Abstract
Pollutants inhibit thallus growth and development or alter the metabolism and associated anatomical and morphophysiological characteristics of lichens. Since agricultural matrices can act as sources of pollution by dispersing agrochemicals to vegetation fragments, this study tested the hypothesis that Parmotrema tinctorum can serve as the indicator of edge effect in such fragments. In other words, we assumed the impact of pollutant accumulation to be greater at the vegetation edges and explored the utility of this lichen as a bioindicator of pollutants dispersed from agricultural matrices. Differences in the anatomical layers of P. tinctorum thalli sampled from the edge and center of four vegetation fragments (CER, SSF, SSC, and ENP) were evaluated, and the effects of agricultural matrices on macro- and micronutrient levels, heavy metal levels, and photosynthetic pigment content were analyzed. Anatomical layers were thicker in P. tinctorum thalli from the edges of SSC and ENP, indicating the need for photobiont protection at these sites. Edge effect was observed on Al accumulation in the thallus, indicating dispersion of this metal from agricultural matrices and its greater impact in the edge populations. Edge effect was also evident on photosynthetic pigment content, macro- and micronutrient levels, and heavy metal concentration in the thallus, and the values reflected high ecological imbalance currently verified at the edge of ENP, an area of permanent protection. In areas within ENP, chlorophyll a/b ratio reflected stress factors acting on the thallus, indicating that even legally protected areas are not free from the impact of atmospheric pollutants. P. tinctorum may serve as an effective indicator of edge effects and may be used for biomonitoring pollutant dispersion from agricultural matrices.
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References
Abas A, Mazlan SM, Latif MT, Aiyub K, Muhammad N, Nadzir MSM (2021) Lichens reveal the quality of indoor air in Selangor, Malaysia. Ecol Process 10:1–8. https://doi.org/10.1186/s13717-020-00274-1
Asad MAU, Lavoie M, Song H, Jin Y, Fu Z, Qian H (2017) Interaction of chiral herbicides with soil microorganisms, algae and vascular plants. Sci Total Environ 580:1287–1299. https://doi.org/10.1016/j.scitotenv.2016.12.092
Assmann BR, Capellesso ES, Dariva G (2017) Edge effect in lichens aluminum and lead concentration within an urban, rural and industrial area. Caderno Meio Amb Sust 10:22–36
Atafar Z, Mesdaghinia A, Nouri J, Homaee M, Yunesian M, Ahmadimoghaddam M, Mahvi AH (2010) Effect of fertilizer application on soil heavy metal concentration. Environ Monit Assess 160:83–89. https://doi.org/10.1007/s10661-008-0659-x
Bajpai R, Karakoti N, Upreti DK (2013) Performance of a naturally growing Parmelioid lichen Remototrachyna awasthii against organic and inorganic pollutants. Environ Sci Pollut Res 20:5577–5592. https://doi.org/10.1007/s11356-013-1583-3
Bajpai R, Upreti DK (2012) Accumulation and toxic effect of arsenic and other heavy metals in a contaminated area of West Bengal, India, in the lichen Pyxine cocoes (Sw.) Nyl. Ecotoxicol Environ Saf 83:63–70. https://doi.org/10.1016/j.ecoenv.2012.06.001
Bajpai R, Upreti DK, Nayaka S, Kumari B (2010) Biodiversity, bioaccumulation and physiological changes in lichens growing in the vicinity of coal-based thermal power plant of Raebareli district, north India. J Hazard Mater 174:429–436. https://doi.org/10.1016/j.jhazmat.2009.09.071
Bačkor M, Fahselt D (2004) Physiological attributes of the lichen Cladonia pleurota in heavy metal-rich and control sites near Sudbury (Ont., Canada). Environ Exp Bot 52:149–159. https://doi.org/10.1016/j.envexpbot.2004.01.014
Bačkor M, Fahselt D, Wu CT (2004) Free proline content is positively correlated with copper tolerance of the lichen photobiont Trebouxia erici (Chlorophyta). Plant Sci 167:151–157. https://doi.org/10.1016/j.plantsci.2004.03.012
Bačkor M, Fahselt D, Davidson RD, Wu CT (2003) Effects of copper on wild and tolerant strains of the lichen photobiont Trebouxia erici (Chlorophyta) and possible tolerance mechanisms. Arch Environ Contam Toxicol 45:159–167. https://doi.org/10.1007/s00244-002-0134-6
Bačkor M, Klejdus B, Vantová I, Kováčik J (2009) Physiological adaptations in the lichens Peltigera rufescens and Cladina arbuscula var. mitis, and the moss Racomitrium lanuginosum to copper-rich substrate. Chemosphere 76:1340–1343. https://doi.org/10.1016/j.chemosphere.2009.06.029
Bačkor M, Váczi P (2002) Copper tolerance in the lichen photobiont Trebouxia erici (Chlorophyta). Environ Exp Bot 48:11–20. https://doi.org/10.1016/s0098-8472(02)00004-7
Bednaříková M, Váczi P, Lazár D, Barták M (2020) Photosynthetic performance of Antarctic lichen Dermatocarpon polyphyllizum when affected by desiccation and low temperatures. Photosynth Res 145:159–177. https://doi.org/10.1007/s11120-020-00773-4
Benítez Á, Medina J, Vásquez C, Loaiza T, Luzuriaga Y, Calva J (2019) Lichens and bromeliads as bioindicators of heavy metal deposition in Ecuador. Diversity 11:28. https://doi.org/10.3390/d11020028
Boamponsem LK, Freitas CR (2017) Validation of Parmotrema reticulatum as a biomonitor of elemental air pollutants in Auckland, New Zealand. J R Soc N Z 47:275–293. https://doi.org/10.1080/03036758.2017.1296472
Boonpeng C, Boonpragob K, Homsudthai K (2014) The relationship between photosynthetic processes of the lichen Parmotrema tinctorum and rainfall at Khao Yai National Park. Aust J Bot 6:67–76
Boonpeng C, Polyiam W, Sriviboon C, Sangiamdee D, Watthana S, Nimis PL, Boonpragob K (2017) Airborne trace elements near a petrochemical industrial complex in Thailand assessed by the lichen Parmotrema tinctorum (Despr. ex Nyl.) Hale. Environ Sci Pollut Res 24:12393–12404. https://doi.org/10.1007/s11356-017-8893-9
Boonpeng C, Sangiamdee D, Noikrad S, Boonpragob K (2021) Influence of washing thalli on element concentrations of the epiphytic and epilithic lichen Parmotrema tinctorum in the tropic. Environ Sci Pollut Res 28:9723–9730. https://doi.org/10.1007/s11356-020-11459-8
Boonpeng C, Sangiamdee D, Noikrad S, Watthana S, Boonpragob K (2020) Metal accumulation in lichens as a tool for assessing atmospheric contamination in a natural park. Environ Nat Resour J 18:166–176. https://doi.org/10.32526/ennrj.18.2.2020.16
Boonpragob K (2002) Monitoring physiological change in lichens: total chlorophyll content and chlorophyll degradation. In: Nimis PL, Scheidegger C, Wolseley PA (eds) Monitoring with lichens - Monitoring Lichens. Kluwer Academic Publishers, Dordrecht, pp 323–326
Brazil (2016). Normative Instruction SDA N° 27, June 5, 2006 (Amended by IN SDA N°. 7, of April 12, 2016, republished on May 2, 2016).
Büdel B, Scheidegger C (2008) Thallus morphology and anatomy. In: Nash T III (ed) Lichen biology, 2nd edn. Cambridge University Press, Cambridge, pp 40–68
Carrera MF, Carreras HA (2011) Effects of the application of glyphosate on chemical physiological parameters of Usnea amblyoclada [Müll. Arg.] Zahlbr. Ecol Austral 21:353–361
Chettri MK, Cook CM, Vardaka E, Sawidis T, Lanaras T (1998) The effect of Cu, Zn and Pb on the chlorophyll content of the lichens Cladonia convoluta and Cladonia rangiformis. Environ Exp Bot 39:1–10. https://doi.org/10.1016/S0098-8472(97)00024-5
Chiari M, Anhê ACBM, Costa WR, Senhuk APMS (2020) Biomonitoring of air pollution: a dichotomous key for lichen species identification. Ci e Nat 42:e77. https://doi.org/10.5902/2179460X41851
Colesie C, Williams L, Büdel B (2017) Water relations in the soil crust lichen Psora decipiens are optimized via anatomical variability. Lichenologist 49:483–492. https://doi.org/10.1017/s0024282917000354
De Andrade LRM, Barros LMG, Echevarria GF, Velho do Amaral LI, Cotta MG, Rossatto DR, Haridasan M, Franco AC (2011) Al-hyperaccumulator Vochysiaceae from the Brazilian Cerrado store aluminum in their chloroplasts without apparent damage. Environ Exp Bot 70:37–42. https://doi.org/10.1016/j.envexpbot.2010.05.013
França H, Ramos Neto MB, Setzer A (2007) O fogo no Parque Nacional das Emas. MMA, Ministério do Meio Ambiente, Brasília
Garty J (2001) Biomonitoring atmospheric heavy metals with lichens: theory and application. Crit Rev Plant Sci 20:309–371. https://doi.org/10.1080/20013591099254
Gauslaa Y, Coxson D (2011) Interspecific and intraspecific variations in water storage in epiphytic old forest foliose lichens. Botany 89:787–798. https://doi.org/10.1139/b11-070
Gimeno-García E, Andreu V, Boluda R (1996) Heavy metals incidence in the application of inorganic fertilizers and pesticides to rice farming soils. Environ Pollut 92:19–25. https://doi.org/10.1016/0269-7491(95)00090-9
Guilherme LRG, Marchi G (2007) Metais em Fertilizantes Inorgânicos: avaliação de risco à saúde após a aplicação. Associação Nacional para Difusão de Adubos, São Paulo
Hale ME (1981) Pseudocyphellae and pored epicortex in the Parmeliaceae: their delimitation and evolutionary significance. Lichenologist 13:1–10. https://doi.org/10.1017/S0024282981000030
Hamutoğlu R, Derici MK, Aras ES, Aslan A, Cansaran-Duman (2020) The physiological and dna damage response of in the lichen Hypogymnia physodes to UV and heavy metal stress. Appl Ecol Environ Res 18:2315–2338. https://doi.org/10.15666/aeer/1802_23152338
Hurtado W, Gómez H, Fernández R, Galarraga F, Hernández J, González R (2013) Liquen Parmotrema sancti angelii como biomonitor de los metales provenientes de la mina loma de níquel, estado Aragua. Geos 44:5–12
Käffer MI, Lemos AT, Apel MA, Rocha JV, de Martins SMA, Vargas VMF (2012) Use of bioindicators to evaluate air quality and genotoxic compounds in an urban environment in Southern Brazil. Environ Pollut 163:24–31. https://doi.org/10.1016/j.envpol.2011.12.006
Kallenborn R, Christensen G, Evenset A, Schlabach M, Stohl A (2007) Atmospheric transport of persistent organic pollutants (POPs) to Bjørnøya (Bear island). J Environ Monit 9:1082. https://doi.org/10.1039/b707757m
Karakoti N, Bajpai R, Upreti DK, Mishra GK, Srivastava A, Nayaka S (2014) Effect of metal content on chlorophyll fluorescence and chlorophyll degradation in lichen Pyxine cocoes (Sw.) Nyl.: a case study from Uttar Pradesh, India. Environ Earth Sci 71:2177–2183. https://doi.org/10.1007/s12665-013-2623-5
Kilca RV, Schiavini I, Monteiro GA (2014) Floristic patterns on two seasonal forests types in the Cerrado. Biosci J 30:903–913
Kirk PM, Cannon PF, David JC, Stalpers JA (2001) Dictionary of the Fungy, 9th edn. CABI Bioscience, Wallingford
Kitajima K, Hogan KP (2003) Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant Cell Environ 26:857–865. https://doi.org/10.1046/j.1365-3040.2003.01017.x
Koch NM, Branquinho C, Matos P, Pinho P, Lucheta F, Martins SMA, Vargas VMF (2016) The application of lichens as ecological surrogates of air pollution in the subtropics: a case study in South Brazil. Environ Sci Pollut Res 23:20819–20834. https://doi.org/10.1007/s11356-016-7256-2
Kučera T, Horáková H, Šonská A (2008) Toxic metal ions in photoautotrophic organisms. Photosynthetica 46:481–489. https://doi.org/10.1007/s11099-008-0083-z
Kukachka BF, Miller RB (1980) A chemical spot-test for aluminum and its value in wood identification. IAWA Bull 1:104–109. https://doi.org/10.1163/22941932-90000699
Kumar KS, Dahms H-U, Lee J-S, Kim HC, Lee WC, Shin K-H (2014) Algal photosynthetic responses to toxic metals and herbicides assessed by chlorophyll a fluorescence. Ecotoxicol Environ Saf 104:51–71. https://doi.org/10.1016/j.ecoenv.2014.01.042
López Carnelo LG, De Miguez SR, Marban L (1997) Heavy metals input with phosphate fertilizers used in Argentina. Sci Total Environ 204:245–250. https://doi.org/10.1016/S0048-9697(97)00187-3
Lucadamo L, Corapi A, Gallo L (2018) Evaluation of glyphosate drift and anthropogenic atmospheric trace elements contamination by means of lichen transplants in a southern Italian agricultural district. Air Qual Atmos Health 11:325–339. https://doi.org/10.1007/s11869-018-0547-7
Majewska M, Harshkova D, Pokora W, Baścik-Remisiewicz A, Tułodziecki S, Aksmann A (2021) Does diclofenac act like a photosynthetic herbicide on green algae? Chlamydomonas reinhardtii synchronous culture-based study with atrazine as reference. Ecotoxicol Environ Saf 208:111630. https://doi.org/10.1016/j.ecoenv.2020.111630
Malavolta E (1997) Avaliação do estado nutricional das plantas princípios e aplicações, second edn. Associação Brasileira para Pesquisa da Potássio e do Fosfato, Piracicaba
Mansournia MR, Wu B, Matsushita N, Hogetsu T (2012) Genotypic analysis of the foliose lichen Parmotrema tinctorum using microsatellite markers: association of mycobiont and photobiont, and their reproductive modes. Lichenologist 44:419–440. https://doi.org/10.1017/s0024282911000909
Marques AP, Freita MC, Wolterbeek HT, Steinebach OM, Verburg T, De Goeij JJM (2005) Cell-membrane damage and element leaching in transplanted Parmelia sulcata lichen related to ambient SO2, temperature, and precipitation. Environ Sci Technol 39:2624–2630. https://doi.org/10.1021/es0498888
Martins AP, Galvani E (2020) Relationship between land cover and biophysical parameters in the Brazilian Savanna. Rev Depart Geogr 40:48–162
Martins-Mazzitelli SMA, Mota Filho FO, Pereira EC, Figueira R (2006) Utilização de liquens no biomonitoramento da qualidade do ar. In: Xavier Filho L, Legaz ME, Córdoba CV, Pereira EC (eds) Biologia de Liquens. v. 3, 4th edn. Âmbito Cultural, Rio de Janeiro, pp 101–133
Nakajima H, Yamamoto Y, Yoshitani A, Itoh K (2013) Effect of metal stress on photosynthetic pigments in the Cu-hyperaccumulating lichens Cladonia humilis and Stereocaulon japonicum growing in Cu-polluted sites in Japan. Ecotoxicol Environ Saf 97:154–159. https://doi.org/10.1016/j.ecoenv.2013.07.026
Nash TH (2008) Lichen Biology, 2nd edn. University Press, Cambridge
Nguyen K-H, Chollet-Krugler M, Gouault N, Tomasi S (2013) UV-protectant metabolites from lichens and their symbiotic partners. Nat Prod Rep 30:1490. https://doi.org/10.1039/c3np70064j
Nicolardi V, Cai G, Parrotta L, Puglia M, Bianchi L, Bini L, Gaggi C (2012) The adaptive response of lichens to mercury exposure involves changes in the photosynthetic machinery. Environ Pollut 160:1–10. https://doi.org/10.1016/j.envpol.2011.09.015
O'brien TP, Mccully ME (1981) The study of plant structure: principles and selected methods. Termarcarphy Pry Ltd., Melbourne
Ohmura Y, Kawachi M, Kasai F, Watanabe MM, Takeshita S (2006) Genetic combinations of symbionts in a vegetatively reproducing lichen, Parmotrema tinctorum, based on ITS rDNA sequences. Bryologist 109:43–59. https://doi.org/10.1639/0007-2745(2006)109[0043:GCOSIA]2.0.CO;2
Port RK, Käffer MI, Schmitt JL (2018) Morphophysiological variation and metal concentration in the thallus of Parmotrema tinctorum (Despr. ex Nyl.) Hale between urban and forest areas in the subtropical region of Brazil. Environ. Sci Pollut Res Int 25:33667–33677. https://doi.org/10.1007/s11356-018-3246-x
Purvis W (2000) Lichens. Smithsonian Institution Press, Washington
R Core Team (2021) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. Avaliable from: https://www.R-project.org/. Accessed 20 Fev 2021
Rasi JR, Neto MM, Bernardo R (2020) Design and development of an unmanned aerial vehicle for agricultural spraying in Brazil. Int J Innov Educ Res 8:405–419. https://doi.org/10.31686/ijier.vol8.iss12.2866
Ribeiro JF, Walter BMT (1998) Fitofisionomias do bioma Cerrado. In: Sano SM, Almeida SP (eds) Cerrado: ambiente e flora. Planaltina, Embrapa-CPAC, Brasília, pp 87–166
Sanders WB (2001) Lichens: the interface between mycology and plant morphology. BioScience 51:1025–1035. https://doi.org/10.1641/0006-3568(2001)051[1025:LTIBMA]2.0.CO;2
Sadowsky A, Ott S (2015) Symbiosis as a successful strategy in continental Antarctica: performance and protection of Trebouxia photosystem II in relation to lichen pigmentation. Polar Biol 39:139–151. https://doi.org/10.1007/s00300-015-1677-0
Safitri RR, Sudirman LI, Koesmaryono Y (2020) Exploration of Parmotrema tinctorum and Leptogium sp. lichens as bioindicator of air quality in Mekarsari fruit park. IOP Conf Ser Earth Environ Sci 457:012006. https://doi.org/10.1088/1755-1315/457/1/012006
Sano EE, Rosa R, Brito JLS, Ferreira LG (2010) Land cover mapping of the tropical savanna region in Brazil. Environ Monit Assess 166:113–124. https://doi.org/10.1007/s10661-009-0988-4
Sen G, Eryilmaz IE, Ozakca D (2014) The effect of aluminium-stress and exogenous spermidine on chlorophyll degradation, glutathione reductase activity and the photosystem II D1 protein gene (psbA) transcript level in lichen Xanthoria parietina. Phytochemistry 98:54–59. https://doi.org/10.1016/j.phytochem.2013.11.021
Sonina A, Rumjantseva AD, Tsunskaya AA, Androsova VI (2017) Adaptations of epilthic Lichens to microclimate conditions of the White Sea Coast. Czech Polar Rep 7:133–143. https://doi.org/10.5817/CPR2017-2-13
Sujetovienė G, Gasauskaitė K, Žaltauskaitė J (2020) Toxicity of a phenoxy herbicide on the lichen Ramalina fraxinea. Toxicol Environ Chem 101:1–17. https://doi.org/10.1080/02772248.2020.1747466
Traba HM, Dominguez-Morueco N, Barreno E, Catala M (2017) Lichen microalgae are sensitive to environmental concentrations of atrazine. J Environ Sci Health B 52:223–228. https://doi.org/10.1080/03601234.2016.1270679
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. https://doi.org/10.1016/s0176-1617(11)81192-2
Van Dijk H, Guicherit R (1999) Atmospheric dispersion of currentuse pesticides: a review of the evidence from monitoring studies. Water Air Soil Pollut 115:21–70. https://doi.org/10.1023/A:1005293020536
Vannini A, Guarnieri M, Bačkor M, Bilová I, Loppi S (2015) Uptake and toxicity of glyphosate in the lichen Xanthoria parietina (L.) Th. Fr. Ecotoxicol Environ Saf 122:193–197. https://doi.org/10.1016/j.ecoenv.2015.07.030
Vannini A, Paoli L, Vichi M, Bačkor M, Bačkorová M, Loppi S (2018) Toxicity of diclofenac in the fern Azolla filiculoides and the lichen Xanthoria parietina. Bull Environ Contam Toxicol 100:430–437. https://doi.org/10.1007/s00128-017-2266-4
Viana CO, Vaz RP, Cano A, Santos AP, Cançado LG, Ladeira LO, Junior AC (2015) Physiological changes of the lichen Parmotrema tinctorum as result of carbon nanotubes exposition. Ecotoxicol Environ Saf 120:110–116. https://doi.org/10.1016/j.ecoenv.2015.05.034
Yotsova EK, Stefanov MA, Dobrikova AG, Apostolova EL (2017) Different sensitivities of photosystem II in green algae and cyanobacteria to phenylurea and phenol-type herbicides: effect on electron donor side. Zeitschrift Für Naturforschung C 72:315–324. https://doi.org/10.1515/znc-2016-0089
Zhang DY, Chen LP, Zhang RR, Xu G, Lan YB, Hoffmann WC, Xiu W, Min X (2015) Evaluating effective swath width and droplet distribution of aerial spraying systems on M-18B and Thrush 510G airplanes. Int J Agric & Biol Eng 8:21–30. https://doi.org/10.3965/j.ijabe.20150802.1493
Zulaini AAM, Muhammad N, Asman S, Hashim NH, Jusoh S, Abas A, Yusof H, Din L (2019) Evaluation of transplanted lichens, Parmotrema tinctorum and Usnea diffracta as bioindicator on heavy metals accumulation in southern peninsular Malaysia. J Sustain Sci Manag 14:1–13
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We are grateful to the Goiás State Research Foundation (FAPEG) for master stipends and the Rio Verde campus of the Goiano Federal Institute (IFGoiano), for providing the infrastructure necessary for the realization of the present study.
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The authors contributed to the study conception and design. Sample collection, material preparation, and analysis were conducted by Kelly Maria Zanuzzi Palharini. The first draft of the manuscript was written by Kelly Maria Zanuzzi Palharini, Layara Alexandre Bessa, and Sebastião de Carvalho Vasconcelos Filho. Luciana Cristina Vitorino and Fabiano Guimarães Silva thoroughly checked the first draft. All authors have read and approved the final manuscript.
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Palharini, .M.Z., Vitorino, L.C., Bessa, L.A. et al. Parmotrema tinctorum as an indicator of edge effect and air quality in forested areas bordered by intensive agriculture. Environ Sci Pollut Res 28, 68997–69011 (2021). https://doi.org/10.1007/s11356-021-15411-2
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DOI: https://doi.org/10.1007/s11356-021-15411-2