(3):310-315.
[32]李新红,赵文阁,郭玉民,薛建华.中国林蛙性腺的发育及温度对其性别分化的影响.动物学研究,2001,22(5):351-356.
[33]田秀华,赵文阁,柏永明,段玉宝.东北林蛙人工养殖存在问题及发展对策.野生动物杂志,2009,30(4):214-216.
[34]MerilJ,Laurila A,Laugen A T,Rsnen K.Heads or tails?Variation in tadpole body proportions in response to temperature and food stress.Evolutionary Ecology Research,2004,6(5):727-738.