Biomass response of Schinus terebinthifolia to elevated ozone: evidence for a dose-dependent hormetic effect

Matheus Casarini Siqueira , Barbara Baesso Moura , Yasutomo Hoshika , Elena Paoletti , Armando Reis Tavares , Marisa Domingos

Journal of Forestry Research ›› 2026, Vol. 37 ›› Issue (1) : 90

PDF
Journal of Forestry Research ›› 2026, Vol. 37 ›› Issue (1) :90 DOI: 10.1007/s11676-026-02033-y
Original Paper
research-article
Biomass response of Schinus terebinthifolia to elevated ozone: evidence for a dose-dependent hormetic effect
Author information +
History +
PDF

Abstract

Schinus terebinthifolia (Raddi) is a tropical fast-growing broadleaf tree species in Brazil’s Atlantic Forest, a threatened biodiversity hotspot. The species has socioeconomic importance, is used in forest restoration programs and urban greening. In urban environments, plants are exposed to several abiotic stressors such as atmospheric pollution. Tropospheric ozone (O3) is one of the main secondary pollutants that affect plant growth and survival. Therefore, determining the critical levels (CL) of phytotoxic O3 is essential. Ozone risk assessment for S. terebinthifolia is unknown. Forty-five S. terebinthifolia seedlings were cultivated in pots and submitted to five ozone treatments for three months in an O3-free-air controlled facility. Ozone risk assessment was based on environmental data, measurements of stomatal O3 uptake and seedling biomass. To find the best model for predicting O3-induced biomass loss, we tested the accumulated ozone exposure over a threshold of 40 ppb (AOT40) and the phytotoxic ozone dose above a threshold ‘y’ (PODy) using linear and 116 nonlinear statistical models. POD16 and POD15 when applied with the four-parameter nonlinear logarithmic model “Bragg4” provided the best fit for assessing O3 risk based on total biomass and leaf biomass, respectively. The species had a 4% biomass loss at 2.56 mmol O3 m−2 POD16 and in leaf biomass at 3.37 mmol O3 m−2 POD15. The results indicate that biomass accumulation was stimulated at low to moderate O3 levels but reduced at higher levels. Overall, S. terebinthifolia demonstrated a high tolerance to tropospheric O3.

Graphical abstract

Keywords

Tropical environments / Ozone-stress / Tolerance / Hormetic biomass response / Schinus terebinthifolia

Cite this article

Download citation ▾
Matheus Casarini Siqueira, Barbara Baesso Moura, Yasutomo Hoshika, Elena Paoletti, Armando Reis Tavares, Marisa Domingos. Biomass response of Schinus terebinthifolia to elevated ozone: evidence for a dose-dependent hormetic effect. Journal of Forestry Research, 2026, 37(1): 90 DOI:10.1007/s11676-026-02033-y

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Agathokleous E, Araminiene V, Belz RG, Calatayud V, De Marco A, Domingos M, Feng ZZ, Hoshika Y, Kitao M, Koike T, Paoletti E, Saitanis CJ, Sicard P, Calabrese EJ. A quantitative assessment of hormetic responses of plants to ozone. Environ Res. 2019, 176. 108527

[2]

Agathokleous E, Belz RG, Calatayud V, De Marco A, Hoshika Y, Kitao M, Saitanis CJ, Sicard P, Paoletti E, Calabrese EJ. Predicting the effect of ozone on vegetation via linear non-threshold (LNT), threshold and hormetic dose-response models. Sci Total Environ. 2019, 649: 61-74.

[3]

Baier M, Kandlbinder A, Golldack D, Dietz KJ. Oxidative stress and ozone: perception, signalling and response. Plant Cell Environ. 2005, 28(8): 1012-1020.

[4]

Bičárová S, Sitková Z, Pavlendová H, Fleischer P, Fleischer P, Bytnerowicz A. The role of environmental factors in ozone uptake of Pinus mugo Turra. Atmos Pollut Res. 2019, 10(1): 283-293.

[5]

Bona C, da Silva MYB, de Rezende IM, de Oliveira Santos G, de Souza LA, Inckot RC. Efeito do solo contaminado com óleo diesel na estrutura da raiz e da folha de plântulas de Sebastiania commersoniana (Euphorbiaceae) e Schinus terebinthifolius (Anacardiaceae). Acta Bot Bras. 2011, 25(2): 277-285.

[6]

Calabrese EJ, Blain RB. Hormesis and plant biology. Environ Pollut. 2009, 157(1): 42-48.

[7]

Cassimiro JC, Moura BB, Alonso R, Meirelles ST, Moraes RM. Ozone stomatal flux and O3 concentration-based metrics for Astronium graveolens Jacq., a Brazilian native forest tree species. Environ Pollut. 2016, 213: 1007-1015.

[8]

CETESB (2024) Qualidade do ar no estado de São Paulo. CETESB, São Paulo. 140 p. (Série Relatórios). Available at: https://cetesb.sp.gov.br/ar/wp-content/uploads/sites/28/2025/06/Relatorio-de-Metodologia-para-Avaliacao-da-Qualidade-do-Ar.pdf

[9]

CLRTAP (2015) Mapping critical levels for vegetation. chapter III of manual on methodologies and criteria for modelling and mapping critical loads and levels and air pollution effects. risks and trends. UNECE convention on long-range transboundary air pollution; accessed on 11 Jul 2025 on Web at: www.icpmapping.org

[10]

Conte A, Otu-Larbi F, Alivernini A, Hoshika Y, Paoletti E, Ashworth K, Fares S. Exploring new strategies for ozone-risk assessment: a dynamic-threshold case study. Environ Pollut. 2021, 287. 117620

[11]

da Silva PN, dos Reis CHG, Duarte VP, de Castro EM, de Pádua MP, Pereira FJ. Toxicity of iron mining tailings and potential for revegetation using Schinus terebinthifolia raddi based on the emergence, growth, and anatomy of the species. Mining. 2024, 4(3): 719-732.

[12]

da Silva Engela MRG, Furlan CM, Esposito MP, Fernandes FF, Carrari E, Domingos M, Paoletti E, Hoshika Y. Metabolic and physiological alterations indicate that the tropical broadleaf tree Eugenia uniflora L. is sensitive to ozone. Sci Total Environ. 2021, 769. 145080

[13]

de Souza Oliveira V, Covre AM, Gouvea DS, Canal L, dos Santos KTH, Santos JSH, Santos GP, Pinheiro APB, Schmildt O, Posse RP, Czepak MP, Arantes SD, Alexandre RS, do Amaral JAT, da Vitória EL, Schmildt ER. Determination of the leaflet area of Schinus terebinthifolius Raddi in function of linear dimensions. J Agric Sci. 2019, 11(14. 198

[14]

Dewan S, Lakhani A. Tropospheric ozone and its natural precursors impacted by climatic changes in emission and dynamics. Front Environ Sci. 2022, 10. 1007942

[15]

Elshorbany Y, Ziemke JR, Strode S, Petetin H, Miyazaki K, De Smedt I, Pickering K, Seguel RJ, Worden H, Emmerichs T, Taraborrelli D, Cazorla M, Fadnavis S, Buchholz RR, Gaubert B, Rojas NY, Nogueira T, Salameh T, Huang M. Tropospheric ozone precursors: global and regional distributions, trends, and variability. Atmos Chem Phys. 2024, 2421): 12225-12257.

[16]

Erofeeva EA. Environmental hormesis of non-specific and specific adaptive mechanisms in plants. Sci Total Environ. 2022, 804. 150059

[17]

Fernandes FF, Esposito MP, da Silva Engela MRG, Cardoso-Gustavson P, Furlan CM, Hoshika Y, Carrari E, Magni G, Domingos M, Paoletti E. The passion fruit liana (Passiflora edulis Sims, Passifloraceae) is tolerant to ozone. Sci Total Environ. 2019, 656: 1091-1101.

[18]

Hayes F, Wagg S, Mills G, Wilkinson S, Davies W. Ozone effects in a drier climate: implications for stomatal fluxes of reduced stomatal sensitivity to soil drying in a typical grassland species. Glob Change Biol. 2012, 18(3): 948-959.

[19]

Hobbie SE, Grimm NB. Nature-based approaches to managing climate change impacts in cities. Philos Trans R Soc Lond B Biol Sci. 2020, 375(1794. 20190124

[20]

Hoshika Y, Watanabe M, Inada N, Koike T. Modeling of stomatal conductance for estimating ozone uptake of Fagus crenata under experimentally enhanced free-air ozone exposure. Water Air Soil Pollut. 2012, 2237): 3893-3901.

[21]

Hoshika Y, Watanabe M, Kitao M, Häberle KH, Grams TEE, Koike T, Matyssek R. Ozone induces stomatal narrowing in European and Siebold’s beeches: a comparison between two experiments of free-air ozone exposure. Environ Pollut. 2015, 196: 527-533.

[22]

Hoshika Y, Moura B, Paoletti E. Ozone risk assessment in three oak species as affected by soil water availability. Environ Sci Pollut Res. 2018, 25(9): 8125-8136.

[23]

Hoshika Y, Carrari E, Mariotti B, Martini S, De Marco A, Sicard P, Paoletti E. Flux-based ozone risk assessment for a plant injury index (PII) in three European cool-temperate deciduous tree species. Forests. 2020, 11(1. 82

[24]

Hoshika Y, Agathokleous E, Moura BB, Paoletti E. Ozone risk assessment with free-air controlled exposure (FACE) experiments: a critical revisit. Environ Res. 2024, 255. 119215

[25]

Jarvis PG. The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philos Trans R Soc Lond B Biol Sci. 1976, 273927): 593-610.

[26]

Kaylor SD, Snell Taylor SJ, Herrick JD. Estimates of biomass reductions of ozone sensitive herbaceous plants in California. Sci Total Environ. 2023, 878. 163134

[27]

Lamb WF, Wiedmann T, Pongratz J, Andrew R, Crippa M, Olivier JGJ, Wiedenhofer D, Mattioli G, Al Khourdajie A, House J, Pachauri S, Figueroa M, Saheb Y, Slade R, Hubacek K, Sun LX, Ribeiro SK, Khennas R, de la Rue du Can S, Chapungu L, Davis SJ, Bashmakov I, Dai HC, Dhakal S, Tan XC, Geng Y, Gu BH, Minx J. A review of trends and drivers of greenhouse gas emissions by sector from 1990–2018. Environ Res Lett. 2021, 16(7. 073005

[28]

Li ZZ, Yang J, Shang B, Agathokleous E, Rubert-Nason KF, Xu YS, Feng ZZ. Nonlinear responses of foliar phenylpropanoids to increasing O3 exposure: ecological implications in a Populus model system. Sci Total Environ. 2021, 767. 144358

[29]

Lorenzi H. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. 20167 edNova Odessa, Plantarum

[30]

Manzini J, Hoshika Y, Danti R, Moura BB, Paoletti E, Della Rocca G. Ozone risk assessment of common cypress (Cupressus sempervirens L.) clones and effects of Seiridium cardinale infection. J Environ Sci. 2025, 151: 441-453.

[31]

Marques MCM, Grelle CEV. The Atlantic forest: history, biodiversity, threats and opportunities of the mega-diverse forest. 2021, Cham, Springer International Publishing.

[32]

Marzuoli R, Faoro F, Picchi V, Gerosa GA. Phytotoxic ozone dose–response relationships for durum wheat (Triticum durum, Desf.). Plants. 2024, 135. 573

[33]

Mattson MP. Hormesis defined. Ageing Res Rev. 2008, 71): 1-7.

[34]

Miller RW, Hauer RJ, Werner LP (2015) Urban forestry: planning and managing urban greenspaces. Waveland press.

[35]

Mills G, Pleijel H, Braun S, Büker P, Bermejo V, Calvo E, Danielsson H, Emberson L, Fernández IG, Grünhage L, Harmens H, Hayes F, Karlsson PE, Simpson D. New stomatal flux-based critical levels for ozone effects on vegetation. Atmos Environ. 2011, 45(28): 5064-5068.

[36]

Mills G, Pleijel H, Malley CS, Sinha B, Cooper OR, Schultz MG, Neufeld HS, Simpson D, Sharps K, Feng ZZ, Gerosa G, Harmens H, Kobayashi K, Saxena P, Paoletti E, Sinha V, Xu XB. Tropospheric Ozone Assessment Report: present-day tropospheric ozone distribution and trends relevant to vegetation. Elementa Sci Anthropocene. 2018, 6. 47

[37]

Mills G, Buker P, Hayes F, Emberson L, Werner W, Gimeno B, Pihl Karlsson G (2003) Developing ozone flux-effect models for white clover from the ICP Vegetation ambient air monitoring experiment. Swed Water Air Pollut Res Lab Publ IVL B: 128–139.

[38]

Moura BB, Alves ES, de Souza SR, Domingos M, Vollenweider P. Ozone phytotoxic potential with regard to fragments of the Atlantic semi-deciduous forest downwind of Sao Paulo, Brazil. Environ Pollut. 2014, 192: 65-73.

[39]

Moura BB, Hoshika Y, Ribeiro RV, Paoletti E. Exposure- and flux-based assessment of ozone risk to sugarcane plants. Atmos Environ. 2018, 176: 252-260.

[40]

Nguyen DH, Lin C, Vu CT, Cheruiyot NK, Nguyen MK, Le TH, Lukkhasorn W, Vo TDH, Bui XT. Tropospheric ozone and NOx: a review of worldwide variation and meteorological influences. Environ Technol Innov. 2022, 28. 102809

[41]

Niu JF, Zhao P, Sun ZW, Zhu LW, Ni GY, Zeng XP, Zhang ZZ, Zhao XH, Zhao PQ, Gao JG, Hu YT, Zeng XM, Ouyang L. Stomatal uptake of O3 in a Schima superba plantation in subtropical China derived from sap flow measurements. Sci Total Environ. 2016, 545: 465-475.

[42]

Oliveira KC, Franciscato LMSS, Mendes SS, Barizon FMA, Gonçalves DD, Barbosa LN, Faria MGI, Valle JS, Casalvara RFA, Gonçalves JE, Gazim ZC, Ruiz SP. Essential oil from the leaves, fruits and twigs of Schinus terebinthifolius: chemical composition, antioxidant and antibacterial potential. Molecules. 2024, 29(2. 469

[43]

Olmedo GM, Raguse-Quadros M, Conrado GT, Oliveira JM. Climatic signals on phenological patterns among tree species in a subtropical forest community. Neotrop Biol Conserv. 2023, 183): 191-208.

[44]

Onofri A (2020) The broken bridge between biologists and statisticians: a blog and R package, Statforbiology, IT. https://www.statforbiology.com

[45]

Onofri A (2024) statforbiology: Tools for Data Analyses in Biology. R package version 0.9.9. https://CRAN.R-project.org/package=statforbiology

[46]

Paoletti E, Materassi A, Fasano G, Hoshika Y, Carriero G, Silaghi D, Badea O. A new-generation 3D ozone FACE (free air controlled exposure). Sci Total Environ. 2017, 575: 1407-1414.

[47]

Pleijel H, Danielsson H, Broberg MC. Benefits of the Phytotoxic Ozone Dose (POD) index in dose-response functions for wheat yield loss. Atmos Environ. 2022, 268. 118797

[48]

Ritz C, Baty F, Streibig JC, Gerhard D. Dose-response analysis using R. PLoS ONE. 2015, 10(12. e0146021

[49]

Ruiz E (2023) Automation of statistical testing & non-linear modelling in R package version 0.1.0. https://github.com/leliotruiz/automation

[50]

Santos RS, Alencar JBR, Gallo R. Modeling the current and projected distribution of Brazilian peppertree Schinus terebinthifolia Raddi (Anacardiaceae) in the Americas. Braz J Biol. 2024, 84. e279769

[51]

Seguel RJ, Castillo L, Opazo C, Rojas NY, Nogueira T, Cazorla M, Gavidia-Calderón M, Gallardo L, Garreaud R, Carrasco-Escaff T, Elshorbany Y. Changes in South American surface ozone trends: exploring the influences of precursors and extreme events. Atmos Chem Phys. 2024, 2414): 8225-8242.

[52]

Shang B, Yuan XY, Li P, Xu YS, Feng ZZ. Effects of elevated ozone and water deficit on poplar saplings: changes in carbon and nitrogen stocks and their allocation to different organs. For Ecol Manag. 2019, 441: 89-98.

[53]

Siqueira MC, Kanashiro S, Domingos M, Rinaldi MCS, Tavares AR. Physiological and biochemical changes in tree seedlings growing in urban forest soil contaminated with copper in São Paulo, Brazil. Plant Soil. 2021, 464(1–2): 149-163.

[54]

Tarasick D, Galbally IE, Cooper OR, Schultz MG, Ancellet G, Leblanc T, Wallington TJ, Ziemke J, Liu X, Steinbacher M, Staehelin J, Vigouroux C, Hannigan JW, García O, Foret G, Zanis P, Weatherhead E, Petropavlovskikh I, Worden H, Osman M, Liu J, Chang KL, Gaudel A, Lin MY, Granados-Muñoz M, Thompson AM, Oltmans SJ, Cuesta J, Dufour G, Thouret V, Hassler B, Trickl T, Neu JL. Tropospheric Ozone Assessment Report: tropospheric ozone from 1877–2016, observed levels, trends and uncertainties. Elementa Sci Anthropocene. 2019, 7. 39

[55]

Tredennick AT, Hooker G, Ellner SP, Adler PB. A practical guide to selecting models for exploration, inference, and prediction in ecology. Ecology. 2021, 1026. e03336

[56]

Uliana MP, Fronza M, da Silva AG, Vargas TS, de Andrade TU, Scherer R. Composition and biological activity of Brazilian rose pepper (Schinus terebinthifolius Raddi) leaves. Ind Crops Prod. 2016, 83: 235-240.

[57]

Wickham H. ggplot2: elegant graphics for data analysis. 2016, New York, Springer-Verlag.

[58]

Wickham H (2023) modelr: Modelling Functions that Work with the Pipe. R package version 0.1.11. https://CRAN.R-project.org/package=modelr

[59]

Xu JX, Zhao H, Wang S, Zheng YF, Mai BR, Zhang X. Assessment of photosynthesis and yield loss of winter wheat under ground-level ozone exposure. Environ Technol Innov. 2023, 29. 103013

Funding

Instituto De Pesquisas Ambientais

RIGHTS & PERMISSIONS

The Author(s)

PDF

0

Accesses

0

Citation

Detail

Sections
Recommended

/