Lichen species as element bioindicators for air pollution in the eastern United States of America
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Department of Botany, University of Wisconsin-Madison, 430 Lincoln Drive, Madison, Wisconsin 53706-1381, USA
USDA Forest Service, Portland Forestry Sciences Lab, 620 SW Main, Suite 400, Portland, Oregon 97205, USA
Publication date: 2019-12-16
Plant and Fungal Systematics 2019; 64(2): 137–147
Lichen element (N, S, metals) indicators of local air pollution load (a widely used technique) are recommended for five predefined regions covering central and southern parts of the eastern United States. The final recommendations integrate the advice of regional lichenologists, information from regional floras, and species abundance data from a United States Forest Service Forest Inventory and Analysis Program (FIA) lichen database for 11 of the 21 covered eastern states. Recommended species were frequent in their region, easy for nonspecialists to distinguish in the field after training, and easy to handle using clean protocols. Regression models of species abundance in FIA plots from five southeastern states vs. climate, air pollution (both from a regional lichen response model) and type of nearby landcover (from the National Land Cover Database) identified species’ environmental limitations. Punctelia rudecta is recommended for cooler forested uplands of all regions, with three Physcia species combined and Punctelia missouriensis for isolated woodlands or urban areas of three regions. Parmotrema hypotropum and P. hypoleucinum combined (weak environmental limitation) or P. perforatum. and P. subrigidum combined (limited in more polluted areas) are recommended for warmer Coastal Plains in two regions each. Additional species are recommended for single regions. Each species must be quantitatively evaluated in each region, to demonstrate indication reliability in practice and to calculate element data conversions between species for region-wide bioindication.
Bargagli, R. & Mikhailova, I. 2002. Accumulation of inorganic contaminants. In: Nimis, P. L., Scheidegger & C., Wolseley, P. (eds) Monitoring with Lichens – Monitoring Lichens, pp. 65–84. NATO Science Series. Kluwer Academic Publishers, The Hague, NL.
Bargagli, R. & Nimis, P. L. 2002. Guidelines for the use of epiphytic lichens as biomonitors of atmospheric deposition of trace elements. In: Nimis, P. L., Scheidegger, C. & Wolseley, P. (eds) Monitoring with Lichens – Monitoring Lichens, pp. 295–300. NATO Science Series. Kluwer Academic Publishers, The Hague, NL.
Bari, A., Rosso, A., Minciardi, M. R., Troiani, F. & Piervittori, R. 2001. Analysis of heavy metals in atmospheric particulates in relation to their bioaccumulation in explanted Pseudevernia furfuracea thalli. Environmental Monitoring and Assessment 69: 205–20.
Beeching, S. Q. 2016. Reading up for the Tuckerman Workshop. Evansia 33: 50–53.
Bennett, J. P. & Wetmore, C. M. 1999. Changes in element contents of selected lichens over 11 years in northern Minnesota, USA. Environmental and Experimental Botany 41: 75–82.
Bosserman R. W. & Hagner, J. E. 1981. Elemental composition of epiphytic lichens from Okefenokee Swamp. The Bryologist 84: 39–47.
Boquete, M. T., Fernández, J. A., Aboal, J. R. & Real, C. 2009. Spatial structure of trace elements in extensive biomonitoring surveys with terrestrial mosses. Science of the Total Environment 408: 153–162.
Brodo, I. M. 2016. Keys to lichens of North America. Revised and expanded. Yale University Press, New Haven, Connecticut, USA.
Brodo, I. M., Freebury, C. & Alfonso, N. 2013. Notes on the lichens Physcia aipolia and P. alnophila in North America. Evansia 30: 110–119.
Brodo, I. M., Sharnoff, S. D. & Sharnoff, S. 2001. Lichens of North America. Yale University Press, New Haven, Connecticut, USA.
Buck, W. R. 2016. The Tuckerman Lichen Workshop and the Crum Bryophyte Workshop: a brief history. Evansia 33: 46–49.
Cleavitt, N. L., Hinds, J. W., Poirot, R. L., Geiser, L. H., Dibble, A. C., Leon, B., Perron, R. & Pardo, L. H. 2015. Epiphytic macrolichen communities correspond to patterns of sulfur and nitrogen deposition in the northeastern United States. The Bryologist 118: 304–325.
Cleland, D. T., Freeouf, J. A., Keys, J. E., Nowacki, G. J., Carpenter, C. & McNab, W. H. 2007. Ecological Subregions: Sections and subsections for the conterminous United States. Gen. Tech. Report WO-76D [Map on CD-ROM] (A.M. Sloan, cartographer) presentation scale 1:3,500,000; colored.U.S. Department of Agriculture, Forest Service, Washington, DC. [Accessed 2 March 2019].
Consortium of North American Lichen Herbaria [CNALH]. 2019. Physcia aipolia. map search. [Accessed 7 August 2019].
Conti, M. E. & Cecchetti, G. 2001. Biological monitoring: lichens as bioindicators of air pollution assessment – a review. Environmental Pollution 114: 471–492.
Culberson, W. L. & Culberson, C. F. 1982. Evolutionary modification of ecology in a common lichen species. Systematic Botany 7: 158–169.
DeBolt, A. M., Rosentreter, R. & Martin, E. P. 2007. Macrolichen diversity in subtropical forests of north-central Florida. The Bryologist 110: 254–265.
Donovan, G. H., Jovan, S. E., Gatziolis, D., Burstyn, I., Michael, Y. L., Monleon, V. J. & Amacher, M. C. 2016. Using an epiphytic moss to identify previously unknown sources of atmospheric cadmium pollution. Science of the Total Environment 569: 84–93.
ESR1. 2018. ArcMap 10.5.1. ArcGIS desktop. [Accessed 2 March 2019].
Fenn, M. E., Baron, J. S., Allen, E. B., Rueth, H. M., Nydick, K. R., Geiser, L., Bowman, W. D., Sickman, J. O., Meixner, T., Johnson, D. W. & Neitlich, P. 2003. Ecological effects of nitrogen deposition in the western United States. BioScience 53: 404–420.
Ferry, B. W., Baddeley, M. S. & Hawksworth, D. L. 1973. Air Pollution and Lichens. University of Toronto Press, Ontario, Canada.
Garty, J. 2002. Biomonitoring heavy metal pollution with lichens. In: Kranner, I., Beckett, R. P., Varma, A. K. (eds), Protocols in Lichenology. Culturing, Biochemistry, Ecophysiology and Use in Biomonitoring, pp. 458–482. Springer-Verlag, Berlin, Germany.
Geiser, L. H. & Neitlich, P. 2007. Air pollution and climate gradients in western Oregon and Washington indicated by epiphytic macrolichens. Environmental Pollution 145: 203–218.
Glavich. D. A. & Geiser, L. 2008. Potential approaches to developing lichen-based critical loads and levels for nitrogen, sulfur and metal-containing atmospheric pollutants in North America. The Bryologist 111: 638–649.
Hale, M. E., Jr. & Lawrey, J. D. 1985. Annual rate of lead accumulation in the lichen Pseudoparmelia baltimorensis. The Bryologist 88: 5–7.
Harris, R. C. 1990. Some Florida Lichens. Published by the author, Bronx, NY, USA, 109 pp. Available from Recent Literature on Lichens [Accessed 5 April 2019].
Harris, R. C. & Ladd, D. M. 2019. Lichens of the Ozarks. Floristics and implications for biodiversity conservation. New York Botanical Garden and The Nature Conservancy, Bronx, USA [Accessed 5 April 2019].
Hill, R., Jordan, T., Beeching, S. Q., Parks, P., Drennon, C. & Walker, W. 2007. A guide to twelve common & conspicuous lichens of Georgia’s Piedmont. [plus] lichens of Georgia mountains and coastal plains. [Accessed 5 April 2019 ].
Jovan, S., Riddell, J., Padgett, P. E. & Nash III, T. H. 2012. Eutrophic lichens respond to multiple forms of N: implications for critical levels and critical loads research. Ecological Applications 22: 1910–1922.
Jovan, S., Haldeman, M., Will-Wolf, S., Dillman, K., Geiser, L., Thompson, J. & Shaw, J. 2020a. National Atlas of Epiphytic Lichens in Forested Habitats, U.S.A. Accepted manuscript in preparation for publication (as of October 2019). General Technical Report. PNW-GTR-XXX. U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station, Portland, OR, USA (in press).
Jovan, S., Will-Wolf, S., Geiser, L. & Dillman, K. 2020b. User guide for the national FIA Lichen database (beta). Accepted manuscript in preparation (as of October 2019). General Technical Report. PNW-GTR-XXX. U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station., Portland, OR, USA (in press).
Karakas, S. Y. & Tuncel, S. G. 2004. Comparison of accumulation capacities of two lichen species analyzed by instrumental neutron activation analysis. Journal of Radioanalytical and Nuclear Chemistry 259: 113–118.
Ladd, D. M. 2002. Lichens of the Lower Ozark region of Missouri and Arkansas. Missouri Ozark Forest Ecosystem Project, Missouri. Department of Conservation, Missouri Botanical Garden, Nature Conservancy, St. Louis, USA. 140 p (revision in progress).
Lawrey, J. D. 1984. Biology of Lichenized Fungi. Praeger Publishers, NY, USA. 408 pp.
Lawrey, J. D. 1985. Lichens as lead and sulfur monitors in Shenandoah National Park, Virginia. Contract CX-0001-1-0114/PX-0001-4-1128. U.S. National Park Service, Air Quality Division, Ft. Collins, CO, USA.
Lawrey, J. D. 1993: Lichens as monitors of pollutant elements at permanent sites in Maryland and Virginia. The Bryologist 96: 339–341.
Lawrey, J. D. 2011. A lichen biomonitoring program to protect resources in the National Capital Region by detecting air quality effects. Natural Resource Technical Report NPS/NCRN/NRTR—2011/450. National Park Service, Fort Collins, CO, USA. [Accessed 5 April, 2019].
Lawrey, J. D. & Hale, Jr. , M. E. 1977. Natural history of Plummers Island, Maryland. XXIII. Studies on lichen growth rate at Plummers Island, Maryland. Proceedings of the Biological Society of Washington 90: 698–725.
Lawrey, J. D. & Hale, Jr., M. E. 1979. Lichen growth response to stress induced by automobile exhaust pollution. Science 204: 423–424.
Lawrey, J. D. & Hale, Jr., M. E. 1981. Retrospective study of lichen lead accumulation in the northeastern United States. The Bryologist 84: 449–456.
Lawrey, J. D. & Hale, Jr., M. E. 1988. Lichen evidence for changes in atmospheric pollution in Shenandoah National Park, Virginia. The Bryologist 91: 21–23.
Lendemer, J. C. & Noell. N. 2018. Delmarva Lichens: An illustrated manual. Memoirs of the Torrey Botanical Society 28: 1–386.
Lendemer, J. C. & Ruiz. A. M. 2015. Molecular data confirm morphological variability in the widespread foliose lichen Canoparmelia carolinana (Parmeliaceae). Castanea 80: 29–36.
Lendemer, J. C., Harris, R. C. & Tripp, E. A. 2013. The lichens and allied fungi of Great Smoky Mountains National Park: an annotated checklist with comprehensive keys. Memoirs of the New York Botanical Garden 104: 1–152.
Lendemer, J., Allen, J. & Noell. N. 2015. The Parmotrema acid test: a look at species delineation in the P. perforatum group 40 y later. Mycologia 107: 1120–1129.
Lendemer, J. C.; Harris, R. C. & Ruiz, A. M. 2016. A review of the lichens of the Dare Regional Biodiversity Hotspot in the Mid-Atlantic Coastal Plain of North Carolina, eastern North America. Castanea 81: 1–77.
Lücking, R., Seavey, F., Common, R., Beeching, S. Q., Breuss, O., Buck, W. R., Crane, L. & Hodges, M. et al. 2011. The lichens of Fakahatchee Strand Preserve State Park, Florida: Proceedings from the 18th Tuckerman Workshop. Bulletin of the Florida Museum of Natural History 49: 127–186.
McCune, B., Dey, J. P., Peck, J. E., Heiman, K. & Will-Wolf, S. 1997. Regional gradients in lichen communities of the Southeast United States. The Bryologist 100: 145–158.
McCune, B. & Mefford, M. J. 2019. PC-ORDv6.22. Multivariate analysis of ecological data. Version 6. Wild Blueberry Media LLC, Corvallis, OR. https://www.wildblueberrymedia... [Accessed 5 April 2019].
McCune, B., Arup, U., Breuss, O., Di Meglio. E., Di Meglio, J., Esslinger, T. L., Magain, N., Miadlikowska, J., Miller, A. E., Muggia, L., Nelson, P. R., Rosentreter, R., Schultz, M., Sheard, J. W., Tønsberg, T. & Walton, J. 2018. Biodiversity and ecology of lichens of Katmai and Lake Clark National Parks and Preserves, Alaska. Mycosphere 9: 859–930.
McNab, W. H., Cleland, D. T., Freeouf, J. A., Keys, Jr., J. E., Nowacki, G. J., Carpenter, C. A., compilers. 2007. Description of ecological subregions: sections of the conterminous United States [CD-ROM]. Gen. Tech. Report WO-76B. U.S. Department of Agriculture, Forest Service, Washington, DC, USA. 80 p. [Accessed 2 March, 2019].
Multi-Resolution Land characteristics Consortium [MRLC]. 2019. National Land Cover Database 2011 (NLCD2011). [Accessed 28 March, 2019].
Olmez, I., Gulovali, M. C. & Gordon, G. E. 1985. Trace element concentrations in lichens near a coal-fired power plant. Atmospheric Environment 19: 1663–1669.
New York Botanical Garden [NYBG]. 2019. C. V. Starr Virtual Herbarium. [Accessed 5 April, 2019].
Paoli, L., Guttová, A., Grassi, A., Lackovicová, A., Senko, D. & Loppi, S. 2014. Biological effects of airborne pollutants released during cement production assessed with lichens (SW Slovakia). Ecological Indicators 40: 127–135.
Peck, J. E., Grabner, J., Ladd, D. & Larsen, D. R. 2004. Microhabitat affinities of Missouri Ozarks lichens. The Bryologist 107: 47–61.
Puckett, K. J. 1988. Bryophytes and lichens as monitors of metal deposition. Bibliotheca Lichenologica 30: 231–267.
Pyatt, F. B., Grattan, J. P., Lacy, D., Pyatt, A. J. & Seaward, M. R. D. 1999. Comparative effectiveness of Tillandsia usneoides L. and Parmotrema praesorediosum (Nyl.) Hale as bio-indicators of atmospheric pollution in Louisiana (U.S.A.). Water, Air, and Soil Pollution 111: 317–326.
Root, H. T., Geiser, L. H., Jovan, S. & Neitlich, P. 2015. Epiphytic macrolichen indication of air quality and climate in interior forested mountains of the Pacific Northwest, USA. Ecological Indicators 53: 95–105.
Rosentreter, R., Eldridge, D., Westberg, M., Briegel-Williams, L. & Grube, M. 2016. Structure, Composition, and Function of Biocrust Lichen Communities. In Weber, B., Büdel, B., Belnap, J. (eds). Biological Soil Crusts: An Organizing Principle in Drylands, Ch 7, pp. 121–138. Springer, Berlin, Germany.
Schutte, J. A. 1977. Chromium in two corticolous lichens from Ohio and West Virginia. The Bryologist 80: 279–283.
Seabrook, C. 2018. A close-up look at lichens can reveal a miniature world. [Features Malcolm Hodges, a collaborator on the Georgia Lichen Project]. Atlanta Journal-Constitution/Life. May 11, 2018. [Accessed 5 April 2019].
Showman, R. E. & Hendricks, J. C. 1989. Trace element content of Flavoparmelia caperata (L.) Hale due to industrial emissions. Journal of Air and Waste Management Association [JAPCA] 39: 317–320.
Sloof, J. E. & Wolterbeek, B, T. 1993. Interspecies comparison of lichens as biomonitors of trace-element air pollution. Environmental Monitoring and Assessment 25: 149–157.
SPSS. 2015. IBM SPSS Statistics. Version 23.0.0. 1989–2015.
United States Department of Agriculture, Forest Service [USDA FS]. 2017. Field guides for standard (phase 2) measurements. Phase 2 measurement field guide, Version 7.1 (downloadable pdf). Forest Inventory and Analysis Program. FIA library. [Accessed 5 April 2019].
Walther, D. A., Ramelow, G. J., Beck, J. N., Young, J. C., Callahan, J. D. & Marcon, M. 1990. Temporal changes in metal levels of the lichens Parmotrema praesorediosum and Ramalina stenospora, southwest Louisiana. Water, Air, and Soil Pollution 53: 189–200.
Wetmore, C. M. 1983. Lichens of the air quality class 1 national parks. Final Report. National Park Service – AIR, Denver, Colorado, USA. [­Accessed 5 April 2019].
Wetmore, C. 1992. Lichens and Air Quality in George Washington Carver National Monument. Report submitted to National Park Service – AIR, Denver, Colorado, USA.
Wetmore, C. & Bennett, J. 1997. Lichens and Air Quality in Three Prairie Parks: Effigy Mounds National Monument – Iowa, Homestead National Monument – Nebraska, and Wilson’s Creek National Battlefield – Missouri. Report submitted to Biological Resources Division, U.S. Geological Survey, Washington, DC, USA.
Wilhelm, G. & Ladd, D. 1992. A new species of the lichen genus Punctelia from the midwestern United States. Mycotaxon 44: 495–504.
Wickham, J., Homer, C., Vogelman, J., McKerrow, A., Mueller, R., Herold, N. & Coulston, J. 2014. The Multi-Resolution Land Characteristics (MRLC) Consortium — 20 years of development and integration of USA national land cover data. Remote Sensing 6: 7424–7441.
Will-Wolf, S., Jovan, S., Neitlich, P., Peck, J. L. & Rosentreter, R. 2015a. Lichen-based Indexes evaluate responses to climate and air pollution across northeastern U.S.A. The Bryologist 118: 59–82.
Will-Wolf, S., Makholm, M. M., Nelsen, M. P. & Trest, M. T. 2015b. Element analysis of two common macrolichens supports bioindication of air pollution and lichen response in rural midwestern U.S.A. The Bryologist 118: 371–384.
Will-Wolf, S., Jovan, S. & Amacher, M. C. 2017a. Lichen elemental content bioindicators for air quality in upper Midwest, USA: a model for large-scale monitoring. Ecological Indicators 78: 253–263.
Will-Wolf, S., Jovan, S. & Amacher, M. C. 2017b. Lichen elements as environmental indicators: evaluation of methods for large monitoring programs. The Lichenologist 49: 415–424.
Will-Wolf, S., Jovan, S. & Amacher, M. C. 2018a. Lichen species to bioindicate air quality in eastern U.S. from elemental composition: lessons from the Midwest. In: Potter, K. M. & Conkling, B. L. (eds). Forest health monitoring: national status, trends, and analysis 2017, Ch. 6, pp 101–114. Gen. Tech. Rep. SRS-233. USDA Forest Service, Southern Research Station, Asheville, NC, USA. [Accessed 5 April 2019].
Will-Wolf, S., Jovan, S., Nelsen, M. P., Trest, M. T., Rolih, K. & Reis, A. 2018b. Lichen indexes assess response to climate and air quality in the Mid-Atlantic region, USA. The Bryologist 121: 461–479.
Will-Wolf, S., Jovan, S., Amacher, M. C. & Patterson, P. L. 2020. Lichen elemental indicators for air pollution in Eastern U. S. A. forests; a pilot study in the upper Midwest. Accepted manuscript in preparation for publication (as of October 2019). General Technical Report. U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station, Portland, OR, USA (in press).
Wolterbeek, B. 2002. Biomonitoring of trace element air pollution: principles, possibilities and perspectives. Environmental Pollution 120: 11–21.
Yemets, O. A., Solhaug, K. A. & Gauslaa, Y. 2014. Spatial dispersal of airborne pollutants and their effects on growth and viability of lichen transplants along a rural highway in Norway. The Lichenologist 46: 809–823.
Zschau, T., Getty, S., Gries, C., Ameron, Y., Zambrano, A. & Nash III, T. H. 2003. Historical and current atmospheric deposition to the epilithic lichen Xanthoparmelia in Maricopa County, Arizona. Environmental Pollution 125: 21–30.