Impact of climate change on plant phenology in Mediterranean ecosystems

Global Change Biology

Volumn 16, Issue 3, 2010, Pages 1082-1106

  Gordo, Oscar ^a   Sanz, Juan José ^a,b  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^b University of Castilla La Mancha Av Carlos III ^*  (Spain)

Author keywords

Flowering; Fruiting; Global warming; Growing season; Leaf falling; Leaf unfolding; North Atlantic Oscillation; Precipitation; Spain; Temperature

Indexed keywords

BIOINDICATOR; CLIMATE CHANGE; CLIMATE EFFECT; ECOSYSTEM RESPONSE; FLOWERING; FRUITING; GLOBAL WARMING; LEAF; NORTH ATLANTIC OSCILLATION; PHENOLOGY; PLANT; PRECIPITATION (CLIMATOLOGY); SPATIAL VARIATION; TEMPERATURE EFFECT;

MEDITERRANEAN REGION;

HEXAPODA;

EID: 77149136736     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/j.1365-2486.2009.02084.x     Document Type: Article

References (97)

1. Ahas R, Aasa A. The effects of climate change on the phenology of selected Estonian plant, bird and fish populations. International Journal of Biometeorology 2006, 51:17-26.
2. Alward RD, Detling JK, Milchunas DG. Grassland vegetation changes and nocturnal global warming. Science 1999, 283:229-231.
3. Atlas de plantas para las observaciones fenológicas 1943, Anonymous, Servicio Meteorológico Nacional - Sección de Climatología, Madrid
4. Normas e instrucciones para las observaciones fenológicas 1989, Anonymous, Sección de Meterología Agrícola y Fenología - Instituto Nacional de Meteorología, Madrid
5. Askeyev OV, Tischin D, Sparks TH, Askeyev IV. The effect of climate on the phenology, acorn crop and radial increment of pedunculate oak (Quercus robur) in the middle Volga region, Tatarstan, Russia. International Journal of Biometeorology 2005, 49:262-266.
6. Badeck FW, Bondeau A, Böttcher K, Doktor D, Lucht W, Schaber J, Sitch S. Responses of spring phenology to climate change. New Phytologist 2004, 162:295-309.
7. Blanco G, Fargallo JA, Cuevas JA. Consumption rates of olives by choughs in central Spain: variations and importance. Journal of Field Ornithology 1994, 65:482-489.
8. Cayan DR, Kammerdiener SA, Dettinger MD, Caprio JM, Peterson DH. Changes in the onset of spring in the western United States. Bulletin of the American Meteorological Society 2001, 82:399-415.
9. Chmielewski FM, Müller A, Bruns E. Climate changes and trends in phenology of fruit trees and field crops in Germany, 1961-2000. Agricultural and Forest Meteorology 2004, 121:69-78.
10. Chmielewski FM, Müller A, Küchler W. Possible impacts of climate change on natural vegetation in Saxony (Germany). International Journal of Biometeorology 2005, 50:96-104.
11. Chmielewski FM, Rötzer T. Response of tree phenology to climate change across Europe. Agricultural and Forest Meteorology 2001, 108:101-112.
12. Chuine I, Cour P, Rousseau DD. Selecting models to predict the timing of flowering of temperate trees: implications for tree phenology modelling. Plant, Cell and Environment 1999, 22:1-13.
13. Clevenger AP, Purroy FJ, Pelton MR. Food habits of brown bears (Ursus arctos) in the Cantabrian Mountains, Spain. Journal of Mammalogy 1992, 73:415-421.
14. de Castro M, Martín-Vide J, Alonso S. El clima de España: pasado, presente y escenarios de clima para el siglo XXI. Evaluación preliminar de los impactos en España por efecto del cambio climático 2005, 1-65. Moreno Rodríguez JM. In, ed, Ministerio de Medio Ambiente, Madrid
15. Doi H. Winter flowering phenology of Japanese apricot Prunus mume reflects climate change across Japan. Climate Research 2007, 34:99-104.
16. Doi H, Katano I. Phenological timings of leaf budburst with climate change in Japan. Agricultural and Forest Meteorology 2008, 148:512-516.
17. Doi H, Takahashi M. Latitudinal patterns in the phenological response of leaf colouring and leaf fall to climate change in Japan. Global Ecology and Biogeography 2008, 17:556-561.
18. Estrella N, Menzel A. Responses of leaf colouring in four deciduous tree species to climate and weather in Germany. Climate Research 2006, 32:253-267.
19. Estrella N, Sparks TH, Menzel A. Trends and temperature response in the phenology of crops in Germany. Global Change Biology 2007, 13:1737-1747.
20. Fitter AH, Fitter RSR. Rapid changes in flowering time in British plants. Science 2002, 296:1689-1691.
21. Fitter AH, Fitter RSR, Harris ITB, Williamson MH. Relationships between first flowering date and temperature in the flora of a locality in central England. Functional Ecology 1995, 9:55-60.
22. Galán C, Vázquez L, García-Mozo H, Domínguez E. Forecasting olive (Olea europaea) crop yield based on pollen emission. Field Crops Research 2004, 86:43-51.
23. García Mozo H, Pérez-Badía R, Galán C. Aerobiological and meteorological factors' influence on olive (Olea europaea L.) crop yield in Castilla-La Mancha (Central Spain). Aerobiologia 2008, 24:13-18.
24. González-Solís J, Ruiz X. Alimentación de Turdus philomelos en los olivares mediterráneos ibéricos, durante la migración otoñal. Miscelánea Zoológica 1990, 14:195-206.
25. Goodess CM, Jones PD. Links between circulation and changes in the characteristics of Iberian rainfall. International Journal of Climatology 2002, 22:1593-1615.
26. Gordo O, Sanz JJ. Phenology and climate change: a long-term study in a Mediterranean locality. Oecologia 2005, 146:484-495.
27. Gordo O, Sanz JJ. Climate change and bird phenology: a long-term study in the Iberian Peninsula. Global Change Biology 2006a, 12:1993-2004.
28. Gordo O, Sanz JJ. Temporal trends in phenology of the honey bee Apis mellifera (L.) and the small white Pieris rapae (L.) in the Iberian Peninsula (1952-2004). Ecological Entomology 2006b, 31:261-268.
29. Gordo O, Sanz JJ. Long-term temporal changes of plant phenology in the Western Mediterranean. Global Change Biology 2009, 15:1930-1948.
30. Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø. How does climate warming affect plant-pollinator interactions? Ecology Letters 2009, 12:184-195.
31. Heide OM. High autumn temperature delays spring bud burst in boreal trees, counterbalancing the effect of climatic warming. Tree Physiology 2003, 23:931-936.
32. Hunter AH, Lechowicz MJ. Predicting the timing of budburst in temperate trees. Journal of Applied Ecology 1992, 29:597-604.
33. Hurrell JW, van Loon H. Decadal variations in climate associated with North Atlantic oscillation. Climatic Change 1997, 36:301-326.
34. Inouye DW. The ecological and evolutionary significance of frost in the context of climate change. Ecology Letters 2000, 3:457-463.
35. Irizar I, Laskurain LA, Herrero J. Wild board frugivory in the Atlantic Basque country. Galemys 2004, 16:125-133.
36. Jenni L, Kéry M. Timing of autumn bird migration under climate change: advances in long-distance migrants, delays in short-distance migrants. Proceedings of the Royal Society of London Series B 2003, 270:1467-1471.
37. Kington JA. An application of phenology data to historical climatology. Weather 1974, 29:320-328.
38. Kramer K. Selecting a model to predict the onset of growth of Fagus sylvatica. Journal of Applied Ecology 1994, 31:172-181.
39. Leith M. Phenology and Seasonality Modeling 1974, Springer, New York
40. Llorens L, Peñuelas J. Experimental evidence of future drier and warmer conditions affecting flowering of two co-occurring Mediterranean shrubs. International Journal of Plant Science 2005, 166:235-245.
41. Lloret F, Peñuelas J, Estiarte M. Experimental evidence of reduced diversity of seedlings due to climate modification in a Mediterranean-type community. Global Change Biology 2004, 10:248-258.
42. Lu PL, Yu Q, Liu JD, He QT. Effects of changes in spring temperature on flowering dates of woody plants across China. Botanical Studies 2006, 47:153-161.
43. Margary ID. The Marsham phenological record in Norfolk, 1736-1925, and some others. Quarterly Journal of the Royal Meteorological Society 1926, 52:27-52.
44. Matesanz S, Escudero A, Valladares F. Impact of three global drivers on a Mediterranean shrub. Ecology 2009, 90:2609-2621.
45. Matsumoto K, Ohta T, Irasawa M, Nakamura T. Climate change and extension of the Ginkgo biloba L. growing season in Japan. Global Change Biology 2003, 9:1634-1642.
46. McKnight TL, Hess D. Physical Geography: A Landscape Appreciation 1999, 6th edn, Prentice Hall, Upper Saddle River
47. Menzel A. Plant phenological anomalies in Germany and their relation to air temperature and NAO. Climatic Change 2003, 57:243-263.
48. Menzel A, Estrella N, Testka A. Temperature response rates from long-term phenological records. Climate Research 2005a, 30:21-28.
49. Menzel A, Fabian P. Growing season extended in Europe. Nature 1999, 397:659.
50. Menzel A, Sparks TH, Estrella N. European phenological response to climate change matches the warming pattern. Global Change Biology 2006a, 12:1969-1976.
51. Menzel A, Sparks TH, Estrella N, Eckhardt S. 'SSW to NNE'- North Atlantic Oscillation affects the progress of seasons across Europe. Global Change Biology 2005b, 11:909-918.
52. Menzel A, von Vopelius J, Estrella N, Schleip C, Dose V. Farmers' annual activities are not tracking the speed of climate change. Climate Research 2006b, 32:201-207.
53. Mezquida E, Villarán A, Pascual-Parra J. Timing of autumn bird migration in central Spain in light of recent climate change. Ardeola 2007, 54:251-259.
54. Miller-Rushing AJ, Inouye DW, Primack RB. How well do first flowering dates measure plant responses to climate change? The effects of population size and sampling frequency. Journal of Ecology 2008a, 96:1289-1296.
55. Miller-Rushing AJ, Katsuki T, Primack RB, Ishii Y, Lee SD, Higuchi H. Impact of global warming on a group of related species and their hybrids: cherry tree (Rosaceae) flowering at Mt. Takao, Japan. American Journal of Botany 2007, 94:1470-1478.
56. Miller-Rushing AJ, Primack RB. Effects of winter temperature on two birch (Betula) species. Tree Physiology 2008b, 28:659-664.
57. Miller-Rushing AJ, Primack RB. Global warming and flowering times in Thoreau's Concord: a community perspective. Ecology 2008c, 89:332-341.
58. Nordli Ø, Wielgolaski FE, Bakken AK, Hjeltnes SH, Måge F, Sivle A, Skre O. Regional trends for bud burst and flowering of woody plants in Norway as related to climate change. International Journal of Biometeorology 2008, 52:625-639.
59. Ogaya R, Peñuelas J. Phenological patterns of Quercus ilex, Phillyrea latifolia, and Arbutus unedo growing under a field experimental drought. Ecoscience 2004, 11:264-270.
60. Ottersen G, Planque B, Belgrano A, Post E, Reid PC, Stenseth NC. Ecological effects of the North Atlantic Oscillation. Oecologia 2001, 128:1-14.
61. Parmesan C, Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 2003, 421:37-42.
62. Peñuelas J, Filella I, Comas P. Changed plant and animal life cycles from 1952 to 2000 in the Mediterranean region. Global Change Biology 2002, 8:531-544.
63. Peñuelas J, Filella I, Zhang X. Complex spatiotemporal phenological shifts as a response to rainfall changes. New Phytologist 2004, 161:837-846.
64. Post E, Forchhammer MC, Stenseth NC, Callaghan TV. The timing of life-history events in a changing climate. Proceedings of the Royal Society of London Series B 2001, 268:15-23.
65. Post E, Pedersen C, Wilmers CC, Forschhammer MC. Phenological sequences reveal aggregate life history response to climatic warming. Ecology 2008a, 89:363-370.
66. Post E, Pedersen C, Wilmers CC, Forschhammer MC. Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores. Proceedings of the Royal Society of London Series B 2008b, 275:2005-2013.
67. Post E, Stenseth NC. Climatic variability, plant phenology, and northern ungulates. Ecology 1999, 80:1322-1339.
68. Prieto P, Peñuelas J, Ogaya R, Estiarte M. Precipitation-dependent flowering of Globularia alypum and Erica multiflora in Mediterranean shrubland under experimental drought and warming, and its inter-annual variability. Annals of Botany 2008, 102:275-285.
69. Rey PJ. The role of olive orchards in the wintering of frugivorous birds in Spain. Ardea 1993, 81:151-160.
70. Rodó X, Baert E, Comín FA. Variations in seasonal rainfall in Southern Europe during the present century: relationships with the North Atlantic Oscillation and the El Niño-Southern Oscillation. Climate Dynamics 1997, 13:275-284.
71. Rodó X, Comín FA. Links between large-scale anomalies, rainfall and wine quality in the Iberian Peninsula during the last three decades. Global Change Biology 2000, 6:267-273.
72. Root TL, MacMynowski DP, Mastrandrea MD, Schneider SH. Human-modified temperatures induce species changes: joint attribution. Proceedings of the National Academy of Sciences USA 2005, 102:465-7469.
73. Rosenzweig C, Karoly D, Vicarelli M. Attributing physical and biological impacts to anthropogenic climate change. Nature 2008, 435:353-357.
74. Rötzer T, Chmielewski FM. Phenological maps of Europe. Climate Research 2001, 18:249-257.
75. Roy DB, Sparks TH. Phenology of British butterflies and climate change. Global Change Biology 2000, 6:407-416.
76. Scheifinger H, Menzel A, Koch E, Peter C, Ahas R. Atmospheric mechanisms governing the spatial and temporal variability of phenological phases in central Europe. International Journal of Climatology 2002, 22:1739-1755.
77. Schlichting CD. The evolution of phenotypic plasticity in plants. Annual Review in Ecology and Evolution 1986, 17:667-693.
78. Schwartz MD, Ahas R, Aasa A. Onset of spring starting earlier across the Northern Hemisphere. Global Change Biology 2006, 12:343-351.
79. Schwartz MD, Chen X. Examining the onset of spring in China. Climate Research 2002, 21:157-164.
80. Sherry RA, Zhou X, Gu S, Arnone JA. Divergence of reproductive phenology under climate warming. Proceedings of the National Academy of Sciences USA 2007, 104:198-202.
81. Soler M, Pérez-González JA, Tejero E, Camacho I. Alimentación del zorzal alirrojo (Turdus iliacus) durante su invernada en olivares de Jaén (sur de España). Ardeola 1988, 35:183-196.
82. Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change 2007, Solomon SQin DManning M. (eds), Cambridge University Press, Cambridge
83. Sparks TH, Carey PD, Combes J. First leafing dates of trees in Surrey between 1947 and 1996. London Naturalist 1997, 76:15-20.
84. Sparks TH, Jeffree EP, Jeffree CE. An examination of the relationship between flowering times and temperatures at the national scale using long-term phenological records from the UK. International Journal of Biometeorology 2000, 44:82-87.
85. Stefanescu C, Peñuelas J, Filella I. Effects of climatic change on the phenology of butterflies in the northwest Mediterranean Basin. Global Change Biology 2003, 9:1494-1506.
86. Stöckli R, Vidale PL. European plant phenology and climate as seen in a 20-year AVHRR land-surface parameter dataset. International Journal of Remote Sensing 2004, 25:3303-3330.
87. Trigo RM, Pozo-Vázquez D, Osborn TJ, Castro-Díez Y, Gámiz-Fortis S, Esteban-Parra MJ. North Atlantic oscillation influence on precipitation, river flow and water resources in the Iberian Peninsula. International Journal of Climatology 2004, 24:925-944.
88. Tromp J. Maturity of apple cv. Elstar as affected by temperature during a six-week period following bloom. Journal of Horticultural Science 1997, 72:811-819.
89. Tryjanowski P, Panek M, Sparks TH. Phenological response of plants to temperature varies at the same latitude: case study of dog violet and horse chestnut in England and Poland. Climate Research 2006, 32:89-93.
90. Vicens N, Bosch J. Weather-dependent pollinator activity in an apple orchard, with special reference to Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae and Apidae). Environmental Entomology 2000, 29:413-420.
91. Vicente-Serrano SM, Heredia-Laclaustra A. NAO influence on NDVI trends in the Iberian Peninsula (1982-2000). International Journal of Remote Sensing 2004, 20:2871-2879.
92. von Ende CM. Repeated-measures analysis: growth and other time-dependent measures. Design and Analysis of Ecological Experiments 1993, 113-137. Scheiner SMGurevitch J. In, eds, Champman & Hall, New York
93. Warrington IJ, Fulton TA, Halligan EA, De Silva HN. Apple fruit growth and maturity are affected by early season temperatures. Journal of the American Society for Horticultural Science 1999, 124:468-477.
94. Williams TA, Abberton MT. Earlier flowering between 1962 and 2002 in agricultural varieties of white clover. Oecologia 2004, 138:122-126.
95. Willis CG, Ruhfel B, Primack RB, Miller-Rushing AJ, Davis CC. Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change. Proceedings of the National Academy of Sciences USA 2008, 105:17029-17033.
96. Willmer P, Stone G. Behavioral, ecological, and physiological determinants of the activity patterns of bees. Advances in the Study of Behavior 2004, 34:347-466.
97. Zheng JY, Ge QS, Hao ZX, Wang WC. Spring phenophases in recent decades over eastern China and its possible link to climate changes. Climatic Change 2006, 77:449-462.