Shrinking body size as an ecological response to climate change

Nature Climate Change

Volumn 1, Issue 8, 2011, Pages 401-406

  Sheridan, Jennifer A ^a   Bickford, David ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BODY SIZE; CLIMATE CHANGE; ECOLOGICAL APPROACH; ECOSYSTEM SERVICE; HETEROGENEITY; PROTEIN; TROPHIC CASCADE;

EID: 84866258364     PISSN: 1758678X     EISSN: 17586798     Source Type: Journal    
DOI: 10.1038/nclimate1259     Document Type: Review

References (91)

1. IPCC Climate Change 2001: The Scientific Basis (eds Houghton, J.T. et al.) (Cambridge Univ. Press, 2001
2. IPCC Climate Change 2007: The Physical Science Basis (eds Solomon, S. et al.) (Cambridge Univ. Press, 2007
3. Biro, P.A., Beckmann, C. & Stamps, J.A. Small within-day increases in temperature affects boldness and alters personality in coral reef fish. Proc. R. Soc. B. 277, 71-77 (2010
4. Brodie, E.D. & Russell, N.H. The consistency of individual differences in behaviour: Temperature effects on antipredator behaviour in garter snakes. Anim. Behav. 57, 445-451 (1999
5. Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37-42 (2003
6. Parolin, P., Lucas, C., Piedade, M.T. F. & Wittmann, F. Drought responses of flood-tolerant trees in Amazonian floodplains. Ann. Bot. 105, 129-139 (2010
7. Bizer, J.R. Growth rates and size at metamorphosis of high elevation populations of Ambystoma tigrinum. Oecologia 34, 175-184 (1978
8. Irie, T. & Fischer, K. Ectotherms with a calcareous exoskeleton follow the temperature-size rule-evidence from field survey. Mar. Ecol. Prog. Ser. 385, 33-37 (2009
9. Bickford, D., Sheridan, J.A. & Howard, S.D. Climate change responses: Forgetting frogs, ferns, and flies? Trends Ecol. Evol. http://dx.doi.org/10. 1016/j.tree.2011.06.016 (2011
10. Daufresne, M., Lengfellner, K. & Sommer, U. Global warming benefits the small in aquatic ecosystems. Proc. Natl Acad. Sci. USA 106, 12788-12793 (2009
11. Gardner, J.L., Peters, A., Kearney, M.R., Joseph, L. & Heinsohn, R. Declining body size: A third universal response to warming? Trends Ecol. Evol. 26, 285-291 (2011
12. Smith, J.J., Hasiotis, S.T., Kraus, M.J. & Woody, D.T. Transient dwarfism of soil fauna during the Paleocene-Eocene Thermal Maximum. Proc. Natl Acad. Sci. USA 106, 17655-17660 (2009
13. Hadly, E.A., Kohn, M.H., Leonard, J.A. & Wayne, R.K. A genetic record of population isolation in pocket gophers during Holocene climatic change. Proc. Natl Acad. Sci. USA 95, 6893-6896 (1998
14. Blois, J.L., Feranec, R.S. & Hadly, E.A. Environmental influences on spatial and temporal patterns of body-size variation in California ground squirrels (Spermophilus beecheyi). J. Biogeogr. 35, 602-613 (2008
15. Finkel, Z.V., Katz, M.E., Wright, J.D., Schofield, O.M. E. & Falkowski, P.G. Climatically driven macroevolutionary patterns in the size of marine diatoms over the Cenozoic. Proc. Natl Acad. Sci. USA 102, 8927-8932 (2005
16. Smith, F.A., Betancourt, J.L. & Brown, J.H. Evolution of body-size in the woodrat over the past 25,000 years of climate change. Science 270, 2012-2014 (1995
17. Jokiel, P.L. et al. Ocean acidification and calcifying reef organisms: A mesocosm investigation. Coral Reefs 27, 473-483 (2008
18. Ries, J.B., Cohen, A.L. & McCorkle, D.C. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37, 1131-1134 (2009
19. Gooding, R.A., Harley, C.D. G. & Tang, E. Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. Proc. Natl Acad. Sci. USA 106, 9316-9321 (2009
20. Shi, D., Xu, Y., Hopkinson, B.M. & Morel, F.M. M. Effect of ocean acidification on iron availability to marine phytoplankton. Science 327, 676-679 (2010
21. Hovenden, M.J. et al. Warming and elevated CO2 affect the relationship between seed mass, germinability and seedling growth in Austrodanthonia caespitosa, a dominant Australian grass. Glob. Change Biol. 14, 1633-1641 (2008
22. Kim, S.H. et al. Temperature dependence of growth, development, and photosynthesis in maize under elevated CO2. Environ. Exp. Bot. 61, 224-236 (2007
23. Ledesma, N.A., Nakata, M. & Sugiyama, N. Effect of high temperature stress on the reproductive growth of strawberry cvs. 'Nyoho' and 'Toyonoka'. Sci. Hortic. 116, 186-193 (2008
24. Utsunomiya, N. Effect of temperature on shoot growth, flowering and fruit growth of purple passionfruit (Passiflora edulis Sims var. edulis). Sci. Hortic. 52, 63-68 (1992
25. Williamson, C.E., Grad, G., De Lange, H.J., Gilroy, S. & Karapelou, D.M. Temperature-dependent ultraviolet responses in zooplankton: Implications of climate change. Limnol. Oceanogr. 47, 1844-1848 (2002
26. Desai, A.S. & Singh, R.K. The effects of water temperature and ration size on growth and body composition of fry of common carp, Cyprinus carpio. J. Therm. Biol. 34, 276-280 (2009
27. Sahin, T. Effect of water temperature on growth of hatchery reared Black Sea turbot, Scophthalmus maximus (Linnaeus, 1758). Turk. J. Zool. 25, 183-186 (2001
28. Stillwell, R.C. & Fox, C.W. Geographic variation in body size, sexual size dimorphism and fitness components of a seed beetle: Local adaptation versus phenotypic plasticity. Oikos 118, 703-712 (2009
29. Vincent, G., de Foresta, H. & Mulia, R. Co-occurring tree species show contrasting sensitivity to ENSO-related droughts in planted dipterocarp forests. Forest Ecol. Manage. 258, 1316-1322 (2009
30. Brady, L.D. & Griffiths, R.A. Developmental responses to pond desiccation in tadpoles of the British anuran amphibians (Bufo bufo, B. calamita and Rana temporaria). J. Zool. 252, 61-69 (2000
31. Crump, M.L. Effect of habitat drying on developmental time and size at metamorphosis in Hyla pseudopuma. Copeia 1989, 794-797 (1989
32. Denver, R.J., Mirhadi, N. & Phillips, M. Adaptive plasticity in amphibian metamorphosis: Response of Scaphiopus hammondii tadpoles to habitat desiccation. Ecology 79, 1859-1872 (1998
33. Yom-Tov, Y. & Geffen, E. Geographic variation in body size: The effects of ambient temperature and precipitation. Oecologia 148, 213-218 (2006
34. Jacoby, G.C. & Darrigo, R.D. Tree ring width and density: Evidence of climatic and potential forest change in Alaska. Glob. Biogeochem. Cycles 9, 227-234 (1995
35. Reich, P.B. et al. Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440, 922-925 (2006
36. Barber, V.A., Juday, G.P. & Finney, B.P. Reduced growth of Alaskan white spruce in the twentieth century from temperature-induced drought stress. Nature 405, 668-673 (2000
37. Franks, S.J. & Weis, A.E. A change in climate causes rapid evolution of multiple life-history traits and their interactions in an annual plant. J. Evol. Biol. 21, 1321-1334 (2008
38. Reading, C.J. Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia 151, 125-131 (2007
39. Loehr, V.J. T., Hofmeyr, M.D. & Henen, B.T. Growing and shrinking in the smallest tortoise, Homopus signatus signatus: The importance of rain. Oecologia 153, 479-488 (2007
40. Wikelski, M. & Thom, C. Marine iguanas shrink to survive El Niño. Nature 403, 37-38 (2000
41. Gardner, J.L., Heinsohn, R. & Joseph, L. Shifting latitudinal clines in avian body size correlate with global warming in Australian passerines. Proc. R. Soc. B 276, 3845-3852 (2009
42. Yom-Tov, Y., Yom-Tov, S., Wright, J., Thorne, C.J. R. & Du Feu, R. Recent changes in body weight and wing length among some British passerine birds. Oikos 112, 91-101 (2006
43. Teplitsky, C., Mills, J.A., Alho, J.S., Yarrall, J.W. & Merila, J. Bergmann's rule and climate change revisited: Disentangling environmental and genetic responses in a wild bird population. Proc. Natl Acad. Sci. USA 105, 13492-13496 (2008
44. Yom-Tov, Y. Global warming and body mass decline in Israeli passerine birds. Proc. R. Soc. Lond. B 268, 947-952 (2001
45. Smith, F.A., Browning, H. & Shepherd, U.L. The influence of climate change on the body mass of woodrats Neotoma in an arid region of New Mexico, USA. Ecography 21, 140-148 (1998
46. Ozgul, A. et al. The dynamics of phenotypic change and the shrinking sheep of St. Kilda. Science 325, 464 (2009
47. Post, E., Stenseth, N.C., Langvatn, R. & Fromentin, J.M. Global climate change and phenotypic variation among red deer cohorts. Proc. R. Soc. Lond. B. 264, 1317-1324 (1997
48. Regehr, E.V., Amstrup, S.C. & Stirling, I. Polar Bear Population Status in the Southern Beaufort Sea Open-File Report 2006-1337 (US Geological Survey, 2006
49. Rode, K.D., Amstrup, S.C. & Regehr, E.V. Reduced body size and cub recruitment in polar bears associated with sea ice decline. Ecol. Appl. 20, 768-782 (2010
50. Vitousek, P.M., Gosz, J.R., Grier, C.C., Melillo, J.M. & Reiners, W.A. A comparative analysis of potential nitrification and nitrate mobility in forest ecosystems. Ecol. Monogr. 52, 155-177 (1982
51. Ojima, D.S. The Short-Term and Long-Term Effect of Burning on Tallgrass Prairie Ecosystem Properties and Dynamics PhD thesis, Colorado State Univ. (1987
52. Reiners, W.S. Nitrogen cycling in relation to ecosystem succession: A review. Ecol. Bull. 33, 507-528 (1981
53. Austin, A.T. & Vitousek, P.M. Nutrient dynamics on a precipitation gradient in Hawai'i. Oecologia 113, 519-529 (1998
54. Gillooly, J.F., Brown, J.H., West, G.B., Savage, V.M. & Charnov, E.L. Effects of size and temperature on metabolic rate. Science 293, 2248-2251 (2001
55. Bickford, D., Howard, S.D., Ng, D.J. J. & Sheridan, J.A. Impacts of climate change on the amphibians and reptiles of Southeast Asia. Biodivers. Conserv. 19, 1043-1062 (2010
56. Atkinson, D. in Advances in Ecological Research Vol. 25 (eds Begon, M. & Fitter, A.H.) 1-58 (Academic Press, 1994
57. van der Have, T.M. & de Jong, G. Adult size in ectotherms: Temperature effects on growth and differentiation. J. Theor. Biol. 183, 329-340 (1996
58. Li, W.K. W., McLaughlin, F.A., Lovejoy, C. & Carmack, E.C. Smallest algae thrive as the Arctic Ocean freshens. Science 326, 539 (2009
59. Peck, L.S., Clark, M.S., Morley, S.A., Massey, A. & Rossetti, H. Animal temperature limits and ecological relevance: Effects of size, activity and rates of change. Funct. Ecol. 23, 248-256 (2009
60. Wikelski, M. & Thom, C. Marine iguanas shrink to survive El Niño. Nature 403, 37-38 (2000
61. Blueweiss, L. et al. Relationships between body size and some life history parameters. Oecologia 37, 257-272 (1978
62. Watt, C., Mitchell, S. & Salewski, V. Bergmann's rule; A concept cluster? Oikos 119, 89-100 (2010
63. Blackburn, T.M. & Hawkins, B.A. Bergmann's rule and the mammal fauna of northern North America. Ecography 27, 715-724 (2004
64. Diniz-Filho, J.A., Bini, L.M., Rodriguez, M.A., Rangel, T. & Hawkins, B.A. Seeing the forest for the trees: Partitioning ecological and phylogenetic components of Bergmann's rule in European Carnivora. Ecography 30, 598-608 (2007
65. Ramirez, L., Diniz, J.A. F. & Hawkins, B.A. Partitioning phylogenetic and adaptive components of the geographical body-size pattern of new world birds. Glob. Ecol. Biogeogr. 17, 100-110 (2008
66. Heatwole, H., Torres, F., Deaustin, S.B. & Heatwole, A. Studies on anuran water balance -I. Dynamics of evaporative water loss by the coqui, Eleutherodactylus portoricensis. Comp. Biochem. Physiol. 28, 245-269 (1969
67. Gill, R.A., Anderson, L.J., Polley, H.W., Johnson, H.B. & Jackson, R.B. Potential nitrogen constraints on soil carbon sequestration under low and elevated atmospheric CO2. Ecology 87, 41-52 (2006
68. Phillips, O.L. et al. Increasing dominance of large lianas in Amazonian forests. Nature 418, 770-774 (2002
69. ter Hofstede, R. & Rijnsdorp, A.D. Comparing demersal fish assemblages between periods of contrasting climate and fishing pressure. ICES J. Mar. Sci. 68, 1189-1198 (2011
70. Food and Agriculture Organization How to Feed the World in 2050 (United Nations, 2009); Available via http://go.nature.com/WFBRBm
71. Thresher, R.E., Koslow, J.A., Morison, A.K. & Smith, D.C. Depth-mediated reversal of the effects of climate change on long-term growth rates of exploited marine fish. Proc. Natl Acad. Sci. USA 104, 7461-7465 (2007
72. Todd, C.D. et al. Detrimental effects of recent ocean surface warming on growth condition of Atlantic salmon. Glob. Change Biol. 14, 958-970 (2008
73. Chamaille-Jammes, S., Massot, M., Aragon, P. & Clobert, J. Global warming and positive fitness response in mountain populations of common lizards Lacerta vivipara. Glob. Change Biol. 12, 392-402 (2006
74. Guillemain, M. et al. Wintering French mallard and teal are heavier and in better body condition than 30 years ago: Effects of a changing environment? Ambio 39, 170-180 (2010
75. Yom-Tov, Y. & Yom-Tov, S. Decrease in body size of Danish goshawks during the twentieth century. J. Ornithol. 147, 644-647 (2006
76. Salewski, V., Hochachka, W.M. & Fiedler, W. Global warming and Bergmann's rule: Do central European passerines adjust their body size to rising temperatures? Oecologia 162, 247-260 (2010
77. Moreno-Rueda, G. & Rivas, J.M. Recent changes in allometric relationships among morphological traits in the dipper (Cinclus cinclus). J. Ornithol. 148, 489-494 (2007
78. Kanuscak, P., Hromada, M., Tryjanowski, P. & Sparks, T. Does climate at different scales influence the phenology and phenotype of the river warbler Locustella fluviatilis? Oecologia 141, 158-163 (2004
79. Proffitt, K.M., Garrott, R.A., Rotella, J.J., Siniff, D.B. & Testa, J.W. Exploring linkages between abiotic oceanographic processes and a top-trophic predator in an Antarctic ecosystem. Ecosystems 10, 119-126 (2007
80. Yom-Tov, Y., Yom-Tov, S. & Jarrell, G. Recent increase in body size of the American marten Martes americana in Alaska. Biol. J. Linn. Soc. 93, 701-707 (2008
81. Yom-Tov, Y. & Yom-Tov, J. Global warming, Bergmann's rule and body size in the masked shrew Sorex cinereus Kerr in Alaska. J. Anim. Ecol. 74, 803-808 (2005
82. Yom-Tov, Y. & Yom-Tov, S. Climatic change and body size in two species of Japanese rodents. Biol. J. Linn. Soc. 82, 263-267 (2004
83. Meiri, S., Guy, D., Dayan, T. & Simberloff, D. Global change and carnivore body size: Data are stasis. Glob. Ecol. Biogeogr. 18, 240-247 (2009
84. Luque, S.P. & Ferguson, S.H. Ecosystem regime shifts have not affected growth and survivorship of eastern Beaufort Sea belugas. Oecologia 160, 367-378 (2009
85. Yom-Tov, Y., Heggberget, T.M., Wiig, O. & Yom-Tov, S. Body size changes among otters, Lutra lutra, in Norway: The possible effects of food availability and global warming. Oecologia 150, 155-160 (2006
86. Koontz, T.L., Shepherd, U.L. & Marshall, D. The effects of climate change on Merriam's kangaroo rat, Dipodomys merriami. J. Arid Environ. 49, 581-591 (2001
87. Yom-Tov, Y. et al. Recent changes in body size of the Eurasian otter Lutra lutra in Sweden. Ambio 39, 496-503 (2010
88. Stillwell, R.C. Are latitudinal clines in body size adaptive? Oikos 119, 1387-1390 (2010
89. Arft, A.M. et al. Responses of tundra plants to experimental warming: Meta-analysis of the international tundra experiment. Ecol. Monogr. 69, 491-511 (1999
90. Yom-Tov, Y. Body sizes of carnivores commensal with humans have increased over the past 50 years. Funct. Ecol. 17, 323-327 (2003
91. Urban, M.C., Phillips, B.L., Skelly, D.K. & Shine, R. The cane toad's (Chaunus [Bufo] marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proc. R. Soc. B. 274, 1413-1419 (2007