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INDIGENOUS AND CULTIVATED PLANTS AS BIOINDICATORS Leonard H. Weinstein John A. Laurence Boyce Thompson Institute Ithaca, NY 14853 ABSTRACT In most geographical regions, indigenous or cultivated species of plants are present for use as indicators of pollution from ozone, sulfur dioxide, hydrogen fluoride, hydrochloric acid, chlorine, and other phytotoxicants. Where they do not occur, portable "gardens" or lichen "boards" can be distributed in appropriate areas, or gardens can be planted in situ Careful selection of indicator species can not only identify the pollutant or pollutant mixture, but can provide approximate estimates of geographic distribution, source strength, pollutant dose, and can aid in locating particular sources. A useful adjunct is measurement of pollutant accumulation by chemical analyses, especially for metals and fluoride. Evaluations are made by: (a) Studies of species depletion, such as lichen deserts. (b) specific types of foliar lesions and field distribution of sensitive species. Plant bioindicators are low in cost and maintenance, and are applicable to urban and rural areas, to wide geographical areas, and to remote areas where electrical power is unavailable. INTRODUCTION Plant bioindicators or biomonitors are living entities that respond, usually at the organismal level, in characteristic and reliable ways to physical or chemical factors in their environment. The occurrence, distribution, vigor, and appearance of indigenous or cultivated plants, or their capacity to accumulate toxicants, have been used for more than 75 years to detect the presence and amount of airborne pollutants (44~. Plants range in sensitivity to airborne pollutants from highly sensitive to highly tolerant. Often there is significant range in sensitivity between cultivars of the same species. In ecosystems, plants are often the most susceptible receptors of toxicants, and their response, whether in the production of foliar lesions, change in form, or altered metabolism, may be more easily measured than chemical or physical detection of pollutants. Generally, by the response of one or more bioindicators/biomonitors can help to identify ecological problems, to document changes and trends in the general quality of forest ecosystems, and to predict effects on wildlife habitats. Specifically, they have been used to (i) establish the presence of a pollutant, (ii) aid in its identification, (iii) relate dose of the pollutant to response of the receptor, (iv) delineate the spatial and temporal distribution of the pollutant, and (v) measure pollutant accumulation (gases, particles, heavy metals, etc.~. Since the general methods of using plant receptors were first introduced, many different approaches have been used for each type or species and 195

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196 many of these will be reviewed briefly. The minor differences in the methods used to biomonitor forest, agricultural, or urban ecosystems, will not be discussed. Plant bioindicators can be compared to the use of litmus paper to indicate that a substance is acidic. However, little quantitative information, except perhaps the identity of the toxicant through the production of specific symptoms, is provided. Plant biomonitors, on the other hand, may provide a quantitative estimate of the amount of a toxicant accumulated by a selected species, as a pH electrode quantitates acidity. Under appropriate conditions, biomonitors can substitute for instruments, and they have the advantage that, unlike instruments, they integrate the effects of the toxicants over a range of environments (20, 2S, 39, 52~. Thus, in this context, they are biointegrators, expressing the biological effect of a dose of pollutant and integrating climatic, cultural, and other biological factors into their response. In some cases, bioindicators and biomonitors may substitute for mechanical collectors or analytical instruments, especially where access to utilities is limited. In addition, biomonitoring programs may be less costly than physical or chemical systems. In other cases, however, the use of receptor organisms may be preferred, since they are "tuned" to the ecosystem and will respond to climatic changes taking place. The State of Maryland has chosen to include plant biomonitoring, by assessing foliar fluoride concentration, in its standard to evaluate effects of fluorides on plants. GENERAL CONSIDERATIONS To an ecologist, a bioindicator is a species of plant or animal that responds characteristically to the conditions that occur in a particular region or habitat (31~. In air pollution studies, it is used to define a plant which exhibits a specific symptomology when exposed to a phytotoxicant (14, 15~. The useful bioindicator is a plant that is (a) genetically uniform to minimize natural variability (14, 15~; (b) sensitive to a specific pollutant by producing a characteristic and easily recognizable symptom; (c) abundant and with a large geographical distribution (13~; (~) capable of growth throughout the field season (19~; and (e) capable of absorbing a pollutant in a predictable manner if it is to be used as a measure of accumulation (14, 15, 17~. Selection of Plant Materials Lists of plant species exhibiting varying degrees of sensitivity to air pollution have been catalogued (3, 4, 5, 7, 14, 15, 24, 25, 26, 29, 34, 49, 50, 51, 54, 55~. In general, those sensitive species with the widest distribution in an area of concern are the preferred bioindicators (12~. If the purpose of a survey is to determine a simple "yes" or "no" answer that one or more pollutants are causing a problem, all sensitive vegetation should be inspected regardless of species. If the purpose of the survey is to provide information for mapping, for example, based upon the degree of injury observed, a single, widely distributed species should be used. Often, lower forms of plant life are employed, including mosses and lichens. These lower forms may not only be widely distributed but they may also have other attributes, such as extreme sensitivity to the pollutantts), e.g., lichens and sulfur dioxide ant! fluoride. One major drawback to the use of lichens is that they are very slow-growing and severe damage or destruction can eliminate them from an ecosystem. But the absence of lichens in a particular area is also valuable information, and the lichen "deserts" in cities and around certain industrial sources are well known (27, 2S, 41~. If there are no sensitive indigenous species present, surrogate

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197 species may be introduced at selected sites. Where a single pollutant is known or suspected to be responsible for an ecological problem, only a single species may be needed. Where the problem might be caused by more than one pollutant, an array of species is selected and distributed in key sites. Indicator Species Indicator plant species may be used to detect and evaluate all important ecotoxicants by exhibiting extreme sensitivity, e.g., the production of characteristic symptoms in the form of necrotic or chlorotic lesions, distortion of plant growth or other changes in form, alterations in pigment development, or the capacity for accumulation. It is rare that the indigenous or cultivated species in an area do not include some suitable bioindicators in agricultural or forest ecosystems. It is often possible to use a dominant crop or tree species as the principal bioindicator. For example, white pine shows great sensitivity to ozone and sulfur dioxide, and the symptoms are different (23~. In Ontario, silver maple is used as a biomonitor through accumulation of airborne fluoride, where measured values above a given concentration in the foliage indicate a polluted condition. If one or more native species are not available, introduced species may be used. Outstanding examples are the use of gladiolus plants as an indicator of fluoride pollution (54, 55), or of Bel-W3 tobacco (21, 22) and Japanese morning glory as indicators of photochemical oxidant pollution (32, 38~. Many species of mosses and lichens are used to evaluate air purity (16, IS, 33, 35, 36, 37, 42, 43, 48) or accumulation of heavy metals (11, 41~. White ash, wild cherry, yellow poplar, and many other deciduous trees are sensitive to ozone; birch, beech, catalpa, and many maples are examples of trees sensitive to sulfur dioxide; most pines, boxelder, apricot, peach, and many other deciduous and coniferous tree species are sensitive to fluoride. Goldenrods, a widely distributed indigenous weed, are excellent accumulators of PCBs (10~. Kinds of Symptoms The most common characteristic of an indicator species is the production of foliar lesions in response to a given pollutant. Measurements of injury can be very simple, e.g., injured vs. non-injured, or more complex, e.g., assignment of subjective or objective numerical values to denote severity. Additional variables used to assess the effects of pollutants have included percentage of leaves injured, percentage of leaf area injured, growth in length, fresh mass, dry mass, photosynthesis, respiration, transpiration, or chlorophyll content (19, 40~. Plants are also used as accumulators of specific toxicants and many of these systems are in use throughout the world to measure fluorine, sulfur, heavy metals, PCBs, etc. (17, 19, 30, 40, 41~. The presence or absence of certain characteristic traits or diseases can also be used. For example, the relative abundance of tarspot of maple (6) or blackspot of rose (45), both diseases caused by fungi, have been used to judge air quality. Field Monitoring Systems Several field biomonitoring systems have been developed and deployed. Several are described below. Indicator Gardens - Perhaps the simplest system is the indicator garden, consisting of species of plants that respond differentially to pollutants (3, 14, 15, 40, 53~. Such a

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198 bioindicator garden is in use in Minnesota to monitor sulfur dioxide and ozone concentrations ( 1 ) (Fig. 1~. Indicator gardens are grown in indigenous soil or in a soil mixture of known composition and they utilize species of known and defined sensitivity. For instance, genetic isolines of tobacco, which differ in their sensitivity to ozone, have been used. By comparing the slopes of injury (size of foliar lesions) vs. time curves for line Bel-W3 (sensitive) to line Bel-B (tolerant), air quality can be categorized as poor, moderate, fair, or good (15~. Ouaking Aspen . 1.4 m- .3 m- 1~1 _1 1 I I 1 1 ~ 1 1 1 1~ =~ .112131Bl2ll all I I AItelte-Vernal / ~ 1 Ragweed 2 Batchelore Buttons 3Milkweed E cat u) ~ Transportable Trays Replaced 8011 Figure 1. Bioindicator plot design used in Minnesota to monitor ozone and sulfur dioxide. Portable Exposure Benches- , , Often locations where bioindicators are used are isolated, maintenance Watering, weeding, fertilizing, etc.) becomes a concern. This problem is partly solved by the use of special growth benches (2, 3~. These benches not only support potted indicator plants above the ground for protection from animals, but also provide an automatic watering system (Fig. 2~. Exposure benches are used extensively in Europe for supporting indicator trees or other sensitive species. Lichen Transplants- Disks of corticolous lichen thalli with their bark substrate have been transplanted from areas of clean air to trees growing in polluted air (S. 9~. A more successful system, where lichen disks are placed in holes in boards and mounted on posts, is in use in Germany. Lichens may also be transplanted to small blocks of wood that are attached to the vanes of an anemometer, thus insuring continuous exposure of the lichen

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199 transplant to the prevailing winds (3, 41, 47~. One disadvantage of using lichens is that they respond slowly to changes in air quality and seldom recover once damaged severely. _1 - ! 14q~ ~5 ne'" ,,, it, At, an,; .~ , \,, - . I, /1~/' ,=7~,, l I ~ ,,, ~ To, do ,' At' Few ~ ~ Ad, ~1 Figure 2. Exposure bench for multiple bioindicator plants, supported by a galvanized steel frame and with automatic watering. The water reservoir, Styrofoam support, and potted plant are shown. Source: Resprinted with permission of Staub-Reinh from Luft 1985. Copyright 1985 by Staub- Reinh.

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200 Grass Cultures- Standard methods have been devised for determinating the accumulation of several air pollutants over short- and long-term periods using ryegrass cultures (3, 46) (Fig. 3~. The methods are primarily used in Germany for monitoring fluoride, sulfur, chloride, lead, cadmium, zinc, copper, nickel, vanadium, and other elements. In general, the cultures consist of seedlings of ryegrass growing in a defined medium, provided with a water supply, and mounted above the ground. By removing samples at specific intervals for elemental analysis, the rate of uptake, geographical distribution, and total accumulation of toxicant can be determined. 5 Figure 3. Self-watering grass culture containers for biomonitoring of heavy metals, fluoride, etc. Left: (1) standard soil mix, (2) ceramic cylinder, (3) filter plate, (4) wick, (5) water reservoir, (6) overflow hole, (7) double-walled container, (~) connector flange. Right: ( 1 ~ standard soil mix, (2) glass fiber wick, (3) water reservoir, )4) overflow hole, (5) outer container, (6) connector flange.

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201 Conclusions - Biomonitor systems can be attractive alternatives to the usual physical-chemical methods for detecting and measuring air pollutants. The success of biomonitor programs is dependent on the geographic area where they are used, and the amount of research devoted to developing and calibrating the system. Biomonitors have some advantages over more traditional monitoring systems. They are biointegrators, expressing the biological effects of the dose of pollutant. They are generally low cost and low maintenance systems, applicable to urban and rural areas, to wide geographical areas, and to remote forest ecosystems. They are, perhaps, the best early warning systems available. REFERENCES 2. 3. 5. Anonymous. 1984. Development of a Biological Air Quality Indexing System. A Report to the Minnesota Air Quality Board. 380 pp. St. Paul, MN 55101. Arndt, U., Erhardt, W., Keitel, A., Michenfelder, K., Nobel, W., and C. Schluter. 1985. Standardisierte Exposition van pflanzlichen Reaktionsindikatoren. Staub-Reinh. Luft 45:481 -483. Arndt, U., Nobel, W., and B. Schweizer. 1987. Bioindikatoren. Moglichtkeiten, Grenzen und neue Erkenntnisse. 388 pp. Eugen Ulmer GmbH & Co., Stuttgart, FRG. Benedict, H.M., and W.H. Breen. 1955. The use of weeds as a means of evaluating vegetation damage caused by air pollution. Proc. Natl. Air Pollution Symp., 3rd, pp. 177- 190. Berge, H. 1973. Plants as indicators of air pollution. Toxicology 1:79-89. 6. Bevan, R.J., and G.N. Greenhalgh. 1976. Rhytissma acerinum as a biological indicator of air pollution. Environ. Pollut. 10:271 -285. Brandt, C.S., and W.W. Heck. 1968. Use of plants for pollutant identification and field monitoring. Pp. 428-443 in A.C. Stern, (ed.), Air Pollution, Vol. 1, 2nd ed. Academic Press, New York. Brodo, I.M. 1961. Transplant experiments with corticolous lichens using a new technique. Ecology 42:838-841. 9. Brodo, I.M. 1966. Lichen growth and cities: A study on Long Island, New York. Bryologist 69:427-449. 10. Buckley, E. H. 1987. PCBs in the atmosphere and their accumulation in foliage and crops. Chapter 7. Pp. 175-201 in Phytochemical Effects of Environmental Compounds, J.A. Saunders, L. Kosak-Channing, and E. Conn (eds.~. Plenum Publ. Corp. Clough, W.S. 1975. The deposition of particles on moss and grass surfaces. Atmos. Environ. 9:1113-1119. 12. Cole, G.A. 1958. Air pollution with relation to agronomic crops. III. Vegetation survey methods in air pollution studies. Agron. J. 50:553-555.

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202 13. Darley, E.F. 1960. Use of plants for air pollution monitoring. J. Air Pollut. Control Assoc. 10: 198- 199. 14. Feder, W.A. 1978. Plants as bioassay systems for monitoring atmospheric pollutants. Environ. Health Perspect. 27:139- 147. 15. Feder, W.A., and W.J. Manning. 1979. Living plants as indicators and monitors. In W.W. Heck, S.V. Krupa, and S.N. Linzon, Handbook of Methodology for the Assessment of Air Pollution Effects on Vegetation. TE-2 Agricultural Committee, Air Pollution Control Association, Pittsburgh, PA. 16. Gilbert, O.L. 1968. Bryophytes as indicators of air pollution in the Tyne Valley. New Phytol. 67:15-30. 17. Guderian, R. 1977. Air pollution: Phytotoxicity of acidic gases and its significance in air pollution control. Chapter 4 in Ecological Studies, Vol. 22, Springer-Verlag, Berlin. 18. Hawksworth, D.L., and F. Rose. 1971. Lichens as litmus for air pollution: A historical review. Int. J. Environ. Stud. 1:281-296. 19. Heck, W.W. 1966. The use of plants as indicators of air pollution. Air Water Pollut. 10:99- 111. Heck, W.W., Dunning, J.A., and I.J. Hindawi. 1966. Ozone: Nonlinear relation of dose and injury in plants. Science 151:577-578. 21. Heck, W.W., and A.S. Heagle. 1970. Measurement of photochemical air pollution with a sensitive monitoring plant. J. Air Pollut. Control Assoc. 20:97-99. 22. Heggestad, H.E., and H.A. Menser. 1962. Leaf spot-sensitive tobacco strain Bel-W3, a biological indicator of the air pollutant ozone. Phytopathol. 52:735. 23. Hepting, G.H. 1966. Air pollution impacts to some important species of pine. J. Air Pollut. Control Assoc. 16:63-65. 24. Hindawi, I.J. 1968. Injury by sulfur dioxide, hydrogen fluoride, and chlorine as observed and reflected in vegetation in the field. I. Air Pollut. Control Assoc. 1 S:307-312. 25. Jacobson, J.S. 1977. Plants as indicators of photochemical oxidants in the U.S.A. VDI-Berichte Nr. 270:191-196. 26. Jacobson, J.S., and A.C. Hill. (eds.) 1970. Recognition of Air Pollut;ion Injury to Vegetation: A Pictorial Atlas. Air Pollution Control Association, Pittsburgh, PA. 102 pp. 27. LeBlanc, F. 1969. Epiphytes and air pollution. Pp. 211-221 in Air Pollution, Proc. First European Congress on the Influence of Air Pollution on Plants and Animals, Wageningen, 1968.

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203 28. LeBlanc, F., and J. DeSloover. 1970. Relation between industrialization and the distribution and growth of epiphytic lichens and mosses in Montreal. Can. J. Bot. 48: 1485- 1496. 29. Leone, I.A., Brennan, E., and R.H. Daines. 1964. indicators. Proc. Northeast. Weed Control Conf. 18:451-457. Plant life as air pollution 30. Lihnell, D. 1969. Sulphate contents of tree leaves as an indicator of SO2 air pollution in industrial areas. Pp. 341-352 in Air Pollution. 31. Mellanby, K. 1978. Biological methods of environmental monitoring. Pp. 1-13 in J. Lenihan and W.W. Fletcher, eds. Environment and Man, Vol. 7: Measuring and Monitoring the Environment. Academic Press, New York. 32. Nakamura, H., and S. Matsunaka. 1974. Indicator plants for air pollutants. Susceptibility of morning glory to photochemical oxidants: Varietal difference and effect of environmental factors. Proc. Crop Sci. Soc. Jpn. 43:522. 33. Nash, T.H., III. 1973. Sensitivity of lichens to sulfur dioxide. Bryologist 76:333- 339. 34. Nash, T.H., III. 1976. Lichens as indicators of air pollution. Naturwiss. 63:364-367. 35. Nash, T.H., III, and E.H. Nash. 1974. Sensitivity of mosses to sulfur dioxide. Oecologia 17:257-263. 36. Nash, T.H., III, and L.L. Sigal. 1980. Sensitivity of lichens to air pollution with an emphasis on oxidant air pollutants. Pp. 117- 124 in Proc. Symp. on Effects of Air Pollutants on Mediterranean and Temperate Forest Ecosystems. June 22-27, 1980, Riverside, CA. 37. Nash, T.H., III, and L. Sigal. 1981. Ecological approaches to the use of lichenized fungi as indicators of air pollution. Chapter 25. Pp. 481 -497 in The Fungal Community. D.T. Wicklow and G.C. Carrol, eds. Marcel Decker, Inc., New York., 38. Nouchi, I., and K. Aoki. 1979. Morning glory as a photochemical oxidant indicator. Environ. Pollut. 18:289-303. 39. Oshima, R.J. 1974. A viable system of biological indicators for monitoring air pollutants. J. Air Pollut. Control Assoc. 24:576-578. 40. Posthumus, A.C. 1976. The use of higher plants as indicators for air pollution in the Netherlands. Proc. Kuopio Meeting on Plant Damages Caused by Air Pollution, Sci. Pap. Symp.,1976, pp.ll5-120. 41. Puckett, K.J. 1988. Bryophytes and lichens as monitors of metal deposition. In Assessing Air Quality With Lichens and Bryophytes. T.H. Nash III and V. Wirth, eds. Bibliographica Lichenographica. Stuttgart, FRG. Rao, D.N., and F. LeBlanc. 1965. Effect of sulfur dioxide on the lichen alga, with special reference to chlorophyll. Bryologist 69:69-75. 43. Rao, D.N., and F. LeBlanc. 1967. Influence of an iron-sintering plant on corticolous epiphytes in Wawa, Ontario. Bryologist 70:141-157.

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204 44. Ruston, A.G. 1921. The plant as an index of smoke pollution. Ann. Appl. Biol. 7:390-403. 45. Saunders, P.J.W. 1966. The toxicity of sulphur dioxide to Diplocarpon rosae Wolf causing black spot of roses. Ann. Appl. Biol. 58:103-114. 46. Scholl, G. 1971. Die Immissionsrate van Fluor in Pflanzen als Masstab fur eine Immissionsbegrenzung. VDI Berichte Nr. 164. pp. 39-45. 47. Schonbeck, H. 1969. A method for determining the biological effects of air pollution by transplanted lichens. Staub-Reinh. Luft 29:17-21. 48. Showman, R.E. 1975. Lichens as indicators of air quality around a coal-fired power generating plant. Bryologist 78:1-6. 49. Skye, E. 1979. Lichens as biological indicators of air pollution. Annul Rev. Phytopathol. 17:325-341. 50. Thomas, M.D. 1951. Gas damage to plants. Annul Rev. Plant Physiology 2:293-322. 51. Thomas, M.D. 1961. Effects of air pollution on plants. Pp. 233-278 in Air Pollution. World Health Organization Monograph Series #46. Columbia University Press, New York. 52. Treshow, M. 1965. Evaluation of vegetation injury as an air pollution criterion. J. Air Pollut. Control Assoc. 15:266-269. 53. van Raay, A. 1969. The use of indicator plants to estimate air pollution by SO2 and HF. Pp. 319-335 in Air Pollution. Proc. First European Congr. on the Influence of Air Pollution on Plants and Animals, Wageningen, 1968. 54. Weinstein, L.H. 1977. Fluoride and plant life. J. Occup. Med. 19:49-78. 55. Zimmerman, P.W., and A.E. Hitchcock. 1956. Susceptibility of plants to hydrofluoric acid and sulfur dioxide gases. Contrib. Boyce Thompson Inst. 18:263- 279.