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Low precipitation aggravates the impact of extreme high temperatures on lizard reproduction

  • Physiological ecology - original research
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Abstract

Extreme high temperatures are occurring more frequently with ongoing anthropogenic climate warming, but the experimental tests of the effects of high temperatures on terrestrial vertebrates in natural conditions are rare. In this study, we investigated the effects of extreme high temperatures on female reproduction and offspring traits of multi-ocellated racerunners (Eremias multiocellata) kept in field enclosures in the desert steppe of Inner Mongolia. Our studies indicate that high temperatures significantly affect the gestation period and reproductive output of females and the offspring sex ratio, but have little impact on offspring body size and mass. More interestingly, we found that the effect of extreme high temperatures on female reproductive output was not consistent between two consecutive years that differed in precipitation. Low precipitation may aggravate the impact of climate warming on lizards and negatively affect the survival of lizards in the desert steppe. Our results provide evidence that temperature interacts with precipitation to determine the life history of lizards, and they suggest that a drier and hotter environment, such as the future climate in arid mid-latitude areas, will likely impose severe pressure on lizard populations, which are an important component of the food web in desert areas around the world.

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References

  • Adler PB, Drake JM (2008) Environmental variation, stochastic extinction, and competitive coexistence. Am Nat 172:E186–E195. doi:10.1086/591678

    Article  Google Scholar 

  • Adler RF, Gu GJ, Wang JJ, Huffman GJ, Curtis S, Bolvin D (2008) Relationships between global precipitation and surface temperature on interannual and longer timescales (1979–2006). J Geophys Res-Atmos 113:D22104. doi:10.1029/2008jd010536

    Article  Google Scholar 

  • Angilletta MJ (2009)Thermal Adaptation: A Theoretical and Empirical Synthesis. Oxford University Press

  • Bauerfeind SS, Fischer K (2014) Simulating climate change: temperature extremes but not means diminish performance in a widespread butterfly. Popul Ecol 56:239–250. doi:10.1007/s10144-013-0409-y

    Article  Google Scholar 

  • Bell K, Blomberg S, Schwarzkopf L (2013) Detrimental influence on performance of high temperature incubation in a tropical reptile: is cooler better in the tropics? Oecologia 171:83–91. doi:10.1007/s00442-012-2409-6

    Article  PubMed  Google Scholar 

  • Birchard GF, Deeming DC (2004) Effects of incubation temperature. In: Deeming DC (ed) Reptilian incubation: environment, evolution and behaviour. Nottingham University Press, Nottingham

    Google Scholar 

  • Bonebrake TC, Mastrandrea MD (2010) Tolerance adaptation and precipitation changes complicate latitudinal patterns of climate change impacts. P Natl Acad Sci USA 107:12581–12586. doi:10.1073/pnas.0911841107

    Article  CAS  Google Scholar 

  • Bradshaw WE, Holzapfel CM (2006) Climate change: evolutionary response to rapid climate change. Science 312:1477–1478. doi:10.1126/science.1127000

    Article  CAS  PubMed  Google Scholar 

  • Chamaille-Jammes S, Massot M, Aragon P, Clobert J (2006) Global warming and positive fitness response in mountain populations of common lizards Lacerta vivipara. Glob Chang Biol 12:392–402. doi:10.1111/j.1365-2486.2005.01088.x

    Article  Google Scholar 

  • Choi G et al (2009) Changes in means and extreme events of temperature and precipitation in the Asia-Pacific Network region, 1955–2007. Int J Climatol 29:1906–1925. doi:10.1002/joc.1979

    Article  Google Scholar 

  • Clusella-Trullas S, Blackburn TM, Chown SL (2011) Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change. Am Nat 177:738–751. doi:10.1086/660021

    Article  PubMed  Google Scholar 

  • Costantini D, Carello L, Dell’Omo G (2010) Patterns of covariation among weather conditions, winter North Atlantic Oscillation index and reproductive traits in Mediterranean kestrels. J Zool 280:177–184. doi:10.1111/j.1469-7998.2009.00649.x

    Article  Google Scholar 

  • Deeming DC (2004) Reptilian incubation: environment, evolution and behaviour. Nottingham University Press, Nottingham

    Google Scholar 

  • Dillon ME, Wang G, Huey RB (2010) Global metabolic impacts of recent climate warming. Nature 467:704–706. doi:10.1038/nature09407

    Article  CAS  PubMed  Google Scholar 

  • Dobkin DS, Olivieri I, Ehrlich PR (1987) Rainfall and the interaction of microclimate with larval resources in the population-dynamics of checkerspot butterflies (Euphydryas editha) inhabiting serpentine grassland. Oecologia 71:161–166. doi:10.1007/Bf00377280

    Article  Google Scholar 

  • Du WG, Ji X (2003) The effects of incubation thermal environments on size, locomotor performance and early growth of hatchling soft-shelled turtles, Pelodiscus sinensis. J Therm Biol 28:279–286. doi:10.1016/S0306-4565(03)00003-2

    Article  Google Scholar 

  • Du WG, Ji X (2006) Effects of constant and fluctuating temperatures on egg survival and hatchling traits in the northern grass lizard (Takydromus septentrionalis, Lacertidae). J Exp Zool 305A:47–54. doi:10.1002/jez.a.243

    Article  Google Scholar 

  • Du W-G, Shine R (2015) The behavioural and physiological strategies of bird and reptile embryos in response to unpredictable variation in nest temperature. Biol Rev 90:19–30. doi:10.1111/brv.12089

    Article  PubMed  Google Scholar 

  • Du W-G, Yan S-J, Ji X (2000) Selected body temperature, thermal tolerance and thermal dependence of food assimilation and locomotor performance in adult blue-tailed skinks, Eumeces elegans. J Therm Biol 25:197–202. doi:10.1016/S0306-4565(99)00022-4

    Article  Google Scholar 

  • Dubey S, Shine R (2011) Predicting the effects of climate change on reproductive fitness of an endangered montane lizard, Eulamprus leuraensis (Scincidae). Clim Change 107:531–547. doi:10.1007/s10584-010-9963-x

    Article  Google Scholar 

  • Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068–2074. doi:10.1126/science.289.5487.2068

    Article  CAS  PubMed  Google Scholar 

  • Fieldhouse DJ, Palmer WC (1965) The climate of the northeast: meteorological and agricultural drought. University of Delaware, Agricultural Experiment Station, Newark

    Google Scholar 

  • Glickman TS (2000) Glossary of Meteorology, 2nd edn. American Meteorological Society, Boston, Mass

    Google Scholar 

  • Hoffmann AA, Anderson A, Hallas R (2002) Opposing clines for high and low temperature resistance in Drosophila melanogaster. Ecol Lett 5:614–618. doi:10.1046/j.1461-0248.2002.00367.x

    Article  Google Scholar 

  • Huey RB, Tewksbury JJ (2009) Can behavior douse the fire of climate warming? P Natl Acad Sci USA 106:3647–3648. doi:10.1073/pnas.0900934106

    Article  CAS  Google Scholar 

  • Ihlow F et al (2012) On the brink of extinction? How climate change may affect global chelonian species richness and distribution. Glob Chang Biol 18:1520–1530. doi:10.1111/j.1365-2486.2011.02623.x

    Article  Google Scholar 

  • IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

  • James CD, Whitford WG (1994) An experimental study of phenotypic plasticity in the clutch size of a lizard. Oikos 70:49–56. doi:10.2307/3545698

    Article  Google Scholar 

  • Janzen FJ (1994) Climate-change and temperature-dependent sex determination in reptiles. P Natl Acad Sci USA 91:7487–7490. doi:10.1073/pnas.91.16.7487

    Article  CAS  Google Scholar 

  • Jentsch A, Kreyling J, Beierkuhnlein C (2007) A new generation of climate-change experiments: events, not trends. Front Ecol Environ 5:365–374. doi:10.1890/1540-9295(2007)5[365:angoce]2.0

    Article  Google Scholar 

  • Ji X, Lin L-H, Luo L-G, Lu H-L, Gao J-F, Han J (2006) Gestation temperature affects sexual phenotype, morphology, locomotor performance and growth of neonatal brown forest skink, Sphenomorphus indicus. Biol J Linn Soc 88:453–463. doi:10.1111/j.1095-8312.2006.00633.x

    Article  Google Scholar 

  • Johnston IA, Bennett AF (1996) Animals and temperature: phenotypic and evolutionary adaptation. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Kearney M, Shine R, Porter WP (2009) The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. P Natl Acad Sci USA 106:3835–3840. doi:10.1073/pnas.0808913106

    Article  CAS  Google Scholar 

  • Li H, Qu Y-F, Ding G-H, Ji X (2011) Life-history variation with respect to experienced thermal environments in the lizard, Eremias multiocellata (Lacertidae). Zool Sci 28:332–338. doi:10.2108/zsj.28.332

    Article  PubMed  Google Scholar 

  • Lorenzon P, Clobert J, Massot M (2001) The contribution of phenotypic plasticity to adaptation in Lacerta vivipara. Evolution 55:392–404

    Article  CAS  PubMed  Google Scholar 

  • Lu H-L, Wang Y, Tang W-Q, Du W-G (2013) Experimental evaluation of reproductive response to climate warming in an oviparous skink. Integr Zool 8:175–183. doi:10.1111/1749-4877.12025

    Article  PubMed  Google Scholar 

  • Lu Z-C, Wang Y-M, Zhu S-G, Yu H, Guo J-Y, Wan F-H (2014) Trade-offs between survival, longevity, and reproduction, and variation of survival tolerance in Mediterranean Bemisia tabaci after temperature stress. J Insect Sci 14:1–11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma L, Sun B-J, Li S-R, Sha W, Du W-G (2014) Maternal thermal environment induces plastic responses in the reproductive life history of oviparous lizards. Physiol Biochem Zool 87:677–683. doi:10.1086/678050

    Article  PubMed  Google Scholar 

  • Madsen T, Shine R (2000) Rain, fish and snakes: climatically driven population dynamics of Arafura filesnakes in tropical Australia. Oecologia 124:208–215. doi:10.1007/s004420050008

    Article  Google Scholar 

  • Marquis O, Massot M, Le Galliard JF (2008) Intergenerational effects of climate generate cohort variation in lizard reproductive performance. Ecology 89:2575–2583. doi:10.1890/07-1211.1

    Article  PubMed  Google Scholar 

  • McKinnon L, Picotin M, Bolduc E, Juillet C, Bêty J (2012) Timing of breeding, peak food availability, and effects of mismatch on chick growth in birds nesting in the High Arctic. Can J Zool 90:961–971. doi:10.1139/z2012-064

    Article  Google Scholar 

  • Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997. doi:10.1126/science.1098704

    Article  CAS  PubMed  Google Scholar 

  • Meehl GA, Tebaldi C, Teng H, Peterson TC (2007) Current and future US weather extremes and El Nino. Geophys Res Lett 34:6. doi:10.1029/2007gl031027

    Google Scholar 

  • Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant–pollinator interactions. Ecol Lett 10:710–717. doi:10.1111/j.1461-0248.2007.01061.x

    Article  PubMed  Google Scholar 

  • Mitchell NJ, Kearney MR, Nelson NJ, Porter WP (2008) Predicting the fate of a living fossil: how will global warming affect sex determination and hatching phenology in tuatara? P Roy Soc B-Biol Sci 275:2185–2193. doi:10.1098/rspb.2008.0438

    Article  Google Scholar 

  • Ohlberger J (2013) Climate warming and ectotherm body size—from individual physiology to community ecology. Funct Ecol 27:991–1001. doi:10.1111/1365-2435.12098

    Article  Google Scholar 

  • Olsson M, Shine R (1997) The seasonal timing of oviposition in sand lizards (Lacerta agilis): why early clutches are better. J Evol Biol 10:369–381. doi:10.1007/s000360050030

    Article  Google Scholar 

  • Pachauri RK, Meyer LA, IPCC (2014) Climate change 2014: synthesis report. IPCC, Geneva, Switzerland

    Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol S 37:637–669. doi:10.1146/annurev.ecolsys.37.091305.110100

    Article  Google Scholar 

  • Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Chang Biol 13:1860–1872. doi:10.1111/j.1365-2486.2007.01404.x

    Article  Google Scholar 

  • Perkins SE, Alexander LV, Nairn JR (2012) Increasing frequency, intensity and duration of observed global heatwaves and warm spells. Geophys Res Lett 39:L20714. doi:10.1029/2012gl053361

    Google Scholar 

  • Pianka ER (1986) Ecology and natural history of desert lizards. Princeton University Press, Princeton

    Google Scholar 

  • Qian T, Dai A, Trenberth KE (2007) Hydroclimatic trends in the Mississippi River basin from 1948 to 2004. J Climate 20:4599–4614. doi:10.1175/Jcli4262.1

    Article  Google Scholar 

  • Qu Y-F, Li H, Gao J-F, Xu X-F, Ji X (2011) Thermal preference, thermal tolerance and the thermal dependence of digestive performance in two Phrynocephalus lizards (Agamidae), with a review of species studied. Curr Zool 57:684–700

    Article  Google Scholar 

  • Robert KA, Thompson MB (2001) Sex determination—Viviparous lizard selects sex of embryos. Nature 412:698–699. doi:10.1038/35089135

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Diaz T, Gonzalez F, Ji X, Brana F (2010) Effects of incubation temperature on hatchling phenotypes in an oviparous lizard with prolonged egg retention: are the two main hypotheses on the evolution of viviparity compatible? Zoology 113:33–38. doi:10.1016/j.zool.2009.05.001

    Article  PubMed  Google Scholar 

  • Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60. doi:10.1038/nature01333

    Article  CAS  PubMed  Google Scholar 

  • Rosa R, Seibel BA (2008) Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator. P Natl Acad Sci USA 105:20776–20780. doi:10.1073/pnas.0806886105

    Article  CAS  Google Scholar 

  • Schulte-Hostedde A, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163

    Article  Google Scholar 

  • Seneviratne SI, Donat MG, Mueller B, Alexander LV (2014) No pause in the increase of hot temperature extremes. Nat Clim Chang 4:320

    Article  Google Scholar 

  • Sinervo B et al (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894–899. doi:10.1126/science.1184695

    Article  CAS  PubMed  Google Scholar 

  • Smith MD (2011) The ecological role of climate extremes: current understanding and future prospects. J Ecol 99:651–655. doi:10.1111/j.1365-2745.2011.01833.x

    Article  Google Scholar 

  • Sun Y, Solomon S, Dai A, Portmann RW (2007) How often will it rain? J Clim 20:4801–4818. doi:10.1175/Jcli4263.1

    Article  Google Scholar 

  • Tang X-L et al (2012) Effects of gestation temperature on offspring sex and maternal reproduction in a viviparous lizard (Eremias multiocellata) living at high altitude. J Therm Biol 37:438–444. doi:10.1016/j.jtherbio.2012.03.002

    Article  Google Scholar 

  • Telemeco RS, Radder RS, Baird TA, Shine R (2010) Thermal effects on reptile reproduction: adaptation and phenotypic plasticity in a montane lizard. Biol J Linn Soc 100:642–655. doi:10.1111/j.1095-8312.2010.01439.x

    Article  Google Scholar 

  • Thompson DM, Cole JE, Shen GT, Tudhope AW, Meehl GA (2015) Early twentieth-century warming linked to tropical Pacific wind strength. Nat Geosci 8:117–121. doi:10.1038/Ngeo2321

    Article  CAS  Google Scholar 

  • Triggs A, Knell RJ (2012) Interactions between environmental variables determine immunity in the Indian meal moth Plodia interpunctella. J Anim Ecol 81:386–394. doi:10.1111/j.1365-2656.2011.01920.x

    Article  PubMed  Google Scholar 

  • Valenzuela N, Lance V (2004) Temperature dependent sex determination in vertebrates. Smithsonian Books, Washington DC

    Google Scholar 

  • Vose RS, Easterling DR, Gleason B (2005) Maximum and minimum temperature trends for the globe: an update through 2004. Geophys Res Lett 32:L23822. doi:10.1029/2005gl024379

    Article  Google Scholar 

  • Wang Z, Lu H-L, Ma L, Ji X (2014) Viviparity in high-altitude Phrynocephalus lizards is adaptive because embryos cannot fully develop without maternal thermoregulation. Oecologia 174:639–649. doi:10.1007/s00442-013-2811-8

    Article  PubMed  Google Scholar 

  • Wapstra E et al (2009) Climate effects on offspring sex ratio in a viviparous lizard. J Anim Ecol 78:84–90. doi:10.1111/j.1365-2656.2008.01470.x

    Article  PubMed  Google Scholar 

  • Warner DA, Shine R (2007) Fitness of juvenile lizards depends on seasonal timing of hatching, not offspring body size. Oecologia 154:65–73. doi:10.1007/s00442-007-0809-9

    Article  PubMed  Google Scholar 

  • Wells N, Goddard S, Hayes MJ (2004) A self-calibrating palmer drought severity index. J Clim 17:2335–2351. doi:10.1175/1520-0442(2004)017<2335:Aspdsi>2.0.Co;2

    Article  Google Scholar 

  • Wernberg T, Smale DA, Thomsen MS (2012) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob Chang Biol 18:1491–1498. doi:10.1111/j.1365-2486.2012.02656.x

    Article  Google Scholar 

  • Wolkovich EM et al (2012) Warming experiments underpredict plant phenological responses to climate change. Nature 485:494–497. doi:10.1038/nature11014

    CAS  PubMed  Google Scholar 

  • Zeng Z-G et al (2014) Effects of habitat alteration on lizard community and food web structure in a desert steppe ecosystem. Biol Conserv 179:86–92. doi:10.1016/j.biocon.2014.09.011

    Article  Google Scholar 

  • Zhang D-J, Tang X-L, Yue F, Chen Z, Li R-D, 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. doi:10.1016/j.jtherbio.2010.01.003

    Article  Google Scholar 

  • Zhao E-M, Zhao K-T, Zhou K-Y (1999) Fauna Sinica Reptilia Vol. 2 Squamata. Chinese Science Press, Beijing

    Google Scholar 

  • Zittier ZMC, Hirse T, Portner HO (2013) The synergistic effects of increasing temperature and CO2 levels on activity capacity and acid-base balance in the spider crab, Hyas araneus. Mar Biol 160:2049–2062. doi:10.1007/s00227-012-2073-8

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Shao-Yong Chen and Zhi-Liang Jie for their assistance in the field and laboratory. This work was supported by grants from the One Hundred Talents Program of the Chinese Academy of Sciences and the National Natural Sciences Foundation of China (31372203).

Author contribution statement

W. G. D. designed the study, Y. W., Z. G. Z., S. R. L. and J. H. B. conducted experiments, W. G. D. and Y. W. analysed data, and wrote the paper.

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Authors and Affiliations

  1. Key Laboratory of Animal Ecology and Conservational Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, People’s Republic of China

    Yang Wang, Zhi-Gao Zeng, Shu-Ran Li & Wei-Guo Du

  2. University of Chinese Academy of Sciences, Beijing, People’s Republic of China

    Yang Wang & Shu-Ran Li

  3. College of Life Sciences, Inner Mongolia Normal University, Hohhot, 010022, Inner Mongolia, China

    Jun-Huai Bi

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  1. Yang Wang
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  2. Zhi-Gao Zeng
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Correspondence to Wei-Guo Du.

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Communicated by Hannu J. Ylonen.

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Wang, Y., Zeng, ZG., Li, SR. et al. Low precipitation aggravates the impact of extreme high temperatures on lizard reproduction. Oecologia 182, 961–971 (2016). https://doi.org/10.1007/s00442-016-3727-x

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