Abstract
Grasses are a taxonomic group of considerable environmental importance, playing a major ecological role as well as making a significant contribution to the world’s economy, since they include valuable crop and pasture species. Grass pollen allergens are also among the main causes of respiratory allergies worldwide. The interpretation of airborne grass pollen concentrations is a particularly complex task, given the marked diversity of pollen-emitting species and the influence of weather-related variables. This paper examines the influence of meteorological variables on flowering in the species contributing most to airborne grass pollen concentrations. This study was carried out in the surroundings of the city of Toledo (Spain), a Mediterranean city located in the center of the Iberian Peninsula. Temperature was the variable most influencing flowering onset, which was also affected by relative humidity, rainfall and hours of sunlight. The flowering period of grass species that flower at the start of spring (Bromus rubens and Hordeum leporinum) began earlier in years with higher mean winter temperatures, while the species that flower from mid to late spring (Trisetaria panicea and Dactylis glomerata subsp. hispanica), the flowering period began earlier in years with higher cumulative rainfall in winter and spring, which were also the years with the highest mean temperatures. Research into the influence of weather-related variables on grass phenology can shed important light on variations in airborne pollen concentrations, which determine the potential period of exposure for allergy sufferers.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aboulaich, N., Achmakh, L., Bouziane, H., Trigo, M. M., Recio, M., Kadiri, M., et al. (2013). Effect of meteorological parameters on Poaceae pollen in the atmosphere of Tetouan (NW Morocco). International Journal of Biometeorology, 57(2), 197–205. https://doi.org/10.1007/s00484-012-0566-2.
Aboulaich, N., Bouziane, H., Kadiri, M., Del Mar Trigo, M., Riadi, H., Kazzaz, M., et al. (2009). Pollen production in anemophilous species of the Poaceae family in Tetouan (NW Morocco). Aerobiologia, 25(1), 27–38. https://doi.org/10.1007/s10453-008-9106-2.
AEMET. (2012). Guía resumida del clima en España (1981–2010). Retrieved November 21, 2018 from https://repositorio.aemet.es/handle/20.500.11765/411.
Alcázar, P., Stach, A., Nowak, M., & Galán, C. (2009). Comparison of airborne herb pollen types in Córdoba (Southwestern Spain) and Poznan (Western Poland). Aerobiologia, 25(2), 55–63. https://doi.org/10.1007/s10453-009-9109-7.
Andersson, K., & Lidholm, J. (2003). Characteristics and immunobiology of grass pollen allergens. International Archives of Allergy and Immunology, 130(2), 87–107. https://doi.org/10.1159/000069013.
Barbieri, R., Botarelli, L., Salsi, A., & Zinoni, F. (1989). Guida Alle Rilevazioni Agrofenologiche Ed Alla Compilazione Delle Schede di Rilevamento per le Colture Erbacee Ed Arboree.
Beggs, P. J. (2004). Impacts of climate change on aeroallergens: past and future. Clinical and Experimental Allergy, 34(10), 1507–1513. https://doi.org/10.1111/j.1365-2222.2004.02061.x.
Bengtsson, J., Bullock, J. M., Egoh, B., Everson, C., Everson, T., O’Connor, T., et al. (2019). Grasslands-more important for ecosystem services than you might think. Ecosphere, 10(2), e02582. https://doi.org/10.1002/ecs2.2582.
Bennie, J., Davies, T. W., Cruse, D., Bell, F., & Gaston, K. J. (2018). Artificial light at night alters grassland vegetation species composition and phenology. Journal of Applied Ecology, 55(1), 442–450. https://doi.org/10.1111/1365-2664.12927.
Bloor, J. M. G., Pichon, P., Falcimagne, R., Leadley, P., & Soussana, J. F. (2010). Effects of warming, summer drought, and CO2 enrichment on aboveground biomass production, flowering phenology, and community structure in an upland grassland ecosystem. Ecosystems. https://doi.org/10.1007/s10021-010-9363-0.
Bosch-Cano, F., Bernard, N., Sudre, B., Gillet, F., Thibaudon, M., Richard, H., et al. (2011). Human exposure to allergenic pollens: A comparison between urban and rural areas. Environmental Research, 111(5), 619–625. https://doi.org/10.1016/j.envres.2011.04.001.
Brennan, G. L., Potter, C., de Vere, N., Griffith, G. W., Skjøth, C. A., Osborne, N. J., et al. (2019). Temperate airborne grass pollen defined by spatio-temporal shifts in community composition. Nature Ecology & Evolution, 3(5), 750–754. https://doi.org/10.1038/s41559-019-0849-7.
Brighetti, M. A., Costa, C., Menesatti, P., Antonucci, F., Tripodi, S., & Travaglini, A. (2014). Multivariate statistical forecasting modeling to predict Poaceae pollen critical concentrations by meteoclimatic data. Aerobiologia, 30(1), 25–33. https://doi.org/10.1007/s10453-013-9305-3.
Cebrino, J., Galán, C., & Domínguez-Vilches, E. (2016). Aerobiological and phenological study of the main Poaceae species in Córdoba City (Spain) and the surrounding hills. Aerobiologia, 32(4), 1–12. https://doi.org/10.1007/s10453-016-9434-6.
Cebrino, J., García-Castaño, J. L., Domínguez-Vilches, E., & Galán, C. (2018). Spatio-temporal flowering patterns in Mediterranean Poaceae. A community study in SW Spain. International Journal of Biometeorology, 62(4), 513–523. https://doi.org/10.1007/s00484-017-1461-7.
Chuine, I., Cour, P., & Rousseau, D. D. (1999). Selecting models to predict the timing of flowering of temperate trees: Implications for tree phenology modelling. Plant, Cell and Environment, 22(1), 1–13. https://doi.org/10.1046/j.1365-3040.1999.00395.x.
Chuine, I., Morin, X., & Bugmann, H. (2010). Warming, photoperiods, and tree phenology. Science, 329(5989), 277–278. https://doi.org/10.1126/science.329.5989.277-e.
Clary, J., Savé, R., Biel, C., & De Herralde, F. (2004). Water relations in competitive interactions of Mediterranean grasses and shrubs. Annals of Applied Biology, 144(2), 149–155. https://doi.org/10.1111/j.1744-7348.2004.tb00328.x.
Dahl, A., Galán, C., Hajkova, L., Pauling, A., Sikoparija, B., Smith, M., & Vokou, D. (2013). The onset, course and intensity of the pollen season. In Allergenic Pollen: A review of the production, release, distribution and health impacts (Vol. 9789400748, pp. 29–70). https://doi.org/10.1007/978-94-007-4881-1_3.
D’amato, G., Cecchi, L., Bonini, S., Nunes, C., Annesi-Maesano, I., Behrendt, H., et al. (2007). Allergenic pollen and pollen allergy in Europe. Allergy: European Journal of Allergy and Clinical Immunology, 62(9), 976–990. https://doi.org/10.1111/j.1398-9995.2007.01393.x.
De Weger, L. A., Bergmann, K. C., Rantio-Lehtimäki, A., Dahl, A., Buters, J., Déchamp, C., et al. (2013). Impact of pollen. In Allergenic Pollen: A review of the production, release, distribution and health impacts (Vol. 9789400748, pp. 161–215). Dordrecht: Springer Netherlands. https://doi.org/10.1007/978-94-007-4881-1_6.
Emberlin, J., Mullins, J., Corden, J., Jones, S., Millington, W., Brooke, M., et al. (1999). Regional variations in grass pollen seasons in the UK, long-term trends and forecast models. Clinical and Experimental Allergy: Journal of the British Society for Allergy and Clinical Immunology, 29(3), 347–356.
Fernández-Martínez, M., Belmonte, J., & Maria Espelta, J. (2012). Masting in oaks: Disentangling the effect of flowering phenology, airborne pollen load and drought. Acta Oecologica, 43, 51–59. https://doi.org/10.1016/j.actao.2012.05.006.
Galán, C., Smith, M., Thibaudon, M., Frenguelli, G., Oteros, J., Gehrig, R., et al. (2014). Pollen monitoring: minimum requirements and reproducibility of analysis. Aerobiologia, 30(4), 385–395. https://doi.org/10.1007/s10453-014-9335-5.
García-Mozo, H. (2017). Poaceae pollen as the leading aeroallergen worldwide: A review. Allergy, 72(12), 1849–1858. https://doi.org/10.1111/all.13210.
García-Mozo, H., Galán, C., Alcázar, P., delaGuardia, C. D., Nieto-Lugilde, D., Recio, M., et al. (2010a). Trends in grass pollen season in southern Spain. Aerobiologia, 26(2), 157–169.
García-Mozo, H., Mestre, A., & Galán, C. (2010b). Phenological trends in southern Spain: A response to climate change. Agricultural and Forest Meteorology, 150(4), 575–580. https://doi.org/10.1016/j.agrformet.2010.01.023.
Garnier, E. (1992). Growth analysis of congeneric annual and perennial grass species. The Journal of Ecology, 80(4), 665. https://doi.org/10.2307/2260858.
Ghitarrini, S., Galán, C., Frenguelli, G., & Tedeschini, E. (2017). Phenological analysis of grasses (Poaceae) as a support for the dissection of their pollen season in Perugia (Central Italy). Aerobiologia, 33(3), 339–349. https://doi.org/10.1007/s10453-017-9473-7.
Heide, O. M. (1994). Control of flowering and reproduction in temperate grasses. New Phytologist, 128(2), 347–362. https://doi.org/10.1111/j.1469-8137.1994.tb04019.x.
Hejl, C., Wurtzen, P. A., Kleine-Tebbe, J., Johansen, N., Broge, L., & Ipsen, H. (2009). Phleum pratense alone is sufficient for allergen-specific immunotherapy against allergy to Pooideae grass pollens. Clinical and Experimental Allergy, 39(5), 752–759. https://doi.org/10.1111/j.1365-2222.2008.03195.x.
Hirst, J. M. (1952). An automatic volumetric spore trap. Annals of Applied Biology, 39(2), 257–265. https://doi.org/10.1111/j.1744-7348.1952.tb00904.x.
Jato, V., Rodríguez-Rajo, F. J., Fernandez-González, M., & Aira, M. J. (2015). Assessment of Quercus flowering trends in NW Spain. International Journal of Biometeorology, 59(5), 517–531. https://doi.org/10.1007/s00484-014-0865-x.
Kmenta, M., Bastl, K., Berger, U., Kramer, M. F., Heath, M. D., Pätsi, S., et al. (2017). The grass pollen season 2015: a proof of concept multi-approach study in three different European cities. World Allergy Organization Journal, 10(1), 31. https://doi.org/10.1186/s40413-017-0163-2.
Larsson, O., Hellkvist, L., Peterson-Westin, U., & Cardell, L. O. (2016). Novel strategies for the treatment of grass pollen-induced allergic rhinitis. Expert Opinion on Biological Therapy, 16(9), 1143–1150. https://doi.org/10.1080/14712598.2016.1190829.
León-Ruiz, E., Alcázar, P., Domínguez-Vilches, E., & Galán, C. (2011). Study of Poaceae phenology in a Mediterranean climate. Which species contribute most to airborne pollen counts? Aerobiologia, 27(1), 37–50. https://doi.org/10.1007/s10453-010-9174-y.
Llorens, L., & Peñuelas, J. (2005). Experimental evidence of future drier and warmer conditions affecting flowering of two co-occurring mediterranean shrubs. International Journal of Plant Sciences. https://doi.org/10.1086/427480.
Marcucci, F., Sensi, L., Di Cara, G., Incorvaia, C., Puccinelli, P., Scurati, S., et al. (2010). Which allergen extract for grass pollen immunotherapy? An in vitro study. Immunological Investigations, 39(6), 635–644. https://doi.org/10.3109/08820131003796876.
McMaster, G. S., & Wilhelm, W. W. (1997). Growing degree-days: One equation, two interpretations. Agricultural and Forest Meteorology, 87(4), 291–300. https://doi.org/10.1016/S0168-1923(97)00027-0.
Meier, U. (2001). Phenological growth stages—Mono- and dicotyledonous plants. Phenology: An Integrative Environmental Science, 39, 269–283. http://www.wkap.nl.
Miranda, J. D., Armas, C., Padilla, F. M., & Pugnaire, F. I. (2011). Climatic change and rainfall patterns: Effects on semi-arid plant communities of the Iberian Southeast. Journal of Arid Environments, 75(12), 1302–1309. https://doi.org/10.1016/j.jaridenv.2011.04.022.
Munson, S. M., & Long, A. L. (2017). Climate drives shifts in grass reproductive phenology across the western USA. New Phytologist, 213(4), 1945–1955. https://doi.org/10.1111/nph.14327.
Nilsson, S., & Persson, S. (1981). Tree pollen spectra in the Stockholm region (Sweden), 1973–1980. Grana, 20(3), 179–182. https://doi.org/10.1080/00173138109427661.
Nyffeler, R. (2003). Plant systematics and evolution, 239(3/4), 292–294. http://www.jstor.org/stable/23645181.
Oduber, F., Calvo, A. I., Blanco-Alegre, C., Castro, A., Vega-Maray, A. M., Valencia-Barrera, R. M., et al. (2019). Links between recent trends in airborne pollen concentration, meteorological parameters and air pollutants. Agricultural and Forest Meteorology, 264, 16–26. https://doi.org/10.1016/j.agrformet.2018.09.023.
Peñuelas, J., Filella, I., Zhang, X., Llorens, L., Ogaya, R., Lloret, F., et al. (2004). Complex spatiotemporal phenological shifts as a response to rainfall changes. New Phytologist, 161(3), 837–846. https://doi.org/10.1111/j.1469-8137.2004.01003.x.
Pereira, C., Valero, A., Loureiro, C., Dávila, I., Martinez-Cócera, C., Murio, C., et al. (2006). Iberian study of aeroallergens sensitisation in allergic rhinitis. European Annals of Allergy and Clinical Immunology, 38(6), 186–94. http://www.ncbi.nlm.nih.gov/pubmed/16929745.
Prieto-Baena, J. C., Hidalgo, P. J., Domínguez, E., & Galán, C. (2003). Pollen production in the Poaceae family. Grana, 42, 153–159. https://doi.org/10.1080/00173130310011810.
Quinn, J. A., & Wetherington, J. D. (2002). Genetic variability and phenotypic plasticity in flowering phenology in populations of two grasses. Journal of the Torrey Botanical Society, 129(2), 96. https://doi.org/10.2307/3088723.
R Core Team. (2018). A Language and environment for statistical computing. Vienna, Austria: ISBN 3-900051-07-0. http://www.r-project.org/.
Recio, M., Docampo, S., García-Sánchez, J., Trigo, M. M., Melgar, M., & Cabezudo, B. (2010). Influence of temperature, rainfall and wind trends on grass pollination in Malaga (western Mediterranean coast). Agricultural and Forest Meteorology, 150(7–8), 931–940. https://doi.org/10.1016/j.agrformet.2010.02.012.
Rivas-Martínez, S., Díaz, T. E., Fernández-González, F., Izco, J., Loidi, J., Lousa, M., et al. (2002). Vascular plant communities of Spain and Portugal. Itinera Geobotanica, 15(2), 433–922.
Rojo, J., & Pérez-Badia, R. (2014). Effects of topography and crown-exposure on olive tree phenology. Trees—Structure and Function, 28(2), 449–459. https://doi.org/10.1007/s00468-013-0962-1.
Rojo, J., Picornell, A., & Oteros, J. (2019). AeRobiology: The computational tool for biological data in the air. Methods in Ecology and Evolution, 10(8), 2041–210X.13203. https://doi.org/10.1111/2041-210x.13203.
Rojo, J., Rivero, R., Romero-Morte, J., Fernández-González, F., & Pérez-Badia, R. (2017). Modeling pollen time series using seasonal-trend decomposition procedure based on LOESS smoothing. International Journal of Biometeorology, 61(2), 335–348. https://doi.org/10.1007/s00484-016-1215-y.
Romero-Morte, J., Rojo, J., Rivero, R., Fernández-González, F., & Pérez-Badia, R. (2018). Standardised index for measuring atmospheric grass-pollen emission. Science of the Total Environment, 612, 180–191. https://doi.org/10.1016/j.scitotenv.2017.08.139.
Scaparrotta, A., Verini, M., Consilvio, N. Pietro, Cingolani, A., Rapino, D., Attanasi, M., et al. (2013). Sensitization to timothy grass pollen allergenic molecules in children. Multidisciplinary Respiratory Medicine, 8(3), 17. https://doi.org/10.1186/2049-6958-8-17.
Schauber, E. M., Kelly, D., Turchin, P., Simon, C., Lee, W. G., Allen, R. B., et al. (2002). Masting by eighteen New Zealand plant species: The role of temperature as a synchronizing cue. Ecology. https://doi.org/10.1890/0012-9658(2002)083%5b1214:mbenzp%5d2.0.co;2.
Simon, B. K., Clayton, W. D., Harman, K. T., Vorontsova, M., Brake, I., Healy, D., & Alfonso, Y. (2011). GrassWorld. Retrieved May 26, 2019 from http://grassworld.myspecies.info.
Soreng, R. J., Peterson, P. M., Romaschenko, K., Davidse, G., Teisher, J. K., Clark, L. G., et al. (2017). A worldwide phylogenetic classification of the Poaceae (Gramineae) II: An update and a comparison of two 2015 classifications. Journal of Systematics and Evolution, 55(4), 259–290. https://doi.org/10.1111/jse.12262.
Soreng, R. J., Peterson, P. M., Romaschenko, K., Davidse, G., Zuloaga, F. O., Judziewicz, E. J., et al. (2015, March). A worldwide phylogenetic classification of the Poaceae (Gramineae). Journal of Systematics and Evolution. https://doi.org/10.1111/jse.12150.
Swanton, C. J., Huang, J. Z., Shrestha, A., Tollenaar, M., Deen, W., & Rahimian, H. (2000). Effects of temperature and photoperiod on the phenological development of barnyardgrass. Agronomy Journal, 92(6), 1125–1134.
Watson, L., & Dallwitz, M. J. (1992). Grass genera of the world: Descriptions, illustrations, identification, and information retrieval; including synonyms, morphology, anatomy, physiology, phytochemistry, cytology, classification, pathogens, world and local distribution, and references. Retrieved December 1, 2018 from https://www.delta-intkey.com/grass/index.htm.
Westritschnig, K., Horak, F., Swoboda, I., Balic, N., Spitzauer, S., Kundi, M., et al. (2008). Different allergenic activity of grass pollen allergens revealed by skin testing. European Journal of Clinical Investigation, 38(4), 260–267. https://doi.org/10.1111/j.1365-2362.2008.01938.x.
Wiersema, J. H., & León, B. (2016). World economic plants: A standard reference, 2nd edn. CRC Press. Retrieved August 19, 2019 from https://www.crcpress.com/World-Economic-Plants-A-Standard-Reference-Second-Edition/Wiersema-Leon/p/book/9781439821428.
Zeb, S., Perveen, A., & Khan, M. (2018). Biochemical characterization and allergenic potential of cenchrus pennisetiformis hochst. & steud. ex steud. pollen grains. Pakistan Journal of Botany, 50(6), 2347–2350. Retrieved July 16, 2019 from https://inis.iaea.org/search/search.aspx?orig_q=RN:49076724.
Ziello, C., Böck, A., Estrella, N., Ankerst, D., & Menzel, A. (2012). First flowering of wind-pollinated species with the greatest phenological advances in Europe. Ecography, 35(11), 1017–1023. https://doi.org/10.1111/j.1600-0587.2012.07607.x.
Acknowledgements
This study was supported by the University of Castilla-La Mancha through the “Plan Propio de I + D+I.” The authors are very grateful to all the members of Castilla-La Mancha Aerobiology Network (AEROCAM) for their contribution throughout the development of the present study and also thank Castilla-La Mancha Regional Government for their support to AEROCAM.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
10453_2020_9647_MOESM1_ESM.jpg
Fig S1. Study area. Sampling sites in the province of Toledo (central Spain). The pollen trap is located in the city of Toledo (coordinates: 39° 51′ 55″ N, 4° 2′ 31″ W). (JPEG 307 kb)
10453_2020_9647_MOESM2_ESM.png
Fig S2. Species sampled per site and year. Sampling site abbreviations: 1.Bar, Bargas; 2.Bur, Burguillos; 3.Cam, Campus University; 4.Gua, Guajaraz reservoir; 5.Oli, Olías del Rey; 6.Per, Peraleda park; 7.Saf, Safont park; 8.San, St Anton park; 9.Vad, Valdelobos; 10.Val, Tagus valley. Sampled species abbreviations: AeGe Aegilops geniculata; ArAl Arrhenaterum album; AvBa Avena barbata; AvSt Avena sterilis; BrDi Bromus diandrus; BrHo Bromus hordeaceus; BrPh Brachypodium phoenicoides; BrRu Bromus rubens; BrTe Bromus tectorum; CeGi Celtica gigantea; CyEc Cynosurus echinatus; DaHi Dactylis glomerata subsp. hispanica; EcCa Echinaria capitata; ElCa Elymus pungens subsp. campestris; HoDi Hordeum distichon; HoLe Hordeum murinum subsp. leporinum; HyHi Hyparrhenia sinaica; LaAu Lamarckia aurea; LoRi Lolium rigidum; MaTe Machrochloa tenacissima; MeCi Melica ciliata; PiMi Piptatherum miliaceum; PoAn Poa annua; RoCr Rostraria cristata; StCa Stipa capensis; TrAe Triticum aestivum; TrPa Trisetaria panicea; VuBr Vulpia bromoides. (PNG 478 kb)
10453_2020_9647_MOESM3_ESM.png
Fig S3. Flowering season start and end dates for the grass species sampled for each study year (2013, 2015, 2016, 2017 and 2018). Days are expressed in Day Of the Year, DOY. Sampled species abbreviations are given in the caption of Fig S2. (PNG 1465 kb)
Rights and permissions
About this article
Cite this article
Romero-Morte, J., Rojo, J. & Pérez-Badia, R. Meteorological factors driving airborne grass pollen concentration in central Iberian Peninsula. Aerobiologia 36, 527–540 (2020). https://doi.org/10.1007/s10453-020-09647-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10453-020-09647-7