Abstract
Thalli of the lichen Pseudevernia furfuracea were transplanted for 3 months (November 2010–January 2011) at 61 monitoring sites around a cement plant near Castrovillari (Calabria, southern Italy). NH3, NO x and SO2 concentrations were monitored monthly in a subarea of 10 sites (SA10) where the cement plant was located. At the end of the exposure period, the integrity of cell membranes; membrane lipid peroxidation (thiobarbituric acid reactive substances, TBARS level); vitality (cell respiration); chlorophyll a; chlorophyll b; carotenoids; phaeophytization quotient; photosynthetic efficiency and thalli concentrations of Al, Ca, Mg, V and Fe were measured. NO x concentrations correlated with the site distance from the cement plant while NH3 concentrations correlated with lichen vitality within SA10. For the monitoring area as a whole, only Fe and Mg concentrations correlated with membrane lipid peroxidation, while TBARS levels showed a significant increase and chlorophyll a, chlorophyll b and carotenoids a significant decrease with respect to the lichen origin area. Multivariate analysis (detrended correspondence analysis, cluster analysis and multi-response permutation procedure) of the eco-physiological parameters × monitoring sites data set resulted in four clusters termed C1, C2, C3 and C4. The eco-physiological parameters were compared among the four clusters and lichen origin area by one-way ANOVA. An index of environmental favourableness (IEF) to lichens was calculated to evaluate the spatial recovery of impaired values of TBARS, chlorophyll a, chlorophyll b, xanthophylls + carotenoids and phaeophytization quotient. The results indicate that there is no clear spatial trend in mycobiont impairment even though the IEF values suggest a higher number of sites with low levels of membrane lipid peroxidation in the 2-–3-km distance band from the cement plant (the outermost) than in the two other distance bands (0–1 and 1–2 km). The photobiont seems to be damaged mainly in the inner distance band of the study area as suggested by the gradual but significant recovery trend of pigment levels and phaeophytization quotient from the inner distance band to the outer one (as shown by the IEF values). Conversion of chlorophyll to phaeophytin probably is not the only process affecting pigment levels.
Similar content being viewed by others
References
ARPACAL (2011) Centro Funzionale Multirischi – Dati Storici. http://www.cfd.calabria.it/index.php?option = com_wrapper&view = wrapper&Itemid = 41
Asta, J., Erhardt, W., Ferretti, M., Fornasier, F., Kirschbaum, U., Nimis, P. L., Purvis, O. W., Pirintsos, S., Scheidegger, C., Van Haluwyn, C., & Wirth, V. (2002). Mapping lichen diversity as an indicator of environmental quality. In P. L. Nimis, C. Scheidegger, & P. A. Wolseley (Eds.), Monitoring with lichens—monitoring lichens (pp. 273–279). Dordrecht: Kluwer Academic Publishing.
Azmat, R., & Hasan, S. (2008). Photochemistry of light harvesting pigments and some biochemical changes under aluminium stress. Pakistan Journal of Botany, 40(2), 779–784.
Bačkor, M., & Fahlset, D. (2004). Physiological attributes of the lichen Cladonia pleurota in heavy metal-rich and control sites near Sudbury (Ont., Canada). Environmental and Experimental Botany, 52(2), 149–159.
Bačkor, M., & Fahselt, D. (2005). Tetrazolium reduction as an indicator of environmental stress in lichens and isolated bionts. Environmental and Experimental Botany, 53(2), 125–133.
Bačkor, M., & Loppi, S. (2009). Interactions of lichens with heavy metals. Biologia Plantarum, 53, 214–222.
Bates, J. W., & Farmer, A. M. (1990). An experimental study on calcium acquisition and its effects on calcifuge moss Pleurozium schreberi. Annals of Botany, 6581, 87–96.
Cape, J. N., van der Eerden, L. J., Sheppard, L. J., Leith, I. D., & Sutton, M. A. (2009). Evidence for changing the critical level for ammonia. Environmental Pollution, 157, 1033–1037.
Carreras, H. A., & Pignata, M. L. (2007). Effects of the heavy metals Cu2+, Ni2+, Pb2+ and Zn2+ on some physiological parameters of the lichen Usnea amblyocada. Ecotoxicology and Environmental Safety, 67, 59–66.
Chaunsali, P., & Peethamparan, S. (2013). Influence of the composition of cement kiln dust of its interaction with fly ash and slag. Cement and Concrete Research, 54, 106–113.
Cieslinski, S., & Jaworska, E. (1986). Zmiany we florze porostowsosny (Pinus sylvestris) pod wplywen emisji zakladow przemyslu cemetowo-wapienniczego i wydobwczego. Acta Mycologica, 22, 3–14.
Conti, M. E., & Cecchetti, G. (2001). Biological monitoring: lichens as bioindicator of air pollution assessment: a review. Environmental Pollution, 114, 471–479.
Corapi, A. (2011). Studio della qualità dell’aria nella zona limitrofa al sito industriale Italcementi di Castrovillari attraverso una batteria di test ecofisiologici, quali indicatori precoci di stress ambientale, utilizzando i licheni come organismi sensibili. Tesi Dottorato di Ricerca in Biologia Vegetale XXIV Ciclo, Settore Disciplinare BIO/07, Facoltà di Scienze Matematiche, Fisiche, Naturali, Università della Calabria, Anno Accademico 2010–2011.
Cuny, D., Pignata, M. L., Kranner, I., & Beckett, R. (2002). Biomarker of pollution-induced oxidative stress and membrane damage in lichens. In P. L. Nimis, C. Scheidegger, & P. A. Wolseley (Eds.), Monitoring with lichens—monitoring lichens (pp. 97–100). Dordrecht: Kluwer Academic Publishing.
Czaja, A. T. (1966). Uber die Einwirkung von Stauben, speziell von Zementofenstaub auf Pflanzen. Journal of Applied Botany – Angewandte Botanik, 40, 106–120.
Das, K., Dey, U., Bhaumik, R., Datta, J. K., & Mondal, N. K. (2011). A comparative study of lichen biochemistry and air pollution status of urban, semi urban and industrial areas of Hooghly and Burdwan district, West Bengal. Journal of Stress Physiology and Biochemistry, 7(4), 311–323.
Davies, L., Bates, J. W., Bell, J. N. B., James, P. W., & Purvis, O. W. (2007). Diversity and sensitivity of epiphytes to oxides of nitrogen in London. Environmental Pollution, 146, 299–310.
Downes, J. D., Barmuta, L. A., Fairweather, P. G., Faith, D. P., Keough, M. J., Lake, P. S., Mapstone, B. D., & Quinn, G. P. (2002). Monitoring ecological impacts—concepts and practice in flowing waters. Cambridge:Cambridge University Press.
Egger, R., Schlee, D., & Turk, R. (1994). Changes of physiological and biochemical parameters in the lichen Hypogymnia physodes (L) Nyl. due to the action of air pollutants—a field study. Phyton, 34, 229–242.
EPA (2003). National air quality and emissions trends report, 2003. NC:Office of Air Quality Planning and Standards, Research Triangle Park.
EPA (2015) Portland Cement Manufacturing. http://www.epa.gov/ttnchie1/ap42/ch11/final/c11s06.pdf (last access June 2015)
Estrabou, C., Stiefkens, L., Hadid, M., Rodriguez, J. M., & Perez, A. (2004). Effects of air pollutants on morphology and reproduction in four lichen species in Cordoba, Argentina. Ecologia in Bolivia, 39(2), 33–45.
E.U. & C. (2008) DIRECTIVE 2008/50/EC OF THE EUROPEAN PARLAMENT AND OF THE COUNCIL of 21 May 2008 on ambient air quality and cleaner air for Europe. Official Journal of the European Union, 11.6.2008, L 152/1.
Farmer, A. M. (1993). The effects of dust on vegetation—a review. Environmental Pollution, 79, 63–75.
Frati, L., Caprasecca, E., Santoni, S., Gaggi, C., Guttatova, A., Gaudino, S., Pati, A., Rosamilia, S., Pirintsos, S. A., & Loppi, S. (2006). Effects of NO2 and NH3 from road traffic on epiphytic lichens. Environmental Pollution, 142, 58–64.
Frati, L., Brunialti, G., Gaudino, S., Pati, A., Rosamilia, S., & Loppi, S. (2011). Accumulation of nitrogen and changes in assimilation pigments of lichens transplanted in an agricultural area. Environmental Monitoring and Assessment, 178, 19–24.
Gahan, P. B., Ishkanes, S. T., Crevecouer, M., & Greppin, H. (1998). Calcium stimulation of glucose-6-phosphate dehydrogenase activity in shoot apices of Spinacia oleracea during floral evocation. Cell Biochemistry and Function, 16(1), 29–34.
Gallo, L., Corapi, A., Loppi, S., & Lucadamo, L. (2014). Element concentrations in the lichen Pseudevernia furfuracea (L.) Zopf transplanted around a cement factory (S Italy). Ecological Indicators, 46, 566–574.
Garty, J., Karary, Y., & Harel, J. (1993). The impact of air pollution on the integrity of cell membranes and chlorophyll in the lichen Ramalina duriaei (De Not.) Bagl. transplanted to industrial sites in Israel. Archives of Environmental Contamination and Toxicology, 24, 455–460.
Garty, J., Tomer, S., Levin, T., & Lehr, H. (2003). Lichens as biomonitors around a coal-fired power station in Israel. Environmental Research, 91, 186–198.
Gauslaa, Y., Lie, M., Asbjorn Solhaug, K., & Ohlson, M. (2006). Growth and ecophysiological acclimation of the foliose lichen Lobaria pulmonaria in forests with contrasting light climates. Oecologia, 147, 406–416.
Gilbert, O. L. (1976). An alkaline dust effect on epiphytic lichens. The Lichenologist, 8, 173–178.
Giri, S., Shrivastava, D., Deshmukh, K., & Dubey, P. (2013). Effect of air pollution on chlorophyll content of leaves. Current Agriculture Research Journal, 1(2), 93–98.
Goodwin, T.W. (1954). Carotenoids—their comparative biochemistry. New York. Chemical Publishing Co. Inc. http://archive.org/stream/carotenoidstheir00good/carotenoidstheir00good_djvu.txt. Accessed 2 September 2014
Gonzalez, C. M., & Pignata, M. L. (1997). Chemical response of the lichen Punctelia subrudecta (Nyl.) Krog transplanted close to a power station in an urban-industrial environment. Environmental Pollution, 97(3), 195–203.
Gonzalez, C. M., Orellana, L. C., Casanovas, S. S., & Pignata, M. L. (1998). Environmental conditions and chemical response of a transplanted lichen to an urban area. Journal of Environmental Management, 53, 73–81.
Halliwell, B., & Gutteridge, J. M. C. (2007). Free radicals in biology and medicine (4th ed., ). Oxford:Oxford Press University.
Hawksworth, D. L., & Rose, F. (1970). Qualitative scale for estimating sulphur dioxide air pollution in England and Wales using epiphytic lichens. Nature, 227, 145–148.
Herzig, R., & Urech, M. (1991). Flechten als Bioindikatoren Integriertes biologisches Messsystem der Luftverschmutzung fur das Schweizer. Mittelland, Bibliotheca Lichenologica, 43, 1–283.
Huang, Z. A., Jiang, D. A., Yang, Y., Sun, Y. W., & Jin, S. H. (2004). Effects of nitrogen deficiency on gas exchange, chlorophyll fluorescence, and antioxidant enzymes in leaves of rice plants. Photosynthetica, 42, 357–364.
IFC (2015) International Finance Corporation. Environmental health and safety guidelines. Glass manufacturing. http://www.ifc.org/wps/wcm/connect/384e20804885574ebc0cfe6a6515bb18/Final%2B-%2BGlass%2Bmanufacturing.pdf?MOD = AJPERES&id = 1323152002618 (accessed, 16 June, 2015)
Jensen, M. (2002). Measurement of chlorophyll fluorescence in lichens. In I. Kranner, R. P. Beckett, & A. K. Varma (Eds.), Protocols in lichenology—culturing, biochemistry, ecophysiology and use in biomonitoring (pp. 135–151). Berlin Hidelberg: Springer Verlag.
Johansson, O. (2011). Epiphytic lichen response to nitrogen deposition. Doctoral Thesis. Umea University, Department of Ecology and Environmental Sciences
Kartick, C. P., Mondal, N. K., Bhaumik, R., Banerjee, A., & Datta, J. K. (2012). Incorporation of fluoride in vegetation and associated biochemical changes due to fluoride contamination in water and soil: a comparative field study. Annals of Environmental Sciences, 6, 123–139.
Kumar, S. R., & Thambavani, S. D. (2012). Effect of cement dust deposition on physiological behaviors of some selected plant species. International Journal of Scientific and Technological Research, 1(9), 98–105.
Lai, J. C., Di Lorenzo, J. C., & Sheu, K. F. (1988). Pyruvate dehydrogenase complex is inhibited in calcium loaded cerebrocortical mitochondria. Neurochemistry Research, 13(11), 1043–1048.
Lieberman, M. A., & Marks, A. (2012). Mark’s basic medical biochemistry (4th ed., ). Baltimore:Lippincott Williams & Wilkins Publisher.
Lin, C. H., Chen, B. S., Yu, C. W., & Chiang, S. W. (2001). A water based triphenyltetrazolium chloride method for the evaluation of green plant tissue viability. Phytochemical Analysis, 12, 211–213.
Loppi, S. (2006). Licheni come bioaccumulatori di elementi in traccia: stato della ricerca in Italia. Biologia Amientale, 20(2), 69–78.
Madejon, P. (2013). Vanadium. In B. J. Alloway (Ed.), Heavy metals in soils—trace metals and metalloids in soils and their bioavalability (3rd ed., pp. 579–588). London: Springer.
Marini, L., Nascimbene, J., & Nimis, P. L. (2011). Large scale patterns of epiphytic species richness: photobiont dependent response to climate and forest structure. Science of the Total Environment, 409(20), 4381–4386.
Marques, A. P., Freitas, M. C., Wolterbeek, H. T., Steinebach, O. M., Verburg, T., & De Goeii, J. J. (2005). Cell-membrane damage and element leaching in transplanted Parmelia sulcata lichen related to ambient SO2, temperature and precipitation. Environmental Science and Technology, 39, 2624–2630.
McNulty, I. B. (1958). Effects of fluorides on basic plant processes. Progress report N.1. Salt Lake City:University of Utah.
Mihailovic, N., Drazic, G., & Vucinic, Z. (2008). Effects of aluminium on photosynthetic performance in Al-sensitive and Al-tolerant maize inbred lines. Photosynthetica, 46(3), 476–480.
Miller, G. W., Pushnik, J. C., Giannini, J., & Manwarning, J. (1984). Effects of excessive fluoride. Utah Science, 45(3), 89–95.
Minambiente (2015) Ministero dell’Ambiente, e della Tutela del Territorio e del Mare. Inquinamento Atmosferico. Qualità dell’aria. Gli Inquinanti. http://www.minambiente.it/pagina/gliinquinanti. (accessed 16 June 2016)
Munzi, S., Pisani, T., & Loppi, S. (2009). The integrity of lichen cell membrane as a suitable parameter for monitoring biological effects of acute nitrogen pollution. Ecotoxicology and Environmental Safety, 72, 2009–2012.
Nash, T. H. (1976). Sensitivity of lichens to nitrogen dioxide fumigations. Bryologist, 79, 103–106.
Nash, T. H. (2008). Lichen biology. London:Cambridge University Press.
Nimis, P.L., Bargagli, R. (1999). Linee-guida per l’utilizzo di licheni epifiti come bioac-cumulatori di metalli in traccia. In: Atti del workshop Biomonitoraggio dellaqualità dell’aria sul territorio nazionale, 26–27 Novembre 1998, Roma. ANPA, pp. 279–287, Atti 2/1999
Odum, E. P., & Barrett, G. W. (2005). Fundamentals of ecology. Belmont:Thomson Brooks/Cole.
O’Hare, G. P., & Williams, P. (1975). Some effects of sulphur dioxide flow on lichens. The Lichenologist, 7, 116–120.
Pananjay Kartikey Tiwari, G. B. G. (2008). Lichens as an indicator of air pollution: a review. Indian Journal of Air Pollution, 8(1), 8–17.
Paoli, L., Benesperi, R., Proietti Pannunzi, D., Corsini, A., & Loppi, S. (2014). Biological effects of ammonia released from a composting plant assessed with lichens. Environmental Science and Pollution Research International, 21(9), 5861–5872.
Paoli, L., Guttova, A., Grassi, A., Lackovicova, A., Senko, D., Sorbo, S., Basile, A., & Loppi, S. (2015). Ecophysiological and ultrastructural effects of dust pollution in lichens exposed around a cement plant (SW Slovakia). Environmental Science and Pollution Research. doi:10.1007/s11356-015-4807-x Published on line 06 June 2015.
Pinho, P., Theobald, M. R., Dias, T., Tang, Y. S., Cruz, C., Martins-Loucao, M. A., Maguas, C., Sutton, M., & Branquinho, C. (2012). Critical loads of nitrogen deposition and critical levels of atmospheric ammonia for semi-natural Mediterranean evergreen woodlands. Biogeosciences, 9, 1205–1215.
Pirintsos, A., Paoli, L., Loppi, S., & Kotzabasis, K. (2011). Photosynthetic performance of lichen transplants as early indicator of climatic stress along an altitudinal gradient in the arid Mediterranean area. Climatic Change, 107, 305–328.
Pisut, I., & Pisut, P. (2006). Changes in the epiphytic lichens in the surroundings of magnesite factories near Jelsava (SE Slovakia) in the period 1973–2004. Ekologia (Bratislava), 25(2), 176–187.
Richards, J., Goshaw, D., Speer, D., Holder, T. (2008). Air emissions data summary for Portland cement pyroprocessing operations firing tire-derived fuels. PCA R&D Serial No. 3050. Portland Cement Association – 5420 Old Orchard Road, Skokie, Illinois 60077–1083.
Richardson, D. H. S. (1992). Pollution monitoring with lichens. Naturalists’ handbook 19. Slough:Richmond Publishing Co. Ltd..
Riddell, J., Padgett, P. E., & Nash III, T. H. (2012). Physiological responses of lichens to factorial fumigations with nitric acid and ozone. Environmental Pollution, 170, 202–210.
Ronen, R., & Galun, M. (1984). Pigment extraction from lichens with dimethyl sulphoxide (DMSO) and estimation of chlorophyll degradation. Environmental and Experimental Botany, 24(3), 239–245.
Russanov, E., Zaporowska, H., Ivancheva, M., Kirkova, M., & Konstantinova, S. (1994). Lipid peroxidation and antioxidant enzymes in vanadate-treated rats. Comparative Biochemistry and Physiology, 107C, 415–421.
Simon, E. W. (1974). Phospholipids and plant membrane permeability. New Phytologist, 73, 377–420.
Tretiach, M., Piccotto, M., & Baruffo, L. (2007). Effects of ambient NOx on chlorophyll a fluorescence in transplanted Flavoparmelia caperata (Lichen). Environmental Science and Technology, 41, 2978–2984.
Tyler, G. (1989). Uptake, retention and toxicity of heavy metals in lichens. A brief review. Water, Air, and Soil Pollution, 47, 321–333.
UN ECE (1992) Critical levels of air pollutants for Europe. Background Papers Prepared for UN ECE. Workshop on critical levels in Egham (U.K.), 23–26 March 1992. Air Quality Division, Department of the Environment. London (U.K.) 209 pp
Walker, C. H., Sibly, R. M., Hopkin, S. P., & Peakall, D. B. (2006). Principles of ecotoxicology. Boca Raton:CRC Press – Taylor and Francis Group.
Wallis, W. J., Miller, G. W., Psenak, M., & Bellingham, J. S. (1974). Fluoride effects on chlorophyll biosynthesis. Fluoride, 7(2), 69–77.
Wellburn, A. R. (1994). The spectral determination of chlorophyll a and chlorophyll b, as well as total carotenoids, using various solvents with spectrophotometers of different resolutions. Journal of Plant Physiology, 144(3), 307–313.
Williamson, B. J., Purvis, O. W., Mikhailova, I. N., Spiro, B., & Udachin, V. (2008). The lichen transplant methodology in the source apportionment of metal deposition around a copper smelter in the former mining town of Karabash, Russia. Environmental Monitoring and Assessment, 141(1–3), 227–236.
Wittman, H., & Turk, R. (1988). Immissionsokologischer Untersuchungen uber den epiphytischen Fiechtenbewuchs in der Umbebung des Magnesitwerkes in Hochfilzen (Tirol/Osterreich). Central Ges Fortwesen, 105, 35–45.
Wolseley, P. A., James, P. W., Theobold, M. R., & Sutton, M. A. (2006). Detecting changes in epiphytic lichen communities at sites affected by atmospheric ammonia from agricultural sources. The Lichenologist, 38(2), 161–176.
Wolterbeek, H. T., Garty, J., Reis, M. A., & Freitas, M. C. (2003). Biomonitors in use: lichens and metal air pollution. In B. A. Market, A. M. Breure, & H. G. Zechmeister (Eds.), Bioindicators and biomonitors—principles, concepts and applications (pp. 377–419). Oxford: Elsevier Science.
Zaharopoulou, A., Lanaras, T., & Arianoutsou, M. (1993). Influence of dust from a limestone quarry on chlorophyll degradation of the lichen Physcia adscendens (Fr.) Oliv. Bulletin of Environmental Contamination and Toxicology, 50, 852–855.
Zhu, Z., Gerendas, J., Bendixen, R., Schinner, K., Tabrizi, H., Sattelmacher, B., & Hansen, U. P. (2000). Different tolerance to light stress in NO3 − and NH4 + grown Phaseolus vulgaris L. Plant Biology, 2, 558–570.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lucadamo, L., Corapi, A., Loppi, S. et al. Spatial variation of eco-physiological parameters in the lichen Pseudevernia furfuracea transplanted in an area surrounding a cement plant (S Italy). Environ Monit Assess 187, 500 (2015). https://doi.org/10.1007/s10661-015-4712-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10661-015-4712-2