Zhongwen JIANG,Liang Ma,Shiang Tao,et al.Higher Body Temperatures and Earlier Parturition in Response to Hypoxia Experienced by Pregnant Lizards[J].Asian Herpetological Research(AHR),2021,12(2):228-233.[doi:10.16373/j.cnki.ahr.200102]
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Higher Body Temperatures and Earlier Parturition in Response to Hypoxia Experienced by Pregnant Lizards
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Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

2021 VoI.12 No.2
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Higher Body Temperatures and Earlier Parturition in Response to Hypoxia Experienced by Pregnant Lizards
Zhongwen JIANG12 Liang Ma13* Shi’ang Tao4 Xingzhi Han5
1 Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
2 University of Chinese Academy of Sciences, Beijing 100049, China
3 Princeton School of Public and International Affairs, Princeton University, Princeton, New Jersey 08544, USA
4 College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua 321004, Zhejiang, China
5 College of Wildlife and Protected Area, Northeast Forestry University, Harbin 150040, Heilongjiang, China
climate change hypoxia offspring pregnant female reproduction viviparous lizard
Many species are shifting towards higher altitudes in response to global warming, but how these upslope-shifting species will respond to hypoxic environments at high altitudes remains unclear. Hypoxia can be especially challenging for viviparous reproduction because of the limitation of oxygen supply to the female and her developing embryos. To investigate the effect of hypoxia on viviparous females and their offspring we acclimated pregnant females of a high-altitude dwelling viviparous lizard (Phrynocephalus vlangalii) to local oxygen and hypoxia conditions, respectively. We then recorded maternal body temperatures, postpartum body condition, as well as offspring morphology and locomotor performance. We found that pregnant females had higher body temperatures and advanced their parturition under hypoxic acclimation. However, maternal body condition, offspring morphology and locomotor performance were unaffected by the hypoxic conditions during gestation. Our study suggests that upslope-shifting viviparous lizards respond to hypoxic environments by plastically adjusting their body temperatures to reduce parturition time, without short-term costs to offspring traits.


Angilletta M. J., Hill T., Robson M. A. 2002. Is physiological performance optimized by thermoregulatory behavior?: A case study of the eastern fence lizard, Sceloporus undulatus. J Therm Biol, 27: 199–204
Bani L., Luppi M., Rocchia E., Dondina O., Orioli V. 2019. Winners and losers: How the elevational range of breeding birds on Alps has varied over the past four decades due to climate and habitat changes. Ecol Evol, 9: 1289–1305
Bellard C., Bertelsmeier C., Leadley P., Thuiller W., Courchamp F. 2012. Impacts of climate change on the future of biodiversity. Ecol Lett, 15: 365–377
Beuchat C. A. 1988. Temperature effects during gestation in a viviparous lizard. J Therm Biol, 13: 135–142
Blackburn D.G. 1993. Chorioallantoic placentation in squamate reptiles: structure, function, development, and evolution. J Exp Zool, 266: 414–430
Cadena V., Tattersall G. J. 2009. Decreased precision contributes to the hypoxic thermoregulatory response in lizards. J Exp Biol, 212: 137–144
Cano A., Fons J., Brines J. 2001. The effects on offspring of premature parturition. Hum Reprod Update, 7: 487–494
Carretero M. A., Roig J. M., Llorente G. A. 2005. Variation in preferred body temperature in an oviparous population of Lacerta (Zootoca) vivipara. Herpetol J, 15: 51–55
Chen I. C., Hill J. K., Ohlemüller R., Roy D. B., Thomas C. D. 2011. Rapid range shifts of species associated with high levels of climate warming. Science, 333: 1024–1026
Davies D. G., Thomas J. L., Smith E. N. 1982. Effect of body temperature on ventilatory control in the alligator. J Appl Physiol, 52: 114–118
Deeming D. C., Ferguson M. W. J. 1991. Physiological effects of incubation temperature on embryonic development in reptiles and birds. In Egg Incubation: Its Effect On Embryonic Development In Birds and Reptiles (eds. Deeming D. C. and Ferguson M. W. J.), Cambridge: Cambridge University Press, 147–171
DeMarco V. 1993. Metabolic rates of female viviparous lizards (Sceloporus jarrovi) throughout the reproductive cycle: do pregnant lizards adhere to standard allometry? Physiol Zool, 66: 166–180
Du W. G., Lü D. 2009. An experimental test of body volume constraint on female reproductive output. J Exp Zool Part A Ecol Genet Physiol, 313: 123–128
Freeman B. G., Freeman A. M. C. 2014. Rapid upslope shifts in New Guinean birds illustrate strong distributional responses of tropical montane species to global warming. Proc Natl Acad Sci USA, 111: 4490–4494
Griffith S. C., Mainwaring M. C., Sorato E., Beckmann C. 2016. High atmospheric temperatures and ‘ambient incubation’drive embryonic development and lead to earlier hatching in a passerine bird. R Soc Open Sci, 3: 150371
He J., Xiu M., Tang X., Yue F., Wang N., Yang S., Chen Q. 2013. The different mechanisms of hypoxic acclimatization and adaptation in lizard Phrynocephalus vlangalii living on Qinghai‐Tibet Plateau. J Exp Zool Part A: Ecol Genet Physiol, 319: 117–123
Herman J., Ingermann R. 1996. Effects of hypoxia and hyperoxia on oxygen-transfer properties of the blood of a viviparous snake. J Exp Biol, 199: 2061–2070
Hickling R., Roy D. B., Hill J. K., Fox R., Thomas C. D. 2006. The distributions of a wide range of taxonomic groups are expanding polewards. Glob Chang Biol, 12: 450–455
Hicks J. W., Wood S. C. 1985. Temperature regulation in lizards: effects of hypoxia. Am J Physiol Integr Comp Physiol, 248: R595–R600
Husak J. F. 2006. Do female collared lizards change field use of maximal sprint speed capacity when gravid? Oecologia, 150: 339–343
Huey R. B., Kearney M. R., Krockenberger A., Holtum J. A. M., Jess M., Williams S. E. 2012. Predicting organismal vulnerability to climate warming: Roles of behaviour, physiology and adaptation. Philos Trans R Soc B: Biol Sci, 367: 1665–1679
Ji X., Du W. G., Sun P. Y. 1996. Body temperature, thermal tolerance and influence of temperature on sprint speed and food assimilation in adult grass lizards, Takydromus septentrionalis. J Therm Biol, 21: 155–161
Kouyoumdjian L., Gangloff E. J., Souchet J., Cordero G. A., Dupoué A., Aubret F. 2019. Transplanting gravid lizards to high elevation alters maternal and embryonic oxygen physiology, but not reproductive success or hatchling phenotype. J Exp Biol, 222: jeb206839
Kuznetsova A., Brockhoff P. B., Christensen R. H. B. 2017. lmerTest package: tests in linear mixed effects models. J Stat Softw, 82. doi: 10.18637/jss.v082.i13
Li H., Qu Y. F., Hu R. B., Ji X. 2009. Evolution of viviparity in cold-climate lizards: testing the maternal manipulation hypothesis. Evol Ecol, 23: 777–790
Li X .H., Wu P. F., Ma L., Huebner C., Sun B. J., Li S. R. 2020. Embryonic and post‐embryonic responses to high‐elevation hypoxia in a low‐elevation lizard. Integr Zool, 15: 338–348
Liang L., Sun B. J., Ma L., Du W. G. 2015. Oxygen-dependent heat tolerance and developmental plasticity in turtle embryos. J Comp Physiol B, 185: 257–263
López-Alcaide S., Nakamura M., Macip-Rios R., Martínez-Meyer E. 2014. Does behavioural thermoregulation help pregnant Sceloporus adleri lizards in dealing with fast environmental temperature rise? Herpetol J, 24: 41–47
Manlik O. 2019. The importance of reproduction for the conservation of slow-growing animal populations.Springer Press. (Cited pages can be provided, e. g., 13–39)
Mathies T., Andrews R. M. 1997. Influence of pregnancy on the thermal biology of the lizard, Sceloporus jarrovi: why do pregnant females exhibit low body temperatures? Funct Ecol, 11: 498–507
Munns S. L. 2013. Gestation increases the energetic cost of breathing in the lizard Tiliqua rugosa. J Exp Biol, 216: 171–180
Munns S. L., Daniels C. 2006. Breathing with big babies: ventilation and oxygen consumption during pregnancy in the lizard Tiliqua rugosa. Physiol Biochem Zool, 80: 35–45
Parmesan C., Yohe G. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421: 37–42
Piercy J., Rogers K., Reichert M., Andrade D. V, Abe A. S., Tattersall G. J., Milsom W. K. 2015. The relationship between body temperature, heart rate, breathing rate, and rate of oxygen consumption, in the tegu lizard (Tupinambis merianae) at various levels of activity. J Comp Physiol B, 185: 891–903
Pinheiro J, Bates D, DebRoy S., Sarkar D. R. Core Team. 2020. nlme: Linear and nonlinear mixed effects models. Retrieved from https://svn.r-project.org/R-packages/trunk/nlme/
Plasman M., McCue M. D., Reynoso V. H., Terblanche J. S., Clusella-Trullas S. 2019. Environmental temperature alters the overall digestive energetics and differentially affects dietary protein and lipid use in a lizard. J Exp Biol, 222: jeb194480
Radder R. S., Elphick M. J., Warner D. A., Pike D. A., Shine R. 2008. Reproductive modes in lizards: measuring fitness consequences of the duration of uterine retention of eggs. Funct Ecol, 22: 332–339
Robert K. A., Thompson M. B. 2000. Energy consumption by embryos of a viviparous lizard, Eulamprus tympanum, during development. Comp Biochem Physiol Part A: Mol Integr Physiol, 127: 481–486
Shine R. 1980. “Costs” of reproduction in reptiles. Oecologia, 46: 92–100
Sun B. J., Wang T. T., Pike D. A., Liang L., Du W. G. 2014. Embryonic oxygen enhances learning ability in hatchling lizards. Front Zool, 11: 21
Tattersall G. J., Gerlach R. M. 2005. Hypoxia progressively lowers thermal gaping thresholds in bearded dragons, Pogona vitticeps. J Exp Biol, 208: 3321–3330
Thomas C. D. 2010. Climate, climate change and range boundaries. Divers Distrib, 16: 488–495
Timmerman C. M., Chapman L. J. 2003. The effect of gestational state on oxygen consumption and response to hypoxia in the sailfin molly, Poecilia latipinna. Environ Biol Fishes, 68: 293–299
Warkentin K. M. 1995. Adaptive plasticity in hatching age: a response to predation risk trade-offs. Proc Natl Acad Sci USA, 92: 3507–3510
Warkentin K. M. 2007. Oxygen, gills, and embryo behavior: mechanisms of adaptive plasticity in hatching. Comp Biochem Physiol A: Mol Integr Physiol, 148: 720–731
Wong B., Candolin U. 2015. Behavioral responses to changing environments. Behav Ecol, 26: 665–673
Wu Y., Fu J., Yue B., Qi Y. 2015. An atypical reproductive cycle in a common viviparous Asia Agamid Phrynocephalus vlangalii. Ecol Evol, 5: 5138–5147
Zhang D. J., Tang X. L., Yue F., Chen Z., Chen Q. 2010. Effect of gestation temperature on sexual and morphological phenotypes of offspring in a viviparous lizard, Eremias multiocellata. J Therm Biol, 35: 129–133
Zani P. A., Neuhaus R. A., Jones T. D., Milgrom J. E. 2008. Effects of reproductive burden on endurance performance in side-blotched lizards (Uta stansburiana). J Herpetol, 42: 76–81
Zhao D., Wu S. 2019. Projected changes in permafrost active layer thickness over the Qinghai‐Tibet Plateau under climate change. Water Resour Res, 55: 7860–7875
Zhao E. M., Zhao K. T., Zhou K. Y. 1999. Fauna Sinica: Reptilia. Squamata, Lacertilia. Science Press (In Chinese) (Cited pages can be provided, e. g., 189–191)


Last Update: 2021-06-25