Bewertung der Gef~hrdung yon Mensch und Umwelt durch ausgew/ihlte Schadstoffe. Texte. 38/95, Umweltbundesamt, Berlin, Germany. van Wezel, A.P., de ...
Chemosphere, Vol. 35, No. 9, pp. 1875-1885, 1997
Pergamon
© 1997 Elsevier Science Ltd All rights reserved, Printed in Great Britain 00,15-6535/97 $17.00+0.00
P I h S0045-6535(97)00239-7
POTENTIAL FOR SECONDARY POISONING AND BIOMAGNIFICATION
IN MARINE ORGANISMS
M. Nendza j*, T. Herbs¢, C. Kussatz2 and A. Gies2 ': Analytisches Laboratorium Dr. Herbst & Dr. Nendza, BahnhofstraBe 1, D-24816 Luhnstedt, Germany 2: Umweltbundesamt, Bismarckplatz 1, D-14193 Berlin, Germany (Received in Germany 16 April 1997; accepted 28 April 1997)
Abstract: For selected priority pollutants, like organochiorine pesticides, PAHs and PCBs, and mercury and cadmium, the transfer along marine food chains was assessed based on monitoring data. Comparison of the acquired body burden for marine fish and the toxicity thresholds for predating marine birds and mammals provides evidence for the relevance of contaminant uptake with the food and the liability for secondary poisoning. As a consequence, contaminant residues in prey organisms (critical body burden) should be used for marine hazard and risk assessments. Evaluations solely from aquatic exposure concentrations are not adequate to account for potential secondary effects in marine ecosystems. © 1997 Elsevier Science Ltd Keywords: Marine Food Chain, Accumulation, Critical Body Burden, Secondary Poisoning, Organochlorine Pesticides, PAHs, PCBs, Mercury, Cadmium
Introduction: The impact assessment for pollutants in marine environments cannot be based on the same methodology as used for freshwater ecosystems due to major differences in the spatial and temporal exposure levels of the chemicals. Limnic ecosystems are of limited dimensions and average concentrations of chemicals may be determined readily, whilst in an ocean, due to the vast amount of water, every contaminant is mathematically in a state of infinite dilution. The distribution of xenobiotics in the seas, however, is not homogeneous and considerable concentrations may occur regionally. In contrast to a river, which is steadily decontaminated by washing out, the contaminations in the sea may last for a long period of time even if the emissions of the contaminants are stopped. These long-term aqueous concentration levels are determinant for the contaminant burden accumulated in marine fish, which in turn serve as a source of food for predating * Author to whom correspondence should be addressed 1875
1876 animals. The accumulation of chemical substances along food chains may result in'toxic concentrations in organisms (secondary poisoning) even if the concentration in the erivironment remains below the threshold level for direct toxicity. The food chain accumulation is a major risk for the top predators of trophic webs, in marine ecosystems especially for birds and mammals. In contrast to fish (Opperhuizen 1991), the consumption of contaminated food is the major source for xenobiotics in predating marine birds and mammals, whilst the direct uptake of chemicals from the environment, i.e. from water, sediment and air, is of only minor relevance (Biddinger and Gloss 1984). Therefore, the concentration of a contaminant in prey animals is the essential measure for evaluating it's potential for secondary poisoning.
Materials and Methods:
For this study monitoring data on selected compounds were retrieved from the literature. The following chemicals were chosen due to their environmental relevance as well as the availability of monitoring data (ASMO 1995): Pentachlorophenol (PCP), hexachlorobenzene (HCB), 1,1,1-trichloro-2,2-bis(p-chlorophenyl)ethane (DDT), 1,1,-dichloro-2,2-bis(p-chlorophenyl)ethene (DDE), lct,2a,313,4ct,5ct,613-hexachlorocyclohexane (lindane or "/-HCH), 1,2,3,4,10,10-hexachloro-6,7-epoxy-l,4,4a,5,6,7,8,8a-octahydro-endo,exo1,4:5,8-dimethanonaphthalene
(dieldrine), naphthalene, anthracene, fluoranthene, benzo[a]pyrene, poly-
chlorinated biphenyls (PCBs), chloroparaffins (CPs), tributyltinoxide (TBTO), cadmium and mercury (Table 1). Residue data were collected for marine fish, birds and mammals. The data obtained for several species caught at different locations made adjustment necessary, this was achieved by using the geometric mean values of measured concentrations in the organisms. These mean values proved to be useful to compare the hazard potential of the chemicals in question. However, there is a lack of consistent data sets for marine environmental assessment purposes, even for priority pollutants. The existing data from monitoring campaigns are far from being harmonised: Reported pollutant concentrations in environmental media, e.g. fish, are based on wet weight (ww) or dry weight (dw), corrected for lipid content or not, for whole fish or specific organs, muscle etc. Hence, for each compound merely a variety of non-comparable data can be retrieved from the literature. Furthermore, the results of chemical analyses are strongly influenced by the techniques used for sampling, sample storage, extraction procedures, clean-up and the measurement techniques for identification and quantification of the chemicals. Since details on the basic analytical specifications, e. g. recovery rates, detection limits, determination limits etc., are rarely given in the literature and the application of international standard procedures, e.g. US-EPA-, ISO- (international standards), EN- (European standards) methods, is not agreed upon, the available data are not strictly comparable and they might not have the quality necessary to justify regulatory actions. Furthermore, the monitoring of chemicals in the environment is obviously concentrated on those compounds, for which sensitive analytical detection is readily available, e.g. chlorinated pesticides are easily detected with an
1877 electron capture detector (ECD) in trace amounts, or mercury and cadmium with atomic adsorption spectrometry (AAS). Other contaminants, more difficult to detect and to determine, are rarely subject to intensive studies despite the fact that their impacts on the environment may be even more severe.
Table 1: List o f compounds CAS Name
MW
log Pow
Ref.
266.35 284,80 354.50 318.04 290.85 380.93
5.06 5.73 6.91 6.96 3.69 5.40
1 2 2 2 2 2
128.18 178.24 202.26 252.32
3.32 4.49 4.95 6.12
1 1 1 1
257.54 291.99 326.43 326.43 360.88 360.88 395.32
5.71 5.79 6.40 6,74 6,73 6.80 7.21 4-8
3 3 3 4 3 3 3 5
3.2- 3.8
5
Chloropesticides 87-86-5 Pentaehlorophenol 118-74-1 Hexachlorobenzene 50-29-3 DDT 72-55-91DDE 58-89-9 Lindane 60-57-1 Dieldrine
PAHs 91-20-2 120-12-7 206-44-0 50-32-8
Naphthalene Anthracene Fluoranthene Benzo[a]p~ene
PCBs 7012-37-5 35693-99-3 37680-73-2 31508-00-6 35065-28-2 35065-27-1 35065-29-3 8535-84-8
PCB 28 PCB 52 PCB 101 PCB 118 PCB 138 PCB 153 PCB 180 Chloroparaffins
Organotincompounds 36-35-9 TBTO
Heavy Metals Cadmium Mercury (org.) Mercury (inorg.) 1: Miiller & Klein (1992), 2: Sicbaldi & Del Re (1993), 3: Mackay et al. (1992), 4: Hawker & Connell (1988), 5: LrBA(1995)
Results and Discussion:
The comparative analysis o f accumulation and toxicity data for marine fish, birds and mammals with residue data from monitoring campaigns reveals that it is more appropriate to determine critical body concentrations than critical environmental concentrations for the purpose o f risk identification and risk evaluations in marine environments.
The accumulation o f chemicals in fish depends on the aquatic concentration and the bioconcentration factor (BCF), but the respective data have rarely been measured with marine species. Evaluation o f the available
1878 literature data revealed that the accumulation in marine and freshwater fish differs generally by less than a factor of 10, i.e. within the range of experimental and interspecies variance. The bioconcentration factors in marine species appear to be systematically lower, hence it may be justified to use freshwater BCF data also for hazard assessments for marine ecosystems if the respective measurements are unavailable. Combining the BCF values with toxicity data (no observed effect concentration "NOEC") for fish yields the critical body burden (CBB), the contaminant level inside the organisms above which the fish will be impaired.
CBB=NOEC.BCF
For a worst-case assessment, the lowest toxicity values for chronic exposure and the highest BCF, preferably determined with salt water fish, were evaluated (Table 2). The use of calculated CBBs for these assessments is possible, though a comparison of measured and calculated critical body burden shows that the calculated CBBs tend to be systematically higher than the measured residues (Figure 1) and hence the obtained quotients may be underprotective by one order of magnitude. The deviations in the estimates may be partly due to the fact that BCF values are considered steady state and for toxicity tests of short duration with chemicals with log Pow > 3 steady state may not be reached (McKim and Schmieder 1991). On the other hand, measured CBB data may vary by one order of magnitude within a population, with approximately 50 % of this variation being attributable to the lipid content of the individuals (van Wezel et al. 1995). As compared to laboratory accumulation, residues in field populations may be considerably higher for persistent chemicals, e.g. PCBs, but lower for less persistent compounds (Hendriks 1995).
CBB exp. 100
10
1
0.1
0.01
0.01
0.1
1
10
100
CBB celt.
Figure 1: Measured vs. calculated (LC50. BCF) CBBs, data for measured CBBs are taken from Sijm et al. (1993) and McKim & Schmieder (1991).
1879 Table 2: Fish NOEC body burden (CBB) and monitoring data NOEC Fish
BCF Fish
CBB Monit.Fish [ng/g] [ng/gww]
Quotient Monit./CBB
Chloropesticides Pentachlorophenol Hexachlorobenzene DDT DDE Lindane Dieldrine
0.02 0.04
400 45000 30000 51500 JMP 730 EC 10000
EC EC FW FW EC EC
0.003 0.01 0.001 0.003 0.2
EC EC JMP EC EC D
500 1000 1500 5000 68000 7800
EC 2000 FW 3 FW 15 FW 15 A 204 B ~1560
0.001
EC
3000
EC 13
0.1 0.05 0.003
:EC EC EC
40 2250 90 14.6 400
2.8 1.7 22 50 7.2 2,0
ECM ECM ECM ECM ECM ECM
0.07 0.0008 0.24
5 27 29 110
ECM ECM C B
0.33 5.4 0.14 0.07
0.49 0.005
PAl-Is Naphthalene Anthracene Fluoranthene Benzo[a]pyrene
PCBs Chloroparaffins Organotincompounds TBTO
Heavy Metals JMP 540 FW 270 280 E 1.04 Cadmium 0.5 JMP 14000 FW 350 58" F 0.17 0.025 Mercury (org.) JMP 5700 FW 142 58" F 0.41 0.025 Mercury (inorg.) EC: lowest (Tox.) resp. highest (BCF) Value from ECDIN (1993), JMP: Data from JMP Report (ASMO 1994), FW: BCF-Values determined with freshwater fish, A: Zaroogian et al. (1985), B: Greenpeace (1995), C: geometric mean value from data by: de Boer et al. (1993), Bowes & Jonkel (1975), Romijn et al. (1993), Shaw & Connell (1982) and Muir et al. (1988), D: calculated, E: geometric mean value from data by: Thompson (1990), Romijn (1993), Suedel et al. (1994), F: geometric mean value from data by: Suedel et al. (1994), ECM: geometric mean value from data from ECDIN (1993), *: Total-Hg
The actual hazard potential o f the individual chemicals for direct fish toxicity can be characterised by comparing the critical body burden with measured concentrations in marine fish. Since no consistent monitoring data for prey fish are available, data from a number of studies had to be combined, on diverse fish species from various geographic and climatic regions with different habitats and differing contaminant levels. The resultant bias can only partly be absorbed by using geometric mean values of the fish contaminations. But even the largely diverse sources did not provide sufficiently representative monitoring data for all of the selected chemicals. For the remaining data set, the quotient of the critical body burden and the actual concentrations in the fish (Monit.) is given in table 2. The smaller the quotient is, the less likely is the direct toxic impact o f the given chemical. Quotient values < 0.01 indicate compounds for which the actual contamination is at least 100 times lower than the lowest observed toxicity value. Such a safety margin was only found for two o f the compounds in this study: Hexachlorobenzene and dieldrine. Quotient values between 0.01 and 0.1 indicate compounds for which the actual contamination is at least 10 times lower than the toxicity threshold, e.g. pentachlorophenol and chloroparaffins. A direct impact by these compounds is unlikely, but they may contribute to the joint toxicity of the sum of chemical releases. Quotient values between 0.1 and 1 indicate compounds for which the actual contamination is in the same order of magnitude as the toxicity threshold. A direct impact by these compounds has to be assumed, e.g.
880
I
1 000
l
100 [pg/kg] 10
1 HCB Fish
•
2
BirdWhole
[]
Bird Muscle
•
DDE
22
50
Lindane Dielddn 7
1 100 10
Bird Fatty Tissue~ Bird Liver
DDT
1 100
310
380
•
950
CI-Parat
29
110
210
4 600
1 500
Cd
Hg (org,
280
58
8 720
2 660
250
2 000
17
PCBs
2
30
700
140
740
10 000
I 000
100 [pg/kg] 10
1 HCB 2
DDT
DDE
22
50
Fish
[]
~ammal Whole ~emmal Muscle
[]
10
160
160
Mammal Fatty
[]
43
1 1(30
~ammal Liver
[]
50
500
Lindane Dieldrin PCBs CI-Paraf. 7
2
29
10
130
2 500
50
180
2 20()
580
500
38
630
110
Cd
Hg (org.)
280
58
270
680
4 800
4 000
230
Figure 2: Comparison of contaminant concentrations measured in marine species [~tg/kg]: fish and birds (top), fish and mammals (bottom)
1881 for DDT, lindane, fluoranthene, PCBs and mercury. If the quotient values exceed 1, toxicity is likely to occur, e.g. for benzo[a]pyrene and cadmium. This analysis of several ubiquitous contaminants reveals that more than half o f them is present at exposure concentrations in marine ecosystems which are directly toxic to fish. Either alone or in combination with co-contaminants they constitute a substantial hazard for aquatic biota.
The contaminated fish is the main source of xenobiotics for predating birds and mammals. Accumulation may result in considerable body burden. Steady-state levels in birds may be reached within weeks, depending on the biological half-life time of the chemical (Pearce et al. 1989), while contamination levels in mammals may continually increase with age, with a plateau only after several years (Thompson 1990, Teigen et al. 1993). The monitoring data on pollutant levels in marine birds and mammals vary even more than for fish, and the inconsistent data merely allow to analyse general trends. Still, the comparison of the concentrations of the chemicals in fish on the one hand and in the predators on the other hand (Figure 2) reveals that bioaccumulation does occur along food chains: For all compounds analysed, organic as well as inorganic, the mean concentrations in fish eating birds and marine mammals are considerably higher than in the fish on which they feed. The contaminants preferably accumulate in the liver and fatty tissue of the predators, the concentrations exceed the respective values for fish by a factor 10 - 100. The accumulation into muscle tissue ranges about one order of magnitude, according to the increased lipid content and the reduced elimination potential of the birds and mammals. With regard to the birds, not only the accumulation in the adult organisms, but also the transfer into the eggs may affect the viability o f the populations. Comparisons of reported concentration levels revealed that contaminants are transferred from birds into their eggs: The contaminant concentrations are of the same magnitude in adult birds and in the eggs (Custer and Custer 1995). Further increase of the contaminant levels in the fledgelings may occur due to further uptake with the food (Burger and Gochfeld 1993). Among the compounds in this study DDT, DDE,
Table 3: Toxicity data [mg/kg diet] for birds and mammals (Romijn et al. 1993)
LC50
Birds NOEC
extrap. NOEC
LC50
Mammals NOEC
extrap. NOEC
Chloropestieides Lindane Dieldrine PCBs
425 - 5000 107 - 1500
1.6 - 100 0.5 - 10 20
0.16 0.05 2.0
Chloroparaffins Heavy Metals Cadmium 562 - 3065 0.2 - 38 0.02 Mercury (org.) 40 0.25 - 4.3 0.025 Mercury (inorg.) 2805 - 3764 4 - 250 0.40 ": extrapol, from UBA (1995) according to Romijn et al. (1993)
333 - 872 300
25 - 400 1 - 15 10 164
2.5 0.1 1.0 16.4"
3 - 50 0.22 - 2.25 20
0.3 0.022 2.0
1882 dieldrine, PCBs and mercury revealed the highest potential to bioaccumulate along trophic webs. The extent of the PCB and mercury accumulation in predators is illustrated by the fact that the seal corpses after the epidemic in the wadden sea in 1988 had'to be classified hazardous waste (Schleswig-Holsteinischer Landtag 1989).
Reliable toxicity data for predating marine birds (e.g. gulls and penguins) and mammals (e.g. seals, dolphins and polar bears) are hardly available. Instead, threshold levels are extrapolated from terrestrial species, i.e. interspecies correlations are assumed to hold for chicken and gulls, albatross or pelicans, and for rats and seals, whales or polar bears, respectively. The validity of these extrapolations is highly questionable and can only be justified by the current lack of better data. Further uncertainty in the relevance of the conventional toxicity data is due to the fact that in marine ecosystems most individual contaminants are present in subtoxic concentrations and impacts may be rather due to the joint toxicity of a multitude of components than to a specific chemical. The issue of mixture toxicity assessments is thus of major importance for a sustainable protection of marine ecosystems. Despite the recognised shortcomings of the current practice of toxicity quantifications, NOEC values for food exposure were extrapolated (Romijn et al. 1993). Birds appear significantly, i.e. up to a factor of 100, more sensitive to marine pollutants than mammals (Table 3).
Concentration in fish/extrap.NOEC
10
0.1
0.01
0.001
Lindane
Dlelddn
PCBs IBB Bird ~
CI-Paraf. Mammal
Cd
Hg (org.)
Figure 3: Hazard quotients (concentration in fish / extrap. NOEC) for secondary poisoning of fish eating marine birds and mammals
1883 A joint evaluation for the two groups of organisms therefore seems to be inappropriate. The comparison of non-toxic concentrations of contaminants in the food for birds and mammals (extrap. NOEC) with actual concentrations in marine fish (Figure 3) leads to the following conclusions: For several compounds, the concentration levels in the marine fish have exceeded the toxicity thresholds for birds and mammals and none of the other compounds in this study satisfies the demand for a safety factor of 1000 between the CBBs and the actual concentrations. Especially the heavy metals and chlorinated paraffins constitute substantial hazard for fish eating predators. The mercury and cadmium accumulation in fish may cause both, direct toxicity to fish as well as indirect poisoning of predating species. The direct toxicity to fish is less important for the chlorinated paraffins, since their concentration level in fish is about tenfold below the NOEC to fish. Despite the lack of substantial biomagnification (mean concentration in fish: 110 }tg/kg ww, mean concentration in mammals: 230 ~tg/kg ww), which does not indicate unacceptable risk, the consideration of the toxicity of chloroparaffins to predating birds and mammals shows that secondary poisoning of fish eating predators is of evident relevance because of the higher toxicity to mammals. The findings for chlorinated paraffins emphasise the necessity to include the aspect of secondary poisoning in hazard assessment schemes for aquatic pollutants. The determination of threshold concentrations for marine environments solely on the basis of aquatic toxicity data is not suitable to protect the entire ecosystem, especially top predators like sea birds, marine mammals and eventually men.
Conclusions: The outcome of this study emphasises the necessity to include the aspect of secondary poisoning in hazard assessment schemes for aquatic pollutants. Critical body burden are a suitable means to account for food chain accumulation. Since calculated CBB values may be too high, i.e. underprotective, measured CBBs are to be preferred. The determination of threshold concentrations or quality criteria for marine environments solely on the basis of aquatic toxicity data for single substances does not protect the entire ecosystem, including top predators like sea birds, marine mammals and eventually men.
Acknowledgement: This study was supported by the German Federal Environment Agency (Umweltbundesamt PO Box 330022 D-14191 Berlin). A more detailed study (in German) is available from the Umweltbundesarnt: "Kriterien zur Bewertung der Biomagnifikation von Pflanzenschutzmitteln mad Industrieehemikalien in marinen Organismen (1995)".
1884 References:
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