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DO3SE model applicability and O3 flux performance compared to AOT40 for an O3-sensitive tropical tree species (Psidium guajava L. ‘Paluma’)


Phytotoxic ozone (O3) levels have been recorded in the Metropolitan Region of São Paulo (MRSP). Flux-based critical levels for O3 through stomata have been adopted for some northern hemisphere species, showing better accuracy than with accumulated ozone exposure above a threshold of 40 ppb (AOT40). In Brazil, critical levels for vegetation protection against O3 adverse effects do not exist. The study aimed to investigate the applicability of O3 deposition model (Deposition of Ozone for Stomatal Exchange (DO3SE)) to an O3-sensitive tropical tree species (Psidium guajava L. ‘Paluma’) under the MRSP environmental conditions, which are very unstable, and to assess the performance of O3 flux and AOT40 in relation to O3-induced leaf injuries. Stomatal conductance (g s) parameterization for ‘Paluma’ was carried out and used to calculate different rate thresholds (from 0 to 5 nmol O3 m−2 projected leaf area (PLA) s−1) for the phytotoxic ozone dose (POD). The model performance was assessed through the relationship between the measured and modeled g sto. Leaf injuries were analyzed and associated with POD and AOT40. The model performance was satisfactory and significant (R 2 = 0.56; P < 0.0001; root-mean-square error (RMSE) = 116). As already expected, high AOT40 values did not result in high POD values. Although high POD values do not always account for more injuries, POD0 showed better performance than did AOT40 and other different rate thresholds for POD. Further investigation is necessary to improve our model and also to check if there is a critical level of ozone in which leaf injuries arise. The conclusion is that the DO3SE model for ‘Paluma’ is applicable in the MRSP as well as in temperate regions and may contribute to future directives.

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  1. Alonso R, Elvira S, Sanz MJ, Gerosa G, Emberson LD, Bermejo V, Gimeno BS (2008) Sensitivity analysis of a parameterization of the stomatal component of the DO3SE model for Quercus ilex to estimate ozone fluxes. Environ Pollut 155:473–480

  2. Ashmore MR (2005) Assessing the future global impacts of ozone on vegetation. Plant Cell Environ 28:949–964

  3. Azuchi F, Kinose Y, Matsumura T, Kanomata T, Uehara Y, Kobayashi A, Yamaguchi M, Izuta T (2014) Modeling stomatal conductance and ozone uptake of Fagus crenata grown under different nitrogen loads. Environ Pollut 184:481–487

  4. Baumgarten M, Huber C, Büker P, Emberson L, Dietrich H-P, Nunn AJ, Heerdt C, Beudert B, Matyssek R (2009) Are Bavarian Forests (southern Germany) at risk from ground-level ozone? Assessment using exposure and flux based ozone indices. Environ Pollut 157:2091–2107

  5. Calatayud V, Cerveró J, Calvo E, García-Breijo FJ, Reig-Armiñana J, Sanz MJ (2011) Responses of evergreen and deciduous Quercus species to enhanced ozone levels. Environ Pollut 159:55–63

  6. CETESB (2012) Companhia Ambiental do Estado de São Paulo. Air quality report at São Paulo State. Report series. Available at: Accessed 23 June 2013 (in Portuguese)

  7. Danielsson H, Karlsson GP, Karlsson P-E (2003) Ozone uptake modelling and flux-response relationships—an assessment of ozone-induced yield loss in spring wheat. Atmos Environ 37:475–485

  8. Dias APS, Dafré M, Rinaldi MCS, Domingos M (2011) How the redox state of tobacco ‘Bel-W3’ is modified in response to ozone and other environmental factors in a sub-tropical area? Environ Pollut 159:458–465

  9. Dizengremel P, Thiec DL, Bagard M, Jolivet Y (2008) Ozone risk assessment for plants: central role of metabolism-dependent changes in reducing power. Environ Pollut 156:11–15

  10. El-Khatib AA (2003) The response of some common Egyptian plants to ozone and their use as biomonitors. Environ Pollut 124:419–428

  11. Emberson LD, Ashmore MR, Cambridge HM, Simpson D, Tuovinen JP (2000) Modelling stomatal ozone flux across Europe. Environ Pollut 109:403–413

  12. Emberson LD, Buker P, Ashmore MR (2007) Assessing the risk caused by ground level ozone to European forest trees: a case study in pine, beech and oak across different climate regions. Environ Pollut 147:454–466

  13. Emberson LD, Bueker P, Ashmore MR, Mills G, Jackson LS, Agrawal M, Atikuzzaman MD, Cinderby S, Engardt M, Jamir C, Kobayashi K, Oanh NTK, Quadir QF, Wahid A (2009) A comparison of North American and Asia exposure-response data for ozone effects on crop yields. Atmos Environ 43:1945–1953

  14. Fares S, Park JH, Ormeno E, Gentner DR, McKay M, Loreto F, Karlik J, Goldstein AH (2010) Ozone uptake by citrus trees exposed to a range of ozone concentrations. Atmos Environ 44:3404–3412

  15. Fares S, Weber R, Park JH, Gentner D, Karlik J, Goldstein AH (2012) Ozone deposition to an orange orchard: partitioning between stomatal and non-stomatal sinks. Environ Pollut 169:258–266

  16. Fowler D, Flechard C, Cape JN, Storeton-West RL, Coyle M (2001) Measurements of ozone deposition to vegetation quantifying the flux, the stomatal and non-stomatal components. Water Air Soil Pollut 130:65–74

  17. Fuhrer J, Skärby L, Ashmore MR (1997) Critical levels for ozone effects on vegetation in Europe. Environ Pollut 97:91–106

  18. Furlan CM, Moraes RM, Bulbovas P, Domingos M, Salatino A, Sanz MJ (2007) Psidium guajava ‘Paluma’ as a new bio-indicator of ozone in the tropics. Environ Pollut 147:691–695

  19. Gerosa G, Marzuoli R, Desotgiu R, Bussotti F, Ballarin-Denti A (2008) Visible leaf injury in young trees of Fagus sylvatica and Quercus robur in relation to ozone uptake and ozone exposure. An open top chambers experiment in south alpine environmental conditions. Environ Pollut 152:274–284

  20. Gerosa B, Marzuoli R, Desotgiu R, Bussotti F, Ballarin-Denti A (2009) Validation of the stomatal flux approach for the assessment of ozone visible injury in young forest trees. Results from the TOP (transboundary ozone pollution) experiment at Curno, Italy. Environ Pollut 157:1497–1505

  21. González-Fernández I, Bermejo V, Elvira S, Sanz J, Gimeno B, Alonso R (2010) Modelling annual pasture dynamics: applications to stomatal ozone deposition. Atmos Environ 44:2507–2517

  22. González-Fernández I, Bermejo V, Elvira S, de la Torre D, González A, Navarrete L, Sanz J, Calvete H, García-Gómez H, López A, Serra J, Lafarga A, Armesto AP, Calvo A, Alonso R (2013) Modelling ozone stomatal flux of wheat under Mediterranean conditions. Atmos Environ 67:149–160

  23. González-Fernández I, Calvo E, Gerosa G, Bermejo V, Marzuoli R, Calatayud V, Alonso R (2014) Setting ozone critical levels for protecting horticultural Mediterranean crops: case study of tomato. Environ Pollut 185:178–187

  24. Heath RL, Lefohn AS, Musselman RC (2009) Temporal processes that contribute to nonlinearity in vegetation responses to ozone exposure and dose. Atmos Environ 43:2919–2928

  25. Jarvis PG (1976) The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philos Trans R Soc Lond B 273:593–610

  26. Karlsson P-E, Uddling J, Braun S, Broadmeadow M, Evira S, Gimeno BS, Le Thiec D, Oksanen E, Vandermeiren K, Wilkinson M, Emberson L (2004) New critical levels for ozone effects on young trees based on AOT40 and simulated cumulative leaf uptake of ozone. Atmos Environ 38:2283–2294

  27. Karlsson P-E, Braun S, Broadmeadow M, Elvira S, Emberson L, Gimeno BS, Le Thiec D, Novak K, Oksanen E, Schaub M, Uddling J, Wilkinson M (2007) Risk assessments for forest trees: the performance of the ozone flux versus the AOT concepts. Environ Pollut 146:608–616

  28. LRTAP Convention (2011) Mapping Manual 2004. Manual on methodologies and criteria for modeling and mapping critical loads & levels and air pollution effects, risks and trends. Chapter 3. Mapping critical levels for vegetation, 2011 revision Available at Accessed 11 November 2011

  29. Manes F, Vitale M, Fabi AM, De Santis F, Zona D (2007) Estimates of potential ozone stomatal uptake in mature trees of Quercus ilex in a Mediterranean climate. Environ Exp Bot 59:235–241

  30. Massman WJ (1998) A review of the molecular diffusivities of H2O, CO2, CH4, CO, O3, SO2, NH3, N2O, NO, and NO2 in air, O2 and N2 near STP—polar and polyatomic gases. Atmos Environ 32:1111–1127

  31. Matyssek R, Bytnerowicz A, Karlsson P-E, Paoletti E, Sanz M, Schaub M, Wieser G (2007) Promoting the O3 flux concept for European forest trees. Environ Pollut 146:587–607

  32. Medina JC, Castro JV, Sigrist JMM, Martin ZN, Kato K, Maia ML, Garcia AEB, Leite RSSF (1988) Guava: cultivation, raw material, processing and economic aspects. (2 Eds.), Instituto de Tecnologia de Alimentos (ITAL), Campinas, Brazil (In Portuguese)

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

  34. Musselman RC, Lefohn AS, Massman WJ, Heath RL (2006) A critical review and analysis of the use of exposure and flux-based ozone indices for predicting vegetation effects. Atmos Environ 40:1869–1888

  35. Paoletti E, Ranieri A, Lauteri M (2008) Moving toward effective ozone flux assessment. Environ Pollut 156:16–19

  36. Pina J (2010) Gas Exchange, visible foliar symptoms and antioxidative enzyme activity in young plants of Psidium guajava ‘Paluma’ exposed to ozone at the Parque Estadual das Fontes do Ipiranga, São Paulo, SP. PhD thesis. Instituto de Botânica, Brazil (in Portuguese)

  37. Pina JM, Moraes RM (2007) Ozone-induced foliar injury in saplings of Psidium guajava ‘Paluma’ in São Paulo, Brazil. Chemosphere 66:1310–1314

  38. Rezende FM, Furlan CM (2009) Anthocyanins and tannins in ozone-fumigated guava trees. Chemosphere 76:1445–1450

  39. Schmidt U, Thoni H, Kaupenjohann M (2000) Using a boundary line approach to analyze N2O flux data from agricultural soils. Nutr Cycl Agroecosyst 57:119–129

  40. Silva DT, Meirelles ST, Moraes RM (2012) Relationship between ozone, meteorological conditions, gas exchange and leaf injury in Nicotiana tabacum Bel-W3 in a sub-tropical region. Atmos Environ 60:211–216

  41. Silva SF, Meirelles ST, Moraes RM (2013) The guava tree as bioindicator during the process of fuel replacement of an oil refinery. Ecotoxicol Environ Saf 91:39–45

  42. Tang H, Pang J, Zhang G, Takigawa M, Liu G, Zhu J, Kobayashi K (2014) Mapping ozone risks for rice in China for years 2000 and 2020 with flux-based and exposure-based doses. Atmos Environ 86:74–83

  43. Tresmondi F, Alves ES (2011) Structural changes in Psidium guajava ‘Paluma’ leaves exposed to tropospheric ozone. Acta Bot Bras 25:122–129

  44. Yamaguchi M, Hoshino D, Inada H, Akhtar N, Sumioka C, Takeda K, Izuta T (2014) Evaluation of the effects of ozone on yield of Japanese rice (Oryza sativa L.) based on stomatal ozone uptake. Environ Pollut 184:472–480

  45. Yan K, Chen W, He X, Zhang G, Xu S, Wang L (2010) Responses of photosynthesis, lipid peroxidation and antioxidant system in leaves of Quercus mongolica to elevated O3. Environ Exp Bot 69:198–204

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The authors acknowledge the Post-Graduation Program of Instituto de Botânica (São Paulo, Brazil), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, proc.2011/51233-0), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, proc.4738931/2011-8) for supporting our project and for the Master scholarship granted to the first author (proc.131830/2012-0).

Conflict of interest

We declare that there is not any actual or potential conflict of interest with the authors or contents of this study including any financial, personal, or other relationships with other people or organizations that could inappropriately influence the evaluation of this manuscript.

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Correspondence to Pedro I. L. S. Assis.

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Responsible editor: Michael Matthies

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Assis, P.I.L.S., Alonso, R., Meirelles, S.T. et al. DO3SE model applicability and O3 flux performance compared to AOT40 for an O3-sensitive tropical tree species (Psidium guajava L. ‘Paluma’). Environ Sci Pollut Res 22, 10873–10881 (2015).

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  • DO3SE model
  • Stomatal ozone flux
  • Ozone
  • O3-induced leaf injuries
  • Tropical species
  • Psidium guajava ‘Paluma’