Abstract
Estimates of airborne pollen concentrations at the urban scale would be useful for epidemiologists, land managers, and allergy sufferers. Mechanistic models could be well suited for this task, but their development will require data on pollen production across cities, including estimates of pollen production by individual trees. In this study, we developed predictive models for pollen production as a function of trunk size, canopy area, and height, which are commonly recorded in tree surveys or readily extracted from remote sensing data. Pollen production was estimated by measuring the number of flowers per tree, the number of anthers per flower, and the number of pollen grains per anther. Variability at each morphological scale was assessed using bootstrapping. Pollen production was estimated for the following species: Acer negundo, Acer platanoides, Acer rubrum, Acer saccharinum, Betula papyrifera, Gleditsia triacanthos, Juglans nigra, Morus alba, Platanus × acerifolia, Populus deltoides, Quercus palustris, Quercus rubra, and Ulmus americana. Basal area predicted pollen production with a mean R2 of 0.72 (range 0.41–0.99), whereas canopy area predicted pollen production with a mean R2 of 0.76 (range 0.50–0.99). These equations are applied to two tree datasets to estimate total municipal pollen production and the spatial distribution of street tree pollen production for the focal species. We present some of the first individual-tree based estimates of pollen production at the municipal scale; the observed spatial heterogeneity in pollen production is substantial and can feasibly be included in mechanistic models of airborne pollen at fine spatial scales.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguilera, F., & Valenzuela, L. R. (2012). Microclimatic-induced fluctuations in the flower and pollen production rate of olive trees (Olea europaea L.). Grana, 51(January), 228–239. https://doi.org/10.1080/00173134.2012.659203.
Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control, 19(6), 716–723.
Blaiss, M. S., Hammerby, E., Robinson, S., Kennedy-Martin, T., & Buchs, S. (2018). The burden of allergic rhinitis and allergic rhinoconjunctivitis on adolescents: A literature review. Annals of Allergy, Asthma & Immunology, 121(1), 43–52.e3. https://doi.org/10.1016/j.anai.2018.03.028.
Bousquet, J., Khaltaev, N., Cruz, A. A., Denburg, J., Fokkens, W. J., Togias, A., et al. (2008). Allergic rhinitis and its impact on asthma (ARIA) 2008 update (in collaboration with the World Health Organization, GA2LEN and AllerGen). European Journal of Allergy and Clinical Immunology, 63(SUPPL. 86), 8–160. https://doi.org/10.1111/j.1398-9995.2007.01620.x.
Bunderson, L. D., Wells, H., & Levetin, E. (2012). Predicting and quantifying pollen production in Juniperus ashei forests. Phytologia, 94(December), 417–438.
Canty, A., & Ripley, B. D. (2019). boot: Bootstrap R (S-Plus) Functions.
Cardell, L. O., Olsson, P., Andersson, M., Welin, K. O., Svensson, J., Tennvall, G. R., et al. (2016). TOTALL: High cost of allergic rhinitis—a national Swedish population-based questionnaire study. Primary Care Respiratory Medicine, 26(15082), 1–5. https://doi.org/10.1038/npjpcrm.2015.82.
Charalampopoulos, A., Damialis, A., Tsiripidis, I., Mavrommatis, T., Halley, J. M., & Vokou, D. (2013). Pollen production and circulation patterns along an elevation gradient in Mt Olympos (Greece) National Park. Aerobiologia, 29(4), 455–472. https://doi.org/10.1007/s10453-013-9296-0.
City of Ann Arbor. (2013). i-Tree ecosystem analysis: Ann Arbor. Ann Arbor, MI: City of Ann Arbor. https://doi.org/10.15421/031606.
City of Ann Arbor. (2019). Ann Arbor street tree database. Retrieved January 10, 2019, from https://www.a2gov.org/services/data/Pages/default.aspx.
Damialis, A., Fotiou, C., Halley, J. M., & Vokou, D. (2011). Effects of environmental factors on pollen production in anemophilous woody species. Trees - Structure and Function, 25(2), 253–264. https://doi.org/10.1007/s00468-010-0502-1.
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.
Forrester, D. I., Tachauer, I. H. H., Annighoefer, P., Barbeito, I., Pretzsch, H., Ruiz-Peinado, R., et al. (2017). Generalized biomass and leaf area allometric equations for European tree species incorporating stand structure, tree age and climate. Forest Ecology and Management, 396, 160–175. https://doi.org/10.1016/j.foreco.2017.04.011.
Fortier, J., Truax, B., Gagnon, D., & Lambert, F. (2017). Allometric equations for estimating compartment biomass and stem volume in mature hybrid poplars: General or site-specific? Forests, 8(9), 1–23. https://doi.org/10.3390/f8090309.
Gerst, K. L., Rossington, N. L., & Mazer, S. J. (2017). Phenological responsiveness to climate differs among four species of Quercus in North America. Journal of Ecology. https://doi.org/10.1111/1365-2745.12774.
Gómez-Casero, M. T., Hidalgo, P. J., García-Mozo, H., Domínguez, E., & Galán, C. (2004). Pollen biology in four Mediterranean Quercus species. Grana, 43(March), 22–30. https://doi.org/10.1080/00173130410018957.
Groffman, P. M., Cavender-Bares, J., Bettez, N. D., Grove, J. M., Hall, S. J., Heffernan, J. B., et al. (2014). Ecological homogenization of urban USA. Frontiers in Ecology and the Environment, 12(1), 74–81. https://doi.org/10.1890/120374.
Henry, M., Bombelli, A., Trotta, C., Alessandrini, A., Birigazzi, L., Sola, G., et al. (2013). GlobAllomeTree: International platform for tree allometric equations to support volume, biomass and carbon assessment. IForest, 6(6), 1–5. https://doi.org/10.3832/ifor0901-006.
Hidalgo, P. J., Galán, C., & Domínguez, E. (1999). Pollen production of the genus Cupressus. Grana, 38(5), 296–300. https://doi.org/10.1080/001731300750044519.
Hijams, R. J., & van Etten, J. (2019). raster: Geographic analysis and modeling with raster data. Retrieved January 1, 2019, from https://cran.r-project.org/web/packages/raster/index.html.
Hulshof, C. M., Swenson, N. G., & Weiser, M. D. (2015). Tree height–diameter allometry across the United States. Ecology and Evolution, 5(6), 1193–1204. https://doi.org/10.1002/ece3.1328.
Ishibashi, A., & Sakai, K. (2019). Dispersal of allergenic pollen from Cryptomeria japonica and Chamaecyparis obtusa: Characteristic annual fluctuation patterns caused by intermittent phase synchronisations. Scientific Reports, 9(1), 1–9. https://doi.org/10.1038/s41598-019-47870-6.
Karlik, J. F., & Winer, A. M. (1999). Comparison of calculated and measured leaf masses of urban trees. Ecological Applications, 9(4), 1168–1176.
Katz, D. S. W., & Batterman, S. A. (2019). Allergenic pollen production across a large city for common ragweed (Ambrosia artemisiifolia). Landscape and Urban Planning, 190(March), 103615. https://doi.org/10.1016/j.landurbplan.2019.103615.
Katz, D. S. W., & Batterman, S. A. (in press). Urban-scale variation in pollen concentrations: A single station is insufficient to characterize daily exposure. Aerobiologia.
Katz, D. S. W., Dzul, A., Kendel, A., & Batterman, S. A. (2019). Effect of intra-urban temperature variation on tree flowering phenology, airborne pollen, and measurement error in epidemiological studies of allergenic pollen. Science of the Total Environment, 653, 1213–1222. https://doi.org/10.1016/j.scitotenv.2018.11.020.
Ketterings, Q. M., Coe, R., Van Noordwijk, M., Ambagau’, Y., & Palm, C. A. (2001). Reducing uncertainty in the use of allometric biomass equations for predicting above-ground tree biomass in mixed secondary forests. Forest Ecology and Management, 146(1–3), 199–209. https://doi.org/10.1016/S0378-1127(00)00460-6.
Khanduri, V. P., Kumar, K. S., & Sharma, C. M. (2015). Role of pollen production in mating success in some tropical tree species. Revista Brasileira de Botanica, 38(1), 107–112. https://doi.org/10.1007/s40415-014-0114-x.
Khosravipour, A., Skidmore, A. K., Isenburg, M., Wang, T., & Hussin, Y. A. (2014). Generating pit-free canopy height models from airborne LiDAR. Photogrammetric Engineering & Remote Sensing, 80(9), 863–872. https://doi.org/10.14358/PERS.80.9.863.
Klein, E., Lavigne, C., Foueillassar, X., Gouyon, P., & Laredo, C. (2003). Corn pollen dispersal: Quasi-mechanistic models and field experiments. Ecological Monographs, 73(1), 131–150.
La Rosa, M., Lionetti, E., Reibaldi, M., Russo, A., Longo, A., Leonardi, S., et al. (2013). Allergic conjunctivitis: A comprehensive review of the literature. Italian Journal of Pediatrics, 39, 18. https://doi.org/10.1186/1824-7288-39-18.
Linneberg, A., Henrik Nielsen, N., Frølund, L., Madsen, F., Dirksen, A., & Jørgensen, T. (2002). The link between allergic rhinitis and allergic asthma: A prospective population-based study. The Copenhagen Allergy Study. Allergy: European Journal of Allergy and Clinical Immunology, 57(11), 1048–1052. https://doi.org/10.1034/j.1398-9995.2002.23664.x.
Lovasi, G. S., O’Neil-Dunne, J. P. M., Lu, J. W. T., Sheehan, D., Perzanowski, M. S., Macfaden, S. W., et al. (2013). Urban tree canopy and asthma, wheeze, rhinitis, and allergic sensitization to tree pollen in a New York city birth cohort. Environmental Health Perspectives, 121(4), 494–500. https://doi.org/10.1289/ehp.1205513.
McHale, M. R., Burke, I. C., Lefsky, M. A., Peper, P. J., & McPherson, E. G. (2009). Urban forest biomass estimates: Is it important to use allometric relationships developed specifically for urban trees? Urban Ecosystems, 12(1), 95–113. https://doi.org/10.1007/s11252-009-0081-3.
McKinney, M. L. (2006). Urbanization as a major cause of biotic homogenization. Biological Conservation, 127(3), 247–260. https://doi.org/10.1016/j.biocon.2005.09.005.
McPherson, E. G., Van Doorn, N. S., & Peper, P. J. (2016). Urban tree database and allometric equations. https://doi.org/10.2737/RDS-2016-0005.
Meltzer, E. O. (2016). Allergic rhinitis: Burden of illness, quality of life, comorbidities, and control. Immunology and Allergy Clinics of North America, 36(2), 235–248. https://doi.org/10.1016/j.iac.2015.12.002.
Meltzer, E. O., Blaiss, M. S., Derebery, M. J., Mahr, T. A., Gordon, B. R., Sheth, K. K., et al. (2009). Burden of allergic rhinitis: Results from the pediatric allergies in America survey. Journal of Allergy and Clinical Immunology, 124(3 SUPPL. 1), 43–70. https://doi.org/10.1016/j.jaci.2009.05.013.
Molina, R. T., Rodríguez, A. M., Palaciso, I. S., & López, F. G. (1996). Pollen production in anemophilous trees. Grana, 35(1), 38–46. https://doi.org/10.1080/00173139609430499.
Nathan, R. (2007). The burden of allergic rhinitis. Allergy and Asthma Proceedings, 28(1), 3–9. https://doi.org/10.2500/aap.2007.28.2934.
National Climate Data Center. (2019). Global summary of the day. Retrieved July 8, 2019, from www.ncdc.noaa.gov/‎.
Oliveira, N., Rodríguez-Soalleiro, R., Pérez-Cruzado, C., Cañellas, I., & Sixto, H. (2017). On the genetic affinity of individual tree biomass allometry in poplar short rotation coppice. Bioenergy Research, 10(2), 525–535. https://doi.org/10.1007/s12155-017-9818-7.
Owusu, S. A., Schlarbaum, S. E., Carlson, J. E., & Gailing, O. (2016). Pollen gene flow and molecular identification of full-sib families in small and isolated population fragments of Gleditsia triacanthos L. Botany, 94(7), 523–532. https://doi.org/10.1139/cjb-2015-0244.
Pebesma, E. (2018). Simple features for R: Standardized support for spatial vector data. The R Journal, 10(1), 439–446. https://doi.org/10.32614/RJ-2018-009.
R Core Team. (2018). R: A language and environment for statistical computing. Vienna: R Core Team. https://doi.org/10.1145/192593.192639.
Ranta, H., Hokkanen, T., Linkosalo, T., Laukkanen, L., Bondestam, K., & Oksanen, A. (2008). Male flowering of birch: Spatial synchronization, year-to-year variation and relation of catkin numbers and airborne pollen counts. Forest Ecology and Management, 255(3–4), 643–650. https://doi.org/10.1016/j.foreco.2007.09.040.
Reddi, C. S., & Reddi, N. S. (1986). Pollen production in some anemophilous angiosperms. Grana, 25(April 2015), 55–61. https://doi.org/10.1080/00173138609429933.
Rojo, J., Salido, P., & Perez-Badia, R. (2015). Flower and pollen production in the Cornicabra olive (Olea europaea L.) cultivar and the influence of environmental factors. Trees - Structure and Function, 29(4), 1235–1245. https://doi.org/10.1007/s00468-015-1203-6.
Roussel, J., & Auty, D. (2017). lidR: Airborne LiDAR data manipulation and visualization for forestry applications. Retrieved January 1, 2019, from https://github.com/Jean-Romain/lidR.
Salo, P., Calatroni, A., Gergen, P., Hoppin, J., Sever, M., Jaramillo, R., et al. (2011). Allergy-related outcomes in relation to serum IgE: Results from the National Health and Nutrition Examination Survey 2005–2006. Journal of Allergy and Clinical Immunology, 127(5), 1226–1235. https://doi.org/10.1016/j.jaci.2010.12.1106.Allergy-related.
Schnabel, A., & Hamrick, J. L. (1995). Understanding the population genetic structure of Gleditsia triacanthos L.: The scale and pattern of pollen gene flow. Evolution, 49(5), 921–931.
Sofiev, M., & Bergmann, K.-C. (Eds.). (2012). Allergenic pollen: A review of the production, release, distribution and health impacts. New York, NY: Springer.
Taylor, S., & White, E. P. (2019). Automated data-intensive forecasting of plant phenology throughout the United States. Ecological Applications. https://doi.org/10.1002/eap.2025.
Ter-Mikaelian, M. T., & Korzukhin, M. D. (1997). Biomass equations for sixty-five North American tree species. Forest Ecology and Management, 97(1), 1–24. https://doi.org/10.1016/S0378-1127(97)00019-4.
Thomas, S. C. (1996). Reproductive allometry in Malaysian rain forest trees: Biomechanics versus optimal allocation. Evolutionary Ecology, 10(5), 517–530. https://doi.org/10.1007/BF01237882.
Tseng, Y.-T., Kawashima, S., Kobayashi, S., Takeuchi, S., & Nakamura, K. (2020). Forecasting the seasonal pollen index by using a hidden Markov model combining meteorological and biological factors. Science of the Total Environment, 698, 134246. https://doi.org/10.1016/j.scitotenv.2019.134246.
Wang, K., Wang, T., & Liu, X. (2019). A review: Individual tree species classification using integrated airborne LiDAR and optical imagery with a focus on the urban environment. Forests, 10(1), 1–18. https://doi.org/10.3390/f10010001.
Weiner, J., Campbell, L. G., Pino, J., & Echarte, L. (2009). The allometry of reproduction within plant populations. Journal of Ecology, 97(6), 1220–1233. https://doi.org/10.1111/j.1365-2745.2009.01559.x.
Wickham, H. (2009). ggplot2: Elegant graphics for data analysis. New York, NY: Springer.
Xiao, L., Yang, Q., He, H., Zhao, J., Ye, C., Wu, Y., et al. (2016). An improved method for pollen release from anther: A case study with mangroves. Grana, 55(4), 302–310. https://doi.org/10.1080/00173134.2015.1120775.
Yasaka, M., Kobayashi, S., Takeuchi, S., Tokuda, S., Takiya, M., & Ohno, Y. (2009). Prediction of birch airborne pollen counts by examining male catkin numbers in Hokkaido, northern Japan. Aerobiologia, 25(2), 111–117. https://doi.org/10.1007/s10453-009-9116-8.
Ye, R., Huang, H., Alexander, J., Liu, W., Millwood, R. J., Wang, J., et al. (2016). Field studies on dynamic pollen production, deposition, and dispersion of glyphosate-resistant horseweed (Conyza canadensis). Weed Science, 64(1), 101–111. https://doi.org/10.1614/WS-D-15-00073.1.
Yoon, T. K., Park, C. W., Lee, S. J., Ko, S., Kim, K. N., Son, Y., et al. (2013). Allometric equations for estimating the aboveground volume of five common urban street tree species in Daegu, Korea. Urban Forestry and Urban Greening, 12(3), 344–349. https://doi.org/10.1016/j.ufug.2013.03.006.
Zandbergen, P. A. (2009). Accuracy of iPhone locations: A comparison of assisted GPS, WiFi and cellular positioning. Transactions in GIS, 13(SUPPL. 1), 5–25. https://doi.org/10.1111/j.1467-9671.2009.01152.x.
Zhen, Z., Quackenbush, L. J., & Zhang, L. (2016). Trends in automatic individual tree crown detection and delineation-evolution of LiDAR data. Remote Sensing, 8(4), 1–26. https://doi.org/10.3390/rs8040333.
Zianis, D., Muukkonen, P., Mäkipää, R., & Mencuccini, M. (2005). Biomass and stem volume equations for tree species in Europe. Silva Fennica Monographs, 4, 1–63.
Acknowledgements
This work was supported by the National Institute of Environmental Health through a NRSA postdoctoral fellowship (Grant Number F32 ES026477). It was also supported by the Michigan Institute for Clinical Health Research through the Postdoctoral Translational Scholars Program (Grant Number UL1 TR002240). S. Batterman also acknowledges support from grant P30ES017885 from the National Institute of Environmental Health Sciences, National Institutes of Health. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. We thank the Ann Arbor Department of Public Works for providing i-Tree Eco data. We also thank Victoria Bankowski and John Kost for their contributions to this project.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
No potential conflict of interest was reported by the authors.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Katz, D.S.W., Morris, J.R. & Batterman, S.A. Pollen production for 13 urban North American tree species: allometric equations for tree trunk diameter and crown area. Aerobiologia 36, 401–415 (2020). https://doi.org/10.1007/s10453-020-09638-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10453-020-09638-8