Temperature variation makes ectotherms more sensitive to climate change

Global Change Biology

Volumn 19, Issue 8, 2013, Pages 2373-2380

  Paaijmans, Krijn P ^a,b   Heinig, Rebecca L ^a   Seliga, Rebecca A ^a   Blanford, Justine I ^a   Blanford, Simon ^a   Murdock, Courtney C ^a   Thomas, Matthew B ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Anopheles stephensi; Climate change; Conservation; Diurnal temperature fluctuation; Ectotherm fitness; Jensen's inequality; Thermal fitness curve; Thermal reaction norm

Indexed keywords

CLIMATE CHANGE; CONSERVATION; DIURNAL VARIATION; ECTOTHERMY; FITNESS; MOSQUITO; TEMPERATURE EFFECT; WARMING;

ADAPTATION; ANIMAL; ANOPHELES; ANOPHELES STEPHENSI; ARTICLE; BIOLOGICAL MODEL; CLIMATE CHANGE; CONSERVATION; DIURNAL TEMPERATURE FLUCTUATION; ECTOTHERM FITNESS; GENETICS; INSECT; JENSEN'S INEQUALITY; LARVA; PHYSIOLOGY; REPRODUCTIVE FITNESS; TEMPERATURE; THERMAL FITNESS CURVE; THERMAL REACTION NORM;

ANOPHELES STEPHENSI; CLIMATE CHANGE; CONSERVATION; DIURNAL TEMPERATURE FLUCTUATION; ECTOTHERM FITNESS; JENSEN'S INEQUALITY; THERMAL FITNESS CURVE; THERMAL REACTION NORM;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANOPHELES; CLIMATE CHANGE; GENETIC FITNESS; INSECTS; LARVA; MODELS, BIOLOGICAL; TEMPERATURE;

ANOPHELES STEPHENSI; HEXAPODA;

EID: 84880136004     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/gcb.12240     Document Type: Article

References (57)

1. Amarasekare P, Savage V (2012) A framework for elucidating the temperature dependence of fitness. American Naturalist, 179, 178-191.
2. Angert AL, Sheth SN, Paul JR (2011) Incorporating population-level variation in thermal performance into predictions of geographic range shifts. Integrative and Comparative Biology, 51, 733-750.
3. Asbury D, Angilletta M (2010) Thermodynamic effects on the evolution of performance curves. American Naturalist, 176, E40-E49.
4. Atkins KE, Travis JMJ (2010) Local adaptation and the evolution of species' ranges under climate change. Journal of Theoretical Biology, 266, 449-457.
5. Bayoh MN, Lindsay SW (2003) Effect of temperature on the development of the aquatic stages of Anopheles gambiae sensu stricto (Diptera: Culicidae). Bulletin of Entomological Research, 93, 375-381.
6. Bonebrake TC, Deutsch CA (2012) Climate heterogeneity modulates impact of warming on tropical insects. Ecology, 93, 449-455.
7. Bowler K, Terblanche JS (2008) Insect thermal tolerance: what is the role of ontogeny, ageing and senescence? Biological Reviews, 83, 339-355.
8. Boyles JG, McKechnie AE (2010) Energy conservation in hibernating endotherms: why "suboptimal" temperatures are optimal. Ecological Modelling, 221, 1644-1647.
9. Bozinovic F, Bastias DA, Boher F, Clavijo-Baquet S, Estay SA, Angilletta MJ (2011) The mean and variance of environmental temperature interact to determine physiological tolerance and fitness. Physiological and Biochemical Zoology, 84, 543-552.
10. Chen IC, Hill JK, Ohlemuller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science, 333, 1024-1026.
11. Chevin L-M, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. Plos Biology, 8, e1000357.
12. Clusella-Trullas S, Blackburn TM, Chown SL (2011) Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change. American Naturalist, 177, 738-751.
13. Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences, 105, 6668-6672.
14. Duncan AB, Fellous S, Kaltz O (2011) Temporal variation in temperature determines disease spread and maintenance in Paramecium microcosm populations. Proceedings of the Royal Society B-Biological Sciences, 278, 3412-3420.
15. Easterling DR, Horton B, Jones PD et al. (1997) Maximum and minimum temperature trends for the globe. Science, 277, 364-367.
16. Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modelling, and impacts. Science, 289, 2068-2074.
17. 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. Population Ecology, 53, 53-58.
18. Folguera G, Bastias DA, Bozinovic F (2009) Impact of experimental thermal amplitude on ectotherm performance: adaptation to climate change variability? Comparative Biochemistry and Physiology A-Molecular & Integrative Physiology, 154, 389-393.
19. Folguera G, Bastias DA, Caers J, Rojas JM, Piulachs MD, Belles X, Bozinovic F (2011) An experimental test of the role of environmental temperature variability on ectotherm molecular, physiological and life-history traits: implications for global warming. Comparative Biochemistry and Physiology A-Molecular & Integrative Physiology, 159, 242-246.
20. Geerts B (2003) Empirical estimation of the monthly-mean daily temperature range. Theoretical and Applied Climatology, 74, 145-165.
21. Hamilton PT, Richardson JML, Govindarajulu P, Anholt BR (2012) Higher temperature variability increases the impact of Batrachochytrium dendrobatidis and shifts interspecific interactions in tadpole mesocosms. Ecology and Evolution, 2, 2450-2459.
22. Heikkinen RK, Luoto M, Leikola N et al. (2010) Assessing the vulnerability of European butterflies to climate change using multiple criteria. Biodiversity and Conservation, 19, 695-723.
23. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965-1978.
24. Hoffmann AA (2010) Physiological climatic limits in Drosophila: patterns and implications. Journal of Experimental Biology, 213, 870-880.
25. Hofmann GE, Todgham AE (2010) Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annual Review of Physiology, 72, 127-145.
26. Huey RB, Deutsch CA, Tewksbury JJ, Vitt LJ, Hertz PE, Álvarez PH, Garland T (2009) Why tropical forest lizards are vulnerable to climate warming. Proceedings of the Royal Society B: Biological Sciences, 276, 1939-1948.
27. Huey RB, Kearney MR, Krockenberger A, Holtum JAM, Jess M, Williams SE (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philosophical Transactions of the Royal Society B-Biological Sciences, 367, 1665-1679.
28. Jaramillo J, Chabi-Olaye A, Kamonjo C, Jaramillo A, Vega FE, Poehling H-M, Borgemeister C (2009) Thermal tolerance of the coffee berry borer Hypothenemus hampei: predictions of climate change impact on a tropical insect pest. PLoS ONE, 4, e6487.
29. Jaramillo J, Muchugu E, Vega FE, Davis A, Borgemeister C, Chabi-Olaye A (2011) Some like it hot: the influence and implications of climate change on coffee berry borer (Hypothenemus hampei) and coffee production in East Africa. PLoS ONE, 6, e24528.
30. 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.
31. Krenek S, Petzoldt T, Berendonk TU (2012) Coping with temperature at the warm edge - patterns of thermal adaptation in the microbial eukaryote Paramecium caudatum. PLoS ONE, 7, e30598.
32. Lassalle G, Crouzet P, Gessner J, Rochard E (2010) Global warming impacts and conservation responses for the critically endangered European Atlantic sturgeon. Biological Conservation, 143, 2441-2452.
33. Liu SS, Zhang GM, Zhu J (1995) Influence of temperature variations on rate of development in insects: analysis of case studies from entomological literature. Annals of the Entomological Society of America, 88, 107-119.
34. Martin TL, Huey RB (2008) Why "Suboptimal" is optimal: Jensen's inequality and ectotherm thermal preferences. American Naturalist, 171, E102-E118.
35. McMillan DM, Fearnley SL, Rank NE, Dahlhoff EP (2005) Natural temperature variation affects larval survival, development and Hsp70 expression in a leaf beetle. Functional Ecology, 19, 844-852.
36. Milanovich JR, Peterman WE, Nibbelink NP, Maerz JC (2010) Projected loss of a salamander diversity hotspot as a consequence of projected global climate change. PLoS ONE, 5, e12189.
37. Mironidis GK, Savopoulou-Soultani M (2008) Development, survivorship, and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae) under constant and alternating temperatures. Environmental Entomology, 37, 16-28.
38. Mordecai EA, Paaijmans KP, Johnson LR et al. (2013) Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecology Letters, 16, 22-30.
39. Niehaus AC, Angilletta MJ, Sears MW, Franklin CE, Wilson RS (2012) Predicting the physiological performance of ectotherms in fluctuating thermal environments. Journal of Experimental Biology, 215, 694-701.
40. Paaijmans KP, Jacobs AFG, Takken W, Heusinkveld BG, Githeko AK, Dicke M, Holtslag AAM (2008) Observations and model estimates of diurnal water temperature dynamics in mosquito breeding sites in western Kenya. Hydrological Processes, 22, 4789-4801.
41. Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB (2010) Influence of climate on malaria transmission depends on daily temperature variation. Proceedings of the National Academy of Sciences, 107, 15135-15139.
42. Parton WJ, Logan JA (1981) A model for diurnal variation in soil and air temperature. Agricultural Meteorology, 23, 205-216.
43. Piyaphongkul J, Pritchard J, Bale J (2012) Can tropical insects stand the heat? A case study with the brown planthopper Nilaparvata lugens (Stål). PLoS ONE, 7, e29409.
44. R Development Core Team (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org.
45. Raffel TR, Romansic JM, Halstead NT, McMahon TA, Venesky MD, Rohr JR (2013) Disease and thermal acclimation in a more variable and unpredictable climate. Nature Climate Change, 3, 146-151.
46. Ribeiro PL, Camacho A, Navas CA (2012) Considerations for assessing maximum critical temperatures in small ectothermic animals: insights from leaf-cutting ants. PLoS ONE, 7, e32083.
47. Rohr JR, Raffel TR (2010) Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proceedings of the National Academy of Sciences, 107, 8269-8274.
48. Rohr JR, Dobson AP, Johnson PTJ et al. (2011) Frontiers in climate change-disease research. Trends in Ecology and Evolution, 26, 270-277.
49. Ruel JJ, Ayres MP (1999) Jensen's inequality predicts effects of environmental variation. Trends in Ecology and Evolution, 14, 361-366.
50. Santos M, Castañeda LE, Rezende EL (2011) Making sense of heat tolerance estimates in ectotherms: lessons from Drosophila. Functional Ecology, 25, 1169-1180.
51. Santos M, Castañeda LE, Rezende EL (2012) Keeping pace with climate change: what is wrong with the evolutionary potential of upper thermal limits? Ecology and Evolution, 2, 2866-2880.
52. Siddiqui WH, Barlow CA, Randolph PA (1973) Effects of some constant and alternating temperatures on population growth of the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae). The Canadian Entomologist, 105, 145-156.
53. Stevenson RD (1985a) Body size and limits to the daily range of body temperature om terrestrial ectotherms. American Naturalist, 125, 102-117.
54. Stevenson RD (1985b) The relative importance of behavioral and physiological adjustments controlling body temperature in terrestrial ectotherms. American Naturalist, 126, 362-386.
55. Terblanche JS, Nyamukondiwa C, Kleynhans E (2010) Thermal variability alters climatic stress resistance and plastic responses in a globally invasive pest, the Mediterranean fruit fly (Ceratitis capitata). Entomologia Experimentalis et Applicata, 137, 304-315.
56. Tewksbury JJ, Huey RB, Deutsch CA (2008) Putting the heat on tropical animals. Science, 320, 1296-1297.
57. Worner SP (1992) Performance of phenological models under variable temperature regimes: consequences of the Kaufmann or rate summation effect. Environmental Entomology, 21, 689-699.