Atmospheric deposition of persistent pollutants governs uptake by zooplankton in a pond in southern...

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Atmosphenc Enuironment Vol. 23, No. 10, pp. 2151-2158, 1989. cOw6981/89 13.00+0.00 Printed in Great Britain. c 1989 Pergamon Press plc ATMOSPHERIC DEPOSITION OF PERSISTENT POLLUTANTS GOVERNS UPTAKE BY ZOOPLANKTON IN A POND IN SOUTHERN SWEDEN PER LARSSON Limnology, Department of Ecology, P.O. Box 65, S-221 00 Lund, Sweden (First receioed 4 November 1988 and receivedfor publication 18 April 1989) Abstract-The atmospheric fallout of PCBs, ZDDT and y-HCH (lindane) to a pond in southern Sweden was studied in relation to uptake by freshwater zooplankton. The extent of the atmospheric deposition of PCBs and lindane was reflected in the uptake by the zooplankton; high deposition in the spring and autumn resulted in high uptake by the organisms while a lower uptake during summer was a result of lower deposition. The atmospheric deposition of ZDDT was dominated by p,p-DDT, p,p-DDE and o,p-DDT, while p,p-DDE and p,p-DDD were dominant in zooplankton. These differences in XDDT composition are probably attributed to microbial conversion; as a result, levels in the zooplankton appeared not to be governed by atmospheric deposition. The availability of the previously airborne, persistent pollutants to zooplankton was a function of the compounds chemical properties, e.g. water solubility, and the form of deposition. The results show that atmospheric deposition is an important route by which persistent pollutants are transported to Holarctic, aquatic ecosystems. Key word index: Atmospheric deposition. airborne fallout, zooplankton, Daphnia magna, chlorinated hydrocarbon, PCB, DDT, lindane, HCH. INTRODUCTION Numerous investigations have shown the importance of the atmosphere as a transport route for persistent pollutants. PCBs, lindane and DDT have been detec- ted in the air over the Arctic and Antarctic, as well as in the atmosphere overlying the Sargasso Sea and Indian Ocean (Oehme and Maiio, 1984; Tanabe et nl., 1983; Bidleman and Olney, 1975; Bidleman and Leon- ard, 1982). For chemicals used in industrial processes, concentrations decrease along a gradient from urban areas to more remote regions, as has been reported for phthalate esters in Norway (Lunde et al., 1977) and for polyaromatic hydrocarbons along the Niagara River in the U.S. (Hoff and Chan, 1987). Persistent and toxic compounds may be formed when more or less harm- less precursors are incinerated, as in the case of chlorinated dioxins being formed when phenol and hydrochloric acid are burned (Eklund et al., 1986). In the atmosphere these pollutants are mainly pre- sent in the gas phase, which faciliates their transport over long distances (Doskey and AndrCn, 1981). Dur- ing rain events the compounds may partition to airborne water or adsorb to particles resulting from human activity or released by natural sources. They subsequently reach the ground as airborne fallout. Presumably they are additionally transported to ter- restrial and aquatic ecosystems in their volatilized stage. Although our knowledge regarding the atmospheric transport of chlorinated HCs is extensively studied, the uptake of transported substances by organisms as well as their biological effects in the ecosystem is terra incognito. This is true for both terrestrial and aquatic environments. In contrast, the effects of acidic fallout and acidic rain on ecosystems are better known (e.g. Jensen and Snekvik, 1972). This is also the case for heavy metals, where high atmospheric fallout resulting from emissions by the smelting industries results in high uptake by animals nearby the sources (e.g. Havas and Hutchinson, 1982). Zooplankton have been proposed as playing a major role in distributing organochlorine residues from atmospheric fallout throughout the ocean depths (Harding, 1986). Similarly, Ware and Addison (1973) related temporal irregularities in PCB uptake in zoo- and phytoplankton to variability in atmospheric in- puts. Zooplankton, which serve as food for many species of fish, provide an important link in the transfer of dissolved and particle-bound persistent pollutants to higher levels in aquatic food webs (McManus et al., 1983). However, there is no exper- imental evidence suggesting that zooplankton accu- mulate pollutants resulting from atmospheric depo- sition. However, the uptake of previously airborne or- ganic, persistent pollutants in aquatic biota can be followed. If the airborne fallout of a given pollutant is studied in an ecosystem not receiving inflow from any other source, while uptake of the compound by the biota is recorded simultaneously, the importance of atmosphere as a source can be evaluated. There are two major prerequisites for such an approach. First, atmospheric fallout has to be determined with reason-

Transcript of Atmospheric deposition of persistent pollutants governs uptake by zooplankton in a pond in southern...

Page 1: Atmospheric deposition of persistent pollutants governs uptake by zooplankton in a pond in southern Sweden

Atmosphenc Enuironment Vol. 23, No. 10, pp. 2151-2158, 1989. cOw6981/89 13.00+0.00

Printed in Great Britain. c 1989 Pergamon Press plc

ATMOSPHERIC DEPOSITION OF PERSISTENT POLLUTANTS GOVERNS UPTAKE BY ZOOPLANKTON IN

A POND IN SOUTHERN SWEDEN

PER LARSSON

Limnology, Department of Ecology, P.O. Box 65, S-221 00 Lund, Sweden

(First receioed 4 November 1988 and receivedfor publication 18 April 1989)

Abstract-The atmospheric fallout of PCBs, ZDDT and y-HCH (lindane) to a pond in southern Sweden was studied in relation to uptake by freshwater zooplankton. The extent of the atmospheric deposition of PCBs and lindane was reflected in the uptake by the zooplankton; high deposition in the spring and autumn resulted in high uptake by the organisms while a lower uptake during summer was a result of lower deposition. The atmospheric deposition of ZDDT was dominated by p,p-DDT, p,p-DDE and o,p-DDT, while p,p-DDE and p,p-DDD were dominant in zooplankton. These differences in XDDT composition are probably attributed to microbial conversion; as a result, levels in the zooplankton appeared not to be governed by atmospheric deposition. The availability of the previously airborne, persistent pollutants to zooplankton was a function of the compounds chemical properties, e.g. water solubility, and the form of deposition. The results show that atmospheric deposition is an important route by which persistent pollutants are transported to Holarctic, aquatic ecosystems.

Key word index: Atmospheric deposition. airborne fallout, zooplankton, Daphnia magna, chlorinated hydrocarbon, PCB, DDT, lindane, HCH.

INTRODUCTION

Numerous investigations have shown the importance of the atmosphere as a transport route for persistent pollutants. PCBs, lindane and DDT have been detec- ted in the air over the Arctic and Antarctic, as well as in the atmosphere overlying the Sargasso Sea and Indian Ocean (Oehme and Maiio, 1984; Tanabe et nl., 1983; Bidleman and Olney, 1975; Bidleman and Leon- ard, 1982). For chemicals used in industrial processes, concentrations decrease along a gradient from urban areas to more remote regions, as has been reported for phthalate esters in Norway (Lunde et al., 1977) and for polyaromatic hydrocarbons along the Niagara River in the U.S. (Hoff and Chan, 1987). Persistent and toxic compounds may be formed when more or less harm- less precursors are incinerated, as in the case of chlorinated dioxins being formed when phenol and hydrochloric acid are burned (Eklund et al., 1986).

In the atmosphere these pollutants are mainly pre- sent in the gas phase, which faciliates their transport over long distances (Doskey and AndrCn, 1981). Dur- ing rain events the compounds may partition to airborne water or adsorb to particles resulting from human activity or released by natural sources. They subsequently reach the ground as airborne fallout. Presumably they are additionally transported to ter- restrial and aquatic ecosystems in their volatilized stage.

Although our knowledge regarding the atmospheric transport of chlorinated HCs is extensively studied, the uptake of transported substances by organisms as

well as their biological effects in the ecosystem is terra incognito. This is true for both terrestrial and aquatic environments. In contrast, the effects of acidic fallout and acidic rain on ecosystems are better known (e.g. Jensen and Snekvik, 1972). This is also the case for heavy metals, where high atmospheric fallout resulting from emissions by the smelting industries results in high uptake by animals nearby the sources (e.g. Havas and Hutchinson, 1982).

Zooplankton have been proposed as playing a major role in distributing organochlorine residues from atmospheric fallout throughout the ocean depths (Harding, 1986). Similarly, Ware and Addison (1973) related temporal irregularities in PCB uptake in zoo- and phytoplankton to variability in atmospheric in- puts. Zooplankton, which serve as food for many species of fish, provide an important link in the transfer of dissolved and particle-bound persistent pollutants to higher levels in aquatic food webs (McManus et al., 1983). However, there is no exper- imental evidence suggesting that zooplankton accu- mulate pollutants resulting from atmospheric depo- sition.

However, the uptake of previously airborne or- ganic, persistent pollutants in aquatic biota can be followed. If the airborne fallout of a given pollutant is studied in an ecosystem not receiving inflow from any other source, while uptake of the compound by the biota is recorded simultaneously, the importance of atmosphere as a source can be evaluated. There are two major prerequisites for such an approach. First, atmospheric fallout has to be determined with reason-

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ably good temporal resolution. Second, the organism to be studied must have a short generation time, i.e. no longer than the time needed to measure the airborne fallout. The latter condition is met by cladoceran zooplankton (Larsson, 1986) that have a generation time of 4-5 days and a lifespan of 20-30 days at a water temperature of 25°C (Pennak, 1978). If these two prerequisites are fullfilled, uptake of the pollutants by different generations of the organism can be related to the extent of airborne fallout on the various sampling occasions. If, however, the generation time of the organism is too long (ranging over several measure- ments of the airborne fallout), this relation cannot be established. Instead a high fallout of the pollutant would result in high levels in the organism and ‘camouflage’ any subsequent uptake associated with reduced fallout.

In order to evaluate the atmospheric fallout of persistent pollutants in relation to uptake by aquatic organisms, the fallout of PCBs, DDT and its metab- olites and lindane (y-hexachlorocyclohexane) were recorded at a small pond in southern Sweden. Simul- taneously, zoopIankton cladocerans (~aphnia magna) were sampled and analyzed.

MATERIALS AND METHODS

Sampling

The study was performed at a small (2 ha) eutrophic pond with a mean depth of 0.9 m. The pond is situated near to the sea and receives no PC&, DDT or lindane from sources other than the atmosphere. The pond water contains the nutrients phosphorous and nitrate in high amounts, about 1 mg L’ - 1 and 3 mg 8 - I, re- spectively. The pH of the water was 8.7 during the summer; the alkalinity was 4 meqv e - 1 and the con- ductivity about 78 mSm_r. The temperature of the pond was 58°C in April; it then increased, reaching a peak of 20-22°C in July and decreased to 8-10°C in September/October.

In April 1986 two fallout samplers were placed nearby the pond, 25 m apart and 2.5 m above ground. The equipment, the same as that used by Sadergren (1972,1975) and Larsson and Okla (1989), consisted of a nylon net imprecated with a silicone oil. The lipophilic oil retains chlorinated hydrocarbons in rainwater as well as dry deposition. The samplers were exposed for about 3 weeks, which was the minimum time needed to obtain a sample with a pollutant amount significantly higher than that measured on non-exposed nets. The samplers were then removed and unexposed ones set in place.

Beginning in April 1986, zoc+ankton in the pond were sampled with a net. Sampling was carried out once or twice a week. The zooplankton samples were dominated by Daphnia magna, a large (< 4 mm) clado- ceran zooplankton. The sampling of atmospheric fall- out and zooplankton was terminated in November 1986.

Analytical methods

Persistent pollutants adsorbed to the fallout screens were extracted with hexane in a Soxhlet extractor according to Sodergren (1972,1975). The extracts were treated with concentrated H,SO, until no colour was observed in the acid phase (revealing that no oxidation was still occurring), and then evaporated to 0.5 ml.

Zooplankton (l&20 g) were dried at 60°C to con- stant weight. The pollutants and fat were extracted with acetone/hexane (1: 1) in an ultrasonic bath (Lars- son, 1986). The extract was then divided into two samples. One subextract was used for fat determin- ation; it was heated in a water bath (70°C) to dryness; acetone was added to remove water and the residue was determined as fat on a balance. The other sub- extract, used to analyze persistent pollutants was treated with concentrated H2S0, as described above, evaporated to 0.5 ml and the pollutants analyzed by gas chromatography.

PCBs, XDDT and lindane were analyzed by capil- lary gas chromatography according to Okla and We&n (1984). The chromatographic properties were optimized for PCBs; in this way 28 PCB congeners could be quantified (Ballschmiter and Zell, 1980; Drinker and H~llebr~d, 1984). PCB congeners were identified according to their IUPAC numbers (Balls- chmiter and Zell, 1980). The elution of the PCB compounds in the field samples were compared with those of an industrial PCB mixture, Clophen A 60 (a mixture containing 60 weight% Cl), a comparison that resulted in the best ‘match’ for PCBs in atmospheric fallout (Larsson and Okla, 1989) and in zooplankton.

PCB evaluation technique

To compare the PCB composition in atmospheric fallout to that in zooplankton a frequency analysis was performed. In zooplankton samples, five PCB congeners were always found: PCB,, (2,2’,3,5’,6- pentachlorobiphenyl), PCBlo, (2,2’,4,5,5’-pentachloro- biphenyl), PCB, i0 (2,3,3’,4’,6pentachlorobiphenyl), PCB*~*(2,~,3,4,~5’-hexachlorobiphenyl) and PCB,,, (2,2’,4,4’,5,5’-hexachlorobiphenyl). The next most fre- quent congeners were 2,2’,3,4’,5’,6-hexa- (PCB,,,) and 2,2’,3,5,5’,6-hexachlorobiphenyl (PCB, 5 r). which oc- curred in 93 and 87% of the zooplankton samples, respectively. Levels of these five most frequent PCBS were quantified in the zooplankton. The same five PCB congeners were quantified in the atmospheric fallout samples in order to be able to compare the extent of PCBs in the fallout with that of the ZOO-

plankton. In the following context the PCB values given below represent the sum of these five congeners.

RESULTS

The atmospheric fallout of PCBs and lindane was reflected in the zooplankton (Figs 1, 2). Thus, uptake

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Zooplankton uptake of persistent pollutants 2153

F 3000

E N

$2000 c Lo

8 ; 1000

4 =; IL 0

-800 2 P

- 600 E s 2 s

-400 z

V' :

-200 -f

z

-I Apr 'May ' Jun ' Jul ' Aug ' Sep' Oci ' NW L

'

1986

Fig. 1. Atmospheric fallout of PCBs and uptake by zooplankton in a pond in southern Sweden. The correlation between atmospheric deposition of the compounds and levels

in zooplankton is shown in the box (R,=0.71, p<O.OOl).

/ 3000 2000 1000

a

g

g gj 5 2 w .c

G 0 s.

1986

Fig. 2. Atmospheric fallout of Iindane and uptake by zo- oplankton in a pond in southern Sweden. The correlation between atmospheric deposition of the compounds and levels in the zooplankton is shown in the box (R, =0.75, p <O.OOl).

of PCBs by the zooplankton was high in the spring (200-700 ngg-i extractable fat) when atmospheric fallout of the compounds was high (about 0.7 pgm-’ month-‘). During the summer as the atmospheric fallout decreased to a low value of 0.2 pg PCB m-* month- I, levels in zooplankton decreased to 100 ngg-‘. As the atmospheric deposition of PCBs increased during October, to 2.2 pgm-* month- ‘, levels in zooplankton increased, reaching 600 ng g- i. The atmospheric fallout of PCBs and levels in D. magna were correlated (Spearman rank correlation, R, =0.71, p<O.OOl).

The PCB congener taken up to the highest degree by zooplankton was PCB,, (Fig. 3) followed by

PCB,,, and PCB,,,, compared to the amounts in atmospheric deposition. The fat content of the zo- oplankton varied between 0.5 and 8.7% of the dry weight. No relation between the percent of fat and pollutant levels in the organisms could be established.

The atmospheric fallout of lindane was higher than that of PCBs, and a deposition of 8.0 ,ug m-* month-’ in April and May resulted in an uptake of

b n PCB95 n PC8101

1986

Fig. 3. Atmospheric fallout of the five domi- nating PCB congeners (lower) to a pond in southern Sweden and uptake of the same congeners by zooplankton (D. magna, upper).

400-2700 ng g- ’ extractable fat in zooplankton. Dur- ing June to September less fallout was recorded (about 1.0 pgrne2 month-‘) and levels of lindane in zooplankton decreased to below 200 ng g- ‘. In Octo- ber lindane levels increased in zooplankton to 2400 ngg-’ as the atmospheric deposition increased (to6.0pgmV2 month- ‘). The atmospheric deposition of lindane and uptake by zooplankton were correlated (R,=0.75, p<O.OOl).

For ZDDT, there was no apparent correlation recorded between atmospheric fallout and uptake by zooplankton (Fig. 4). A high deposition of EDDT in April and May (about 4.4 pgrn-’ month-‘) did not result in a high uptake. During summer lower at- mospheric fallout of EDDT was associated with low levels of EDDT in zooplankton. In October, when the atmospheric deposition of EDDT increased to 4.3 pgm-’ month-‘, levels in zooplankton also in- creased reaching 3700 ng g- ’ extractable fat.

The DDT metabolites in atmospheric fallout and in zooplankton were not the same. The atmospheric deposition was dominated by p,p-DDE and p,p-DDT and some o,p-DDT (Fig. 5). In contrast, zooplankton

Fig. 4. The atmospheric fallout of ZDDT and the uptake by zooplankton in a pond in southern Sweden.

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1986

Fig. 5. Composition (%) of p, p-DDT and metabolites in atmospheric fallout and zooplankton.

was dominated by p,p-DDE followed by p,p-DDD, while p,p-DDT was only occasionally found in zoo- plankton, and o,p-DDT was absent.

The availability to zooplankton of the persistent pollutants entering the pond via atmospheric depo- sition was defined as the quotient: uptake in zo- oplankton (ng g- ‘)/atmospheric deposition of the compound (pg m-’ month-‘). The highest quotient was recorded for the pentachlorobiphenyls: for PCB95 the quotient was 1660, while 570 and 560 were re- corded for PCBllO and PCBlOl, respectively. For the hexachlorobiphenyls PCB138 and PCB153 the quo- tients were lower, being 240 and 430. These quotient values were comparable to that of lindane, which was 190.

DISCUSSION

When released into the atmosphere, PCB, DDT and related compounds may be transported far from the source in gaseous or particulate states. The persistent pollutants enter the aquatic environment in gas-, liquid or particulate state, depending on the com- pounds’ physical or chemical properties, as well as on climatic factors, like temperature, wind velocity, pre- cipitation, etc (Larsson and Okla, 1989). The more water-soluble lindane is probably released into the pond water by precipitation, while the more lipophilic PCBs and DDT enter as vapors or associated to particles. Within the water the compounds are either dissolved or associated with dead or living particles (phytoplankton) or they form micelles again owing to their physical properties (Larsson and Sodergren, 1987). Lindane dissolves in water to a higher degree than do PCBs or DDT, which readily adsorb to particles. The compounds are then taken up by zooplankton directly from the water as a result of

equilibrium partitioning, and/or from dead or living particles as a result of the animals’ feeding activity (filtration).

As the atmospheric fallout of the pollutants varies over time, and, since fallout is the only source for the pond, total (dissolved + particulate) levels of the com- pounds in the water will correspondingly vary. The zooplankton will take up the chlorinated HCs at a rate determined by the partitioning of each compound; a high level in the water will result in a high uptake, a lower level in a lower uptake (Clayton et u!., 1977; Pavlou and Dexter, 1979). As D. magna has a life span of 20-30 days at 25°C and a generation time of 4-5 days (Pennak, 1978), each generation of daphnids will equilibrate with new levels of pollutant in the water. In this way atmospheric deposition of persistent pollu- tants to the pond are reflected in the zooplankton population.

The fallout samplers can only be regarded as semi- quantitative indicators of atmospheric deposition. This problem have been discussed by Sodergren (1975) for the silicone impregnated nets used in this study, by Bidleman and Christensen (1979) using Al pans sprayed with glycerine/water and by Eisenreich et al. (198 1) measuring the deposition of organochlorine pollutants using glycerol-coated glass-plates. In neither of these studies the efficiency with which the samplers capture vapor or particle-phase PCBs was known. Additionally, due to the multicomponent nature of the persistent pollutants, like the various vapor pressures, studies of the efficiency of fallout samplers have not been performed. However, depo- sition rates of PCBs in airborne fallout over southern Sweden (Siidergren, 1975), where similar to that meas- ured for sedimentation of PCBs in marine and limnic environments (Larsson, 1984). The author concluded in this study that PCBs deposited to the sediments of aquatic ecosystems originated from the atmosphere.

PCBS

The atmospheric deposition of PCBs was in the same order as that found by Larsson and Okla (1989) when comparing the five congeners chosen. The depo- sition of pollutants also showed the same seasonal pattern, with high fallout in the spring and autumn and lower in the summer. Uptake by zooplankton followed a similar pattern, reflecting the extent of the atmospheric fallout. The dominating mechanism de- termining uptake of PCBs by zooplankton in the field has been proposed to be equilibrium partitioning; i.e. the partitioning of the compounds between the sur- rounding medium and the fat pool of the animals (Hamelink et al., 1971,1976; Pavlou and Dexter, 1979; Clayton et al., 1977). Zooplankton have a high sur- face-to-volume ratio, and the effective surface area exposed to the pollutant is enhanced by the animals filtering activity. Thus uptake is fast, being a matter of hours (Wyman and O’Connors, t980; Brown et al.,

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1982; O’Connors et al., 1982), and follows a first order rate of kinetics (e.g. Harding, 1986). However, the hypothesis that uptake is governed by a true equilib- rium partitioning has been questioned (Larsson, 1986). If the proposal is correct, then the compounds should equilibrate with the lipid pool of the animals in accordance with levels in the water, resulting in depur- ation from the zooplankton as pollutant levels de- crease in the medium. This depuration could be apparent and explained, at least for cladocerans, by the generation time effect described above.

It has been speculated by McNaught (1982) that zooplankton consume airborne contaminants directly from surface slicks. As PCBs and other lipophilic contaminants are enriched in the surface film (e.g. Seba and Corcoran, 1969) this intake route of pollu- tants by cladocerans could be substantial. As the water body studied in this paper was shallow, the enrichment effect of the surface film in the presence of atmospheric deposition should have been greater compared with that occurring in a deep lake with a greater water volume. In shallow waters, the pollu- tants hit the surface and are readily taken up by the most abundant ‘particles’, i.e. the phyto- and zooplankton. These plankton only remain active for a short period, after which they die and add to the bottom sediment. The pollutants are withdrawn from the water phase and replaced by atmospheric depo- sition. The high productivity and short sedimentation time of the plankton results in that the major break- down occurs at the sediment surface, from where the pollutants may redistribute. However, the breakdown of biological material in shallow, eutrophic ponds is often incomplete (Wetzel, 1983) and the organic mate- rial strongly binds the pollutants. On the other hand, in deep lakes the main breakdown of biological matter occurs in the water phase, resulting in a circulation of pollutants in the upper water stratum (the epilimnion). This circulation probably leads to a mixing of these pollutants with those pollutants recently deposited from the atmosphere. Consequently, it is questionable whether the correlation between atmospheric depo- sition of pollutants and uptake by zooplankton can be shown for deep lakes, though this uptake route is of significance.

Penta- and hexachlorobiphenyls were the PCBs most frequently found in zooplankton. These chloro- biphenyls were the least chlorinated of the PCB congeners representing more than 1% of the total atmospheric deposition. Other PCBs were detected in zooplankton, especially in the spring and autumn, when the atmospheric deposition was higher than in the summer. It has been shown that biphenyls with a higher number of Cl substituents are more lipophilic and persistent than compounds with fewer Cl substi- tuents. Thus the former also accumulate in aquatic organisms to a higher extent than the latter (e.g. Hutzinger et al., 1974). This was, however, not the case for uptake by zooplankton in this study-for two possible reasons. (1) PCBs substituted with a high

number of chlorines take longer time to reach satura- tion in zooplankton when partitioned between water and the fat pool of the organisms (Zhang et al., 1983) compared with less chlorinated PCBs. The uptake of less chlorinated PCBs is thus faster and reach satura- tion in the fat during the lifespan of a short lived cladoceran. (2) The availability of highly chlorinated PCBs to zooplankton are less compared to biphenyls substituted with few chlorine atoms. Lower chlorina- ted congeners are more soluble in water, thereby increasing their availability, via direct uptake to cla- docerans. PCB,, has a water solubility of 54 fig/- ’ while the solubility of the two other pentachlorobi- phenyls are considerably lower, 26 pcge- ’ for PCBiol and 29 pg/-’ for PCB,,,, (Murphy et al., 1987). This could explain the higher bioavailability for PCB,,. More highly chlorinated PCBs may be more readily adsorbed to particles already in the atmosphere (Bid- leman et al., 1987), or they may be associated to particles in the water (Larsson and Siidergren, 1987), leiding to lower availability.

LINDANE

Lindane is generally one of the dominant persistent pollutants in the atmosphere over Sweden (Bidleman et al., 1987) as well as in other parts of the world. In Sweden the insecticide is used mainly for protecting timber and certain crops like Brassicae (e.g. rape). About 5700 t a- 1 is used in Europe, and the dominant route by which lindane reaches Sweden has been postulated to be LRT in the atmosphere from remote sources (Bidleman et al., 1987).

Lindane is the most water-soluble compound of the persistent pollutants. investigated in this study, l-5 mg K l. Therefore, it is reasonable to assume that most of the lindane entering the aquatic ecosystem from the atmosphere dissolves in the water. The availability of lindane to zooplankton is thus high, and the compound is presumably taken up fast as a result of partitioning. It has been reported that lindane adsorbed to particles at least 20 times less than did DDE (Hamelink et al., 1976), which would reduce the amount in food (phytoplankton and detritus) for zooplankton. A minor part of the lindane should, therefore, be taken up via food. This form of uptake should not interfere with direct uptake from water. Consequently, it seems reasonable to assume that of the persistent pollutants lindane would show the strongest correlation between atmospheric deposition and uptake in zooplankton. This was, in fact, the case.

The less lipophilic nature of lindane compared with PCBs and ZDDT results in lower bioaccumulation in zooplankton (Hamelink et al., 1976). However, as the pollutants entered the pond via atmospheric depo- sition, the availability of the compounds to zooplan- kton additionally affects the uptake. Lindane, which has a high wash-out coefficient (Oehme and Man& 1984), probably hit the pond mainly in the water

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phase. Since it dissolves in the water, its availability to zooplankton is high. On the other hand, highly chlor- inated PCBs, like PCB138, are less available owing to the adsorptive properties of these compounds, They presumably hit the pond surface bound to particles, and as a result their availability to daphnids is low. Consequen~y~ Iindane and PCBf38 had a similar degree of bioavailability, owing to the low bioaccum- ulation and high availability of lindane and the vice versa for PCBl38.

CDDT

DDT has not been used in Sweden for over a decade, owing to governmental restrictions. Thus with regard to the Swedish biota, current sources of DDT must be remote, and transport must occur via the atmosphere (Larsson and Okla, 1989). Atmospheric deposition over Sweden decreases along a gradient from south to north, inferring that exposure of the biota to DDT is greater in the southern part of the country.

No correlation was found between the atmospheric deposition of CDDT and uptake by zooplankton. Thus, a high deposition in the spring did not result in a high uptake by the animals, though levels in the daphnids during summer and autumn seemed to be governed by atmospheric fallout. Nor was there any correlation between deposition and uptake of any of the DDT metabolites. This lack of correlation could be due to the fact that the speciation of DDT metab- olites in atmospheric fallout differed from that occur- ring in zooplankton and due to the high fallout of ZDDT in the spring. ZDDT in atmospheric fallout was dominated by p,p-DDE, p,p-DDT and o,p-DDT. In contrast, CDDT in zoopiankton was strongly dominated by p,p-DDE and to a lesser extent by p.p- DDD.

p,p-DDT, which dominates commercial insecticide mixtures, can be broken down by u.v.-light in the atmosphere as well as by microbial degradation and the metabolism of organisms (Crosby and Moilanen, 1977; Subba-Rao and Alexander, 1985; Jarvinen et al., 1977). In the pond, conversion takes place as a result of microbial activity and invertebrate metabolism. Ma- croinvertebrate metabolism is not IikeIy to affect uptake by zooplankton, since the metabolites of DDT are lipophihc; thus they tend to be accumulated and caught within the bodies of the organisms. If the conversion took place within phytoplankton, the food of zooplankton, or within daphnids, a correlation would have been expected since the analysis is based on XDDT. The only explanation remaining is that conversion is the work of microorganisms.

ATMOSPHERIC DEPOSITlON OF PERSISTENT

POLLUTANTS GOVERNS UPTAKE BY THE BIOTA

The results show that atmospheric deposition is the main source of persistent pollutants taken up by the

aquatic biota of the pond. This is probably also the case for mOSt Holarctic, aquatic ecosystems since the pollutants are seldom used or discharged owing to governmental restrictions.

In this study the data describing the dissolution in time for atmospheric deposition and pollutant uptake by zooplankton are limited by the fallout measure- ments. As each measurement represents amounts ac- cumulated over a 3 week period, short periods of intensive deposition (pulses) cannot be distinguished though such a p&se may have a significant effect on uptake by organisms. As the zooplankton community responds fast to altered concentrations of pollutants in the water, as determined by the generation time, which in turn is governed by water temperature, zooplank- ton uptake varies over short time intervals. There- fore, the zooplankton response is fast during summer, when water temperatures are high (faster generation time) and slower in the spring and autumn. This is illustrated by the uptake curves for autumn, in which uptake by zooplankton ‘lags’ after the atmospheric deposition.

Cladoceran zoopiankton hke D. magna are sensitive to chlorinated HCs. The toxicity of chlorinated HCs to planktonic crustaceans is strongly related to water solubility, i.e. the lower the solubility the higher the toxicity, and to a lesser extent it is determined by the chemical structure of the compounds (Abernethy et al., 1986). Although the most severe effects involve dis- turbed reproduction, filtration rates and movements of the zooplankton are also affected (Ghwicz and Sieniawska, 1986). It has been proposed that pesticides have altered the zooplankton community in eutrophic lakes, negatively affecting large cladocerans to a grea- ter extent than small zooplankton (Gliwicz and Sien- iawska, 1986). The greater number of prereproductive moults in large cladocerans renders them more sensi- tive. As cladocerans serve as food for many species of planktivorous fish, the effect of such a decrease could be severe. In the pond the maximal deposition of lindane was about 8 pg m -’ month-‘, which theor- etically would result in a concentration of 9 ngi‘. I. This is far below the concentration of lindane known to affect zooplankton, i.e. about 50 pg Y- ’ (Gliwicz and Sieniawska, 1986). For p,p-DDT concentrations of over 80 pg g -- ’ dry weight were found to be acutely toxic to Calanus $nmarchicus (Harding and Vass, 1977) and Thysaniiessu raschii at 20 pg g- ’ dry weight. Wyman and O’Connors (1980) reported the toxic concentrations for Acartia tonsu to be 2Opgg. ’ dry weight. The concentration of persistent pollutants in the zooplankton of the pond was below any of the thre- sholds mentioned above, inferring that no effects were induced on the cladoceran community. However, since our knowledge regarding the sublethal effects of chlorinated hydrocarbons on zooplankton is limited, the above conclusion should be considered as tenta- tive, Moreover, in the field, synergistic effects resulting from interactions between pollutants must be consid- ered. Maki and Johnson (1975) reported enhanced

Page 7: Atmospheric deposition of persistent pollutants governs uptake by zooplankton in a pond in southern Sweden

Zooplankton uptake of persistent pollutants 2157

mortality in I). nuzgna when this zooplankton was zooplankton and their environment, a reassessment.

simul~~usly exposed to p,p-DRT and PCBs. Thus, Marine EcoZ.- Progress Series 33, 167-191.

it is possible that incidents of high atmospheric depo- Harding C. G. and Vass W. P. (1977) Uptake from sea water

sition of persistent pollutants have already induced and clearance of p,p-DDT by marine planktonic crustacea. J. Fisheries Res. Board Canada 36, 247-254.

changes in certain zooplankton communities, al- Havas M. and Hutchinson T. C. (1982) Aquatic invertebrates though they have yet to be detected. from the Sudbury Hill,: effects of pH and metals on

mortality. Can. J. Fisheries Aquatic Sci. 39, 890-903.

Acknowiedge~nts-This work was supported financially by Hoff R. My and Chan K. W. (1987) Measurement of poly-

the National Swedish Environmental Protection Board. cyclic aromatic hydrocarbons in the air along the Niagara

I thank D. Tilles for constructive critisism on the earlier draft River. Enuir. Sci. Technol. 21, 556561.

of this manuscript. Hutzinger O., Safe S. and Zitko V. (1974) 7%e Chemistry of

PCBs. Ohio. CRC Press.

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