Daily temperature extremes play an important role in predicting thermal effects

Journal of Experimental Biology

Volumn 218, Issue 14, 2015, Pages 2289-2296

  Ma, Gang ^a   Hoffmann, Ary A ^b   Ma, Chun Sen ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Average temperature; Climate change; Life history trait; Mild temperature; Model prediction; Temperature extreme

Indexed keywords

ANIMAL; APHID; CIRCADIAN RHYTHM; FERTILITY; GROWTH, DEVELOPMENT AND AGING; HEAT; LONGEVITY; NYMPH; PHYSIOLOGY; POPULATION DYNAMICS;

ANIMALS; APHIDS; CIRCADIAN RHYTHM; FERTILITY; HOT TEMPERATURE; LONGEVITY; NYMPH; POPULATION DYNAMICS;

EID: 84946510721     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.122127     Document Type: Article

References (82)

1. Acreman, S. J. and Dixon, A. F. G. (1989). The effects of temperature and host quality on the rate of increase of the grain aphid (Sitobion avenae) on wheat. Ann. Appl. Biol. 115, 3-9.
2. Angilletta, M. J. (2009). Thermal Adaptation: A Theoretical and Empirical Synthesis. New York, NY: Oxford University Press.
3. Asin, L. and Pons, X. (2001). Effect of high temperature on the growth and reproduction of corn aphids (Homoptera: Aphididae) and implications for their population dynamics on the Northeastern Iberian peninsula. Environ. Entomol. 30, 1127-1134.
4. Bale, J. S. and Hayward, S. A. L. (2010). Insect overwintering in a changing climate. J. Exp. Biol. 213, 980-994.
5. Bannerman, J. A. and Roitberg, B. D. (2014). Impact of extreme and fluctuating temperatures on aphid-parasitoid dynamics. Oikos 123, 89-98.
6. Beebee, T. J. C. (1995). Amphibian breeding and climate. Nature 374, 219-220.
7. Bradshaw, W. E., Zani, P. A. and Hozapfel, C. M. (2004). Adaptation to temperate climates. Evolution 58, 1748-1762.
8. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. and West, G. B. (2004). Toward a metabolic theory of ecology. Ecology 85, 1771-1789.
9. Cannon, R. J. C. (1998). The implications of predicted climate change for insect pests in the UK, with emphasis on non-indigenous species. Glob. Change Biol. 4, 785-796.
10. Carrington, L. B., Armijos, M. V., Lambrechts, L., Barker, C. M. and Scott, T. W. (2013). Effects of fluctuating daily temperatures at critical thermal extremes on Aedes aegypti life-history traits. PLoS ONE 8, e58824.
11. Carter, N., Dixon, A. F. G. and Rabbinge, R. (1982). Cereal Aphid Populations: Biology, Simulation and Prediction. Simulation Monograph. Wageningen, The Netherlands: Pudoc.
12. Chidawanyika, F. and Terblanche, J. S. (2011). Rapid thermal responses and thermal tolerance in adult codling moth Cydia pomonella (Lepidoptera: Tortricidae). J. Insect Physiol. 57, 108-117.
13. Clusella-Trullas, S., Blackburn, T. M. and Chown, S. L. (2011). Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change. Am. Nat. 177, 738-751.
14. Colinet, H., Sinclair, B. J., Vernon, P. and Renault, D. (2015). Insects in fluctuating thermal environments. Annu. Rev. Entomol. 60, 123-140.
15. Danks, H. V. (2006). Short life cycles in insects and mites. Can. Entomol. 138, 407-463.
16. Davis, J. A., Radcliffe, E. B. and Ragsdale, D. W. (2006). Effects of high and fluctuating temperatures on Myzus persicae (Hemiptera: Aphididae). Environ. Entomol. 35, 1461-1468.
17. Dean, G. J. (1974). Effect of temperature on the cereal aphids Metopolophium dirhodum (Wlk.), Rhopalosiphum padi (L.) and Macrosiphum avenue (F.) (Hem., Aphididae). Bull. Entomol. Res. 63, 401-409.
18. Denlinger, D. L. and Yocum, G. D. (1998). Physiology of heat sensitivity. In Temperature Sensitivity in Insects and Application in Integrated Pest Management (ed. G. J. Hallman and D. L. Denlinger), pp. 7-57. Oxford: Westview Press.
19. Deutsch, C. A., Tewksbury, J. J., Huey, R. B., Sheldon, K. S., Ghalambor, C. K., Haak, D. C. and Martin, P. R. (2008). Impacts of climate warming on terrestrial ectotherms across latitude. Proc. Natl. Acad. Sci. USA 105, 6668-6672.
20. Easterling, D. R., Horton, B., Jones, P. D., Peterson, T. C., Karl, T. R., Parker, D. E., Salinger, M. J., Razuvayev, V., Plummer, N., Jamason, P. et al. (1997). Maximum and minimum temperature trends for the globe. Science 277, 364-367.
21. Easterling, D. R., Meehl, G. A., Parmesan, C., Changnon, S. A., Karl, T. R. and Mearns, L. O. (2000). Climate extremes: observations, modeling, and impacts. Science 289, 2068-2074.
22. Feder, M. E. and Hofmann, G. E. (1999). Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61, 243-282.
23. Flynn, D. F. B., Sudderth, E. A. and Bazzaz, F. (2006). Effects of aphid herbivory on biomass and leaf-level physiology of Solanum dulcamara under elevated temperature and CO2. Environ. Exp. Bot. 56, 10-18.
24. Folguera, G., Bastías, D. A. and Bozinovic, F. (2009). Impact of experimental thermal amplitude on ectotherm performance: adaptation to climate change variability? Comp. Biochem. Physiol. A Mol. Integr. Physiol. 154, 389-393.
25. Freier, B., Triltsch, H. and Rosserg, M. (1996). GTLAUS - A model of wheat - cereal aphid - predator interaction and its use in complex agroecological studies. J. Plant Dis. Prot. 103, 543-554.
26. Gillespie, D. R., Nasreen, A., Moffat, C. E., Clarke, P. and Roitberg, B. D. (2012). Effects of simulated heat waves on an experimental community of pepper plants, green peach aphids and two parasitoid species. Oikos 121, 149-159.
27. Harmon, J. P., Moran, N. A. and Ives, A. R. (2009). Species response to environmental change: impacts of food web interactions and evolution. Science 323, 1347-1350.
28. Hendrix, D. L. and Salvucci, M. E. (1998). Polyol metabolism in homopterans at high temperatures: accumulation of mannitol in aphids (Aphididae: Homoptera) and sorbitol in whiteflies (Aleyrodidae: Homoptera). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 120, 487-494.
29. Hoffmann, A. A., Chown, S. L. and Clusella-Trullas, S. (2013). Upper thermal limits in terrestrial ectotherms: how constrained are they? Funct. Ecol. 27, 934-949.
30. Hood, G. M. (2011). PopTools version 3.2.5. Available at http://www.poptools.org.
31. Huang, L.-H., Chen, B. and Kang, L. (2007). Impact of mild temperature hardening on thermotolerance, fecundity, and Hsp gene expression in Liriomyza huidobrensis. J. Insect Physiol. 53, 1199-1205.
32. IPCC (2013). Climate Change 2013: The physical science basis. In Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (ed. T. F. Stocker, D. Qin, G. K. Plattner, M. Tignor, S. K. Allen, J. Boschung et al.). Cambridge, NY, USA: Cambridge University Press.
33. Jeffs, C. T. and Leather, S. R. (2014). Effects of extreme, fluctuating temperature events on life history traits of the grain aphid, Sitobion avenae. Entomol. Exp. Appl. 150, 240-249.
34. Karl, I., Stoks, R., De Block, M., Janowitz, S. A. and Fischer, K. (2011). Temperature extremes and butterfly fitness: conflicting evidence from life history and immune function. Glob. Change Biol. 17, 676-687.
35. Kearney, M., Shine, R. and Porter, W. P. (2009). The potential for behavioral thermoregulation to buffer "cold-blooded" animals against climate warming. Proc. Natl. Acad. Sci. USA 106, 3835-3840.
36. Krebs, R. A. and Feder, M. E. (1998). Hsp70 and larval thermotolerance in Drosophila melanogaster: how much is enough and when is more too much? J. Insect Physiol. 44, 1091-1101.
37. Lactin, D. J., Holliday, N. J., Johnson, D. L. and Craigen, R. (1995). Improved rate model of temperature-dependent development by arthropods. Environ. Entomol. 24, 68-75.
38. Li, H. M. (1990). Studies on the population ecology of English grain aphid. J. Jishou Univ. 11, 59-70.
39. Liu, S. Y. and Li, D. X. (1990). Studies on developmental threshold temperature and effective accumulated temperature of Sitobion avenae. Entomol. Knowl. 27, 132-134.
40. Lykouressis, D. P. (1984). A comparative study of different aphid population parameters in assessing resistance in cereals. J. Appl. Entomol. 97, 77-84.
41. Lykouressis, D. P. (1985). Temperature requirements of Sitobion avenae (F.) necessary for ecological studies, by assessing methods for the estimation of instar duration. J. Appl. Entomol. 100, 479-493.
42. Ma, C.-S. (2000). Modelling and Simulation of the Population Dynamics of the Cereal Aphid Metopolophium Dirhodum in Northern Germany. Berlin: Verlag Franzbecker.
43. Ma, C.-S., Hau, B. and Poehling, H.-M. (2004a). Effects of pattern and timing of high temperature exposure on reproduction of the rose grain aphid, Metopolophium dirhodum. Entomol. Exp. Appl. 110, 65-71.
44. Ma, C.-S., Hau, B. and Poehling, H.-M. (2004b). The effect of heat stress on the survival of the rose grain aphid, Metopolophium dirhodum (Hemiptera: Aphididae). Eur. J. Entomol. 101, 327-331.
45. Ma, G., Rudolf, V. H. W. and Ma, C.-S. (2015). Extreme temperature events alter demographic rates, relative fitness, and community structure. Glob. Change Biol. 21, 1794-1808.
46. McMillan, D. M., Fearnley, S. L., Rank, N. E. and Dahlhoff, E. P. (2005). Natural temperature variation affects larval survival, development and Hsp70 expression in a leaf beetle. Funct. Ecol. 19, 844-852.
47. Meehl, G. A. and Tebaldi, C. (2004). More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305, 994-997.
48. Neargarder, G., Dahlhoff, E. P. and Rank, N. E. (2003). Variation in thermal tolerance is linked to phosphoglucose isomerase genotype in a montane leaf beetle. Funct. Ecol. 17, 213-221.
49. Nguyen, T. T. A., Michaud, D. and Cloutier, C. (2009). A proteomic analysis of the aphid Macrosiphum euphorbiae under heat and radiation stress. Insect Biochem. Mol. Biol. 39, 20-30.
50. Overgaard, J. and Sørensen, J. G. (2008). Rapid thermal adaptation during field temperature variations in Drosophila melanogaster. Cryobiology 56, 159-162.
51. Overgaard, J., Kearney, M. R. and Hoffmann, A. A. (2014). Sensitivity to thermal extremes in Australian Drosophila implies similar impacts of climate change on the distribution of widespread and tropical species. Glob. Change Biol. 20, 1738-1750.
52. Paaijmans, K. P., Blanford, S., Bell, A. S., Blanford, J. I., Read, A. F. and Thomas, M. B. (2010). Influence of climate on malaria transmission depends on daily temperature variation. Proc. Natl. Acad. Sci. USA 107, 15135-15139.
53. Paaijmans, K. P., Heinig, R. L., Seliga, R. A., Blanford, J. I., Blanford, S., Murdock, C. C. and Thomas, M. B. (2013). Temperature variation makes ectotherms more sensitive to climate change. Glob. Change Biol. 19, 2373-2380.
54. Parmesan, C. and Yohe, G. (2003). A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37-42.
55. Radchuk, V., Turlure, C. and Schtickzelle, N. (2013). Each life stage matters: the importance of assessing the response to climate change over the complete life cycle in butterflies. J. Anim. Ecol. 82, 275-285.
56. Ragland, G. J. and Kingsolver, J. G. (2008). The effect of fluctuating temperatures on ectotherm life-history traits: comparisons among geographic populations of Wyeomyia smithii. Evol. Ecol. Res. 10, 29-44.
57. Rall, B. C., Vucic-Pestic, O., Ehnes, R. B., Emmerson, M. and Brose, U. (2010). Temperature, predator-prey interaction strength and population stability. Glob. Change Biol. 16, 2145-2157.
58. Reyer, C. P. O., Leuzinger, S., Rammig, A., Wolf, A., Bartholomeus, R. P., Bonfante, A., de Lorenzi, F., Dury, M., Gloning, P., Abou Jaoudé, R. et al. (2013). A plant's perspective of extremes: terrestrial plant responses to changing climatic variability. Glob. Change Biol. 19, 75-89.
59. Rossberg, D., Holz, F., Freier, B. and Wenzel, V. (1986). PESTSIM-MAC - A model for simulation of Macrosiphum avenae Fabr. Populations. In "Computer-Aided Modelling and Simulation of the Winter Wheat Agroecosystjem (AGROSIM-W) for Integrated Pest Management". Tagungsbericht der Akademie der Landwirtschafts-wissenschaften der DDR 242, 87-100.
60. Semenov, M. A. (2009). Impacts of climate change on wheat in England and Wales. J. R. Soc. Interface 6, 343-350.
61. Sengonca, C., Hoffmann, A. and Kleinhenz, B. (1994). Laboruntersuchungen zur Entwicklung, Lebensdauer und Fruchtbarkeit der Getreideblattlausarten Sitobion avenae (F.) und Rhopalosiphum padi (L.) (Horn., Aphididae) bei verschiedenen tieferen Temperaturen. J. Appl. Entomol. 117, 224-233.
62. Sentis, A., Hemptinne, J.-L. and Brodeur, J. (2013). Effects of simulated heat waves on an experimental plant-herbivore-predator food chain. Glob. Change Biol. 19, 833-842.
63. Silbermann, R. and Tatar, M. (2000). Reproductive costs of heat shock protein in transgenic Drosophila melanogaster. Evolution 54, 2038-2045.
64. Smith, M. D. (2011). An ecological perspective on extreme climatic events: a synthetic definition and framework to guide future research. J. Ecol. 99, 656-663.
65. Terblanche, J. S., Clusella-Trullas, S., Deere, J. A. and Chown, S. L. (2008). Thermal tolerance in a south-east African population of the tsetse fly Glossina pallidipes (Diptera, Glossinidae): implications for forecasting climate change impacts. J. Insect Physiol. 54, 114-127.
66. Tobin, P. C., Nagarkatti, S., Loeb, G. and Saunders, M. C. (2008). Historical and projected interactions between climate change and insect voltinism in a multivoltine species. Glob. Change Biol. 14, 951-957.
67. Tomanek, L. (2005). Two-dimensional gel analysis of the heat-shock response in marine snails (genus Tegula): interspecific variation in protein expression and acclimation ability. J. Exp. Biol. 208, 3133-3143.
68. Triltsch, H., Freier, B. and Rossberg, D. (1998). Consequences of new findings on climate change with relatively warmer nights on the wheat-cereal aphid- predator interaction in computer simulations. Arch. Phytopathol. Plant Prot. 31, 363-367.
69. van Asch, M., van Tienderen, P. H., Holleman, L. J. M. and Visser, M. E. (2007). Predicting adaptation of phenology in response to climate change, an insect herbivore example. Glob. Change Biol. 13, 1596-1604.
70. van Emden, H. and Harrington, R. (2007). Aphids as Crop Pests. Wallingford, UK: CABI.
71. Vasseur, D. A., DeLong, J. P., Gilbert, B., Greig, H. S., Harley, C. D. G., McCann, K. S., Savage, V., Tunney, T. D. and O'Connor, M. I. (2014). Increased temperature variation poses a greater risk to species than climate warming. Proc. R. Soc. B. Biol. Sci. 281, 20132612.
72. Vucic-Pestic, O., Ehnes, R. B., Rall, B. C. and Brose, U. (2011). Warming up the system: higher predator feeding rates but lower energetic efficiencies. Glob. Change Biol. 17, 1301-1310.
73. Warren, J. A. and Anderson, G. (2013). Effect of fluctuating temperatures on the development of a forensically important blow fly. Protophormia terraenovae (Diptera: Calliphoridae) 42, 167-172.
74. Welbergen, J. A., Klose, S. M., Markus, N. and Eby, P. (2008). Climate change and the effects of temperature extremes on Australian flying-foxes. Proc. R. Soc. B Biol. Sci. 275, 419-425.
75. Whitney-Johnson, A., Thompson, M. and Hon, E. (2005). Responses to predicted global warming in Pieris rapae L. (Lepidoptera): consequences of nocturnal versus diurnal temperature change on fitness components. Environ. Entomol. 34, 535-540.
76. Xing, K., Hoffmann, A. A. and Ma, C.-S. (2014). Does thermal variability experienced at the egg stage influence life history traits across life cycle stages in a small invertebrate? PLoS ONE 9, e99500.
77. Yin, Q. Y., Zheng, W. Y., Xie, X. S., Li, F., Li, R., Zheng, X. L. and Fan, S. Q. (2003). The effect of temperature on development and fertility of Macrosiphum avenae. Acta Agric. Boreali-Sinica 18, 71-73.
78. Zhang, H. S. (1994). Influence of temperatures on the characterictic parameters of survival rate model of populations of the wheat aphid Macrosiphum avenae (Fabricius). Entomol. J. East China 3, 66-68.
79. Zhang, W., Zhao, F., Hoffmann, A. A. and Ma, C.-S. (2013). A single hot event that does not affect survival but decreases reproduction in the diamondback moth, Plutella xylostella. PLoS ONE 8, e75923.
80. Zhao, F., Zhang, W., Hoffmann, A. A. and Ma, C.-S. (2014). Night warming on hot days produces novel impacts on development, survival and reproduction in a small arthropod. J. Anim. Ecol. 83, 769-778.
81. Zhou, X., Carter, N. and Mumford, J. (1989). A simulation model describing the population dynamics and damage potential of the rose grain aphid, Metopolophium dirhodum (Walker) (Hemiptera: Aphididae), in the UK. Bull. Entomol. Res. 79, 373-380.
82. Zizzari, Z. V. and Ellers, J. (2011). Effects of exposure to short-term heat stress on male reproductive fitness in a soil arthropod. J. Insect Physiol. 57, 421-426.