Phenological asynchrony between herbivorous insects and their hosts: Signal of climate change or pre-existing adaptive strategy?

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1555, 2010, Pages 3161-3176

  Singer, Michael C ^a   Parmesan, Camille ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Climate change; Edith's checkerspot; Life history trade off; Mismatch; Phenological asynchrony; Winter moth

Indexed keywords

ANTHROPOGENIC EFFECT; BUTTERFLY; EXTINCTION; FECUNDITY; HERBIVORE; HOST PLANT; LIFE HISTORY; METAPOPULATION; MORTALITY; MOTH; PHENOLOGY; PLANT-HERBIVORE INTERACTION; PLANT-INSECT INTERACTION; RANGE EXPANSION; STARVATION; TRADE-OFF;

EUPHYDRYAS; EUPHYDRYAS EDITHA; HEXAPODA; LEPIDOPTERA; OPEROPHTERA BRUMATA;

EID: 77958068106     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0144     Document Type: Article

References (118)

1. Balanya, J., Oller, J. M., Huey, R. B., Gilchrist, G. W. & Serra, L. 2006 Global genetic change tracks global climate warming in Drosophila subobscura. Science 313, 1773-1775. (doi:10.1126/science.1131002)
2. Boggs, C. L. 1997 Reproductive allocation from reserves and income in butterfly species with differing adult diets. Ecology 78, 181-191. (doi:10.1890/0012-9658 (1997) 078[0181:RAFRAI]2.0.CO;2)
3. Both, C., van Asch, M., Bijlsma, R., van den Berg, A. B. & Visser, M. E. 2009 Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? J. Anim. Ecol. 78, 73-83. (doi:10.1111/j. 1365-2656.2008.01458.x)
4. Boughton, D. A. 1999 Empirical evidence for complex source-sink dynamics with alternative states in a butterfly metapopulation. Ecology 80, 2727-2739.
5. Bradshaw, W. E. & Holzapfel, C. M. 2001 Genetic shift in photoperiodic response correlated with global warming. Proc. Natl Acad. Sci. USA 98, 14 509-14 511. (doi:10. 1073/pnas.241391498)
6. Buse, A. & Good, J. E. G. 1996 Synchronization of larval emergence in winter moth and budburst in pedunculate oak under simulated climate change. Ecol. Entomol. 21, 335-343. (doi:10.1046/j.1365-2311.1996. t01-1-00001.x)
7. Buse, A., Drury, S. J., Woodburn, R. J. W., Perrins, C. M. & Good, J. E. G. 1999 Effects of elevated temperature on multi-species interactions: the case of pedunculate oak, winter moth and tits. Funct. Ecol. 13 (Suppl. 1), 74-82.
8. Carroll, S. P., Dingle, H., Famula, T. R. & Fox, C. W. 2001 Genetic architecture of adaptive differentiation in evolving host races of the soapberry bug, Jadera haematoloma. Genetica 112-113, 257-272. (doi:10.1023/A: 1013354830907)
9. Charmantier, A., McCleery, R. H., Cole, L. R., Perrins, C., Kruuk, L. E. B. & Sheldon, B. C. 2008 Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800-803.
10. Chown, S. L., Slabber, S., McGeoch, M. A., Janion, C. & Leinaas, H. P. 2007 Phenotypic plasticity mediates climate change responses among invasive and indigenous arthropods. Proc. R. Soc. B 274, 2531-2537. (doi:10. 1098/rspb.2007.0772)
11. Cizek, L., Fric, Z. & Konvicka, M. 2006 Host plant defences and voltinism in European butterflies. Ecol. Entomol. 31, 337-344. (doi:10.1111/j.1365-2311.2006.00783.x)
12. Cleland, E. E., Chuine, I., Menzel, A., Mooney, H. A. & Schwartz, M. D. 2007 Shifting plant phenlogy in response to global change. Trends Ecol. Evol. 22, 357-365. (doi:10. 1016/j.tree.2007.04.003)
13. Cresswell, W. & McCleery, R. 2003 How great tits maintain synchrony of their hatch date with food supply in response to long-term variability in temperature. J. Anim. Ecol. 72, 356-366. (doi:10.1046/j.1365-2656. 2003.00701.x)
14. Cuming, F. G. 1961 The distribution, life history and economic importance of the winter moth, Operophtera brumata, in Nova Scotia. Can. Entomol. 93, 135-142. (doi:10.4039/Ent93135-2)
15. Cushman, J. H., Boggs, C. L., Weiss, S. B., Murphy, D. D., Harvey, A. W. & Ehrlich, P. R. 1994 Estimating female reproductive success of a threatened butterfly-influence of time and hostplant phenology. Oecologia 99, 194-200. (doi:10.1007/BF00317101)
16. Davidowitz, G., Roff, D. A. & Nijhout, H. F. 2005 A physiological perspective on the response of body size and development time to simultaneous directional selection. Integr. Comp. Biol. 45, 525-531. (doi:10.1093/icb/45.3. 525)
17. Dennis, R. L. H. 1993 Butterflies and climate change. Manchester, UK/New York, NY: Manchester University Press.
18. Dewar, R. C. & Watt, A. D. 1992 Predicted changes in the synchrony of larval emergence and budburst under climatic warming. Oecologia 89, 557-559.
19. Dobkin, D. S., Olivieri, I. & Ehrlich, P. R. 1987 Rainfall and the interaction of microclimate with larval resources in the population dynamics of checkerspot butterflies (Euphydryas editha) inhabiting serpentine grassland. Oecologia 71, 161-166. (doi:10.1007/BF00377280)
20. DuMerle, P. 1999 Egg development and diapause: ecophysiologocal and genetic basis of phenological polymorphism and adaptation to different hosts in the green oak tortrix, Tortrix viridana. J. Insect Physiol. 45, 599-611. (doi:10.1016/S0022-1910 (99) 00045-1)
21. Edwards, M. & Richardson, A. J. 2004 Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430, 881-884. (doi:10.1038/nature02808)
22. Ehrlich, P. R. 1961 Intrinsic barriers to dispersal in the checkerspot butterfly Euphydryas editha. Science 134, 108-109. (doi:10.1126/science.134. 3472.108)
23. Ehrlich, P. R. 1965 The population biology of the butterfly Euphydryas editha II. The structure of the Jasper Ridge colony. Evolution 19, 327-336. (doi:10.2307/2406442)
24. Ehrlich, P. R., Murphy, D. D., Singer, M. C. & Sherwood, C. B. 1980 Extinction, reduction, stability and increase: the responses of checkerspot butterfly (Euphydryas) populations to the California drought. Oecologia 46, 101-105. (doi:10.1007/BF00346973)
25. Feeny, P. 1970 Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51, 565-581. (doi:10.2307/1934037)
26. Fleishman, E., Launer, A. E., Weiss, S., Reed, J. M., Boggs, C. L., Murphy, D. D. & Ehrlich, P. R. 1997 Effects of microclimate and oviposition timing on prediapause larval survival of the bay checkerspot butterfly, Euphydryas editha bayensis (Lepidoptera: Nymphalidae). J. Res. Lepid. 36, 31-44.
27. Forkner, R. E., Marquis, R. J. & Lill, J. T. 2004 Feeny revisited: condensed tannins as anti-herbivore defenses in leaf-chewing herbivores of Quercus. Ecol. Entomol. 29, 174-187. (doi:10.1111/j.1365-2311.2004.0590.x)
28. Forkner, R. E., Marquis, R. J., Lill, J. T. & Le Corff, J. 2008 Timing is everything? Phenological synchrony and population variability in leaf-chewing herbivores of Quercus. Ecol. Entomol. 33, 276-285. (doi:10.1111/j.1365-2311. 2007.00976.x)
29. Forrest, J., Inouye, D. W. & Thomson, J. D. 2010 Flowering phenology in subalpine meadows: does climate variation influence community co-flowering patterns? Ecology 91, 431-440. (doi:10.1890/09-0099.1)
30. Friberg, M. & Wiklund, C. 2010 Host-plant-induced larval decision-making in a habitat/host-plant generalist butterfly. Ecology 91, 15-21. (doi:10.1890/09-0328.1)
31. Gienapp, P., Postma, E. & Visser, M. E. 2006 Why breeding time has not responded to selection for earlier breeding in a songbird population. Evolution 60, 2381-2388.
32. Gillespie, J. H. 1977 Natural selection for variances in offspring numbers: a new evolutionary principle. Am. Nat. 111, 1010-1014. (doi:10.1086/283230)
33. Gotthard, K., Nylin, S. & Wiklund, C. 1994 Adaptive variation in growth rate: life history costs and consequences in the speckled wood butterfly, Pararge aegeria. Oecologia 99, 281-289. (doi:10.1007/BF00627740)
34. Gotthard, K., Berger, D. & Walters, R. 2007 What keeps insects small? Time limitation during oviposition reduces the fecundity benefit of female size in a butterfly. Am. Nat. 169, 768-779. (doi:10.1086/516651)
35. Graf, B., Borer, F., Hopli, H. U., Hohn, H. & Dorn, S. 1995 The winter moth, Operophtera brumata L (Lep, Geometridae) on apple and cherry-spatial and temporal aspects of recolonization in autumn. J. Appl. Entomol. 119, 295-301. (doi:10.1111/j.1439-0418.1995.tb01289.x)
36. Hagen, S. B., Jepsen, J. U., Ims, R. A. & Yoccoz, N. G. 2007 Shifting altitudinal distribution of outbreak zones of winter moth Operophtera brumata in sub-arctic birch forest: a response to recent climate warming? Ecography 30, 299-307.
37. Harrington, R., Woiwod, I. & Sparks, T. 1999 Climate change and trophic interactions. Trends Ecol. Evol. 14, 146-150. (doi:10.1016/S0169-5347 (99) 01604-3)
38. Harrison, S., Murphy, D. D. & Ehrlich, P. R. 1988 Distribution of the bay checkerspot butterfly, Euphydryas editha bayensis. Evidence for a metapopulation model. Am. Nat. 132, 360-382. (doi:10.1086/284858)
39. Harrison, S., Quinn, J. F., Baughman, J. F., Murphy, D. D. & Ehrlich, P. R. 1991 Estimating the effects of scientific study on 2 butterfly populations. Am. Nat. 137, 227-243. (doi:10.1086/285155)
40. Hellmann, J. J. 2002 The effect of an environmental change on mobile butterfly larvae and the nutritional quality of their hosts. J. Anim. Ecol. 71, 925-936. (doi:10.1046/j. 1365-2656.2002.00658.x)
41. Hellmann, J. J., Weiss, S. B., McLaughlin, J. F., Boggs, C. L., Ehrlich, P. R., Murphy, D. D. & Launer, A. E. 2003 Do hypotheses from short-term studies hold in the long term? An empirical test. Ecol. Entomol. 28, 74-84. (doi:10. 1046/j.1365-2311.2003.00484.x)
42. Hellmann, J. J., Weiss, S. B., McLaughlin, J. F., Ehrlich, P. R., Murphy, D. D. & Launer, A. E. 2004 Structure and dynamics of Euphydryas editha populations. In On the wings of checkerspots: a model system for population biology (eds P. R. Ehrlich & I. Hanski), pp. 34-62. Oxford, UK: Oxford University Press.
43. Higgins, L. 2000 The interaction of season length and development time alters size at maturity. Oecologia 122, 51-59. (doi:10.1007/PL00008835)
44. Hobbs, R. J. & Mooney, H. A. 1985 Community and population dynamics of serpentine annual grasslands in relation to gopher disturbance. Oecologia 67, 342-351. (doi:10.1007/BF00384939)
45. Hoeksema, J. D. & Forde, S. E. 2008 A meta-analysis of factors affecting local adaptation between interacting species. Am. Nat. 171, 275-290. (doi:10.1086/527496)
46. Hoffmann, A. A. & Blows, M. W. 1994 Species borders: ecological and evolutionary perspectives. Trends Ecol. Evol. 9, 223-227. (doi:10.1016/0169-5347 (94) 90248-8)
47. Holliday, N. J. 1977 Population ecology of winter moth (Operophtera brumata) on apple in relation to larval dispersal and time of bud burst. J. Appl. Ecol. 1, 803-813.
48. Holliday, N. J. 1985 Maintenance of the phenology of the winter moth (Lepidoptera: Geometridae). Biol. J. Linn. Soc. 25, 221-234. (doi:10.1111/j.1095-8312.1985. tb00394.x)
49. Huey, R. B. & Kingsolver, J. G. 1993 Evolutionary responses to extreme temperatures in ectotherms. Am. Nat. 142, S21-S46. (doi:10.1086/285521)
50. Hunter, M. D. 1990 Differential susceptibility to variable plant phenology and its role in competition between two insect herbivores on oak. Ecol. Entomol. 15, 401-408. (doi:10.1111/j.1365-2311.1990.tb00823.x)
51. Hunter, M. D. 1992 A variable plant-insect interaction: the relationship between tree budburst phenology and population levels of insect herbivores among trees. Ecol. Entomol. 16, 91-95.
52. Hunter, M. D., Varley, G. C. & Gradwell, G. R. 1997 Estimating the relative roles of top-down and bottom-up forces on insect herbivore populations: a classic study revisited. Proc. Natl Acad. Sci. USA 94, 9176-9181. (doi:10.1073/pnas.94.17.9176)
53. IPCC 2001 Climate change 2001: impacts, adaptation, and vulnerability. In Contribution of Working Group II to the Intergovernmental Panel on Climate Change Third Assessment Report (eds J. J. McCarthy, O. F. Canziani, N. A. Leary, D. J. Dokken & K. S. White). Cambridge, UK: Cambridge University Press.
54. IPCC 2007 Climate change 2007: impacts, adaptations and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds M. L. Parry, O. F. Canziani, J. P. Palutikof, P. J. van der Linden & C. E. Hanson). Cambridge, UK: Cambridge University Press.
55. Jepsen, J. U., Hagen, S. B., Karlsen, S. R. & Ims, R. A. 2009 Phase-dependent outbreak dynamics of geometrid moth linked to host plant phenology. Proc. R. Soc. B 276, 4119-4128. (doi:10.1098/rspb.2009.1148)
56. Kingsolver, J. G. 2009 The well-temperatured biologist. Am. Nat. 174, 755-768. (doi:10.1086/648310)
57. Kirkpatrick, M. 2009 Patterns of quantitative genetic variation in multiple dimensions. Genetica 136, 271-284. (doi:10.1007/s10709-008-9302-6)
58. Labine, P. A. 1968 The population biology of the butterfly Euphydryas editha VIII. Oviposition and its relation to the pattern of oviposition in other butterflies. Evolution 22, 799-805. (doi:10.2307/2406904)
59. Martin, T. L. & Huey, R. B. 2008 Why suboptimal is optimal: Jensen's inequality and ecotherm thermal preferences. Am. Nat. 171, E102-E118.
60. McCleery, R. H. & Perrins, C. M. 1998 Temperature and egg-laying trends. Nature 391, 30-31. (doi:10.1038/34073)
61. McLauglin, J. F., Hellmann, J. J., Boggs, C. L. & Ehrlich, P. R. 2002a The route to extinction: population dynamics of a threatened butterfly. Oecologia 132, 538-548.
62. McLauglin, J. F., Hellmann, J. J., Boggs, C. L. & Ehrlich, P. R. 2002b Climate change hastens population extinctions. Proc. Natl Acad. Sci. USA 99, 6070-6074.
63. Memmott, J., Craze, P. G., Waser, N. M. & Price, M. V. 2007 Global warming and the disruption of plant-pollinator interactions. Ecol. Lett. 10, 710-717. (doi:10. 1111/j.1461-0248.2007.01061.x)
64. Menzel, A. & Dose, V. 2005 Analysis of long-term time-series of beginning of flowering by Bayesian function estimation. Meteorol. Zeitschrift 14, 429-434. (doi:10. 1127/0941-2948/2005/0040)
65. Menzel, A. et al. 2006 European phenological response to climate change matches the warming pattern. Glob. Change Biol. 12, 1969-1976. (doi:10.1111/j.1365-2486. 2006.01193.x)
66. Miller-Rushing, A. J. & Primack, R. B. 2008 Global warming and flowering times in Thoreau's Concord: a community perspective. Ecology 89, 332-341. (doi:10. 1890/07-0068.1)
67. Miller-Rushing, A. J., Høye, T. T., Inouye, D. W. & Post, E. 2010 The effects of phenological mismatches on demography. Phil. Trans. R. Soc. B 365, 3177-3186. (doi:10.1098/rstb.2010.0148)
68. Moore, R. A. & Singer, M. C. 1987 Effects of maternal age and adult diet on egg weight in the butterfly Euphydryas editha. Ecol. Entomol. 12, 401-408. (doi:10.1111/j.1365-2311.1987.tb01021.x)
69. Morin, X., Lechowicz, M. J., Augspurger, C., O'Keefe, J., Viner, D. & Chuine, I. 2009 Leaf phenology in 22 North American tree species during the 21st century. Glob. Change Biol. 15, 961-975. (doi:10.1111/j.1365-2486.2008. 01735.x)
70. Neve, G. & Singer, M. C. 2008 Protandry and postandry in two related butterflies: conflicting evidence about sexspecific trade-offs between adult size and emergence time. Evol. Ecol. 22, 701-709.
71. Nylin, S. 1988 Host plant specialization and seasonality in a polyphagous butterfly, Polygonia c-album (Nymphalidae). Oikos 53, 381-386. (doi:10.2307/3565539)
72. Parmesan, C. 1996 Climate and species' range. Nature 382, 765-766. (doi:10.1038/382765a0)
73. Parmesan, C. 2003 Butterflies as bio-indicators of climate change impacts. In Evolution and ecology taking flight: butterflies as model systems (eds C. L. Boggs, W. B. Watt & P. R. Ehrlich), pp. 541-560. Chicago, IL: University of Chicago Press.
74. Parmesan, C. 2006 Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637-669.
75. Parmesan, C. 2007 Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob. Change Biol. 13, 1860-1872. (doi:10.1111/j.1365-2486.2007.01404.x)
76. Parmesan, C. & Yohe, G. 2003 Globally coherent fingerprints of climate change impacts across natural systems. Nature 421, 37-42. (doi:10.1038/nature01286)
77. Parmesan, C., Gaines, S., Gonzalez, L., Kaufman, D. M., Kingsolver, J., Peterson, A. T. & Sagarin, R. 2005 Empirical perspectives on species' borders: from traditional biogeography to global change. Oikos 108, 58-75. (doi:10.1111/j.0030-1299.2005.13150.x)
78. Price, T., Kirkpatrick, M. & Arnold, S. J. 1988 Directional selection and the evolution of breeding date in birds. Science 240, 798-799. (doi:10.1126/science.3363360)
79. Reznick, D., Nunney, L. & Tessier, A. 2000 Big houses, big cars, superfleas and the costs of reproduction. Tr e n d s E c o l. Evol. 15, 421-425. (doi:10.1016/S0169-5347 (00) 01941-8)
80. Roff, D. A. 1992 The evolution of life histories: theory and analysis. New York, NY: Chapman & Hall.
81. Roff, D. A. & Fairbairn, D. J. 2007 The evolution of tradeoffs; where are we? J. Evol. Biol. 20, 433-447. (doi:10. 1111/j.1420-9101.2006.01255.x)
82. Root, T. L. & Schneider, S. 2006 Conservation and climate change: the challenges ahead. Conserv. Biol. 20, 706-708. (doi:10.1111/j.1523-1739.2006. 00465.x)
83. Root, T. L., Price, J. T., Hall, K. R., Schneider, S. H., Rosenzweig, C. & pounds, J. A. 2003 Fingerprints of global warming on wild animals and plants. Nature 421, 57-60. (doi:10.1038/nature01333)
84. Ruel, J. J. & Ayres, M. P. 1999 Jensen's inequality predicts effects of environmental variation. Trends Ecol. Evol. 14, 361-366. (doi:10.1016/S0169- 5347 (99) 01664-X)
85. Sagarin, R. D., Barry, J. P., Gilman, S. E. & Baxter, C. H. 1999 Climate-related change in an intertidal community over short and long time scales. Ecol. Monogr. 69, 465-490. (doi:10.1890/0012-9615 (1999) 069[0465:CR CIAI]2.0.CO;2)
86. Scriber, J. M. & Lederhouse, R. C. 1992 The thermal environment as a resource dictating geographic patterns of feeding specialization of insect herbivores. In The effects of resource distribution on animal-plant interactions (eds M. R. Hunter, T. Ohgushi & P. W. Price), pp. 429-466. New York, NY: Academic Press.
87. Sherry, R. A., Zhou, X., Gu, S., Arnone, J. A., Schimel, D. S., Verburg, P. S., Wallace, L. L. & Luo, Y. 2006 Divergence of reproductive phenology under climate warming. Proc. Natl Acad. Sci. USA 104, 198-202. (doi:10.1073/pnas.0605642104)
88. Singer, M. C. 1971 Ecological studies on the butterfly Euphydryas editha. PhD thesis, Stanford University, CA.
89. Singer, M. C. 1972 Complex components of habitat suitability within a butterfly colony. Science 176, 75-77. (doi:10.1126/science.176.4030.75)
90. Singer, M. C. & Ehrlich, P. R. 1979 Population dynamics of the checkerspot butterfly Euphydryas editha. Fortschr. Zool. 25, 53-60.
91. Singer, M. C. & Hanski, I. 2004 Dispersal behavior and evolutionary metapopulation dynamics. In On the wings of checkerspots: a model system for population biology (eds P. R. Ehrlich & I. Hanski), pp. 181-198. Oxford, UK: Oxford University Press.
92. Singer, M. C. & Thomas, C. D. 1996 Evolutionary responses of a butterfly metapopulation to human-and climate-caused environmental variation. Am. Nat. 148, S9-S39. (doi:10.1086/285900)
93. Sparks, T. H. & Yates, T. J. 1997 The effect of spring temperature on the appearance dates of British butterflies 1883-1993. Ecography 20, 368-374. (doi:10.1111/j. 1600-0587.1997.tb00381.x)
94. Stenseth, N. Chr. & Mysterud, A. 2002 Climate, changing phenology, and other life history traits: nonlinearity and match-mismatch to the environment. Proc. Natl Acad. Sci. USA 99, 13 379-13 381. (doi:10.1073/pnas. 212519399)
95. Thackeray, S. J. et al. 2010 Trophic level asynchrony in rates of phenological change for marine, terrestrial and freshwater environments. Glob. Change Biol. (doi:10.1111/j. 1365-2486.2010.02165.x)
96. Thomas, C. D. & Lennon, J. J. 1999 Birds extend their ranges northwards. Nature 399, 213. (doi:10.1038/20335)
97. Thomas, C. D., Singer, M. C. & Boughton, D. A. 1996 Catastrophic extinction of population sources in a butterfly metapopulation. Am. Nat. 148, 957-975. (doi:10.1086/285966)
98. Tikkanen, O.-P. & Julkunen-Tiitto, R. 2003 Phenological variation as protection against defoliating insects: the case of Quercus robur and Operophtera brumata. Oecologia 136, 244-251. (doi:10.1007/s00442-003-1267-7)
99. Tikkanen, O.-P., Woodcock, B., Watt, A. & Lock, K. 2006 Are polyphagous geometrid moths with wingless females adapted to budburst phenology of local host species? Oikos 112, 83-90. (doi:10.1111/j.0030-1299.2006. 13855.x)
100. van Asch, M. & Visser, M. E. 2007 Phenology of forest caterpillars and their host trees: the importance of synchrony. Annu. Rev. Entomol. 52, 37-55. (doi:10.1146/annurev. ento.52.110405.091418)
101. van Asch, M., Holleman, L. J. & Visser, M. E. In preparation. Climate change induced genetic shifts in an insect herbivore's temperature sensitivity.
102. van Asch, M., van Tienderen, P. H., Holleman, L. J. & Visser, M. E. 2007 Predicting adaptation of phenology in response to climate change, an insect herbivore example. Glob. Change Biol. 13, 1596-1604. (doi:10. 1111/j.1365-2486.2007.01400.x)
103. van Dongen, S., Backeljau, T., Matthyssen, E. & Dhondt, A. A. 1997 Synchronization of hatching date with budburst of individual host trees (Quercus robur) in the winter moth, Operophtera brumata and its fitness consequences. J. Anim. Ecol. 66, 113-121. (doi:10. 2307/5969)
104. Van Noordwijk, A. J., McCleery, R. H. & Perrins, C. M. 1995 Selection for the timing of great tit breeding in relation to caterpillar growth and temperature. J. Anim. Ecol. 64, 451-458. (doi:10.2307/5648)
105. Van Nouhuys, S. & Lei, G. C. 2004 Parasitoid-host metapopulation dynamics: the causes and consequences of phenological asynchrony. J. Anim. Ecol. 73, 526-535. (doi:10.1111/j.0021-8790.2004.00827.x)
106. Varley, G. C., Gradwell, G. R. & Hassell, M. P. 1973 Insect population ecology: an analytical approach. Oxford UK: Blackwell.
107. Visser, M. E. & Both, C. 2005 Shifts in phenology due to global climate change: the need for a yardstick. Proc. R. Soc. Lond. B 272, 2561-2569. (doi:10.1098/rspb.2005.3356)
108. Visser, M. E. & Holleman, L. J. M. 2001 Warmer springs disrupt the synchrony of oak and winter moth phenology. Proc. R. Soc. Lond. B 268, 289-294. (doi:10.1098/rspb. 2000.1363)
109. Visser, M. E., van Noordwijk, A. J., Tinbergen, J. M. & Lessels, C. M. 1998 Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc. R. Soc. Lond. B 265, 1867-1870. (doi:10.1098/rspb.1998.0514)
110. Visser, M. E., Both, C. & Lambrechts, M. 2004 Global climate change leads to mistimed avian reproduction. Adv. Ecol. Res. 35, 89-110. (doi:10.1016/S0065-2504 (04) 35005-1)
111. Visser, M. E., Holleman, L. J. M. & Gienapp, P. 2006 Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia 147, 164-172. (doi:10.1007/s00442-005-0299-6)
112. Weiss, S. B., Murphy, D. D. & White, R. R. 1988 Sun, slope and butterflies: topographic determinants of habitat quality for Euphydryas editha. Ecology 69, 1486-1496.
113. Weiss, S. B., Murphy, D. D., Ehrlich, P. R. & Metzler, C. F. 1993 Adult emergence phenology in checkerspot butterflies-the effects of macroclimate, topoclimate and population history. Oecologia 96, 261-270. (doi:10. 1007/BF00317740)
114. Willis, C. G., Ruhfel, B. R., Primack, R. B., Miller-Rushing, A. J. & Davis, C. C. 2008 Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change. Proc. Natl Acad. Sci. USA 105, 17 029-17 033. (doi:10. 1073/pnas.0806446105)
115. Willis, C. G., Ruhfel, B. R., Primack, R. B., Miller-Rushing, A. J., Losos, J. B. & David, C. C. 2010 Favorable climatechange response explains non-native species' success in Thoreau's woods. PLoS ONE 5, e8878. (doi:10.1371/journal.pone.0008878)
116. Winder, M. & Schindler, D. E. 2004 Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85, 2100-2106. (doi:10.1890/04-0151)
117. Wint, W. 1983 The role of alternative host plant species in the life of a polyphagous moth, Operophtera brumata (Geometridae). J. Anim. Ecol. 52, 439-450.
118. Zalucki, M. P., Clarke, A. R. & Malcolm, S. B. 2002 Ecology and behavior of first-instar larval Lepidoptera. Annu. Rev. Entomol. 47, 361-393. (doi:10.1146/annurev. ento.47. 091201.145220)