Abstract
Climate change poses one of the greatest threats to biodiversity. Most analyses of the impacts have focused on changes in mean temperature, but increasing variance will also impact organisms and populations. We assessed the combined effects of the mean and the variance of temperature on thermal tolerances—i.e., critical thermal maxima, critical thermal minima, scope of thermal tolerance, and survival in Drosophila melanogaster. Our six experimental climatic scenarios were: constant mean with zero variance or constant variance or increasing variance; changing mean with zero variance or constant variance or increasing variance. Our key result was that environments with changing thermal variance reduce the scope of thermal tolerance and survival. Heat tolerance seems to be conserved, but cold tolerance decreases significantly with mean low as well as changing environmental temperatures. Flies acclimated to scenarios of changing variance—with either constant or changing mean temperatures—exhibited significantly lower survival rate. Our results imply that changing and constant variances would be just as important in future scenarios of climate change under greenhouse warming as increases in mean annual temperature. To develop more realistic predictions about the biological impacts of climate change, such interactions between the mean and variance of environmental temperature should be considered.
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Araújo MB, Ferri-Yáñez F, Bozinovic F, Chown SL, Marquet PA, Valladares F (2013) Heat freezes niche evolution. Ecol Lett 16:1206–1219
Baldanzi S, Weidberg NF, Fusi M, Cunnicci S, McQuaid CD, Porri F (2015) Contrasting environments shape thermal physiology across the spatial range of the sand hopper Talorchestia capensis. Oecologia 179:1067–1078
Borgman CC, Wolf BO (2016) The indirect effects of climate variability on the reproductive dynamics and productivity of an avian predator in the arid southwest. Oecologia 180:279–291
Bowler K, Terblanche JS (2008) Insect thermal tolerance: what is the role of ontogeny, aging and senescence? Biol Rev 83:339–355
Bozinovic F, Pörtner HO (2015) Physiological ecology meets climate change. Ecol Evol 5:1025–1030
Bozinovic F, Calosi P, Spicer JI (2011a) Physiological correlates of geographic range in animals. Annu Rev Ecol Evol Syst 42:155–179
Bozinovic F, Bastías DA, Boher F, Clavijo-Baquet S, Estay SA, Angilletta MJ (2011b) The mean and variance of environmental temperature interact to determine physiological tolerance and fitness. Physiol Biochem Zool 84:543–552
Bozinovic F, Catalán TP, Estay SA, Sabat P (2013) Acclimation to daily thermal variability drives the metabolic performance curve. Evol Ecol Res 15:579–587
Bozinovic F, Orellana MJ, Martel SI, Bogdanovich JM (2014) Testing the heat-invariant and cold-variability tolerance hypotheses across geographic ranges. Comp Biochem Physiol 178:46–50
Bozinovic F, Sabat P, Rezende EL, Canals M (2016) Temperature variability and thermal performance in ectotherms: acclimation, behaviour, and experimental considerations. Evol Ecol Res 17:111–124
Burroughs WJ (2007) Climate change: a multidisciplinary approach. Cambridge University Press, Cambridge
Clavijo-Baquet S, Boher F, Ziegler L, Martel SI, Estay SA, Bozinovic F (2014) Differential responses to thermal variation between fitness metrics. Sci Rep 4:5349. doi:10.1038/srep05349
Colinet H, Sickair BJ, Vernon P, Renault D (2015) Insects in fluctuating thermal environments. Annu Rev Entomol 60:123–140
Cooper BS, Tharp JM II, Jernberg MJ Angilletta (2012) Developmental plasticity of thermal tolerances in temperate and subtropical populations of Drosophila melanogaster. J Therm Biol 37:211–216
Coumou D, Rahmstorf S (2012) A decade of weather extremes. Nat Clim Change 2:491–496
Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068–2074
Estay SA, Clavijo-Baquet S, Lima M, Bozinovic F (2011) Beyond average: an experimental test of temperature variability on the population dynamics of Tribolium confusum. Poppul Ecol 53:53–58
Estay SA, Lima M, Bozinovic F (2014) The role of temperature variability on insect performance and population dynamics in a warming world. Oikos 123:131–140
Folguera G, Bastías DA, Bozinovic F (2009) Impact of experimental thermal amplitude on ectotherm performance: adaptation to climate change variability? Comp Biochem Physiol 154A:389–393
Gilchrist GW, Huey RB (1999) The direct response of Drosophila melanogaster to selection on knockdown temperature. Heredity 83:15–29
Gould SJ (1985) The median isn’t the message. Discover 6:4042
Hoffmann AA (2010) Physiological climatic limits in Drosophila: patterns and implications. J Exp Biol 213:870–880
Hoffmann AA, Shirriffs J, Scott M (2005) Relative importance of plastic vs genetic factors in adaptive differentiation: geographical variation for stress resistance in Drosophila melanogaster from eastern Australia. Funct Ecol 19:222–227
IPCC (2014) Impacts, adaptation, and vulnerability. In: Barros VR, Field CB, Dokken DJ, Mastrandea MD, Macj KJ, Bilir TE, Chaterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracjken S, Mastrandea PR, White LL (eds) Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
Ji X, Gao J, Han J (2007) Phenotypic responses of hatchlings to constant versus fluctuate incubation temperatures in the multi-banded krait, Bungarus multicintus (Elapidae). Zool Sci 24:384–390
Kern P, Cramp RL, Franklin CE (2015) Physiological responses of ectotherms to daily temperature variation. J Exp Biol 218:3068–3076
Kingsolver Ragland GJ JG (2008) The effect of fluctuating temperatures on ectotherm life-history traits: comparisons among geographic populations of Wyeomyia smithii. Evol Ecol Res 10:29–44
Krams I, Daukste J, Kivleniece I, Krama T, Rantala MJ (2011) Overwintering survival on immune defence and body length in male Aquarius najas water striders. Entomol Exp Appl 140:45–51
Kubisch EL, Fernández JB, Ibargüengoytía NR (2016) Vulnerability to climate warming of Liolaemus pictus (Squamata, Liolaemidae), a lizard from the cold temperate climate in Patagonia, Argentina. J Comp Physiol B 186:243–253
Lawson CR, Vindenes Y, Bailey L, van de Pol M (2015) Environmental variation and population responses to global change. Ecol Lett 18:724–736
Levins R (1968) Evolution in changing environments. Princeton University Press, Princeton
Ohtsu T, Kimura MT, Hori SH (1992) Energy storage during reproductive diapause in the Drosophila melanogaster species group. J Comp Physiol B 162:203–208
Orcutt JD, Porter KG (1983) Diel vertical migration by zooplankton: constant and fluctuating temperature effects on life history parameters of Daphnia. Limnol Oceanogr 28:720–730
Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB (2010) Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA 107:15135–15139
Parkash D, Aggarwal DD, Singh D, Lambhod C, Ranga P (2013) Divergence of water balance mechanisms in two sibling species (Drosophila simulans and D. melanogaster): effects of growth temperatures. J Comp Physiol B 183:359–378
Pétavy G, David JR, Debat V, Gibert P, Moreteau B (2004) Specific effects of cycling stressful temperatures upon phenotypic and genetic variability of size traits in Drosophila melanogaster. Evol Ecol Res 6:873–890
Richter S, Kipfer T, Wohlgemuth T, Calderon-Guerrero C, Ghazoul J, Moser B (2012) Phenotypic plasticity facilitates resistance to climate change in a highly variable environment. Oecologia 169:269–279
Rojas JM, Castillo SB, Folguera G, Abades S, Bozinovic F (2014) Coping with daily thermal variability: behavioral performance of an ectotherm model in a warming world. PLoS One 9(9):e106897
Schou MF, Kristensen TN, Kellermann V, Schlötterer C, Loeschke V (2014) A Drosophila laboratory evolution experiment points to low evolutionary potential under increased temperatures likely to be experienced in the future. J Evol Biol 27:1859–1868
Siddiqui WH, Barlow CA (1972) Population growth of Drosophila melanogaster (Diptera: Drosophilidae) at constant and alternating temperatures. Ann Entomol Soc Am 65:993–1001
Somero GN (2011) Comparative physiology: a ‘crystal ball’ for predicting consequences of global change. Am J Physiol 302:R1–R14
StatSoft, Inc. (2001) STATISTICA. http://www.statsoft.com
Sunday JM, Bates AE, Kearney MR, Colwell RK, Dulvy NK, Longino JT, Huey RB (2014) Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc Natl Acad Sci USA 111:5610–5615
Terblanche JS, Klok CJ, Krafsur ES, Chown SL (2006) Phenotypic plasticity and geographic variation in thermal tolerance and water loss of the tsetse Glossina pallidipes (Diptera: Glossinidae): implications for distribution modelling. Am J Trop Med Hyg 74:786–794
Terblanche JS, Nyamukoniwa C, Elsje K (2010) Thermal variability alters climatic stress resistance and plastic response in a global invasive pest, the Mediterranean fruit fly (Ceratitis capitata). Entomol Exp Appl 137:304–315
Vasseur DA, DeLong JP, Gilbert B, Greig HS, Harley CDG, McCann KS, Savage V, Tunney TD, O’Connor MI (2014) Increased temperature variation poses a greater risk to species than climate warming. Proc R Soc B 281:2013–2612
Vazquez DP, Gianoli E, Morris WF, Bozinovic F (2015) Evolutionary and ecological impacts of increased climatic variability. Biol Rev. doi:10.1111/brv.12216
Wang G, Dillon ME (2014) Recent geographic convergence in diurnal and annual temperature cycling flattens global thermal profiles. Nat Clim Change 4:988–999
West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford
Williams CM, Marshall KE, MacMillan HA, Dzursin JDK, Hellmann JJ, Sinclair BJ (2012) Thermal variability increases the impact of autumnal warming and drives metabolic depression in an overwintering butterfly. PLoS One 7:e34470
Zhang W, Rudolf VHW, Ma C (2015) Stage-specific heat effects: timing and duration of heat waves alter demographic rates of a global insect pest. Oecologia 179:947–957
Acknowledgments
All experimental procedures were approved by the Universidad Católica animal care committee. Funded by FONDECYT-1130015, FONDECYT-3140450 to GC and CAPES FB002 line 3 to FB. We thank Claudio Latorre for valuable commentaries and three anonymous referees.
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Communicated by G. Heldmaier.
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Bozinovic, F., Medina, N.R., Alruiz, J.M. et al. Thermal tolerance and survival responses to scenarios of experimental climatic change: changing thermal variability reduces the heat and cold tolerance in a fly. J Comp Physiol B 186, 581–587 (2016). https://doi.org/10.1007/s00360-016-0980-6
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DOI: https://doi.org/10.1007/s00360-016-0980-6