First flowering of wind‐pollinated species with the greatest phenological advances in Europe

Increasing risk of pollinosis (hay fever) is one of the most anticipated consequences of climate change on human health. Wind-pollinated plants are representative of allergenic species because they include species with the highest capability of causing allergy-related diseases in humans. Therefore, changes in wind-pollinated species may reflect impacts of climate change on allergenic plants. In particular, flowering is one of the developmental stages most affected by climate change. This report specifically addresses changes in flowering dates that have occurred during the three decades 1971–2000 as a function of pollination mode and woodiness. The assessment is made using a phenological data set comprising trends of flowering dates of 29 species in 983 locations in Europe. Linear mixed models assessing the statistical significance of trends while adjusting for spatial correlation are used. The main results indicate for the first time that the onset of flowering of wind-pollinated plants advanced more than for insect-pollinated plants, while full flowering phases tended to advance less. These novel findings are contrary to the results of Fitter and Fitter (2002) for Oxfordshire, who reported larger advances of insect-pollinated plants. Onset of flowering and full flowering of insect-pollinated species are more likely to advance for seasons early in the year; instead, wind-pollinated plants showed no dependence of trends on the season (first flowering) or a decreased advance of phases that are early in the year (full flowering). The effect of woodiness could not be unambiguously defined, but seems to be of minor importance. The presented findings suggest a lengthening of the flowering period in general, which might lead to an increasing time of exposure to airborne pollen of allergic subjects, with consequent likely increment in severity and incidence of allergic symptoms.

[1]  M. Laaidi Regional variations in the pollen season of Betula in Burgundy: two models for predicting the start of the pollination , 2001 .

[2]  Terry V. Callaghan,et al.  Impacts of extreme winter warming in the sub‐Arctic: growing season responses of dwarf shrub heathland , 2008 .

[3]  A. Fitter,et al.  Rapid Changes in Flowering Time in British Plants , 2002, Science.

[4]  J. Williams Novelties of the flowering plant pollen tube underlie diversification of a key life history stage , 2008, Proceedings of the National Academy of Sciences.

[5]  Jonathan A. Patz,et al.  Recent warming by latitude associated with increased length of ragweed pollen season in central North America , 2011, Proceedings of the National Academy of Sciences.

[6]  Yiqi Luo,et al.  Divergence of reproductive phenology under climate warming , 2007, Proceedings of the National Academy of Sciences.

[7]  F. Bazzaz,et al.  Production of allergenic pollen by ragweed (Ambrosia artemisiifolia L.) is increased in CO2-enriched atmospheres. , 2002, Annals of allergy, asthma & immunology : official publication of the American College of Allergy, Asthma, & Immunology.

[8]  R. Xu Measuring explained variation in linear mixed effects models , 2003, Statistics in medicine.

[9]  J. Ackerman,et al.  Abiotic pollen and pollination: Ecological, functional, and evolutionary perspectives , 2000, Plant Systematics and Evolution.

[10]  CONTRASTING FLOWERING PHENOLOGY AND SPECIES RICHNESS IN ABIOTICALLY AND BIOTICALLY POLLINATED ANGIOSPERMS , 2003, Evolution; international journal of organic evolution.

[11]  P. Beggs Impacts of climate change on aeroallergens: past and future , 2004, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[12]  G. D'Amato,et al.  Effects of climate change on environmental factors in respiratory allergic diseases , 2008, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[13]  Annette Menzel,et al.  Influence of altitude on phenology of selected plant species in the Alpine region (1971-2000) , 2009 .

[14]  P. Regal POLLINATION BY WIND AND ANIMALS: Ecology of Geographic Patterns , 1982 .

[15]  S. Barrett,et al.  Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants. , 2009, Annals of botany.

[16]  Xuhui Lee,et al.  Advance of tree-flowering dates in response to urban climate change , 2006 .

[17]  Christopher B. Field,et al.  Diverse responses of phenology to global changes in a grassland ecosystem , 2006, Proceedings of the National Academy of Sciences.

[18]  S. Jaeger Exposure to grass pollen in Europe , 2008 .

[19]  J. Peñuelas,et al.  European phenological response to climate change matches the warming pattern , 2006 .

[20]  J. Craine,et al.  Interannual variability of pollen productivity and transport in mid-North America from 1997 to 2009 , 2011 .

[21]  J. Peñuelas,et al.  Phenological patterns of Quercus ilex, Phillyrea latifolia, and Arbutus unedo growing under a field experimental drought1 , 2004 .

[22]  Juergen Kreyling,et al.  Beyond gradual warming: extreme weather events alter flower phenology of European grassland and heath species , 2009 .

[23]  A. Rasmussen The effects of climate change on the birch pollen season in Denmark , 2002 .

[24]  Ignasi Bartomeus,et al.  Climate-associated phenological advances in bee pollinators and bee-pollinated plants , 2011, Proceedings of the National Academy of Sciences.

[25]  D. Rabinowitz,et al.  Phenological Properties of Wind‐ and Insect‐Pollinated Prairie Plants , 1981 .

[26]  D. Whitehead WIND POLLINATION IN THE ANGIOSPERMS: EVOLUTIONARY AND ENVIRONMENTAL CONSIDERATIONS , 1969, Evolution; international journal of organic evolution.

[27]  Betsy Jane Becker,et al.  The Synthesis of Regression Slopes in Meta-Analysis. , 2007, 0801.4442.

[28]  F. Bazzaz,et al.  Interaction of the Onset of Spring and Elevated Atmospheric CO2 on Ragweed (Ambrosia artemisiifolia L.) Pollen Production , 2006, Environmental health perspectives.

[29]  S. Bonini,et al.  Allergenic pollen and pollen allergy in Europe , 2007, Allergy.