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PLOS ONE  2012 

Thermal Variability Increases the Impact of Autumnal Warming and Drives Metabolic Depression in an Overwintering Butterfly

DOI: 10.1371/journal.pone.0034470

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Abstract:

Increases in thermal variability elevate metabolic rate due to Jensen's inequality, and increased metabolic rate decreases the fitness of dormant ectotherms by increasing consumption of stored energy reserves. Theory predicts that ectotherms should respond to increased thermal variability by lowering the thermal sensitivity of metabolism, which will reduce the impact of the warm portion of thermal variability. We examined the thermal sensitivity of metabolic rate of overwintering Erynnis propertius (Lepidoptera: Hesperiidae) larvae from a stable or variable environment reared in the laboratory in a reciprocal common garden design, and used these data to model energy use during the winters of 1973–2010 using meteorological data to predict the energetic outcomes of metabolic compensation and phenological shifts. Larvae that experienced variable temperatures had decreased thermal sensitivity of metabolic rate, and were larger than those reared at stable temperatures, which could partially compensate for the increased energetic demands. Even with depressed thermal sensitivity, the variable environment was more energy-demanding than the stable, with the majority of this demand occurring in autumn. Autumn phenology changes thus had disproportionate influence on energy consumption in variable environments, and variable-reared larvae were most susceptible to overwinter energy drain. Therefore the energetic impacts of the timing of entry into winter dormancy will strongly influence ectotherm fitness in northern temperate environments. We conclude that thermal variability drives the expression of metabolic suppression in this species; that phenological shifts will have a greater impact on ectotherms in variable thermal environments; and that E. propertius will be more sensitive to shifts in phenology in autumn than in spring. This suggests that increases in overwinter thermal variability and/or extended, warm autumns, will negatively impact all non-feeding dormant ectotherms which lack the ability to suppress their overwinter metabolic thermal sensitivity.

References

[1]  Crozier L (2004) Warmer winters drive butterfly range expansion by increasing survivorship. Ecology 85: 231–241.
[2]  Jepsen JU, Hagen SB, Ims RA, Yoccoz NG (2008) Climate change and outbreaks of the geometrids Operophtera brumata and Epirrita autumnata in subarctic birch forest: Evidence of a recent outbreak range expansion. J Anim Ecol 77: 257–264.
[3]  Irwin JT, Lee RE Jr (2003) Cold winter microenvironments conserve energy and improve overwintering survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis. Oikos 100: 71–78.
[4]  Hahn DA, Denlinger DL (2011) Energetics of insect diapause. Ann Rev Entomol 56: 103–121.
[5]  Boggs CL (2009) Understanding insect life histories and senescence through a resource allocation lens. Funct Ecol 23: 27–37.
[6]  O'Brien DM, Fogel ML, Boggs CL (2002) Renewable and nonrenewable resources: Amino acid turnover and allocation to reproduction in Lepidoptera. Proc Natl Acad Sci U S A 99: 4413–4418.
[7]  Angilletta MJ (2009) Thermal adaptation. Oxford: Oxford University Press.
[8]  Ruel JJ, Ayres MP (1999) Jensen's inequality predicts effects of environmental variation. Trends Ecol Evol 14: 361–366.
[9]  Pazstor L, Kisdi E, Meszena G (2000) Jensen's inequality and optimal life-history strategies in stochastic environments. Trends Ecol Evol 15: 117–118.
[10]  Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293: 2248–2251.
[11]  Dillon ME, Wang G, Huey RB (2010) Global metabolic impacts of recent climate warming. Nature 467: 704–706.
[12]  Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, et al. (2010) Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA 107: 15135–15139.
[13]  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. Pop Ecol 53: 53–58.
[14]  Kingsolver JG, Ragland GJ, Diamond SE (2009) Evolution in a constant environment: Thermal fluctuations and thermal sensitivity of laboratory and field populations of Manduca sexta. Evolution 63: 537–541.
[15]  Clarke A (2004) Is there a universal temperature dependence of metabolism? Funct Ecol 18: 252–256.
[16]  Nespolo RF, Castaneda LE, Roff DA (2007) Quantitative genetic variation of metabolism in the nymphs of the sand cricket, Gryllus firmus, inferred from an analysis of inbred-lines. Biol Res 40: 5–12.
[17]  Niehaus AC, Wilson RS, Seebacher F, Franklin CE (2011) Striped marsh frog (Limnodynastes peronii) tadpoles do not acclimate metabolic performance to thermal variability. J Evol Biol 214: 1965–1970.
[18]  Han E, Bauce E (1998) Timing of diapause initiation, metabolic changes and overwintering survival of the spruce budworm, Choristoneura fumiferana. Ecol Entomol 23: 160–167.
[19]  Bosch J, Sgolastra F, Kemp WP (2010) Timing of eclosion affects diapause development, fat body consumption and longevity in Osmia lignaria, a univoltine, adult-wintering solitary bee. J Insect Physiol 56: 1949–1957.
[20]  Prior KM, Dzurisin JDK, Pelini SL, Hellmann JJ (2009) Biology of larvae and adults of Erynnis propertius at the northern edge of its range. Can Entomol 141: 161–171.
[21]  Pelini SL, Dzurisin JDK, Prior KM, Williams CM, Marsico TM, et al. (2009) Translocation experiments with butterflies reveal limits to enhancement of poleward populations under climate change. Proc Natl Acad Sci USA 106: 11160–11165.
[22]  Williams CM, Thomas RH, MacMillan HA, Marshall KE, Sinclair BJ (2011) Triacylglyceride measurement in small quantities of homogenised insect tissue: Comparisons and caveats. J Insect Physiol 57: 1602–1613.
[23]  Williams CM, Pelini SL, Hellmann JJ, Sinclair BJ (2010) Intra-individual variation allows an explicit test of the hygric hypothesis for discontinuous gas exchange in insects. Biol Lett 6: 274–277.
[24]  R Core Development Team (2009) R: A language and environment for statistical computing. ISBN 3-900051-07-0. Available: http://www.R-project.org via the Internet.
[25]  Crawley MJ (2007) The R book. New York: Wiley.
[26]  Pinheiro JC, Bates DM (2000) Mixed effects models in S and S-PLUS. New York: Springer.
[27]  Makarieva AM, Gorshkov VG, Li B, Chown SL (2006) Size- and temperature- independence of minimum life-supporting metabolic rates. Funct Ecol 20: 83–96.
[28]  Angilletta MJ (2006) Estimating and comparing thermal performance curves. J Therm Biol 31: 541–545.
[29]  Pinheiro J, Bates D, SebRoy S, Sarkar D, R Core Team (2009) nlme: Linear and non-linear mixed effects models. R package version 3.1-101.
[30]  Marshall KE, Sinclair BJ (2012) Threshold temperatures mediate the impact of reduced snow cover on overwintering freeze tolerant caterpillars. Naturwissenschaften 99: 33–41.
[31]  Schmidt Nielsen K (1990) Animal physiology - adaptation and environment. Cambridge: Cambridge University Press.
[32]  Hellmann JJ, Pelini SL, Prior KM, Dzurisin JDK (2008) The response of two butterfly species to climatic variation at the edge of their range and the implications for poleward range shifts. Oecologia 157: 583–592.
[33]  van Asch M, Peter H, van Tienderen PH, Holleman LJM, Visser M (2007) Predicting adaptation of phenology in response to climate change, an insect herbivore example. Global Change Biol 13: 1596–1604.
[34]  Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37–42.
[35]  Nijhout HF (1975) A threshold size for metamorphosis in the tobacco hornworm, Manduca sexta. Biol Bull 149: 214–225.
[36]  Davidowitz G, Nijhout HF (2004) The physiological basis of reaction norms: The interaction among growth rate, duration of growth, and body size. Integr Comp Biol 44: 443–449.
[37]  Ishihara M, Ohgushi T (2006) Reproductive inactivity and prolonged developmental time induced by seasonal decline in host plant quality in the willow leaf beetle Plagiodera versicolora (Coleoptera : Chrysomelidae). Environ Entomol 35: 524–530.
[38]  Hochachka PW, Somero GN (2002) Biochemical adaptation. New York: Oxford University Press.
[39]  Schlenker W, Roberts MJ (2009) Nonlinear temperature effects indicate severe damage to U.S. crop yields under climate change. Proc Natl Acad Sci USA 106: 15594–15598.
[40]  Zhang T (2005) Influence of the seasonal snow cover on the ground thermal regime: An overview. Rev Geophys 43: 1–23.
[41]  Parajulee MN, Wilson LT, Rummel DR, Carroll SC, Trichilo PJ, et al. (1997) Relationship between ambient and leaf litter temperature in overwintering habitats of boll weevil (Coleoptera: Curculionidae). Environ Entomol 26: 135–141.
[42]  Chippendale AK, Chu TJF, Rose MR (1996) Complex trade-offs and the evolution of starvation resistance in Drosophila melanogaster. Evolution 50: 753–766.
[43]  Thackeray SJ, Sparks TH, Frederiksen M, Burthes S, Bacon PJ, et al. (2010) Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Global Change Biol 16: 3304–3313.
[44]  Sunday JM, Bates AE, Dulvy NK (2011) Global analysis of thermal tolerance and latitude in ectotherms. Proc R Soc Lond B Biol Sci 278: 1823–1830.
[45]  IPCCCore Writing Team (2007) Climate Change 2007: Synthesis Report. Contributions of Working Groups I, II, and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. In: Pachauri RK, Reisinger A, editors. IPCC, Geneva.

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