Abstract
The strength and direction of phenological responses to changes in climate have been shown to vary significantly both among species and among populations of a species, with the overall patterns not fully resolved. Here, we studied the temporal and spatial variability associated with the response of several insect species to recent global warming. We use hierarchical models within a model comparison framework to analyze phenological data gathered over 40 years by the Japan Meteorological Agency on the emergence dates of 14 insect species at sites across Japan. Contrary to what has been predicted with global warming, temporal trends of annual emergence showed a later emergence day for some species and sites over time, even though temperatures are warming. However, when emergence data were analyzed as a function of temperature and precipitation, the overall response pointed out an earlier emergence day with warmer conditions. The apparent contradiction between the response to temperature and trends over time indicates that other factors, such as declining populations, may be affecting the date phenological events are being recorded. Overall, the responses by insects were weaker than those found for plants in previous work over the same time period in these ecosystems, suggesting the potential for ecological mismatches with deleterious effects for both suites of species. And although temperature may be the major driver of species phenology, we should be cautious when analyzing phenological datasets as many other factors may also be contributing to the variability in phenology.
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References
Altermatt F (2010a) Climatic warming increases voltinism in European butterflies and moths. Proc R Soc Lond B 277:1281–1287
Altermatt F (2010b) Tell me what you eat and I’ll tell you when you fly: diet can predict phenological changes in response to climate change. Ecol Lett 13:1475–1484
Amano T, Smithers RJ, Sparks TH, Sutherland WJ (2010) A 250-year index of first flowering dates and its response to temperature changes. Proc R Soc Lond B 277:2451–2457
Awa M, Kobayas K (2010) Apple (Malus pumila var. domestica) phenology is advancing due to rising air temperature in northern Japan. Glob Change Biol 16:2651–2660
Both C, van Asch M, Bijlsma RG, van den Burg AB, Visser ME (2009) Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? J Anim Ecol 78:73–83
Both C, Van Turnhout CAM, Bijlsma RG, Siepel H, Van Strien AJ, Foppen RPB (2010) Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats. Proc R Soc Lond B 277:1259–1266
Brooks SP, Gelman A (1998) General methods for monitoring convergence of iterative simulations. J Comput Graph Stat 7:434–455
Diamond SE, Frame AM, Martin RA, Buckley LB (2011) Species’ traits predict phenological responses to climate change in butterflies. Ecology 92:1005–1012. doi:10.1890/10-1594.1
Dixon AFG (2003) Climate change and phenological asynchrony. Ecol Entomol 28:380–381
Doi H (2008) Delayed phenological timing of dragonfly emergence in Japan over five decades. Biol Lett 4:388–391
Doi H, Gordo O, Katano I (2008) Heterogeneous intra-annual climatic changes drive different phenological responses at two trophic levels. Clim Res 36:181–190
Fabina NS, Abbott KC, Gilman RT (2010) Sensitivity of plant-pollinator-herbivore communities to changes in phenology. Ecol Model 221:453–458
Forkner RE, Marquis RJ, Lill JT, Le Corff J (2008) Timing is everything? phenological synchrony and population variability in leaf-chewing herbivores of Quercus. Ecol Entomol 33:276–285
Fujihara M, Hara K, Short KM (2005) Changes in landscape structure of “yatsu” valleys: a typical Japanese urban fringe landscape. Landsc Urban Plan 70:261–270
Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, New York
Hegland SJ, Nielsen A, Lazaro A, Bjerknes AL, Totland O (2009) How does climate warming affect plant–pollinator interactions? Ecol Lett 12:184–195
Hickling R, Roy DB, Hill JK, Fox R, Thomas CD (2006) The distributions of a wide range of taxonomic groups are expanding polewards. Glob Change Biol 12:450–455
Hirashima Y, Morimoto K (2008) Iconographia insectorum Japonicum colore naturali edita col. III. Hokuryan, Tokyo
Hodgson JA, Thomas CD, Oliver TH, Anderson BJ, Brereton TM, Crone EE (2010) Predicting insect phenology across space and time. Glob Change Biol 1365–2486. doi:10.1111/j.2010.02308.x
Huberty AF, Denno RF (2004) Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology 85:1383–1398
Ibáñez I et al (2010) Forecasting phenology under global warming. Philos Trans R Soc Lond B 365:3247–3260
IPCC (2007) Climate change 2007: the physical science basis. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller H (eds.) Contribution of working group to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge
Ishida S, Ishida K, Kojima K, Sugimura M (1988) Illustrated guide for identificatino of the Japanese Odonata. Tokai University Press, Tokyo
Itioka T, Yamauti M (2004) Severe drought, leafing phenology, leaf damage and lepidopteran abundance in the canopy of a Bornean aseasonal tropical rain forest. J Trop Ecol 20:479–482
Japan Meteorological Agency (2010). http://www.jma.go.jp/jma/indexe.html
Jentsch A, Kreling J, Boettcher-Treschkow J, Beierkuhnlein C (2009) Beyond gradual warming: extreme weather events alter flower phenology of European grassland and heath species. Glob Change Biol 15:837–849
Kadoya T, Suda S, Washitani I (2009) Dragonfly crisis in Japan: a likely consequence of recent agricultural habitat degradation. Biol Conserv 142:1899–1905
Koike S, Fujita G, Higuchi H (2006) Climate change and the phenology of sympatric birds, insects, and plants in Japan. Glob Environ Res 10:167–174
Leeper DA, Taylor BE (1998) Insect emergence from a South Carolina (USA) temporary wetland pond, with emphasis on the Chironomidae (Diptera). J North Am Benthol Soc 17:54–72
Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant–pollinator interactions. Ecol Lett 10:710–717
Menzel A et al (2006) European phenological response to climate change matches the warming pattern. Glob Change Biol 12:1969–1976
Miller-Rushing AJ, Lloyd-Evans TL, Primack RB, Satzinger P (2008) Bird migration times, climate change, and changing population sizes. Glob Change Biol 14:1959–1972
Mody K, Eichenberger D, Dorn S (2009) Stress magnitude matters: different intensities of pulsed water stress produce non-monotonic resistance responses of host plants to insect herbivores. Ecol Entomol 34:133–143
Moriyama M, Numata H (2008) Diapause and prolonged development in the embryo and their ecological significance in two cicadas, Cryptotympana facialis and Graptopsaltria nigrofuscata. J Insect Physiol 54:1487–1494
Nonomura A, Kitahara M, Masuda T (2009) Impact of land use and land cover changes on the ambient temperature in a middle scale city, Takamatsu, in Southwest Japan. J Environ Manag 90:3297–3304
Oka T (2006) The standard of butterflies in Japan. Gakushu Kenkyusha, Tokyo
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669
Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Change Biol 13:1860–1872
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42
Primack RB et al (2009) Spatial and interspecific variability in phenological responses to warming temperatures. Biol Conserv 142:2569–2577
R Core Development Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing Vienna, Austria
Robinet C, Roques A (2010) Direct impacts of recent climate warming on insect populations. Integrat Zool 5:132–142
Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60
Rosenzweig C et al (2008) Attributing physical and biological impacts to anthropogenic climate change. Nature 453:353–357
Rouault G, Candau JN, Lieutier F, Nageleisen LM, Martin JC, Warzee N (2006) Effects of drought and heat on forest insect populations in relation to the 2003 drought in Western Europe. Ann For Sci 63:613–624
Spiegelhalter DJ, Best NG, Carlin BR, van der Linde A (2002) Bayesian measures of model complexity and fit. J R Stat Soc B 64:583–616
Stefanescu C, Torre I, Jubany J, Paramo F (2011) Recent trends in butterfly populations from north-east Spain and Andorra in the light of habitat and climate change. J Insect Conserv 15:83–93
Sugimura M, Ishida S, Kojima K, Ishida K, Aoki N (1999) Dragonflies of the Japanese archipelago in color. Hokkaido University Press, Japan
Takamizawa K (2005) The Japanese social wasps and bees. Shinanomainichi Shimbun, Nagano
Thackeray SJ et al (2010) Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob Change Biol 16:3304–3313
Thomas CD et al (2001) Ecological and evolutionary processes at expanding range margins. Nature 411:577–581
Thomas A, O’Hara B, Ligges U, Sturtz S (2006) Making BUGS open. R News 6:2–6
Tobin PC, Nagarkatti S, Loeb G, Saunders MC (2008) Historical and projected interactions between climate change and insect voltinism in a multivoltine species. Glob Change Biol 14:951–957
Tryjanowski P, Sparks TH (2001) Is the detection of the first arrival date of migrating birds influenced by population size? a case study of the red-backed shrike Lanius collurio. Int J Biometeorol 45:217–219
Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R Soc Lond B 275:649–659
Zhang ZB, Cazelles B, Tian HD, Stige LC, Brauning A, Stenseth NC (2009) Periodic temperature-associated drought/flood drives locust plagues in China. Proc R Soc Lond B 276:823–831
Acknowledgments
We thank the Japan Meteorological Agency for collecting and making available the phenological data used here. Funding for this research was provided by the US National Science Foundation (DEB 0842465) to R.P., J.S. and I.I.
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Communicated by Jérome Casas.
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Ellwood, E.R., Diez, J.M., Ibáñez, I. et al. Disentangling the paradox of insect phenology: are temporal trends reflecting the response to warming?. Oecologia 168, 1161–1171 (2012). https://doi.org/10.1007/s00442-011-2160-4
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DOI: https://doi.org/10.1007/s00442-011-2160-4