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6. BIOLOGICAL ACCUMULATION AND EFFECT OF ATMOSPHERIC CONTAMINANTS As we saw in the previous chapter, the particular structure of aquatic or terrestrial ecosystems can impose constraints upon interactions between the atmosphere and the biosphere. Terrestrial ecosystems are readily accessible to gaseous and suspended substances in the atmosphere. They present large, rough surface areas for exposure to gases, and where forest canopies impede wind transport, the wind velocity is reduced sufficiently to induce substantial dry deposition of fine particles. Evergreen canopies can be active in this manner year-round, whereas deciduous canopies are less effective in winter. In contrast, aquatic ecosystems are somewhat protected from gases by the air-water interface. The rate of gas exchange between the atmosphere and a body of water depends upon the temperature and turbulence of the air and the water, and the diffusivity and concentration gradient of the gas across the air-water interface (Danckwerts 1970~. The rate of exchange, however, is slow compared to aerial diffusion throughout terrestrial vegetation canopies. ACCUMULATION IN TERRESTRIAL ECOSYSTEMS In terrestrial ecosystems, atmospheric contaminants and pollutants are captured by plant surfaces in a variety of ways. Hairy and glandular plant surfaces can physically trap suspended matter in the form of wet or dry aerosols. Trace metals are an example of substances that tend to be tranported through the atmosphere and deposited in this way. Wet precipitation washes suspended matter from the air and also facilitates the eventual transfer of atmospheric contaminants captured by the vegetative canopy to the soil surface. Some metals, such as lead and cadmium, can even be incorporated as particles into plant cuticles (Hemphill and Rule 1975), and if the aerosol particles are less than 0.1 micron in diameter they can enter directly inside the leaf tissues through the stomata! pores. Ultimately all such material, whether attached to or incorporated into 7

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88 vegetation, is transferred into the soil surface by rainwater wash or by leaf fall and the decomposition of vegetation. Aerosols may enter leaves through epidermal pores, trichomes, or wounds, as well as stomata! pores. In some cases direct penetration of the waxy cuticle is possible, or secretions by the plant may dissolve the aerosols, facilitating their transport and absorption by plant tissue (Hosker and Lindberg 1981~. Factors that affect the size of stomata! apertures can determine how readily gases and aerosols reach the internal tissues of a leaf. The layer of moisture surrounding the palisade and mesophyll cells inside leaves also is crucial to the rate of reaction of the substances in the aerosols or gas with the living protoplasm. Among the substances that enter an ecosystem as aerosols are sulfur, nitrogen, and several of the more volatile heavy metals, such as mercury, selenium, and arsenic. Gaseous pollutants generally react with plant surfaces more readily than aerosols. Some substances, such as hydrochloric acid, are so reactive that they will be absorbed by any plant surface they contact (W. Heck, USDA/SEA, North Carolina State University, Raleigh, NC, personal communication, 1980) while other gases, such as monoxides of carbon and nitrogen and volatile organic compounds, react very slowly with plants. Gaseous substances are also more readily incorporated into plant tissues and translocated by vascular systems than aerosol pollutants. Most studies of pollutant uptake by plants have been of single pollutants on individual leaves or whole plants under laboratory conditions. Estimates of fluxes of pollutants into plant tissues under field conditions have been made using the eddy correlations technique (Eastman and Stedman 1977, Garland et al. 19731. At present there is no satisfactory way of extrapolating such data to whole ecosystems or to mixtures of pollutants. Figure 6.1 shows schematically some of the ways gaseous pollutants may react with plant surfaces, and Table 6.1 summarizes the types of reactions a number of gases have with plant tissues. Lindberg and McLaughlin (1981) have reviewed problems associated with collecting and interpreting data on the interaction of air pollutants with vegetation. ACCUMULATION IN AQUATIC ECOSYSTEMS The pathway followed by atmospheric contaminants entering surface waters depends on several factors, including thermal stratification in the water, the physical form of the contaminant at entry, its solubility, the interactions of organisms with the contaminant, and the affinity of the pollutant for sestonic (suspended) particles or sediment surfaces. Aerosols and large particulate components of the atmosphere tend to become trapped in the surface film of natural waters. As a result, surface films often become enriched in atmospheric contaminants such as trace metals and organic micropollutants by as much as orders of magnitude more than the concentration observed in the bulk water beneath (Duce et al. 1972, MacIntyre 1974, LiSS 1975, Andren et al.

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89 rc1 rs1 IT' ' - / ~~~ ~ EPIDERI\/ IS I NTE RCE LLU LA R ~ rL 1 , -. rL l. . SPACE ~ t.t I l', FL1 XL1 / ' Fa1 ~ GUAR D CE LL 1 kd I 1\ 1 1} 1\ Am. VASCU LAY ~'~.-'T1 l. .; I PALLISADE FLII, ~ PARENCHYMA 1l C E L L I'W-1 ~3' ~~ 1l:7$r.2 ~ ~ v. ~ ~~ AAA_ ~ XL2 STOMATE rc2 Fs2 SPONGY PARENCHYMA ~MESOPHY LL CELL . ~ ra2 . Fa2 FIGURE 6.1 Electrical analog of pollutant exchange between leaf and surrounding air. The circuitry is superposed on a cross-section of an amphistomatous leaf (stomates on both surfaces). Xair, XL1 and xL2, and xint denote gaseous pollutant concentrations in well-mixed surrounding air, at the upper and lower leaf surfaces, and average gas phase concentrations within the leaf mesophyll, respectively. The (variable) resistances ra1 and ra2, rL1 and rL2, and rL1 and rL2 are the upper and lower boundary layer resis- tances, stomata! plus intercellular resistances, and cuticular plus internal resistances, respectively. Resistances rCl and rC2 denote resistance to chemical reaction at the upper and lower leaf surfaces. The fluxes Fa, Fa1 and Fa2, FSl and FS2, FL1 and FL2, and F'L1 and FL2 denote the total flux to both surfaces (Fa = Fa1 + Fa2), surface uptake at the upper and lower surfaces, and the fluxes through the upper and lower stomata and cuticles. The electrical symbols depicting grounds ( _ ) represent the termi- nation of fluxes due to reaction with leaf surface materials. The (variable) capacitor sym- bols (- ~) represent surface adsorption or retention (based on Bennett et al. (1973)). SOURCE: Hosker and Lindberg (1981). a ~ XA I R

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go TABLE 6.1 Types of Interactions of Gases with Plant Surfacesa Type of Reaction Atmospheric Contaminant Primarily react with or are absorbed onto outer surfaces Primarily react within the leaf tissue React both on outer surfaces and in internal tissues React slowly but have potentially important interactions with plants H2O2, HNO3, H2 SO4 SO2, NH3, NO2, PAN, metabolically reactive cO2a, O2a ethylene,b formaldehyde HE, HCl, O3, C12 N2O NO, CO, organic molecules such as hydrocarbons, pheromones, and terpenes aNormal large-scale exchange in photosynthesis and respiration. bEthylene is unusual in that it is a plant hormone and can have a strong effect in plant cells even at very low concentrations. NOTE: Aerosols tend to react more with outer surfaces because they do not pass through stomata as easily as gases. Gases interact more readily with the internal tissues of plants because they can rapidly diffuse into the leaf through stomata! openings and the moist unprotected surfaces of internal tissues present more reaction sites for the gases. SOURCE: After Hosker and Lindbery (1981).

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91 1976, Elzerman and Armstrong 1979~. The fates of such contaminants in surface films are poorly known. Thermal stratification, either in the form of a thermocline or as ice cover, is a barrier to gas exchange and the dispersal of pollutants into aquatic ecosystems. Ice cover totally inhibits exchange of gases between air and water (Schindler 1971) and may be of major significance in temperate lakes, which can be ice covered for as much as 6 months, and in arctic lakes, on which ice cover can last more than 11 months of the year. In winter, oxygen consumption in ice-covered, eutrophic aquatic ecosystems may cause the entire water body to become anoxic. An experiment by Welch and coworkers (1980), simulating a natural gas pipeline break, found that methane discharged into an arctic lake in winter was trapped in the lake under ice cover until spring and that oxygen in the lake was slowly consumed by methane-oxidizing bacteria. On the other hand, atmospheric pollutants that accumulate in the ice cover of a lake over several months are discharged into the lake as a large pulse during ice and snow melt. Figure 6.2 shows one such pulse caused by the acid precipitation that accumulated in winter snow. A larger-scale example of thermal stratification is the thermocline that exists between the surface ocean and the deep ocean. Except at the poles where mixing can occur the thermocline acts as an effective barrier against transfer of substances between surface and deep ocean water. For example, the time needed to achieve equilibrium in CO2 transfer across the ocean thermocline is several hundred years, while the time required for equilibrium between the atmosphere and the surface water of the ocean is only about 8 years. If the ocean surface waters had sufficient capacity for CO2, the equilibration time is short enough that the CO2 released by anthropogenic activities would not accumulate in the atmosphere. The surface ocean, however, cannot absorb all the CO2 that is released. Exchange with the deep ocean is therefore the process that limits the rate of exchange and the achievement of equilibrium for CO2 between the atmosphere and the oceans, and the exchange is so slow that excess CO2 does indeed accumulate in the atmosphere. Likewise, once a substance enters the deep ocean, residence time is very long, not only for carbon dioxide but also for other contaminants emitted into the atmosphere as combustion products (Broecker 1974~. Carbon dioxide, sulfate, nitrate, and ammonium are all required to some degree by algae and other aquatic plants. The carbon, sulfur, and nitrogen are either actively metabolized and passed up the food chain or egested as fecal pellets. Although much of the fecal material is Demineralized in the water column, some of the carbon, nitrogen, and sulfur eventually collect in sediments. Nitrogen, which is usually in greatest demand by plants, tends to be transferred most rapidly. Reactive pollutants adsorbed or absorbed by plankton or other suspended articles travel similar pathways. Less reactive pollutants, which remain in solution, tend to remain trapped above the thermocline, because diffusive transfer across the thermocline is much slower than the settling of particles.

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92 pH r 7 6 5 1 976/77 M FIGURE 6.2 Seasonal changes of pH of lake water taken from the outlet of Little Moose Lake, Adirondacks, New York, and from a 3-m-deep pipe in the lake. The spring acid pulse is greater at the surface than at the 3-m-deep level. SOURCE: Schofield (1980). Reprinted with permission from Ann Arbor Science Publishers, Inc., Ann Arbor, Michigan. A. I ~ fit A

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93 For example, Hesslein et al. (1980) studied the pathways of trace metals by adding radioactive tracers to a whole lake. Iron-59 and cobalt-60, which are quickly adsorbed by particulate matter, settled rapidly from the epilimnion (surface water) to sediments. Iron redissolved in anoxic surface sediments underlying the hypolimnion (deep water). In contrast, cesium-134 remained in solution and was removed from the epilimnion at a much slower rate, chiefly by direct reaction with littoral sediments. Removal times were roughly twice as long as for cobalt and iron. Other metallic tracers had intermediate removal times. Substances that are relatively inert can accumulate in the deep ocean. Examples are the radioactive pollutants argon-39 and krypton- 85, or the halocarbon pollutants CF3C1, CF4, and CC14. All of the above enter surface waters as gases. Cesium-137, which is a product of weapons testing and the nuclear fuel cycle, enters the ocean as an aerosol. It accumulates in the lipid fractions of marine organisms, and from the lipid phase it is ultimately released by metabolism or by rapid mineralization upon the death of the organism. Hence, cesium is removed from salt water as slowly as from fresh water. The volume of the deep ocean is 50 times that of the layer above the thermocline. Pollutants entering the deep ocean are thus diluted 50-fold from their concentration in the surface layer. Some will enter the sediments associated with the depositing inorganic or biological debris. Those with longer residence times--i.e., the less reactive pollutants--will remain in the ocean deeps for millennia. ACCUMULATION IN Sol LS AND AQUATIC SEDIMENTS In both terrestrial and aquatic communities, there is a tendency for most pollutants to accumulate in soils or lake sediments, where they become concentrated by absorption, direct cation exchange, or by chemical precipitation. There are both striking similarities and substantial differences in the response of soils and aquatic sediments to pollutants. Both are depositories for biological and mineral matter and can concentrate any pollutants bound to deposited materials. In terrestrial ecosystems, however, plant roots tend to resorb and recycle materials to some degree, and there is some long-term storage in wood. With the exception of sphagnum bogs and wetlands, there is no such recycling in aquatic ecosystems, and there are no long-lived plants to form long-term living sinks for pollutants although dead organic debris may accumulate in aquatic sediments that are long-term sinks for many substances in the form of organic molecules, insoluble oxides, hydroxides of redox-sensitive metals, or as sulfides under anoxic conditions. In anoxic environments, there may be substantial recycling of many elements that are not mobile in oxic environments from sediments into the hydrosphere and atmosphere. For example, sulfur may be released as hydrogen sulfide or clime thyl sulfide; several metals are released in a methylated form; and nitrogen is released as ammonia, nitrous oxide, and molecular nitrogen. These processes, widespread in aquatic

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94 ecosystems, also occur in waterlogged soils (Tusneem and Patrick 1971, Reddy et al. 1978~. Flux rates for the above substances are poorly known and are highly variable even within one ecosystem. In aquatic ecosystems, some pollutants are rapidly locked into sediments, where they cease to affect planktonic or nektonic organisms. For example, the addition of phosphorus to lakes is objectionable largely because it causes increased growth of phytoplankton. Once deposited in oxic sediments, it is usually no longer a threat. Sediment-water partition coefficients for phosphorus range from 104 to 106. Likewise, most trace metals are rapidly transferred from water to sediments (Hesslein et al. 1980), as are nitrogen and sulfur, although they are less efficiently concentrated in sediments because microbial reduction can rapidly release them (Schindler et al. 1977, 1980a). Under certain circumstances, the high sediment-to-water partition coefficient may become an undesirable feature for the aquatic ecosystem as a whole. Once incorporated into sediments, a pollutant cannot be flushed rapidly from a water body. Some materials may be transferred directly from sediments to pelagic biota; for example, mercury, selenium, and perhaps lead are methylated in sediments and transferred to the water column. Owing to their high affinity for lipids, methylated metals can be taken up and accumulate In fish and other pelagic forms, even though concentrations in water remain low. DOT and many other pesticides, petroleum hydrocarbons, polynuclear aromatic compounds, and polybrominated or polychlorinated biphenyls (PBBs and PCBs) also are known to be highly concentrated in both sediments and the lipids of living organisms. Bottom-living aquatic organisms that ingest sediments many receive very high concentrations of pollutants. The incidence of deformities among the larvae of bottom dwelling chironomids is one of the most sensitive indicators of contamination in the aquatic environment (Warwick 1980a, 1980b). Likewise, surface soils, where high accumulation of pollutants occurs, are occupied by innumerable small invertebrates, including mites, springtails, beetles, earthworms, Crustacea, and midge larvae, and by a variety of fungi, bacteria, and other organisms. The fungi include both important plant pathogens and mycorrhizal fungi crucial for recycling nutrients from soil to plants. All these organisms perform decomposition via many complex pathways, recycling crucial nutrients in forms usable by plants. The seeds, spores, and eggs of many organisms also begin development in these layers. Saprophytic organisms that burrow throughout soil and sediments may cause deposited pollutants to be diluted, or spread throughout the upper layers. As a result, substances deposited in one year may be dispersed through a layer of soil or sediment representing decades or even centuries of accumulation (Davis 1968, Berger and Heath 1968, Rhoads 19731. Such processes will delay both the development of high concentrations of pollutants in surface sediments and the burial of substances after inputs have ceased (Schindler et al. 1977~. This "bioturbation" may be responsible for the fact that concentrations of DDT and PCBs in the fishes and sediments of the Great Lakes have not

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95 decreased greatly in the past decade, despite stringent control of inputs (International Joint Commission 1980~. Acid conditions and high trace-metal concentrations in excess of 500 ppm are known to inhibit litter decomposition, causing undecomposed organic matter to accumulate in both terrestrial and aquatic ecosystems (Watson et al. 1976, Freedman and Hutchin son 1980, Strojan 1980, Hendrey et al. 1976, Traaen 1980~. A number of key enzyme systems appear to be affected (Tyler 1974, 1976a,b). This accumulation assuredly slows nutrient cycling. Soil and aquatic fungi are usually more acid tolerant than bacteria, and thus they become the dominant decomposers in acidic ecosystems. But even fungi appear to be susceptible to extremely high concentrations of metals derived from the atmosphere (Jordan and Lechevalier 1975, Williams et al. 1977~. Fungi with increased tolerance of acids and heavy metals have, however, been obtained from several sites near smelters (Hartman 1976, Freedman 1978, Carter 1978~. Aquatic Sediments as Historical Records Aquatic sediments provide a "history" of changes in the aquatic ecosystem, its terrestrial watershed, and its airshed. The increase in heavy metals in lake sediments in this century is an excellent example (Robbing and Edgington 1977, Norton et al. 1978, Galloway and Likens 1979~. A study of sediment cores from the mouths of tributary streams around the St. Lawrence River and Great Lakes confirms the relationship between such increases and terrestrial watersheds contaminated by human activity (Fitchko and Hutchinson 1975~. Mackereth (1966) and Warwick (1980) were able to show historical evidence for increased weathering of terrestrial watersheds owing to human disturbance. Davis et al. (1980) have been able to decipher an acidification history of lakes in Norway and Maine, using a combination of recent dating methods and changes in the abundance of acidophilic diatoms. No study has yet used paleolimnological methods to construct a history of terrestrial responses to acidification. In most cases, such methods offer at present the only possibility of documenting and dating the course of acidification in either terrestrial or aquatic ecosystems, because of the paucity of regional background data collected prior to the development of the acid rain problem. TRANSFORMATIONS IN Sol LS AND WATERS A number of volatile components of the atmosphere can react with waters or soil constituents and be incorporated into the compounds in the biosphere. How volatile components are removed, the responsible organisms or abiotic mechanisms, and frequently the factors that can affect removal are as yet unclear or wholly unknown. Some removal mechanisms are abiotic, but more often they are entirely biological.

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96 Many organic compounds present in the atmosphere undoubtedly are transformed and decomposed in soils and waters. The evidence for such transformations, however, is derived usually from studies in which the chemical has not been supplied in the volatile form and in which the chemicals were present in water or soil samples at concentrations far higher than are present in nature. Tests with concentrations of contaminants far in excess of ambient levels must be interpreted very cautiously, because chemicals that are biodegraded at high concentrations may degrade slowly or even not at all when present at low concentrations (Boethling and Alexander 1979a,b). If the transformation yields inorganic products (CO2 and H2O), the reaction detoxifies the molecules. Among the organic compounds destroyed--at least at higher concentrations--are certain polycylic aromatic hydrocarbons, phenols, alkanes, esters, and simple aromatic molecules. In some instances, however, the transformations may yield not inorganic products but other organic products, which may themselves be toxic. Certain organic compounds are resistant to microbial transformation and thus persist, for example certain chlorinated aromatics, aliphatics, and several nitrogen heterocycles. The biodegradability of many of the organic atmospheric pollutants has not been directly evaluated, and none has been tested at realistic concentrations. Hence it is not possible at the present time to assess their rate of transformation when introduced into waters or soils or even whether such a transformation does take place. Some of the problems in assessing such kinds of transformations and the types of reactions that occur are considered by Alexander (1981~. Information on the role of soils in removing or generating atmospheric substances is growing constantly, and current assessments will need to be modified as information is obtained from new studies. The following examples have been relatively well researched and are offered as an indication of the current level of understanding for several atmospheric constituents. Methane. A number of bacteria present in soils and lake waters are able to oxidize methane. Although there has been considerable study of which organisms can do so in laboratory media and of the biochemistry of the process, surprisingly little attention has been paid to the rates of biological methane oxidation under natural conditions. Studies of the process in paddy fields indicate that the rate of oxidation is limited by the rate of methane diffusion to the soil (de Bont et al. 1978~. In lakes, the rate of oxidation is usually limited by diffusion of oxygen and methane, as well as by the concentration of nitrogen (Rudd et al. 1976~. During summer thermal stratification, activity is restricted to the metalimnion (the part of the water column where the thermal gradient occurs), although after the fall overturn destroys thermal stratification methane oxidation may occur throughout the water column. Often this activity persists throughout the following winter (Rudd and Hamilton 1975, Welch et al. 1980~.

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97 Carbon monoxide. An increase in ambient levels of carbon monoxide would be expected on the basis of present rates of global emission, but no such major increases are evident; therefore a significant sink for this gas must exist. Many investigators have pointed to soils as a means for removing carbon monoxide from the gas phase. Because carbon monoxide is oxidized in nonsterile but not in sterile soil (K. Smith et al. 1973), the removal mechanism is apparently microbial. Estimates have been made of global uptake by soil of carbon monoxide based on its rapid loss from the head space of a container when soils are incubated in the laboratory with this volatile compound. For example, based upon tests in which several soils were exposed to 100 ppm carbon monoxide, it was calculated that soils of the world remove 14.3 x 1015 g of carbon monoxide per year (Ingersoll et al. 1974~. Such figures are undoubtedly a gross overestimate, because the rate of removal is markedly dependent upon concentration and appears to follow Michaelis-Menten kinetics. The rate of removal at concentrations equivalent to those in the atmosphere is far lower than when abnormally high concentrations are used in the tests (G. W. Bartholomew and M. Alexander, Cornell University, personal communication). Other estimates suggest that the earth's land surface removes 8 x 109 g of carbon monoxide per hour (Heichel 1973) and that the rate of removal ranges from 4.5 to 14 x 1014 g per year (Nozhevnikova and Yurganov 1978~. Despite the disparity in estimates for removal, it is generally believed that soils are a major sink and that microorganisms in soil are chiefly responsible for the removal (NRC 1977d, Liebl and Seller 1976~. Many individual microbial species are able to metabolize carbon monoxide in laboratory culture (Nozhevnikova and Yurganov 1978, Bartholomew and Alexander 1979~. Investigations with soils suggest that, in the few soil samples investigated, the microorganisms consuming carbon monoxide are neither heterotrophs using carbon monoxide as a carbon source nor autotrophs using it as a source of energy; rather the responsible organisms co-metabolize the gas (Bartholomew and Alexander 1979, and personal communication). Ethylene. Soils also remove ethylene from the gas phase. Little of this removal occurs in sterilized or air-dried soil, but the reaction is rapid in moist and nonsterile soil. Such data indicate that the process is microbial. The organisms involved are apparently aerobic species, probably bacteria. The few rates that have been calculated in laboratory studies indicate that from 0.14 to about 14 nmol can be removed per gram of soil per day (K. Smith et al. 1973, Abeles et al. 1971~. In aquatic ecosystems ethylene is oxidized by the same bacteria that oxidize methane. Under similar conditions ethylene usually is used preferentially (Flett et al. 1975~. Acetylene. Acetylene can apparently be readily destroyed, again by microbial processes, since it does not occur in sterilized or air-dried soil. The rate of removal of acetylene at a moisture level of 50 percent of the water-holding capacity of the soil is 0.24 to 3.12 nmol per gram of soil per day, depending on the composition of

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108 water, and soil. Sometimes the influences are indirect; for example, the solubility of many heavy metals is enhanced at low pH--i.e., high hydrogen ion concentration--and toxicity increases correspondingly. When direct interactions enhance the effects of one or both pollutants, the relationship is termed synergism; the result is more than additive. When interactions mitigate harmful effects, the relationship is termed antagonism. - Terrestrial Ecosystems Menser and Heggestad (1966) were the first to demonstrate the synergistic effect of two gaseous pollutants upon plants. They reported injury to several tobacco cultivars when these cultivars were exposed simultaneously to concentrations of SO2 and O3 that individually would not injure the plants. Dochinger et al. (1970) and Houston (1974) reported a similar effect of SO2 and O3 in a tree species, Pinus strobus. Table 6.2 gives a summary of the synergistic effects of SO2 with other gaseous pollutants on native North American trees. SO2 and NO2, and NO2 and NO are known to have additive effects on the pea, Pisum sativum (Figure 6.5~. Reinert et al. (1975) review pollutant interaction effects on terrestrial vegetation, including examples of synergisms and antagonisms. The authors point out that such pollutant interactions depend on the genetics and physiology of the target organism, the environmental conditions, and the concentration of pollutants--which may explain some of the contradictory findings reported in the literature. Holdgate (1979a) has made a more recent review; he believes different investigations have yielded different conclusions because of a lack of standardized methods and experimental conditions. Genetic, physiological, and environmental factors must all be standardized before exact comparisons are possible. Interesting synergistic interactions have been described between ozone and both cadmium and nickel (Czuba and Ormood 1975), in their toxic effects on a number of horticultural crops. In contrast, the presence of copper in Sudbury area soils was reported to reduce the toxicity of fumigations by SO2 for some grass species (Toivonen and Hofstra 1979~. The mechanisms of these metal-gas interactions are not known. Affects through stomata! activity appear likely. A number of authors have observed an increased susceptibility of forests to insect outbreaks after exposure to SO2 and other atmospheric pollutants. This subject is reviewed by Renwick and Potter (1981) who attribute the infestations to an increased output of insect attracting terpenes. Aquatic Ecosystems High contents of hydrogen ion in freshwater bodies enhance the solubility of a number of elements normally present in soils and sediments. These include aluminum, manganese, zinc, and iron. Also

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109 C) C) C) U. C) a Ct P" Cal Ct _, o 5 - o ._ 3 o ._ Ct ._ o C) I: ._ Cal o V, Cat o .~ Ct of A) .~ He o Cal C) o Ct bO o o o C.) . X Ct ~ ._ ~ Cal o . - d c C) ~ ~ ~ _ ~ ~ so ~ ~ U: ~ ~ ~ _ 50 o o Cal Cal ~ ~ ~ ^ = S = .=, ~ ~ ~ ~ O _ ~ 3 ~ ~ 3 o ~ Ct Ct _ ~ ~ ~ . ~ . . 3 ~ , , ~ ~ ~ _ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~o ~ o 0 ~ ~ ~ ~ ~ ~ ~ ,, E X ~ ~ o E -~ ~ ~ ~ =, == D ~ ~ X C ~ ~ .~0 ~ ~ O Z ~ 0m 0 0m P4 ', O ~ ~ O O O ~/ O O ~ ~ . . . . . . . O O O O O O O C~ ,: 3 ~ 3 - , oo o oo C~ _ U, C) o U3 cn Ct C~ C~ .. V O U,

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110 2D _ E 15 ~ - (a) ' 5 (b) / ' ~m~ ~ 2S 25 'at ''K2S \ l E~:::...:~-.. )\ > > ..? ~ ~ 0 26~ ~0~'' 50 50 2 ~ FIGURE 6.5 Interactive effects of pollutants. (a) Effects of SO2 and NO2 pollution on the rate of net photosynthesis in pea, Pisum s~ztivum (from Bull and Mansfield 1974). (b) Effects of NO and NO2 pollution on the rate of net photosynthesis in tomato (from Capron and Mansfield 1977). Note that in both cases combinations of pollutants have a greater effect than either gas does alone. SOURCE: Holdgate (1979b).

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111 increased is the toxicity of metals, including copper, lead, zinc, and nickel {Spry et al. 1981~. The presence of elevated calcium at low pH, however, reduces the otherwise high toxicity of aluminum--i.e., it acts as an ameliorative for both terrestrial higher plants and for aquatic freshwater plankton (Hutchinson and Collins 19781. This appears to be due to competitive inhibition of aluminum uptake by calcium. Higher calcium concentrations also appear to cause Crustacea to be less sensitive to hydrogen ions (Figure 6.6~. Among toxic metals a rather wide range of interactions occur. Nickel and copper in lake waters contaminated by the Sudbury smelters act synergistically in their effects on various green algae (Hutchinson 1973, Hutchinson and Stokes 1975~. Stokes (1975) has shown that this effect relates to the initial separation of copper and nickel in the cell, with copper moving across the plasmalemma while nickel is bound to the cell wall. Eventually, sufficient damage occurs to the cell membrane that it becomes leaky and nickel enters also, this being the synergistic phase. Nickel-copper synergism has also been described for higher plants (Whitby and Hutchinson 1974~. In studies of the floating aquatic plants Lemna valdiviana and Salvinia natans it was found that, in addition, cadmium and zinc also - acted synergistically. Frond numbers increased with the tissues' concentrations of the two elements, and these were mutually enhanced by the presence of the second element (Hutchinson and Czyrska 1973~. Both light intensity and the specific range of concentration influenced the outcome. Water quality criteria based on laboratory tests of single pollutants appear to be inadequate for situations where several pollutants enter a water body. Wong et al. (1978) found that a mixture of heavy metals added to Great Lakes water or culture medium at the maximum permissible concentration levels for each was very toxic to freshwater algae. Diatoms were even more sensitive than either green or blue-green algae. Similar findings were reported by the ME:LIMEX study in Switzerland, where a mixture of metals was added to lake water at maximum permissible concentrations for each. Toxicity to phytoplankton (Gachter and Mares 1979) and heterotrophic microorganisms (Bossard and Gachter 1979) was reported for the mixture of metals, although singly the metals caused no observable damage. On the other hand, the metals caused populations of benthic organisms to increase, presumably because inhibition of the decomposer microbiota allowed more oxygen to accumulate at the mud-water interface (Lang and Lang-Dobler 1979~. Another example of synergistic effects of metals in animals is the strong teratogenicity of the combined injection of cadmium and lead compared to the effects of administration of either of the metals separately. In contrast, metal interactions can protect against the normal toxic effects of a single metal. Such interactions have been described for mammals and fish (Cherian and Goyer 1978, Nordberg 1978, Parizek 1978, Levander 1977, Groth et al. 1976, Ganther et al. 1973~; for invertebrates (Talbot and Magee 1978~; and for unicellular green algae (Hutchinson 1973~. The biochemical mechanism of the protective

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112 I 1.00 an Lid at ~ 0.50 0.30 0.23 B. .................. e ~ . . AS E L LU S AD UAT I C U S: - : ~ - - - ~ P R E S ~ N T . . . . . . ~ ~ . . . ~ ~ . . ~ . . . . . . . . . . . . . . . . . C1 ~ I, n U. o 4.2 4.8 5.2 6.0 7.0 HYDROGEN- ION CONCENTRATION (pH) FIGURE 6.6 A model for tolerance limits of Asellus aquaticus toward low water hardness and low pH. The species is absent in lakes belonging to areas B. C, and D. Arrows indicate that limits may be moved through synergism with other factors. One degree dissolved hardness (1 dH) = 10 mg CaO/l. SOURCE: Okland (1980).

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113 effect is often the induction of metallothionein, which acts nonspecifically to chelate metals (Kagi and Nordberg 1979~. For example, exposure of an organism to any one of cadmium, mercury, silver, copper, or zinc causes increased tolerance to any of the other metals upon subsequent exposure (Winge et al. 1975~. When the protective effect involves selenium (Ganther 1978), the ameliorative action is thought to involve the diversion of metals from the biochemical sites of toxic action (Bark et al. 1974, Komsta-Szumska et al. 19761. Previous exposure also affects the organisms' response to toxic concentrations of metals. Some metals, such as silver, arsenic, cadmium, mercury, lead, and tin are less toxic when sub-lethal doses are given prior to a dose that normally produces mortality. Others, such as barium, chromium, and iron, have toxicity enhanced by pretreatment (Yoshikawa 1970~. In cases where tolerance increases, the underlying mechanism may involve metallothionein (Leber and Miya 1976, Probst et al. 1977), selenoproteins (Sandholm 1974, Prohaska and Ganther 1977), glutathione (Congiu et al. 1979), or other mechanisms (Tendon et al. 1980~. Increased tolerance to metals may also be due to physiological mechanisms, such as increased excretion of metals induced by pre-exposures {Levander and Argrett 1969, McConnell and Carpenter 1971~. A mixture of detergents and mercury or cadmium was found by Calamari and Marchetti (1973) to have effects on rainbow trout different from the effects of detergents or metals alone. Anionic detergents plus metal had more than additive effects, while nonionic detergents plus metal had less than additive effects. On the other hand, phosphorus and nitrogen were found to increase the tolerance of algae for heavy metals, as demonstrated in the tolerance of Stigeoclonium tenue Kutz to heavy metals in South Wales (McLean 1974) and the increased tolerance of microbiota and algae to arsenic in waters enriched with nutrients (Brunskill et al. 1980~. As is well known from experience with human illnesses, stress often renders organisms susceptible to diseases of various types. For example, Hetrick et al. (1979) found that exposure of rainbow trout to copper increased their susceptibility to infectious hematopoetic necrosis and other viral diseases. The general relationship between pollution stress and the incidence of infectious diseases in fish was reviewed by Snieszko (1974~. In the marine environment, mercury contamination is accompanied by enhanced concentrations of selenium in all investigated species of mammals, birds, and fish--possibly due to a normal homeostatic regulation. It seems likely that selenium exerts a protective action against mercury toxicity in the marine environment, decreasing the detrimental effects of mercury on reproduction behavior, growth, etc., and thus protecting the population and the ecosystem. In freshwater ecosystems, high selenium retarded the uptake of mercury by freshwater organisms (Rudd et al. 1980~. On the other hand, Beijer and Jernelov (1978) have shown that high selenium increases the retention of mercury by aquatic organisms leading to bioaccumulation of mercury in fish and a higher body burden in the individual. This might

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114 counteract the positive effect of selenium in decreasing mercury uptake and toxicity. In the environment, the presence of several pollutants and other kinds of stress is the norm. We must develop a fuller understanding of the mechanisms of interactions. Often, synergisms and antagonisms may occur simultaneously, so that no apparent effect may be detectable. For example, Eaton (1973) exposed Pimephales promelas to a mixture of copper, cadmium, and zinc for one year. First analyses showed the mixture to be no more toxic than zinc alone had been in earlier studies. When various effects were evaluated, however, it appeared that zinc toxicity was unchanged, while copper toxicity had increased and cadmium toxicity had decreased. Resistance to Pollutants There is considerable evidence that both individuals and populations can develop resistance to a wide variety of pollutants. At the individual level, increased resistance appears most often to be acquired through enzyme induction and the appearance of toxicant-binding proteins. The degree of resistance that can be acquired appears to vary both from one species to another and one toxicant to another, ranging from no increased tolerance to increases of several thousand times. Resistance to several toxic metals by a wide variety of aquatic organisms appears to be the result of synthesis of metallothionein (G. Brown 1976), a protein that reportedly binds metals to sulfhydryl groups and prevents them from diffusing across cellular membranes into sensitive tissues or interacting with critical enzymes (Cherian and Goyer 1978, Brown and Parsons 19781. This protein develops in the organism in response to exposure to sublethal concentrations of several metals--Hg, Cd, Cu. Zn, Ag, and Sn--(Winge et al. 1975) after which resistance to a number of metals is increased. The amount of resistance that can be developed is high in most fishes but low in zooplankton (Brown and Parsons 1978~. The protein has been shown to occur in most phyla of plants and animals (Brown 19801. Similar multipollutant resistance appears to occur with pesticides and chlorinated hydrocarbons. Exposure to sublethal levels of one chlorinated hydrocarbon often increases tolerance to others. In the case of DOT, three mechanisms have been found to be involved: (1) a membrane barrier to DOT passage, (2) a structural difference in myelin, and (3) an efficient blood-brain barrier. Wells and Yarbrough (1972) and Moffett and Yarbrough (1972) discuss the details of these mechanisms. A high intrinsic genetic variability in a population increases its chances of having some resistant survivors to a broad range of pollutant stresses. Species that occupy a wide variety of habitats under natural conditions tend to have high genetic variability. For example, the ubiquitous algal genera Chlorella and Scenedesmus will survive concentrations of heavy metals lethal to most other algal species (Stokes et al. 1973~.

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115 Structures or behaviors of some organisms protect them from atmospheric pollutants (Jacobson 1980~. Waxy cuticles, surface hairs with hydrophobic properties, flat or narrow shapes, and vertical orientation tend to protect leaf surfaces from penetration of aqueous solutions of pollutants. Reproductive organs may be protected by flowers with inverted openings or flowers that close during cloudy periods. Other flowers open only when triggered by the weight of insects. Duration of pollination and number of pollinating flowers are also considerations. Salts on leaf surfaces or internal buffering reactions may also offer protection (Table 6.3~. Different genotypes in single plant or animal species are known to vary in their susceptibility to pollutants, as do different species within the same genus (Taylor 1978~. Animal populations also evolve characteristics consistent with a polluted environment. For example, in industrial areas of Britain, elimination of pollutant-sensitive lichens from the stems of trees caused the disappearance of light-colored peppered moths, which had relied on the lichens for camouflage from insectivorous birds. A previously rare soot-colored "melanic" variant of the same species replaced the light form as the dominant genotype. The melanic form was also better adapted to eating pollutant-laden vegetation (Kettlewell 1955, 1956~. Some resistance, including that of the melanic peppered moths and tolerance of ryegrass to coal-smoke pollutants, is known to have developed within the past century or two. The gene pools of organisms are well prepared to adapt to changing environmental conditions, as long as the changes occur slowly enough for adaptation to occur. This is usually a function of the length of the generation time for a given species. Microbes can complete a life cycle in hours; larger mammals and tree species may take decades to centuries. In areas of airborne fallout of contaminating metals and on old mine waste dumps, numerous examples of genotypes highly tolerant of normally toxic metal levels have been found. Such selection has been reported for a wide variety of higher plants, ferns, green or blue-green algae, bacteria, and fungi (e.g. Bradshaw 1952; Jowett 1958; Stokes et al. 1973; Tatsuyamo et al. 1975; Allen and Sheppard 1971; Cox and Hutchinson 1979, 1980) and for a number of metals and combinations of metals. Past Efforts to Predict Widespread Toxic Effects Both scientific induction and unplanned-for catastrophes have led to an understanding of biological effects of pollutants. Perhaps most illustrative is the example of DOT. Before its extensive broadcast about the environment as an insecticide following World War II, its potential effects upon nontarget organisms were recognized by several scientists, including Cottam and Higgins (1946~. They pointed out that agricultural applications would affect wildlife and game and were especially concerned about its entry to streams, lakes, and coastal bays, where the crabs and fish would be sensitive to this toxic halogenated hydrocarbon.

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116 TABLE 6.3 Plant Processes and Characteristics That May Increase Tolerance to Acid Precipitation - Exclusion Leaf orientation and morphology Chemical composition of cuticle Flower orientation Protection of sexual organs Pollination mechanism Neutralization Salts on leaf surfaces Buffering capacity of leaves Metabolic Feedback Reactions Enzymatic reactions that consume hydrogen ions or yield alkaline products SOURCE: Jacobson ( 19 80).

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117 Subsequent events have confirmed that higher trophic levels are jeopardized by exposure to DDT. One of the more publicized effects upon the marine ecosystem involved the reproductive failures of the brown pelican population on Anacapa Island, off the California coast, from 1969 to 1972. The accumulation of DDT and its degradation products, primarily DOE, in marine organisms that were the food for the pelicans initiated the problem. The source of the pesticide was allegedly wastes from a manufacturing plant in Los Angeles, which were introduced to the oceans in sewer outfalls. The pelicans produced thin, friable egg shells, which broke easily (Risebrough 1972~. DDT usage has been severely restricted since the early 1970s by the United States and many nations of the Northern Hemisphere. The brown pelican population on Anacapa Island has shown breeding recovery since 1972 when the DDT dumping was stopped. Despite ODE residues in the sediments, the success rate for young per nest had risen from 0.04 in 1972 to 0.88 in 1975 (Schreiber 1980~. This recovery is true in other locations also. With nuclear weapons development in the early 1950s, scientists from several countries became concerned about the entry of artificially produced radionuclides from power plants to the atmosphere and to the oceans. The ingestion of food containing radionuclides from the sea and the exposure of individuals to environmental radioactivity were minimized through limitations of the amounts of wastes emitted from nuclear plants to their surroundings. The greatest amounts of artificial radionuclides introduced to the environment come from the nuclear processing plant at Windscale, England. British environmental scientists have developed protocols to regulate the discharges on the basis of the "critical pathways technique," through which nuclides posing dangers to human health are identified and the critical population for exposure is protected. As a consequence of the resultant regulatory measures, there appears to be no danger to the population liable to exposure at the present time. SUMMARY Accumulation of pollutants in ecosystems is affected by a number of physical factors at the surface of the ecosystem, such as the amount of surface area presented by a forest canopy or turbulence near the air-water interface. The form of the pollutant--gas, aerosol, or large particulates--is also important. Ice and snow cover and thermocline formation may protect freshwater ecosystems from dissolved pollutants at certain times of the year, but can cause higher than average inputs at others. The thermocline regulates the passage of pollutants to and from the deep ocean. Soils and aquatic sediments tend to accumulate many pollutants, thereby lowering toxicity to pelagic or above-ground forms but raising toxicity for benthic or soil organisms. The binding in soils and sediments for some elements depends on oxidation-reduction potentials, which are lowered when anoxic conditions develop. Many organic constituents are transformed by microbes in soils or sediments into

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118 other organic compounds, which might be either toxic or harmless, or into inorganic products, CO2 and H2O. Substances that are not degraded in terrestrial ecosystems will eventually be transferred to aquatic ecosystems via water flow or soil erosion; hence, higher concentrations of toxicants are likely to occur in aquatic ecosystems. Aquatic sediments often provide a reservoir of datable toxic deposits and fossil organisms, from which a history of pollution might be reconstructed. At the species or individual level, pollutants may be bioconcentrated, bioexcluded, or biomagnified by passage up the food chain. Gaseous pollutants have their greatest effect on terrestrial ecosystems, because the air-water interface offers to aquatic organisms some degree of protection from episodic events. When many pollutants are introduced to an ecosystem, effects are in many cases synergistic--i.e., effects are greater than additive. In some other cases less than additive effects have been noted. Natural selection has caused some species to develop resistance to pollutants. Such genetic adaptation requires many life cycles, and no examples are known for species with life cycles over one year long. Individual resistance may, however, develop in individuals exposed to sublethal concentrations of pollutants.