Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Integrated assessment of air pollution by metals and source apportionment using ryegrass (Lolium multiflorum Lam.) in southern Brazil

  • 303 Accesses

  • 10 Citations


One of the biggest environmental problems existing today is air pollution, which is characterized by the presence of toxic gases and metal pollutants, the latter of which is generally associated with emissions of particulate matter (PM) from industries or automotive vehicles. Biomonitoring is a method that can be used to assess air pollution levels because it makes it possible to determine what effects these air pollutants cause in living organisms and their responses. The species Lolium multiflorum Lam., known as ryegrass, is considered a good bioindicator of metals, since it accumulates these substances during exposure. This study proposes to conduct an integrated assessment of air quality using two different monitoring methodologies: biomonitoring with L. multiflorum and active monitoring in areas with different levels of urbanization and industrialization. Concentrations found in ryegrass plants revealed high levels of Pb, Cr, Zn, and Cu, indicating that vehicular and industrial emissions were the main sources of pollution. Analysis of PM also revealed soot and biogenic particles, which can transport metals. Therefore, with the proposed method, the anthropogenic impact on air pollution in the investigated area could be clearly demonstrated.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4


  1. Aas W, Alleman LY, Bieber E, Gladtke D, Houdret J, Karlssone V, Monies C (2009) Comparison of methods for measuring atmospheric deposition of arsenic, cadmium, nickel and lead. J Environ Monit 11:1276–1283

  2. Adachi K, Tainosho Y (2004) Characterization of heavy metal particles embedded in tire dust. Environ Int 30:1009–1017

  3. Adamo P, Giordano S, Naimo D, Bargagli R (2008) Geochemical properties of airborne particulate matter (PM10) collected by automatic device and biomonitors in a Mediterranean urban environment. Atmos Environ 42:346–357

  4. Alcalá J, Sosa M, Moreno M, Quintana C, Quintana G, Miranda S, Rubio A (2008) Heavy metals in tree vegetation as an indicator of the urban environmental quality: city of Chihuahua, Mexico. Latin American Journal of Natural Resources 17:38–54 (in Spanish)

  5. Alleman LY, Lamaison L, Perdrix E, Robache A, Galloo JC (2010) PM10 metal concentrations and source identification using positive matrix factorization and wind sectoring in a French industrial zone. Atmos Res 96:612–625

  6. Allen AG, Nemitz E, Shi JP, Harrison RM, Greenwood JC (2001) Size distributions of trace metals in atmospheric aerosol in the United Kingdom. Atmos Environ 35:4581–4591

  7. Alves DD, Osorio DMM, Rodrigues MAS, Illi JC, Bianchin L, Benvenuti T (2015a) Concentrations of PM2.5–10 and PM2.5 and metallic elements around the Schmidt Stream area, in the Sinos River Basin, southern Brazil. Braz J Biol 75:43–52

  8. Alves DD, Osorio DMM, Rodrigues MAS, Schuck S (2015b) Morphology and composition of the atmospheric particulate matter of the watershed of Sinos River (RS) analyzed by scanning electron microscopy. Geochim Bras 29:45–57 (in Portuguese)

  9. Aquino SMF, Almeida JR, Cunha RR, Lins GA (2011) Vegetable bioindicators: an alternative to monitoring the atmospheric pollution. Revista Internacional de Ciências 1:1–18 (in Portuguese)

  10. Bourotte C, Curi-Amarante AP, Forti MC, Pereira LAA, Braga AL, Lotufo PA (2007) Association between ionic composition of fine and coarse aerosol soluble fraction and peak expiratory flow of asthmatic patients in São Paulo city (Brazil). Atmos Environ 41:2036–2048

  11. Brauer M, Lencar C, Tamburic L, Koehoorn M, Demers P, Karr C (2008) A cohort study of traffic-related air pollution impacts on birth outcomes. Environment Health Perspective 116:680–686

  12. Brook RD, Rajagopalan S, Pope CA III, Brook JR, Bhatnagar A, Diez-Roux AV, Holguin F, Hong Y, Luepker RV, Mittleman MA, Peters A, Siscovick D, Smith SC Jr, Whitsel L, Kaufman JD (2010) Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American Heart Association. Circulation 121:2331–2378

  13. Caggiano R, Micchiato M, Trippetta S (2010) Levels, chemical composition and sources of fine aerosol particles (PM1) in an area of the Mediterranean basin. Sci Total Environ 408:884–895

  14. Camargo M (2002) Carboxyl terminated polyester resins to powder paint: characterization and kinetic study of the cure reaction. Doctoral thesis, Federal University of Rio Grande do Sul, Brazil, 83p (in Portuguese)

  15. Carreras HA, Pignata ML, Saldiva PHN (2006) In situ monitoring of urban air in Córdoba, Argentina using the tradescantia-micronucleus (Trad-MCN) bioassay. Atmos Environ 40:7824–7830

  16. Carreras HA, Rodriguez JH, González CM, Wannaz ED, Ferreyra FG, Perez CA, Pignata ML (2009) Assessment of the relationship between total suspended particles and the response of two biological indicators transplanted to an urban area in central Argentina. Atmos Environ 43:2944–2949

  17. Carreras HA, Segura MEC, Arroyo SG, Tovar MAM, Muñoz OA (2013) Composition and mutagenicity of PAHs associated with urban airborne particles in Córdoba, Argentina. Environ Pollut 178:403–410

  18. Chithra VS, Nagendra SM (2013) Chemical and morphological characteristics of indoor and outdoor particulate matter in an urban environment. Atmos Environ 77:579–587

  19. Cooper CD, Alley FC (2002) Air pollution control: a design approach. Waveland Press, United States of America 738p

  20. Costa GM, Droste A (2012) Genotoxicity on Tradescantia pallida var. purpurea plants exposed to urban and rural environments in the metropolitan area of Porto Alegre, southem Brazil. Braz J Biol 72:801–806

  21. CPRM (2008) Geology sheet of Gravataí. Geological survey of Brazil. http://www.cprm.gov.br/publique/media/rel_gravatai.pdf. Accessed 19 June 2016 (in Portuguese)

  22. Dallarosa J, Teixeira EC, Meira L, Wiegand F (2008) Study of the chemical elements and polycyclic aromatic hydrocarbons in atmospheric particles of PM10 and PM2.5 in the urban and rural areas of South Brazil. Atmos Res 89:76–92

  23. De Paula PHM, Mateus VL, Araripe DR, Duyck CB, Saint’Pierre TD, Gioda A (2015) Biomonitoring of metals for air pollution assessment using a hemiepiphyte herb (Struthanthus flexicaulis). Chemosphere 138:429–437

  24. Divan Junior AM, Oliva MA, Martinez CA, Cambraia J (2007) Effects of fluoride emissions on two tropical grasses: Chloris gayana and Panicum maximum cv. colonião. Ecotoxicol Environ Saf 67:247–253

  25. Divan Junior AM, Oliva MA, Ferreira FA (2008) Dispersal pattern of airborne emissions from aluminium smelter in Ouro Preto, Brazil, as expressed by foliar fluoride accumulation in eight plant species. Ecol Indic 8:454–461

  26. Domingos M, Klumpp A, Klumpp G (1998) Air pollution impact on the Atlantic forest in the Cubatão region, SP, Brazil. Ciência e Cultura 50:230–236

  27. Domingos M, Alves ES, Bulbovas P, Cunha AL, Longui EL, Lourençon DACB, Moraes RM, Rinaldi MCS, Mazzoni-Viveiros SC (2004) Reaction of Caesalpinia echinata Lam., a Brazilian tree species, to urban air pollution stress. In: Klumpp A, Ansel W, Klumpp G (eds) Urban air pollution, bioindication and environmental awareness. Cuvillier Verlag, Göttingen, pp. 279–287

  28. EPA (1996) Method 3052: microwave assisted acid digestion of siliceous and organically based matrices. https://www.epa.gov/sites/production/files/2015-12/documents/3052.pdf. Accessed 22 September 2016

  29. Field A (2009) Discovering statistics using SPSS. Artmed, Porto Alegre (in Portuguese)

  30. FEPAM (2010) Vehicle pollution control plan of Rio Grande do Sul state. Rio Grande do Sul, Brazil, 150p (in Portuguese)

  31. FEPAM (2015) Water quality of the Sinos River basin. http://www.fepam.rs.gov.br/qualidade/qualidade_sinos/sinos.asp. Accessed 10 December 2015 (in Portuguese)

  32. Fernandes JC, Henriques FS (1991) Biochemical, physiological, and structural effects of excess copper in plants. Bot Rev 57:246–273

  33. Foy B, Smyth A, Thompson SL, Gross DS, Olson MR, Sager N, Schauer JJ (2012) Sources of nickel, vanadium and black carbon in aerosols in Milwaukee. Atmos Environ 59:294–301

  34. Gajghate DG, Bhanarkar AD (2005) Characterisation of particulate matter for toxic metals in ambient air of Kochi city, India. Environ Monit Assess 102:119–129

  35. Gietl JK, Lawrence R, Thorpe AJ, Harrison RM (2010) Identification of brake wear particles and derivation of a quantitative tracer for brake dust at a major road. Atmos Environ 44:141–146

  36. Goto MM (2007) Biomonitoring of atmospheric particulate matter in the area of influence of the Complexo Portuário de Ponta da Madeira in São Luís – MA. Dissertation, University of São Luís, Brazil, 72p (in Portuguese)

  37. Gouveia N, Mendonça GAS, Leon AP, Correia JEM, Junger WL, Freitas CU, Martins LC, Giussepe L, Conceição GMS, Manerich A, Cunha-Cruz J (2003) Poluição do ar e efeitos na saúde nas populações de duas grandes metrópoles brasileiras. Epidemiologia e Serviços de saúde 12:29–40 (in Portuguese)

  38. Gupta AK, Nag S, Mukhopadhyay UK (2006) Characterisation of PM10, PM2.5 and benzene soluble organic fraction of particulate matter in an urban area of Kolkata, India. Environ Monit Assess 98:205–222

  39. Hair JF, Anderson RE, Tatham RL, Black WC (2009) Multivariate data analysis. Bookman, Brazil 688p (in Portuguese)

  40. Hopke PK, Xie Y, Raunemaa T, Biegalski S, Landsberger S, Maenhaut W, Artaxo P, Cohen D (1997) Characterization of the Gent stacked filter unit PM10 sampler. Aerosol Sci Technol 27:726–735

  41. INPE (2012) Protocol for collection of atmospheric particulate matter. http://mtc-m16d.sid.inpe.br/col/sid.inpe.br/mtc-m19/2012/ Accessed 12 September 2016 (in Portuguese)

  42. Kabata-Pendias A (2011) Trace elements in soils and plants. Taylor and Francis Group, United States of America 534p

  43. Kampa M, Castanas E (2008) Human health effects of air pollution. Environ Pollut 151:362–367

  44. Kar S, Maity JP, Samal AC, Santra SC (2010) Metallic components of traffic induced urban aerosol, their spatial variation, and source apportionment. Environment Monitoring and Assessment 168:561–574

  45. Kelly FJ, Fussell J (2012) Size, source and chemical composition as determinants of toxicity attributable to ambient particulate matter. Atmos Environ 60:504–526

  46. Khan MF, Hirano K, Masunaga S (2010) Quantifying the sources of hazardous elements of suspended particulate matter aerosol collected in Yokohama, Japan. Atmos Environ 44:2646–2657

  47. Klumpp A, Ansel W, Klumpp G (2004) European network for the assessment of air quality by the use of bioindicator plants. University of Hohenheim, Stuttgart, Germany 139p

  48. Klumpp A, Domingos M, Klumpp G (1996) Assessment of the vegetation risk by fluoride emissions from fertiliser industries at Cubatão, Brazil. The Science of the Total Environmental 192:219–228

  49. Klumpp A, Klumpp G, Domingos M (1994) Plants as bioindicators of air pollution at the Serra do Mar near the industrial complex of Cubatão, Brazil. Environ Pollut 85:109–116

  50. Laden F, Schwartz J, Speizer FE, Dockery DW (2006) Reduction in fine particulate air pollution and mortality: extended follow-up of the Harvard six cities study. Am J Respir Crit Care Med 173:667–672

  51. Lepeule J, Laden F, Dockery D, Schwartz J (2012) Chronic exposure to fine particles and mortality: an extended follow-up of the Harvard six cities study from 1974 to 2009. Environ Health Perspect 120:965–970

  52. Levy JI, Hanna SR (2011) Spatial and temporal variability in urban fine particulate matter concentrations. Environ Pollut 159:2009–2015

  53. Liu C-W, Lin K-H, Kuo Y-M (2003) Application of factor analysis in the assessment of groundwater quality in a blackfoot disease area in Taiwan. Sci Total Environ 313:77–89

  54. Loyola J, Arbilla G, Quiterio SL, Escaleira V, Minho AS (2012) Trace metals in the urban aerosols of Rio de Janeiro city. J Braz Chem Soc 23:628–638

  55. Madejó P, Murillo JM, Maranõn T, Cabrera F, López R (2002) Bioaccumulation of As, Cd, Cu, Fe and Pb in wild grasses affected by the Aznalcóllar mine spill (SW Spain). Sci Total Environ 290:105–120

  56. Maenhaut W, Francois F, Cafmeyer J (1993) The “Gent” stacked filter unit sampler for the collection of atmospheric aerosols in two size fractions: description and instructions for installation and use. Coordinated Research Programme: CRP E4.10.08. International Atomic Energy Agency, Vienna, pp. 249–263

  57. Maioli OLG, Santos JM, Reis Júnior NC, Cassini STA (2008) Foliar biochemical parameters of species Licania tomentosa (Benth.) and Bauhinia forficata (Link.) for evaluation of air quality. Quim Nov. 8:1925–1932 (in Portuguese)

  58. Manahan SE (2005) Environmental chemistry. Lewis, Boca Raton, Florida 783p

  59. Mateus V, Monteiro I, Rocha R, Saint’Pierre T, Gioda A (2013) Study of the chemical composition of particulate matter from Rio de Janeiro metropolitan region, Brazil, by inductively coupled plasma-mass spectrometry and optical emission spectrometry. Spectrochim Acta B 86:131–136

  60. Micic M, Leblanc RM, Markovic AS, Vukelic N, Polic P (2003) Atlas of tropospheric aerosols from Belgrade troposphere. Fresenius Environ Bull 12:1–10

  61. Migliavacca DM (2009) Study of scavenging processes of atmospheric pollutants and use of bioindicators in the metropolitan area of Porto Alegre, RS. Doctoral thesis, Federal University of Rio Grande do Sul, Brazil, 182p (in Portuguese)

  62. Migliavacca D, Teixeira EC, Wiegand F, Machado ACM, Sanchez J (2005) Atmospheric precipitation and chemical composition of an urban site Guaíba hydrographic basin, Brazil. Atmos Environ 39:1829–1844

  63. Migliavacca DM, Teixeira EC, Gervasoni F, Conceição RV, Rodriguez MTR (2012) Metallic elements and isotope of Pb in wet precipitation in urban area, South America. Atmos Res 107:106–114

  64. Mišík M, Nersesyan A, Monarca S, Kim JK, Knasmueller S (2011) Micronucleus assays with Tradescantia pollen tetrads: an update. Mutagenesis 26:215–221

  65. Moreira TCL (2010) Interaction between trees and air pollution in the city of São Paulo. Dissertation, University of São Paulo, Brazil, 81p (in Portuguese)

  66. Nogueira CA (2006) Assessment of atmospheric metallic pollution in the metropolitan region of São Paulo, Brazil, employing Tillandsia usneoides L. as biomonitor. Doctoral thesis, University of São Paulo, Brazil, 112p (in Portuguese)

  67. Okuda T, Nakao S, Katsuno M, Tanaka S (2007) Source identification of nickel in TSP and PM2.5 in Tokyo, Japan. Atmos Environ 41:7642–7648

  68. Oliva MA, Figueiredo JG (2005) Fluoride bioindicator grasses for tropical regions. Brazilian Journal of Botany 28:389–397 (in Portuguese)

  69. Ooki A, Uematsu M, Miura K, Nakae S (2002) Sources of sodium in atmospheric fine particles. Atmos Environ 36:4367–4374

  70. Pandey PK, Patel KS, Subrt P (1998) Trace elemental composition of atmospheric particulate at Bhilai in central-east India. Sci Total Environ 215:123–134

  71. Pant P, Harrison RM (2013) Estimation of the contribution of road traffic emissions to particulate matter concentrations from field measurements: a review. Atmos Environ 77:78–97

  72. Pedroso ANV, Alves ES (2008) Comparative leaf anatomy of Nicotiana tabacum L. cultivars (Solanaceae) sensitive and tolerant to ozone. Acta Botanica Brasilica 22:21–28 (in Portuguese)

  73. Perry CT (2007) Assessment of the bioindicator potential of Psidium guajava and Psidium cattleyanum to air quality evaluation in industrial area. Dissertation, Federal University of Rio Grande do Sul, Brazil, 71p (in Portuguese)

  74. Perry CT, Divan AM Jr, Raya Rodriguez MT, Atz VL (2010) Psidium guajava as a bioaccumulator of nickel around an oil refinery, southern Brazil. Ecotoxicol Environ Saf 73:647–654

  75. Prajapati SK, Tripathi BD (2008) Assessing the genotoxicity of urban air pollutants in Varanasi City using Tradescantia micronucleus (Trad-MCN) bioassay. Environ Int 34:1092–1096

  76. Quiterio SL, Sousa da Silva SCR, Arbilla G, Escaleira V (2004) Metals in airborne particulate matter in the industrial district of Santa Cruz, Rio de Janeiro, in an annual period. Atmos Environ 38:321–331

  77. Ragosta M, Caggiano R, D’Emilio M, Macchiato M (2002) Source origin and parameters influencing levels of heavy metals in TSP, in an industrial background area of southern Italy. Atmos Environ 36:3071–3087

  78. Roberts S (2013) Have the short-term mortality effects of particulate matter air pollution changed in Australia over the period 1993–2007. Environ Pollut 182:9–14

  79. Rocha L, Droste A, Gehlen G, Schmitt JL (2013) Leaf dimorphism of Microgramma squamulosa (Polypodiaceae): a qualitative and quantitative analysis focusing on adaptations to epiphytism. Revista de Biologia Tropical 61:291–299

  80. Rosasco FV, Marini RL, Martins MPP, Pereira EB (2011) Morphological characterization of particles in the atmosphere of José dos Campos—SP, using electron microscopy (SEM). Geochim Bras 25:25–33 (in Portuguese)

  81. Sandrin CZ, Figueiredo RCL, Delitti WBC, Domingos M (2013) Short-term changes of fructans in ryegrass (Lolium multiflorum ‘Lema’) in response to urban air pollutants and meteorological conditions. Ecotoxicol Environ Saf 96:80–85

  82. Schneider IL (2012) Spectroscopic characterization of the sediments of Sinos River basin (RS). Dissertation, Universidade Federal do Rio Grande do Sul (in Portuguese)

  83. Shimazaki K, Sakaki T, Kondo N, Sugahara K (1980) Active oxygen participation in chlorophyll destruction and lipid peroxidation in SO2-fumigated leaves of spinach. Plant Cell Physiol 21:1193–1204

  84. Simon E, Braun M, Vidic A, Bogyó D, Fábián I, Tóthmérész B (2011) Air pollution assessment based on elemental concentration of leaves tissue and foliage dust along an urbanization gradient in Vienna. Environ Pollut 159:1229–1233

  85. Simon E, Baranyai E, Braun M, Cserháti C, Fábián I, Béla Tóthmérész B (2014) Elemental concentrations in deposited dust on leaves along an urbanization gradient. Sci Total Environ 490:514–520

  86. Simon E, Harangi S, Baranyai E, Fábián I, Tóthmérész B (2016) Influence of past industry and urbanization on elemental concentrations in deposited dust and tree leaf tissue. Urban For Urban Green 20:12–19

  87. Thorpe A, Harrison RM (2008) Sources and properties of non-exhaust particulate matter from road traffic: a review. Sci Total Environ 400:270–282

  88. Tian HZ, Lu L, Cheng K, Hao JM, Zhao D, Wang Y, Jia WX, Qiu PP (2012) Anthropogenic atmospheric nickel emissions and its distribution characteristics in China. Sci Total Environ 417–418:148–157

  89. VDI – Verein Deutscher Ingenieure (2001) Biological measuring techniques for determination and evaluation of effects of air pollution plants (bioindication). Method of standardized grass exposure. VDI Guideline 3957/2 (draft). In: VDI/DIN Handbuch Reinhaltung der Luft. Beuth Verlag, Berlin, Germany

  90. Wieser G, Havranek WM (1993) Ozone uptake in the sun and shade crown of spruce: quantifying the physiological effects of ozone exposure. Trees 7:227–232

  91. Wu YS, Fang GC, Lee WJ, Lee JF, Chang CC, Lee CZ (2007) A review of atmospheric fine particulate matter and its associated trace metal pollutants in Asian countries during the period 1995–2005. J Hazard Mater 143:511–515

  92. Xu HM, Cao JJ, Ho KF, Ding H, Han YM, Wang GH, Chow JC, Watson JG, Khol SD, Qiang J, Li WT (2012) Lead concentrations in fine particulate matter after the phasing out of leaded gasoline in Xi’an, China. Atmos Environ 46:217–224

  93. Yatkin S, Bayram A (2007) Elemental composition and sources of particulate matter in the ambient air of a metropolitan city. Atmos Res 85:126–139

Download references

Author information

Correspondence to Darlan Daniel Alves.

Additional information

Responsible editor: Roberto Terzano

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Illi, J.C., Vancetta, T., Alves, D.D. et al. Integrated assessment of air pollution by metals and source apportionment using ryegrass (Lolium multiflorum Lam.) in southern Brazil. Environ Sci Pollut Res 24, 2790–2803 (2017). https://doi.org/10.1007/s11356-016-8041-y

Download citation


  • Air pollution
  • Monitoring
  • Ryegrass
  • L. multiflorum
  • Metallic elements