BIOINDICATION
OF A S U R P L U S
TERRESTRIAL W. H. O. E R N S T ,
OF H E A V Y M E T A L S IN
ECOSYSTEMS*
J. A. C. V E R K L E I J ,
and R. V O O I J S
Biological Laboratory, The Free University, P.O. Box 7161, 1007 MC Amsterdam, The Netherlands
(Received November 1, 1982) Abstract. A survey of the methods of bioindication of heavy metals in terrestrial ecosystems and their effectiveness for predicting the consequences of environmental stress on organisms is presented. Two main inputs of heavy metals for terrestrial ecosystems have been considered: airborne and soil-borne. Airborne metals can be monitored due to physical adsorption on plant surfaces or due to chemical exchange processes in cell walls. Active biomonitoring widely uses both aspects, however, without predictive values. Meaningful bioindication of soilborne heavy metals can only be achieved by passive monitoring. Due to the different functions of heavy metals in organisms - micronutrients and trace elements - the knowledge of natural background values is important, considering the qualitative aspects of metals in the soil. In exceptional situations morphological and anatomical changes of plant organs will facilitate bioindication; in every case chemical analysis of the concentration of heavy metals is an essential part of the monitoring program. A long-term exposure of organisms to heavy metals will influence the genetic structure of populations. Therefore measurement of heavy metal tolerance of plants has to be a standard procedure in monitoring programs.
1. Introduction
Bioindication of heavy metals has a more than two thousand years' old tradition, already used by Greek and Roman ore prospectors (Ernst, 1974). Nowadays the meaning of bioindication is mostly restricted to the indication of emission sources and pollution hazard (Steubing and Jager, 1982). Input of heavy metals to the environment by human activities can occur via air, soil and water: local dustfall around smelter complexes (Ernst, 1972; Joosse and Van Vliet, 1981) and power stations (Folkeson, 1981), regional use of sewage sludge, copper-rich pig manure (de Haan, 1975; Lexmond et aL, 1982), metal based pesticides (Hirst et aL, 1961) and the global dissemination of heavy metals by traffic (Nriagu, 1978). Heavy metals have different functions in biological systems: Fe, Mn, Cu, and Zn as micronutrients in all organisms, Mo, Ni, V, and Co in some groups of organisms. Besides some uncertainties for Cd and As, all other heavy metals occur as trace elements in every organism without any functional necessity. Due to the different functions of heavy metals in biota it is not useful to discriminate between biomonitoring as a quantitative method and bioindication as a qualitative method (Posthumus and Tonneijck, 1982). The only realistic contrast is that of sensitive and resistant organisms. * Paper presented at a Symposium held on 14 and 15 October 1982, in Utrecht, The Netherlands. Environmental Monitoring and Assessment 3 (1983) 297-305. 9 1983 by D. Reidel Publishing Company.
0167-6369/83/0033--.0297501.35.
298
W.H.O.
E R N S T ET AL.
The aim of this contribution is to elaborate the evidence of effectiveness of biological indication of a surplus of heavy metals. 2. Material and Methods
For the aspect of biomonitoring atmospheric metal fallout, plant material has been collected and digested without washing. For monitoring of soil pollution by plants, fresh plant material has been washed twice with demineralized water, dried at 80 ~ and digested with strong inorganic acids (HNO3/HCIO4 7:1). All analyses of heavy metals were carried out by atomic absorption spectrometry. The sampling localities and data as well as the number of analyzed samples are given in the relevant figures and tables. For measuring the metal tolerance of grasses the rooting technique has been applied in a modified form (Ernst, 1982a).
3. Results and Discussion
3. I.
B A C K G R O U N D VALUES OF HEAVY METALS IN PLANTS
Due to the different functions of heavy metals in organisms and to the different metal contents in various geological formations the natural background and/or threshold has to be considered in every bioindication. Plant species with a high metal demand, i.e. that I0.
P*-0.95 5"
1
2
3
~
5
"6 ..~
6
O.295 + 0.063
J
03
0.2
0.3
0,~
05
06
Q
083
I Fig. 1.
2
3
4
5
6 rnrnolMekg-i
The variation in the concentration ofFe, Mn, and Zn in the leaves ofPopulus balsamifera s on a sandy sea clay in North Holland. The leaves have been collected in October 1982.
growing
B I O I N D I C A T I O N O F A S U R P L U S O F H E A V Y M E T A L S IN T E R R E S T R I A L E C O S Y S T E M S
299
of Zn by birch, willow and poplar will indicate less precisely a metal pollution (Denaeyer-De Smet, 1970) than those species with a low demand. Despite this drawback Populus nigra has been proposed for national monitoring programs of heavy metals (Knabe, 1982). Due to the tremendous variation between individuals of one population (Figure 1), sampling of very small numbers of individuals will not give a realistic picture of the effects of pollutants on populations. There is also a time dependent effect. In the case of a smelter pollution the difference between a short (14 days) exposure of standardized Lolium multiflorum (MAGS, 1977) and a long-term exposure of wild plants has been quite obvious (Figure 2). It demonstrates the drawback of active biomonitoring of heavy metal pollution. mrnol Zn kg-l dry wt. 40O ~
Aosculus hip.p_oc_ ostonurn
200.
I00
rg~"
,~ Loliurn I.'.':..- ~.~.~ ~ J3OOrn W " .:~.~a".....1375 m E ",970" ~972 1974 '
Fig. 2. Effects of Zn fallout from a Zn smelter on the Zn concentration of the leaves of Aesculus hippocastanumL. in the autumn of everyyear and Zn concentrationofLolium multiflorumLamk., as the mean of 14 days exposure during the vegetation period (after Ernst, 1980). In monitoring soil-borne heavy metal pollution a further complication is the interaction of heavy metals with other nutrients and especially with the soil organic matter. The speciation of a heavy metal influences the uptake by plants and its translocation from root to shoot (Figure 3). Generally, heavy metals are less taken up if they are complexed in comparison to those in ionic status (Marquenie-van der Werffet al., 1981). 3.2. BIOINDICATION BY PHYSICAL PROCESSES AT THE PLANT SURFACES Wet and dry deposition of heavy metals via rain or dustfall, which can increase to 6.7 kg Zn, 4.5 kg Fe, and 0.4 kg Cu per ha per year in The Netherlands (CBS, 1981), can be fixed by plant organs with sufficient rough and/or hairy surfaces (Ernst, 1982b). The same holds for the bark of trees with a slow turnover rate (Ernst, 1983a). Bioindication by analysing the dry and wet deposition can help to detect emission sources but it will not allow a prediction of biological consequences of such pollution.
300
W. H. O. ERNST ET AL. mrnot Fe kg -t 10-
o 11
50.
FA
FA/HA 3.'t
FA/HA 1:3
HA
100-
150"
200-
Fig. 3. The uptake and translocation of iron by Holcus lanatus. The Fe has been supplied in different chemical forms: ionic and complexed by humic and fulvic acids in various ratios (after I. Riphagen, unpubl.).
3.3.
B I O I N D I C A T I O N BY C H E M I C A L E X C H A N G E P R O C E S S E S IN T H E CELL W A L L
Often bryophytes and lichens have been used as bioindicators of heavy metals (Folkeson, 1981). Due to the high cation exchange capacity of the cryptogamic cell walls H § -ions and other monovalent ions can be exchanged by heavy metal ions. Species specific affinities to heavy metals demands an interspecific calibration (Folkeson, 1979). Passive biomonitoring as well as active biomonitoring by exposition of Sphagnum bags (Goodman and Roberts, 1971) or Hypogymnia physodes transplants (Sch6nbeck, 1969) will help in localizing emission sources, but not in predicting biological effects. A replacement of these systems by the exposition of bags with ion exchange resins may be considered. 3.4. BIOINDICATION BY PHYSIOLOGICALPROCESSES ON SHORT-TERM The first reaction of sessile organism to environmental stress will be a change in physiological processes in such a way that the metabolism tries to regain the physiological equilibrium. Changes in enzymatic activities can be used in connection with heavy metal analysis for biomonitoring, if many conditioning factors will appropriately be taken into account (Ernst, 1980). If this compensating reaction to stress remains insufficient, then more serious changes in the physiology of an organism will facilitate biomonitoring. In such situations physiological changes can cause visual symptoms, such as chlorosis, necrosis, dwarfism and other teratogenic aspects. These symptoms alone, however, are not typical for heavy metal stress. Generally, metal-stressed plants with chlorotic leaves have higher metal concentrations than those with green leaves, as demonstrated for Agrostis tenuis in various
B I O I N D I C A T I O N O F A S U R P L U S O F HEAVY M E T A L S IN T E R R E S T R I A L E C O S Y S T E M S
301
tJmol 1-1 dr. wt.
,~ tO0.
t,
~ 1o. Zn
g
1
w 300
500 700 d~stonce to the smelter
900 m
Fig. 4. The concentration of Z n and Pb in green (filled dots) and chlorotic (open dots) leaves of Agrostis tenuis Sibth in relation to the distance from a Zn smelter in Brabant/The Netherlands (after J. Faber, unpublished).
distances to a Zn smelter in The Netherlands (Figure 4). Owing to a disturbed photosynthesis a reduced production of propagules will affect the stability of the population and can contribute to changes in the vegetation pattern as long-term effect. Necrosis can also indicate a surplus of heavy metals. As in the case of chlorosis, the concentrations of heavy metal(s) in the necrotic leaves is higher than in green ones (Table I). The long-term effects are the same as those mentioned for chlorosis. Even
TABLE I Z n concentrations (mmol k g - ~ dry weight) in leaves and roots of sugar beet, Beta vulgaris L. var. altissima D61l, on fields which have partially been flooded in spring by heavy metal rich sediments from river Innerste at Langelsheim F.R.G. The heavy metals in the river bed are remnants of mining activities in the Hartz mountains during the last centuries (Ernst, 1974, Ernst, unpubl.) Green plants contaminated plants leaves roots uncontaminated plants leaves roots
573 • 58 2290 • 107
120 _+ 17 150 + 12
Chlorotic plants
1450 • 72 3050 • 205
302
w.H.o.
ERNST ET AL.
without chlorosis and necrosis metabolic disturbances diminish growth. Dwarfism is a well-known reaction of plants to a lot of environmental stress such as SO2, phosphorus deficiency, and also metal toxicity (Ernst, 1982b). Further evidence of diminished growth by metal stress has been demonstrated in the vicinity of a Zn smelter, where the needles of coniferous trees were not only small (Figure 5), but their length was asymmetrically distributed. This dwarfism was clearly related to increased amounts of Zn in the needles (Ernst, 1982b). Using physiological parameters, biomonitoring can make valuable predictions for risk assessment (Ernst and Joosse-van Damme, 1983).
40.
~, 30"
~.. 20"
E I0-
1 tO
20
30 length of the
40 50 needle5
mm
Fig. 5. The length of second year old needles of Pinus sylvestris L. from the vicinity of a Zn smelter in Brabant (The Netherlands) in comparison to needles ofnon-poUutedpine trees. The open columns represent healthy needles, the cross-hatched columns needles from trees in the vicinity of a Zn smelter.
3.5. BIOINDICATION VIA PHYSIOLOGICAL AND GENETICAL REACTION ON THE LONG-TERM
The innate different sensitivity to high concentrations of heavy metals can vary within species and within populations. Due to the slow migration of heavy metals through the soil profile (Ernst et al., 1974) a more or less constant or increasing emission rate gives rise to an accumulation of heavy metals in the topsoil. On the long term a high metal stress causes genetic changes within populations. They are the most dramatic effects of environmental pollution (Bradshaw, 1976). However, only a small group of plant species is capable to evolve heavy metal tolerance. Important grassland species such as Lolium perenne L., Dactylis glomerata L., and Trifolium repens L. are very sensitive to a surplus of heavy metals, as already indicated by their absence on geological metal anomalies (Ernst, 1974). Plant species which are not promising for agricultural purposes such as Agrostic species, Festuca ovinaL.,
B IO IN DIC ATI ON OF A SURPLUS OF HEAVY METALS IN T E RRE ST RI A L ECOSYSTEMS
303
Anthoxanthum odoratum L. and Deschampsia cespitosa (1_,.)P.B. can evolve resistance against many heavy metals. Genetic changes in the metal tolerance of grasses and sedges can be monitored by measuring the relative root growth in control and metal containing solutions, the so-called rooting technique (Wilkins, 1978 for a re-evaluation of the technique). Due to the pattern of aerial fallout around smelters bioindication with the aid of the rooting technique can demonstrate that in the immediate vicinity of the smelter the genetic changes are the most severe ones (Figure 6). The rapidity of selection may be demonstrated in the vicinity of a Zn and Cd smelter in Northern Germany (Ernst, 1972, 1976). After coming into operation of the smelter in 1969, populations of Agrostis tenuis and A. canina (Figure 7) became within three distance to the s m e l t e r
I0-
I
I
90kin 1.0-2.0 km
10.4-1.0
km
ul q, .
-=3
0.5 Fig. 6.
1.0
1.5
2.0
tolerance index
The Zn tolerance index o f the roots ofAErostis tenuis from clones in the vicinity ( 0 - 2 km) of a Zn smelter and from clones in a control area (90 km from the smelter).
kg Zn ha -1
index of
zinc- tolerance
150,
150-
tO0
tO0.
50 J, "68
r "70
I
I
IK 50 II '72
"74
'76
"68
70
"72
"74
76
Fig. 7. The rapid evolution of Zn tolerance in Agrostis canina in 400 m distance from a Zn-Cd smelter in Datteln/FRG. The smelter started operation in 1969, first legislative restrictions of emission were given in 1972. For comparison the amounts of the fall-out is presented according to MAGS (1977).
304
w . H . o . ERNST ET AL.
years fully tolerant to Zn. The first year's emission was about 100 kg Zn ha- ~; governmental regulations had only resulted in a reduction of the emission to 50 kg Zn ha- 1 (MAGS, 1977) so that the genetic changes will be present for a long time. Animals, which are less able to evolve metal tolerance (Ireland, 1975) will suffer extremely by metal toxicity, if they are consuming metal-tolerant plants in metal-contaminated areas. Due to the dangerous aspects of resistant plant populations to the non-resistant populations of cattle and other animals the modern biomonitoring system has to look at genetic changes in plants and animals.
4. Concluding Remarks
(1) Bioindication of a contamination by heavy metals is possible. (2) Bioindication by analyzing the metal concentration on plant surfaces (wet and dry deposition) and in plants is only useful for localizing unknown emission sources. (3) Bioindication with a predictive value has to be accompanied by analyzing heavy metal concentrations of plants and metal speciation in soil, because the chemical status of heavy metals severely influences their toxicity and their long-term effects. (4) Bioindication has to regard the genetical changes in populations of plants and, as far as possible, those of animals. References Bradshaw, A. D.: 1976, 'Pollution and Evolution', in T. A. Mansfield (ed.), 'Effects of Air Pollutants on Plants', Cambridge University Press, Cambridge, pp. 135-159. CBS-Centraal Bureau voor de Statistiek: 1981, 'Preliminary Results Air Pollution, Measurements April 1979 - March 1980', Voorburg, pp. 259-160. Denayer-De Smet, S: 1970, 'Consideration sur raccumulation du zinc par les plantes poussant sur sols calaminaires. Bull. Inst. Sci. nat. Belg. 46, 11, 1-13. Ernst, W.: 1972, 'Zink- und Cadmium-Immissionen auf B6den und Pflanzen in der Umgebung einer Zinkhfitte', Ber. Deutsch. Bot. Ges. 85, 295-300. Ernst, W.: 1974, 'Schwermetallvegetation der Erde', G. Fischer Verlag, Stuttgart, 194 p. Ernst, W.: 1976, 'Physiological and Biochemical Aspects of Metal Tolerance', in T. A. Mansfield (ed.), 'Effects of Air Pollutants on Plants', Cambridge University Press, Cambridge, pp. 115-153. Ernst, W. H. O.: 1980, 'Problems of Bioindication on the Level of Individuals', in R. Schubert and J. Schuh (eds.), "Bioindikation, Martin-Luther-Universit~tt, Wiss. Beitr/ige 26 (P 10), 3-9. Ernst, W. H. O.: 1982a, 'Schwermetallpflanzen',in H. Kinzel (ed.), 'Pflanzen6kologie undMineralstoffwechsel', E. Ulmer Verlag, Stuttgart, pp. 427-506. Ernst, W. H. O.: 1982b, 'Monitoring of Air Pollutants', see L. Steubing and H.J. J/iger (eds.), pp. 121-128. Ernst, W. H. O.: 1983a, 'Bioindication of a Surplus of Heavy Metals in Terrestrial Ecosystems', in E. P. H. Best and J. Haeck (eds.), Ecologische indicatoren voor kwaliteitsbeoordeling van lucht, water, bodem, en ecosystemen, Pudoc, Wageningen (in press) (in Dutch). Ernst, W. H. O., Mathys, W., Salaske, J., and Janiesch, P.: 1974, 'Aspekte von Schwermetallbelastungen in Westfalen', Abhandl. Landesmuseum Naturkunde Miinster Wes~Calen, 36 (2), 1-30. Ernst, W. H. O. and Joosse-van Damme, E. N. G.: 1983, 'Umweltbelastung dutch Mineralstoffe', VEB G. Fischer, Jena. Folkeson, L.: 1979, 'lnterspecies Calibration of Heavy Metal Concentrations in Nine Mosses and Lichens: Applicability to Deposition Measurements', Water, Air, and Soil Pollut. 11,253-260. Folkeson, L.: 1981, 'Heavy Metal Accumulation in the Moss Pleurozium in the Surroundings of Two Peat-Fired Power Plants in Finland', Ann. Bot. Fenn. 18, 245-253.
BIOINDICATION OF A SURPLUS OF HEAVYMETALS IN TERRESTRIAL ECOSYSTEMS
305
Goodman, G. T. and Roberts, T. M.: 1971, 'Plants and Soil as Indicators of Metal in the Air', Nature (Lond.) 231,287-292. Haan, S. de: 1975, 'Die chemische Zusammensetzung von Gewachsen auf mit Klarschlamm behandelten B6den', Landw. Forsch. 31/1,220-233. Hirst, J. M., Le Riche, H. H., and Larscomb, C. L.: 1961, 'Copper Accumulation in the Soils of Apple Orchards Near Wisbeck', Plant Pathol. 10, 105-108. Ireland, M. P.: 1975, 'Metal Content of Dendrobeana rubida (Oligochaeta) in a Base Metal Mining Area', Oikos 26, 74-79. Joosse, E. N. G. and Van Vliet, L. H. H.: 1982, 'Impact of Blastfurnace Plant Emissions in a Dune Ecosystem. Bull. Environ. Contamin. Toxicol. 29: 279-284. Knabe, W.: 1982, 'Monitoring of Air Pollutants by Wild Life Plants and Plant Exposure: Suitable Bioindicators for Different Immissions Types', see L. Steubing and H. J. J~ger (eds.). Lexmond, T. M., van Riemsdijk, W. H., and de Haan, F. A. M.: 1982, 'Research of Phosphate and Copper in the Soil, in Particular in Areas with Intensive Animal Husbandry',Bodembescherming7, Staatsdrukkerij, Den Haag (in Dutch). MAGS-Ministerium f'tirArbeit, Gesundheit und Soziales des Landes Nordrhein-Westfalen: 1977, 'Umweltbelastung im Raum Datteln. Analyse und ProblemlSsung', Dtisseldorf, 55 p. Marquenie-van der Werff, M., Ernst, W. H. O., and Faber, J.: 1981, 'Complexing Agents in Soil Organic Matter as Factors in Heavy Metal Toxicity in Plants', Int. Conference 'Heavy Metals in the Environment, Amsterdam 1981', CEP Consultants, Edinburgh pp. 222-225. Nriagu, J. O. (ed.): 1978, 'The Biogeochemistry of Lead in the Environment', Elsevier/North Holland Biomedical Press, Amsterdam, New York, Oxford. Posthumus, A. C. and Tonneijck, A. E. G.: 1982, 'Monitoring of Effects of Photo-oxidants on Plants', see L. Steubing and H. J. J~iger (eds.) pp. 115-119. Sch~nbeck, H.: 1969, 'Eine Methode zur Erfassung der biologischen Wirkung von Luftverunreinigungen durch transplantierte Flechten', Staub-Reinhaltung der Luft 29, 14-18. Steubing, L. and J~iger, H. J. (eds.): 1982, Monitoring of Air Pollutants by Plants. Methods and Problems, W. Junk Publishers, The Hague, Boston, London. Wilkins, D. A.: 1978, 'The Measurement of Tolerance to Edaphic Factors by Means of Root Growth', New Phytol. 80, 623-633.
OF A S U R P L U S
TERRESTRIAL W. H. O. E R N S T ,
OF H E A V Y M E T A L S IN
ECOSYSTEMS*
J. A. C. V E R K L E I J ,
and R. V O O I J S
Biological Laboratory, The Free University, P.O. Box 7161, 1007 MC Amsterdam, The Netherlands
(Received November 1, 1982) Abstract. A survey of the methods of bioindication of heavy metals in terrestrial ecosystems and their effectiveness for predicting the consequences of environmental stress on organisms is presented. Two main inputs of heavy metals for terrestrial ecosystems have been considered: airborne and soil-borne. Airborne metals can be monitored due to physical adsorption on plant surfaces or due to chemical exchange processes in cell walls. Active biomonitoring widely uses both aspects, however, without predictive values. Meaningful bioindication of soilborne heavy metals can only be achieved by passive monitoring. Due to the different functions of heavy metals in organisms - micronutrients and trace elements - the knowledge of natural background values is important, considering the qualitative aspects of metals in the soil. In exceptional situations morphological and anatomical changes of plant organs will facilitate bioindication; in every case chemical analysis of the concentration of heavy metals is an essential part of the monitoring program. A long-term exposure of organisms to heavy metals will influence the genetic structure of populations. Therefore measurement of heavy metal tolerance of plants has to be a standard procedure in monitoring programs.
1. Introduction
Bioindication of heavy metals has a more than two thousand years' old tradition, already used by Greek and Roman ore prospectors (Ernst, 1974). Nowadays the meaning of bioindication is mostly restricted to the indication of emission sources and pollution hazard (Steubing and Jager, 1982). Input of heavy metals to the environment by human activities can occur via air, soil and water: local dustfall around smelter complexes (Ernst, 1972; Joosse and Van Vliet, 1981) and power stations (Folkeson, 1981), regional use of sewage sludge, copper-rich pig manure (de Haan, 1975; Lexmond et aL, 1982), metal based pesticides (Hirst et aL, 1961) and the global dissemination of heavy metals by traffic (Nriagu, 1978). Heavy metals have different functions in biological systems: Fe, Mn, Cu, and Zn as micronutrients in all organisms, Mo, Ni, V, and Co in some groups of organisms. Besides some uncertainties for Cd and As, all other heavy metals occur as trace elements in every organism without any functional necessity. Due to the different functions of heavy metals in biota it is not useful to discriminate between biomonitoring as a quantitative method and bioindication as a qualitative method (Posthumus and Tonneijck, 1982). The only realistic contrast is that of sensitive and resistant organisms. * Paper presented at a Symposium held on 14 and 15 October 1982, in Utrecht, The Netherlands. Environmental Monitoring and Assessment 3 (1983) 297-305. 9 1983 by D. Reidel Publishing Company.
0167-6369/83/0033--.0297501.35.
298
W.H.O.
E R N S T ET AL.
The aim of this contribution is to elaborate the evidence of effectiveness of biological indication of a surplus of heavy metals. 2. Material and Methods
For the aspect of biomonitoring atmospheric metal fallout, plant material has been collected and digested without washing. For monitoring of soil pollution by plants, fresh plant material has been washed twice with demineralized water, dried at 80 ~ and digested with strong inorganic acids (HNO3/HCIO4 7:1). All analyses of heavy metals were carried out by atomic absorption spectrometry. The sampling localities and data as well as the number of analyzed samples are given in the relevant figures and tables. For measuring the metal tolerance of grasses the rooting technique has been applied in a modified form (Ernst, 1982a).
3. Results and Discussion
3. I.
B A C K G R O U N D VALUES OF HEAVY METALS IN PLANTS
Due to the different functions of heavy metals in organisms and to the different metal contents in various geological formations the natural background and/or threshold has to be considered in every bioindication. Plant species with a high metal demand, i.e. that I0.
P*-0.95 5"
1
2
3
~
5
"6 ..~
6
O.295 + 0.063
J
03
0.2
0.3
0,~
05
06
Q
083
I Fig. 1.
2
3
4
5
6 rnrnolMekg-i
The variation in the concentration ofFe, Mn, and Zn in the leaves ofPopulus balsamifera s on a sandy sea clay in North Holland. The leaves have been collected in October 1982.
growing
B I O I N D I C A T I O N O F A S U R P L U S O F H E A V Y M E T A L S IN T E R R E S T R I A L E C O S Y S T E M S
299
of Zn by birch, willow and poplar will indicate less precisely a metal pollution (Denaeyer-De Smet, 1970) than those species with a low demand. Despite this drawback Populus nigra has been proposed for national monitoring programs of heavy metals (Knabe, 1982). Due to the tremendous variation between individuals of one population (Figure 1), sampling of very small numbers of individuals will not give a realistic picture of the effects of pollutants on populations. There is also a time dependent effect. In the case of a smelter pollution the difference between a short (14 days) exposure of standardized Lolium multiflorum (MAGS, 1977) and a long-term exposure of wild plants has been quite obvious (Figure 2). It demonstrates the drawback of active biomonitoring of heavy metal pollution. mrnol Zn kg-l dry wt. 40O ~
Aosculus hip.p_oc_ ostonurn
200.
I00
rg~"
,~ Loliurn I.'.':..- ~.~.~ ~ J3OOrn W " .:~.~a".....1375 m E ",970" ~972 1974 '
Fig. 2. Effects of Zn fallout from a Zn smelter on the Zn concentration of the leaves of Aesculus hippocastanumL. in the autumn of everyyear and Zn concentrationofLolium multiflorumLamk., as the mean of 14 days exposure during the vegetation period (after Ernst, 1980). In monitoring soil-borne heavy metal pollution a further complication is the interaction of heavy metals with other nutrients and especially with the soil organic matter. The speciation of a heavy metal influences the uptake by plants and its translocation from root to shoot (Figure 3). Generally, heavy metals are less taken up if they are complexed in comparison to those in ionic status (Marquenie-van der Werffet al., 1981). 3.2. BIOINDICATION BY PHYSICAL PROCESSES AT THE PLANT SURFACES Wet and dry deposition of heavy metals via rain or dustfall, which can increase to 6.7 kg Zn, 4.5 kg Fe, and 0.4 kg Cu per ha per year in The Netherlands (CBS, 1981), can be fixed by plant organs with sufficient rough and/or hairy surfaces (Ernst, 1982b). The same holds for the bark of trees with a slow turnover rate (Ernst, 1983a). Bioindication by analysing the dry and wet deposition can help to detect emission sources but it will not allow a prediction of biological consequences of such pollution.
300
W. H. O. ERNST ET AL. mrnot Fe kg -t 10-
o 11
50.
FA
FA/HA 3.'t
FA/HA 1:3
HA
100-
150"
200-
Fig. 3. The uptake and translocation of iron by Holcus lanatus. The Fe has been supplied in different chemical forms: ionic and complexed by humic and fulvic acids in various ratios (after I. Riphagen, unpubl.).
3.3.
B I O I N D I C A T I O N BY C H E M I C A L E X C H A N G E P R O C E S S E S IN T H E CELL W A L L
Often bryophytes and lichens have been used as bioindicators of heavy metals (Folkeson, 1981). Due to the high cation exchange capacity of the cryptogamic cell walls H § -ions and other monovalent ions can be exchanged by heavy metal ions. Species specific affinities to heavy metals demands an interspecific calibration (Folkeson, 1979). Passive biomonitoring as well as active biomonitoring by exposition of Sphagnum bags (Goodman and Roberts, 1971) or Hypogymnia physodes transplants (Sch6nbeck, 1969) will help in localizing emission sources, but not in predicting biological effects. A replacement of these systems by the exposition of bags with ion exchange resins may be considered. 3.4. BIOINDICATION BY PHYSIOLOGICALPROCESSES ON SHORT-TERM The first reaction of sessile organism to environmental stress will be a change in physiological processes in such a way that the metabolism tries to regain the physiological equilibrium. Changes in enzymatic activities can be used in connection with heavy metal analysis for biomonitoring, if many conditioning factors will appropriately be taken into account (Ernst, 1980). If this compensating reaction to stress remains insufficient, then more serious changes in the physiology of an organism will facilitate biomonitoring. In such situations physiological changes can cause visual symptoms, such as chlorosis, necrosis, dwarfism and other teratogenic aspects. These symptoms alone, however, are not typical for heavy metal stress. Generally, metal-stressed plants with chlorotic leaves have higher metal concentrations than those with green leaves, as demonstrated for Agrostis tenuis in various
B I O I N D I C A T I O N O F A S U R P L U S O F HEAVY M E T A L S IN T E R R E S T R I A L E C O S Y S T E M S
301
tJmol 1-1 dr. wt.
,~ tO0.
t,
~ 1o. Zn
g
1
w 300
500 700 d~stonce to the smelter
900 m
Fig. 4. The concentration of Z n and Pb in green (filled dots) and chlorotic (open dots) leaves of Agrostis tenuis Sibth in relation to the distance from a Zn smelter in Brabant/The Netherlands (after J. Faber, unpublished).
distances to a Zn smelter in The Netherlands (Figure 4). Owing to a disturbed photosynthesis a reduced production of propagules will affect the stability of the population and can contribute to changes in the vegetation pattern as long-term effect. Necrosis can also indicate a surplus of heavy metals. As in the case of chlorosis, the concentrations of heavy metal(s) in the necrotic leaves is higher than in green ones (Table I). The long-term effects are the same as those mentioned for chlorosis. Even
TABLE I Z n concentrations (mmol k g - ~ dry weight) in leaves and roots of sugar beet, Beta vulgaris L. var. altissima D61l, on fields which have partially been flooded in spring by heavy metal rich sediments from river Innerste at Langelsheim F.R.G. The heavy metals in the river bed are remnants of mining activities in the Hartz mountains during the last centuries (Ernst, 1974, Ernst, unpubl.) Green plants contaminated plants leaves roots uncontaminated plants leaves roots
573 • 58 2290 • 107
120 _+ 17 150 + 12
Chlorotic plants
1450 • 72 3050 • 205
302
w.H.o.
ERNST ET AL.
without chlorosis and necrosis metabolic disturbances diminish growth. Dwarfism is a well-known reaction of plants to a lot of environmental stress such as SO2, phosphorus deficiency, and also metal toxicity (Ernst, 1982b). Further evidence of diminished growth by metal stress has been demonstrated in the vicinity of a Zn smelter, where the needles of coniferous trees were not only small (Figure 5), but their length was asymmetrically distributed. This dwarfism was clearly related to increased amounts of Zn in the needles (Ernst, 1982b). Using physiological parameters, biomonitoring can make valuable predictions for risk assessment (Ernst and Joosse-van Damme, 1983).
40.
~, 30"
~.. 20"
E I0-
1 tO
20
30 length of the
40 50 needle5
mm
Fig. 5. The length of second year old needles of Pinus sylvestris L. from the vicinity of a Zn smelter in Brabant (The Netherlands) in comparison to needles ofnon-poUutedpine trees. The open columns represent healthy needles, the cross-hatched columns needles from trees in the vicinity of a Zn smelter.
3.5. BIOINDICATION VIA PHYSIOLOGICAL AND GENETICAL REACTION ON THE LONG-TERM
The innate different sensitivity to high concentrations of heavy metals can vary within species and within populations. Due to the slow migration of heavy metals through the soil profile (Ernst et al., 1974) a more or less constant or increasing emission rate gives rise to an accumulation of heavy metals in the topsoil. On the long term a high metal stress causes genetic changes within populations. They are the most dramatic effects of environmental pollution (Bradshaw, 1976). However, only a small group of plant species is capable to evolve heavy metal tolerance. Important grassland species such as Lolium perenne L., Dactylis glomerata L., and Trifolium repens L. are very sensitive to a surplus of heavy metals, as already indicated by their absence on geological metal anomalies (Ernst, 1974). Plant species which are not promising for agricultural purposes such as Agrostic species, Festuca ovinaL.,
B IO IN DIC ATI ON OF A SURPLUS OF HEAVY METALS IN T E RRE ST RI A L ECOSYSTEMS
303
Anthoxanthum odoratum L. and Deschampsia cespitosa (1_,.)P.B. can evolve resistance against many heavy metals. Genetic changes in the metal tolerance of grasses and sedges can be monitored by measuring the relative root growth in control and metal containing solutions, the so-called rooting technique (Wilkins, 1978 for a re-evaluation of the technique). Due to the pattern of aerial fallout around smelters bioindication with the aid of the rooting technique can demonstrate that in the immediate vicinity of the smelter the genetic changes are the most severe ones (Figure 6). The rapidity of selection may be demonstrated in the vicinity of a Zn and Cd smelter in Northern Germany (Ernst, 1972, 1976). After coming into operation of the smelter in 1969, populations of Agrostis tenuis and A. canina (Figure 7) became within three distance to the s m e l t e r
I0-
I
I
90kin 1.0-2.0 km
10.4-1.0
km
ul q, .
-=3
0.5 Fig. 6.
1.0
1.5
2.0
tolerance index
The Zn tolerance index o f the roots ofAErostis tenuis from clones in the vicinity ( 0 - 2 km) of a Zn smelter and from clones in a control area (90 km from the smelter).
kg Zn ha -1
index of
zinc- tolerance
150,
150-
tO0
tO0.
50 J, "68
r "70
I
I
IK 50 II '72
"74
'76
"68
70
"72
"74
76
Fig. 7. The rapid evolution of Zn tolerance in Agrostis canina in 400 m distance from a Zn-Cd smelter in Datteln/FRG. The smelter started operation in 1969, first legislative restrictions of emission were given in 1972. For comparison the amounts of the fall-out is presented according to MAGS (1977).
304
w . H . o . ERNST ET AL.
years fully tolerant to Zn. The first year's emission was about 100 kg Zn ha- ~; governmental regulations had only resulted in a reduction of the emission to 50 kg Zn ha- 1 (MAGS, 1977) so that the genetic changes will be present for a long time. Animals, which are less able to evolve metal tolerance (Ireland, 1975) will suffer extremely by metal toxicity, if they are consuming metal-tolerant plants in metal-contaminated areas. Due to the dangerous aspects of resistant plant populations to the non-resistant populations of cattle and other animals the modern biomonitoring system has to look at genetic changes in plants and animals.
4. Concluding Remarks
(1) Bioindication of a contamination by heavy metals is possible. (2) Bioindication by analyzing the metal concentration on plant surfaces (wet and dry deposition) and in plants is only useful for localizing unknown emission sources. (3) Bioindication with a predictive value has to be accompanied by analyzing heavy metal concentrations of plants and metal speciation in soil, because the chemical status of heavy metals severely influences their toxicity and their long-term effects. (4) Bioindication has to regard the genetical changes in populations of plants and, as far as possible, those of animals. References Bradshaw, A. D.: 1976, 'Pollution and Evolution', in T. A. Mansfield (ed.), 'Effects of Air Pollutants on Plants', Cambridge University Press, Cambridge, pp. 135-159. CBS-Centraal Bureau voor de Statistiek: 1981, 'Preliminary Results Air Pollution, Measurements April 1979 - March 1980', Voorburg, pp. 259-160. Denayer-De Smet, S: 1970, 'Consideration sur raccumulation du zinc par les plantes poussant sur sols calaminaires. Bull. Inst. Sci. nat. Belg. 46, 11, 1-13. Ernst, W.: 1972, 'Zink- und Cadmium-Immissionen auf B6den und Pflanzen in der Umgebung einer Zinkhfitte', Ber. Deutsch. Bot. Ges. 85, 295-300. Ernst, W.: 1974, 'Schwermetallvegetation der Erde', G. Fischer Verlag, Stuttgart, 194 p. Ernst, W.: 1976, 'Physiological and Biochemical Aspects of Metal Tolerance', in T. A. Mansfield (ed.), 'Effects of Air Pollutants on Plants', Cambridge University Press, Cambridge, pp. 115-153. Ernst, W. H. O.: 1980, 'Problems of Bioindication on the Level of Individuals', in R. Schubert and J. Schuh (eds.), "Bioindikation, Martin-Luther-Universit~tt, Wiss. Beitr/ige 26 (P 10), 3-9. Ernst, W. H. O.: 1982a, 'Schwermetallpflanzen',in H. Kinzel (ed.), 'Pflanzen6kologie undMineralstoffwechsel', E. Ulmer Verlag, Stuttgart, pp. 427-506. Ernst, W. H. O.: 1982b, 'Monitoring of Air Pollutants', see L. Steubing and H.J. J/iger (eds.), pp. 121-128. Ernst, W. H. O.: 1983a, 'Bioindication of a Surplus of Heavy Metals in Terrestrial Ecosystems', in E. P. H. Best and J. Haeck (eds.), Ecologische indicatoren voor kwaliteitsbeoordeling van lucht, water, bodem, en ecosystemen, Pudoc, Wageningen (in press) (in Dutch). Ernst, W. H. O., Mathys, W., Salaske, J., and Janiesch, P.: 1974, 'Aspekte von Schwermetallbelastungen in Westfalen', Abhandl. Landesmuseum Naturkunde Miinster Wes~Calen, 36 (2), 1-30. Ernst, W. H. O. and Joosse-van Damme, E. N. G.: 1983, 'Umweltbelastung dutch Mineralstoffe', VEB G. Fischer, Jena. Folkeson, L.: 1979, 'lnterspecies Calibration of Heavy Metal Concentrations in Nine Mosses and Lichens: Applicability to Deposition Measurements', Water, Air, and Soil Pollut. 11,253-260. Folkeson, L.: 1981, 'Heavy Metal Accumulation in the Moss Pleurozium in the Surroundings of Two Peat-Fired Power Plants in Finland', Ann. Bot. Fenn. 18, 245-253.
BIOINDICATION OF A SURPLUS OF HEAVYMETALS IN TERRESTRIAL ECOSYSTEMS
305
Goodman, G. T. and Roberts, T. M.: 1971, 'Plants and Soil as Indicators of Metal in the Air', Nature (Lond.) 231,287-292. Haan, S. de: 1975, 'Die chemische Zusammensetzung von Gewachsen auf mit Klarschlamm behandelten B6den', Landw. Forsch. 31/1,220-233. Hirst, J. M., Le Riche, H. H., and Larscomb, C. L.: 1961, 'Copper Accumulation in the Soils of Apple Orchards Near Wisbeck', Plant Pathol. 10, 105-108. Ireland, M. P.: 1975, 'Metal Content of Dendrobeana rubida (Oligochaeta) in a Base Metal Mining Area', Oikos 26, 74-79. Joosse, E. N. G. and Van Vliet, L. H. H.: 1982, 'Impact of Blastfurnace Plant Emissions in a Dune Ecosystem. Bull. Environ. Contamin. Toxicol. 29: 279-284. Knabe, W.: 1982, 'Monitoring of Air Pollutants by Wild Life Plants and Plant Exposure: Suitable Bioindicators for Different Immissions Types', see L. Steubing and H. J. J~ger (eds.). Lexmond, T. M., van Riemsdijk, W. H., and de Haan, F. A. M.: 1982, 'Research of Phosphate and Copper in the Soil, in Particular in Areas with Intensive Animal Husbandry',Bodembescherming7, Staatsdrukkerij, Den Haag (in Dutch). MAGS-Ministerium f'tirArbeit, Gesundheit und Soziales des Landes Nordrhein-Westfalen: 1977, 'Umweltbelastung im Raum Datteln. Analyse und ProblemlSsung', Dtisseldorf, 55 p. Marquenie-van der Werff, M., Ernst, W. H. O., and Faber, J.: 1981, 'Complexing Agents in Soil Organic Matter as Factors in Heavy Metal Toxicity in Plants', Int. Conference 'Heavy Metals in the Environment, Amsterdam 1981', CEP Consultants, Edinburgh pp. 222-225. Nriagu, J. O. (ed.): 1978, 'The Biogeochemistry of Lead in the Environment', Elsevier/North Holland Biomedical Press, Amsterdam, New York, Oxford. Posthumus, A. C. and Tonneijck, A. E. G.: 1982, 'Monitoring of Effects of Photo-oxidants on Plants', see L. Steubing and H. J. J~iger (eds.) pp. 115-119. Sch~nbeck, H.: 1969, 'Eine Methode zur Erfassung der biologischen Wirkung von Luftverunreinigungen durch transplantierte Flechten', Staub-Reinhaltung der Luft 29, 14-18. Steubing, L. and J~iger, H. J. (eds.): 1982, Monitoring of Air Pollutants by Plants. Methods and Problems, W. Junk Publishers, The Hague, Boston, London. Wilkins, D. A.: 1978, 'The Measurement of Tolerance to Edaphic Factors by Means of Root Growth', New Phytol. 80, 623-633.
