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Organotin in the marine surface microlayer and subsurface waters of south-west England: Relation to toxicity thresholds and the UK environmental quality standard
Marine Environmental Research 32 (1991) 213-222
Organotin in the Marine Surface Microlayer and Subsurface Waters of South-West England: Relation to Toxicity Thresholds and the UK Environmental Quality Standard John J. Cleary Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth,DevonPL1 3DH, UK
A BS TRA C T Comparison of organotin concentrations in seawater collected before and after the UK government introduced legislation in 1986 and 1987 to limit the input of tributyltin ( TBT) compounds to the marine environment, shows that the legislation is beginning to take effect. Organotin concentrations began to decline in 1988 and continued to do so in 1989 in both the surface microlayer and sub-surface waters. The greatest changes have occurred in marinas, with a maximum lO-fold decline in sub-surface waters and 20-fold in the microlayer. Nevertheless T B T concentrations throughout the water column still exceed the environmental quality standard and toxicity threshold values known to cause chronic toxic effects in a number of marine species.
INTRODUCTION Because of the high toxicity and the threat posed to many forms of marine life that are sensitive to tributyltin (TBT) (Thain, 1983; Waldock & Thain, 1983; Alzieu & Portmann, 1984; Beaumont & Budd, 1984; Gibbs & Bryan, 1986; Bryan et al., 1986) the UK government introduced legislation in July 1987 banning the sale and use ofTBT anti-foulants for small boats (Abel el al., 1987). The environmental quality target (EQT) for seawater of 20 ng TBT/litre set by the Department of the Environment in 1985, was replaced by an environmental quality standard (EQS) of 2 ng TBT/litre in March 1989 due to the low concentrations of TBT now known to be toxic to some organisms (Gibbs & Bryan, 1987). The EQS is defined as the maximum 213 Marine Environ. Res. 0141-1136/91/$03.50© ]991 ElsevierSciencePublishersLtd, England. Printed in Great Britain
214
John J. Cleary
concentration of a pollutant in water allowed over a particular period or geographical area (DOE, 1977; Holdgate, 1979). At PML we have been analysing organotins in coastal waters of south-west England since 1984, and are able, therefore, to compare annual survey data to determine trends in concentration and the effectiveness of the new legislation following the decline in inputs of TBT to the marine environment. We have studied the vertical distribution of organotins in the water column, particularly in the surface microlayer, which is known to concentrate organotins in both seawater (Cleary & Stebbing, 1987) and freshwater (Maguire et al., 1982), sometimes by orders of magnitude above the concentration in sub-surface waters. The community of organisms which dwells in the surface microlayer, the neuston, is therefore exposed to these elevated levels which exceed values known to be toxic to a variety of marine species. A tidal cycle study was carried out to determine the effect of tidal change on TBT values. Our annual survey samples were always taken in the summer and as near as possible at the same state of the tide to minimise seasonal and tidal effects, but since studies by others have indicated that TBT concentrations can vary from two- to 20-fold over a tidal cycle (Clavell et al., 1986; Waldock et al., 1987), it was important to know if tidal state was a significant factor contributing to seawater TBT concentrations.
MATERIALS A N D METHODS
Collection of water samples Methods used to collect samples of the sea-surface microlayer and subsurface waters have been described previously (Cleary & Stebbing, 1987). Samples were collected annually in the summer from sites along the south coast of Devon and Cornwall (Fig. 1). Surface microlayer samples (1 litre) were collected by the Garrett screen method (Garrett, 1965), and bulk water samples (2 litres) were taken at 0.5 m sub-surface and 10 cm off the bottom. Locations sampled included areas of high pleasure craft activity such as marinas and river moorings, as well as sites of commercial boating activity such as harbours and ports used by large ships.
Chemical analysis Organotins were extracted from unfiltered seawater into toluene prior to analysis by atomic absorption spectrophotometry (Cleary & Stebbing, 1987). This method will extract TBT and dibutyltin (DBT), but not monobutyltin
Organotin in the waters of south-west England
215
NGLAND
DEVON Exeter
CORNWALL 12
,,I Plymouth 7-11
2 - 3I 5e
1;"2F ,mouth
B
C
1kin
1kin
Tamar
Dockyard
~~~~lpT~Torpoint PLYMOUTH 15 Plymouth
Fig. 1. Sampling sites along the south coast of Devon and Cornwall in south-west England.
216
John J. C~ary
or inorganic tin (M & T Chemicals Standard Test Methods). The method may be modified to improve the detection limit by reducing the volume of toluene from 25 to 10 ml, at the same time increasing the shaking time to 30min, and also by using a graphite platform coated with tantalum pentoxide. The toluene extract may be analysed directly or after a concentration step to further improve the detection limit if necessary. Treatment of the solvent extracts with 1M sodium hydroxide (3:1, v/v) removes the DBT from the toluene phase. Recovery from seawater for duplicate samples was 101_ 8% for TBT and 67.5 + 1% for DBT. The detection limit for the method is 1 ng Sn/litre seawater, equivalent to 2.4 ng TBT/litre or 2.0 ng DBT/litre. Concentrations of organotin, TBT and DBT are expressed as ng Sn/litre. RESULTS
Organotins in seawater 1986-1989 Organotin concentrations in 1989 have declined significantly from the preban values of 1986 in both the surface microlayer and sub-surface waters. Maximum organotin concentrations occur in areas of high boating activity such as marinas, particularly where tidal flushing and water exchange is poor and it is at these locations that the greatest decline in concentration has occurred with a maximum 10-fold fall in concentration i n sub-surface waters and 20-fold in the surface microlayer. ~11 Organotin in 0.5m
~J
Organotin in SMIC
ng Sn/L 1400 1200 1000 800 600 400 200 0 labc
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Sample site a-1986;b-1987;c-1988.
Fig. 2. Annual organotin concentrations in surface microlayer (SMIC) and sub-surface waters (0-5m) in south-west England. Samples collected during the summer in 1986, 1987 and 1988.
217
Organotin in the waters o f south-west England
TABLE I Lethal and Sub-lethal Toxicity Threshold Values for Various Life Stages of a Number of Marine Organisms in Relation to the U K EQS Value for Seawater of 2 ng TBT/litre (Equivalent to 0.8 ng Sn/litre) Organism
Toxicity threshold (ng Sn/litre)
Biological effect
Reference
Mussel adult Mussel juvenile Mussel larvae Copepod Oyster spat Oyster adult Dogwhelk Mud Snail
94 82 40 35 4 1 1 1
Reduced growth Reduced growth 15 day LCso value 6 day 21% survival Compensation for hypoxia Gel-formation-shell-chambering Induction of imposex Induction of imposex
Stephenson et al. (1986) Salazar & Salazar (1988) Beaumont & Budd (1984) Hall (1988) Lawler & Aldrich (1987) Alzieu et aL (1989) Bryan et al. (1989) Bryan et al. (1989)
EQS
0.8
UK value for TBT in seawater
In 1987, concentrations were greater than in 1986 at about half the sites, possibly due to a surge of anti-fouling activity by owners of small boats in anticipation of the ban. In 1988, however, the trend was reversed and organotin levels declined in the majority of the microlayer samples, although this was not consistently reflected in the sub-surface samples (Fig. 2). It is clear that the concentrations of organotins in both surface microlayer and sub-surface waters in 1988 were still greater than toxicity threshold values for a number of organisms (Table 1). A more detailed analysis of the 1988 data indicates that both TBT and DBT were detected at all the sampling sites and that enhancement of both species occurs in the surface microlayer (Fig. 3). Most of the organotin is m
TBT 0.5rn
~
DBT 0.5m
TBT SMIC
m
DBT 8MIC
ng Sn/L 350 I
350 I J300
300 i
t 250 i
~200 150~
/'150
100[~
~100
50 0 1
2
3
4
5
6
7
8
9
10
11 12 13 14 15
0
S a m p l e site
Fig. 3.
Concentrations of TBT and DBT in surface microlayer (SMIC) and sub-surface waters (0"5 m) in samples taken in July 1988.
218
John J. Cleary l
1988 bottom
I
1989 bottom
~
1988 0.5m
1989 0.5m
~
1988 SMIC
~
1989 SMIC
ng Sn/L
..........
350
~350
300 250
t 300 I -j 250
200
_i 200
150
-! 150
100
100
50 0
50 1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
0
Sample site Fig. 4.
Decline of TBT concentrations in the surface microlayer (SMIC) and sub-surface waters (0-5m) in 1989 compared with 1988.
present as TBT, and although DBT is detected at all locations, concentrations are much lower in both the microlayer and sub-surface. The minimum TBT concentrations are 18 ng Sn/litre in sub-surface waters and 38 ng Sn/litre in the surface microlayer. In the most polluted sites bulk water TBT concentrations are greater than 100 ng Sn/litre and in the microlayer more than 300 ng/litre TBT. Vertical profiles of TBT in seawater for 1988 and 1989 show clearly that in 1989 concentrations were reduced at all the locations sampled in both the surface microlayer and sub-surface waters (Fig. 4). The pattern of distribution was the same for both sets of samples with maximum concentrations occurring in areas of high boating activity, and minimum values at open water locations. The decline in concentration in 1989 was greater in the surface microlayer than in sub-surface waters and was most marked in marina samples. In sub-surface waters, concentration changes were similar in 0"5 m and bottom samples at both open water sites and marina sites. It is clear also that maximum TBT values occur in the surface microlayer and minimum values in bottom waters. There is no evidence that sediments act as a source of TBT to bottom waters but this may be because samples which are taken 10 cm off the bottom are not close enough to the sedimentwater interface to reflect such an input.
Tidal study cycle Results from tidal cycle samples taken over a 48 h period at Sutton marina, Plymouth (site 7), showed that maximum TBT concentrations occurred at low water and minimum values at high water. Mean TBT values for
Organotin in the waters of south-west England
219
successive tides were 51 and 21 ng Sn/litre at low water and high water respectively in samples taken 0"5 m sub-surface. A calculated high water concentration of 16ng Sn/litre, based on dilution of marina water with typical Plymouth Hoe water, was in good agreement with the measured value of 21 ng Sn/litre. The influence of tidal change on seawater TBT levels in Sutton marina therefore was much closer in magnitude to the two-fold changes found by Waldock et al. (1987) in the River Crouch than it was to the 20-fold changes found by Clavell et al. (1986) in San Diego Bay. Surface microlayer samples did not show a similar relationship with tidal state, but this is not surprising since enhancement or depletion of the microlayer by exchange with sub-surface waters is unlikely to occur quickly unless conditions are particularly turbulent.
DISCUSSION Although the concentrations of organotin in seawater have declined significantly since the introduction of legislation in 1987, TBT concentrations at all sites in 1989 were still greater than values known to cause chronic toxic effects in a variety of marine species, some of which have recently been shown to occur at very low levels (Table 1). The concentrations of TBT in sub-surface waters in 1989 ranged from below detection limits to 30ng Sn/litre, and even in the majority of non-marina sites exceeded threshold values known to cause sub-lethal effects on Crassostrea gigas Spat (LaMer & Aldrich, 1987). In addition, TBT levels in the majority of samples were greater than 1 ng Sn/litre, a concentration which causes gel formation and shell chambering in Crassostrea gigas (Alzieu et al., 1989), initiates imposex in Nucella lapillus and Ilyanassa obsoleta (Bryan et al., 1989) and also exceeds the EQS value for seawater. Concentrations of TBT in the surface microlayer were even greater than in sub-surface waters ranging from 4 to 75 ng Sn/litre in the 1989 survey. Typical inhabitants of the microlayer are the microneuston such as bacteria, ciliates and algae which serve as a food source for copepods and larger organisms (Zaitsev, 1971). In addition, eggs and larvae of many fish and invertebrate species, some of commercial importance (Hardy, 1982), are temporary inhabitants of the surface microlayer. Therefore TBT enrichment in the microlayer may be biologically significant to the organisms which reside there, either temporarily or permanently. For example, in 1989 concentrations were high enough to be potentially biologically significant to the neuston at some locations, since TBT values of 35 ng Sn/litre which are toxic to copepods (Hall, 1988) and 40 ng Sn/litre which are toxic to mussel larvae (Beaumont & Budd, 1984), arewell within the range of concentrations measured.
220
John J. Cleary
The existence of toxicity threshold data does not in itself imply that similar toxic effects will occur in environmental samples of the same or greater toxicant concentration since many factors such as bioavailability, degradation, partitioning, etc. will influence effects. The biological significance of microlayer TBT concentrations also depends on whether the neuston take up and are stressed by the TBT that occurs there. Our primary concern is whether the occurrence of toxic concentrations of contaminants such as TBT in the microlayer leads to actual toxicity of ecologically or economically important microlayer species. A number of studies elsewhere have demonstrated that contaminated microlayers can be toxic to neustonic eggs and larvae (Cross et al., 1987; Hardy et al., 1987). Thus, the existence of high environmental TBT levels does give cause for concern. The high organotin concentration in the surface microlayer may also affect organisms resident in the littoral zone, since they will be exposed to the microlayer deposited on the littoral sub-strata as the tide recedes. The nature of exposure for littoral organisms is therefore different and potentially much greater than for other communities that dwell in sub-surface waters. Since TBT readily adsorbs to surfaces, organisms that live and graze on them may be exposed to even higher concentrations than those in water would suggest. The tidal cycle study showed that marina concentrations of TBT are not affected greatly by tidal state, and in contrast to the 20-fold increases described by Clavell et al. (1986), nearby receiving waters are not strongly influenced by high marina concentrations and vary only by a factor of two over a tidal cycle (G. Bryan, 1990, pers. comm.). Therefore, variations in TBT concentrations over a tidal cycle are small enough not to invalidate samples taken at varying states of the tide. CONCLUSION It is clear that the legislation is becoming effective in south-west England and that environmental concentrations of organotins are declining. Nevertheless, TBT seawater values in 1989 are sufficiently high to continue to be a cause for concern, since throughout the water column they exceed the EQS and toxicity threshold values for a variety of organisms. Concentrations found in the surface microlayer are great enough to pose a serious threat to neustonic and littoral organisms. ACKNOWLEDGEMENTS The author would like to thank Dr A. R. D. Stebbing for his helpful comments on this paper and Mrs M. Brinsley and Miss H. Vine for their
Organotin in the waters of south-west England
221
assistance in various aspects o f the work. Part of the work was carried out under D e p a r t m e n t of the E n v i r o n m e n t contracts nos 7/8/76 and 7/8/103.
REFERENCES Abel, R., Hathaway, R. A., King, N. J., Vosser, J. L. & Wilkinson, T.G. (1987). Assessment and regulatory actions for TBT in the UK. In Proc. Oceans '87 Organotin Symposium, ed. M. A. Champ. Institute of Electrical and Electronic Engineers, New York, USA, pp. 1314-19. Alzieu, C. & Portmann, J. E. (1984). The effect of tributyltin on the culture of Crassostrea gigas and other species. Proc. Ann. Shellfish Conf., 15, 87-100. Alzieu, C., Sanjuan, J., Michel, P., Borel, M. & Dreno, J. P. (1989). Monitoring and assessment of butyltins in Atlantic coastal waters. Mar. Poll. Bull., 20, 22-6. Beaumont, A. R. & Budd, M. D. (1984). High mortality of the common mussel at low concentrations of tributyltin. Mar. Poll. Bull., 15, 402-5. Bryan, G. W., Gibbs, P. E., Hummerstone, L. E. & Burt, G. R. (1986). The decline of the gastropod Nucella lapillus around southwest England: evidence for the effect of tributyltin from antifouling paints. J. Mar. Biol. Ass. UK, 66, 611-40. Bryan, G. W., Gibbs, P. E., Huggett, R. J., Curtis, L. A., Bailey, D. S. & Dauer, D. M. (1989). Effects of tributyltin pollution on the mud snail Ilyanassa obsoleta York river and Sarah creek in Chesapeake Bay. Mar. Poll. BulL, 20, 458-62. Clavell, C., Seligman, P. F. & Stang, P. M. (1986). Automated analysis of organotin compounds: a method for monitoring butyltins in the marine environment. In Proc. Oceans '86 Organotin Symposium, ed. M. A. Champ. Institute of Electrical and Electronic Engineers, New York, USA, pp. ! 152-4. Cleary, J. J. & Stebbing, A. R. D. (1987). Organotin in the surface microlayer and subsurface waters of southwest England. Mar. Poll Bull., 18, 238-46. Cross, J. N., Hardy, J. T., Hose, J. E., Hershelman, G.P., Antrim, L.D., Gossett, R.W. & Crecelius, E.A. (1987). Contaminant concentrations and toxicity of sea-surface microlayer near Los Angeles, California. Mar. Env. Res., 23, 307-23. DOE (1977). Environmental standards. Pollution Paper No. 11. HMSO, London, UK. Garrett, W. D. (1965). Collection of slick-forming materials from the sea surface. Limnol. Oceanogr., 10, 602 5. Gibbs, P. E. & Bryan, G. W. (1986). Reproductive failure in populations of dogwhelk, Nucella Lapillus, caused by imposex induced by tributyltin from antifouling paints. J. Mar. Biol. Ass. UK, 66, 767 77. Gibbs, P. E. & Bryan, G. W. (1987). TBT paints and the demise of the dog-whelk Nucella Lapillus (gastropoda). In Proc. Oceans '87 Organotin Symposium, ed. M.A. Champ. Institute of Electrical and Electronic Engineers, New York, USA, pp. 1482--7. Hall, L. W., Jr (1988) Tributyltin environmental studies in Chesapeake Bay. Mar. Poll. Bull., 19, 431-8. Hardy, J. T. (1982). The sea-surface microlayer: biology, chemistry and anthropogenic enrichment. Prog. Oceanogr., 11,307-28. Hardy, J. T., Kiesser, S. L., Antrim, L. D., Stubin, A. I., Kocan, R. & Strand, J. A.
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(1987). The sea-surface microlayer of Puget Sound: Part 1. Toxic effects on fish eggs and larvae. Mar. Env. Res., 23, 227-49. Holdgate, M. W. (1979). A Perspective of Environmental Pollution. Cambridge University Press, Cambridge. Lawler, I. F. & Aldrich, J. C. (1987). Sublethal effects of bis(tri-n-butyltin) oxide on Crassostrea gigas spat. Mar. Poll. Bull., 18, 274-8. Maguire, R. J., Yiu Kee Chau, Bengert, G. A., Hale, E. G., Wong, P. T. S. & Kramer, O. (1982). Occurrence of organotin compounds in Ontario lakes and rivers. Env. Sci. Technol., 16, 698-702. M and T Chemicals Inc. Standard Test Methods. Research Laboratory Rahway, New Jersey 07065, USA. Salazar, M. H. & Salazar, S. M. (1988). Tributyltin and mussel growth in San Diego Bay. In Proc. Oceans '88 Organotin Symposium, ed. M. A. Champ. Institute of Electrical and Electronic Engineers, New York, USA, pp. 1188-95. Stephenson, M. D., Smith. D. R., Goetzl, J., Ichikawa, G. & Martin, M. (1986). Growth abnormalities in mussels and oysters from areas with high levels of tributyltin in San Diego Bay. In Proc. Oceans '86 Organotin Symposium, ed. M.A. Champ. Institute of Electrical and Electronic Engineers, New York, USA, pp. 1246-51. Thain, J. E. (1983). The acute toxicity of bis(tributyltin) oxide to the adults and larvae of some marine organisms. ICES paper CM 1983/E:13 (mimeograph). International Council for the Exploration of the Sea, Copenhagen, Denmark. Waldock, M. J. & Thain, J. E. (1983). Shell thickening in Crassostrea gigas: organotin antifouling or sediment induced. Mar. Poll. Bull., 14, 411-15. Waldock, M. J., Thain, J. E. & Waite, M. E. (1987). The distribution and potential toxic effects of TBT in UK estuaries during 1986. Appl. Organometallic Chem., 1,287-301. Zaitsev, Y. P. (1971). Marine Neustonology, ed. K. A. Vinogadov. Israel Programmes for Scientific Translations, Jerusalem, Israel.
Organotin in the Marine Surface Microlayer and Subsurface Waters of South-West England: Relation to Toxicity Thresholds and the UK Environmental Quality Standard John J. Cleary Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth,DevonPL1 3DH, UK
A BS TRA C T Comparison of organotin concentrations in seawater collected before and after the UK government introduced legislation in 1986 and 1987 to limit the input of tributyltin ( TBT) compounds to the marine environment, shows that the legislation is beginning to take effect. Organotin concentrations began to decline in 1988 and continued to do so in 1989 in both the surface microlayer and sub-surface waters. The greatest changes have occurred in marinas, with a maximum lO-fold decline in sub-surface waters and 20-fold in the microlayer. Nevertheless T B T concentrations throughout the water column still exceed the environmental quality standard and toxicity threshold values known to cause chronic toxic effects in a number of marine species.
INTRODUCTION Because of the high toxicity and the threat posed to many forms of marine life that are sensitive to tributyltin (TBT) (Thain, 1983; Waldock & Thain, 1983; Alzieu & Portmann, 1984; Beaumont & Budd, 1984; Gibbs & Bryan, 1986; Bryan et al., 1986) the UK government introduced legislation in July 1987 banning the sale and use ofTBT anti-foulants for small boats (Abel el al., 1987). The environmental quality target (EQT) for seawater of 20 ng TBT/litre set by the Department of the Environment in 1985, was replaced by an environmental quality standard (EQS) of 2 ng TBT/litre in March 1989 due to the low concentrations of TBT now known to be toxic to some organisms (Gibbs & Bryan, 1987). The EQS is defined as the maximum 213 Marine Environ. Res. 0141-1136/91/$03.50© ]991 ElsevierSciencePublishersLtd, England. Printed in Great Britain
214
John J. Cleary
concentration of a pollutant in water allowed over a particular period or geographical area (DOE, 1977; Holdgate, 1979). At PML we have been analysing organotins in coastal waters of south-west England since 1984, and are able, therefore, to compare annual survey data to determine trends in concentration and the effectiveness of the new legislation following the decline in inputs of TBT to the marine environment. We have studied the vertical distribution of organotins in the water column, particularly in the surface microlayer, which is known to concentrate organotins in both seawater (Cleary & Stebbing, 1987) and freshwater (Maguire et al., 1982), sometimes by orders of magnitude above the concentration in sub-surface waters. The community of organisms which dwells in the surface microlayer, the neuston, is therefore exposed to these elevated levels which exceed values known to be toxic to a variety of marine species. A tidal cycle study was carried out to determine the effect of tidal change on TBT values. Our annual survey samples were always taken in the summer and as near as possible at the same state of the tide to minimise seasonal and tidal effects, but since studies by others have indicated that TBT concentrations can vary from two- to 20-fold over a tidal cycle (Clavell et al., 1986; Waldock et al., 1987), it was important to know if tidal state was a significant factor contributing to seawater TBT concentrations.
MATERIALS A N D METHODS
Collection of water samples Methods used to collect samples of the sea-surface microlayer and subsurface waters have been described previously (Cleary & Stebbing, 1987). Samples were collected annually in the summer from sites along the south coast of Devon and Cornwall (Fig. 1). Surface microlayer samples (1 litre) were collected by the Garrett screen method (Garrett, 1965), and bulk water samples (2 litres) were taken at 0.5 m sub-surface and 10 cm off the bottom. Locations sampled included areas of high pleasure craft activity such as marinas and river moorings, as well as sites of commercial boating activity such as harbours and ports used by large ships.
Chemical analysis Organotins were extracted from unfiltered seawater into toluene prior to analysis by atomic absorption spectrophotometry (Cleary & Stebbing, 1987). This method will extract TBT and dibutyltin (DBT), but not monobutyltin
Organotin in the waters of south-west England
215
NGLAND
DEVON Exeter
CORNWALL 12
,,I Plymouth 7-11
2 - 3I 5e
1;"2F ,mouth
B
C
1kin
1kin
Tamar
Dockyard
~~~~lpT~Torpoint PLYMOUTH 15 Plymouth
Fig. 1. Sampling sites along the south coast of Devon and Cornwall in south-west England.
216
John J. C~ary
or inorganic tin (M & T Chemicals Standard Test Methods). The method may be modified to improve the detection limit by reducing the volume of toluene from 25 to 10 ml, at the same time increasing the shaking time to 30min, and also by using a graphite platform coated with tantalum pentoxide. The toluene extract may be analysed directly or after a concentration step to further improve the detection limit if necessary. Treatment of the solvent extracts with 1M sodium hydroxide (3:1, v/v) removes the DBT from the toluene phase. Recovery from seawater for duplicate samples was 101_ 8% for TBT and 67.5 + 1% for DBT. The detection limit for the method is 1 ng Sn/litre seawater, equivalent to 2.4 ng TBT/litre or 2.0 ng DBT/litre. Concentrations of organotin, TBT and DBT are expressed as ng Sn/litre. RESULTS
Organotins in seawater 1986-1989 Organotin concentrations in 1989 have declined significantly from the preban values of 1986 in both the surface microlayer and sub-surface waters. Maximum organotin concentrations occur in areas of high boating activity such as marinas, particularly where tidal flushing and water exchange is poor and it is at these locations that the greatest decline in concentration has occurred with a maximum 10-fold fall in concentration i n sub-surface waters and 20-fold in the surface microlayer. ~11 Organotin in 0.5m
~J
Organotin in SMIC
ng Sn/L 1400 1200 1000 800 600 400 200 0 labc
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Sample site a-1986;b-1987;c-1988.
Fig. 2. Annual organotin concentrations in surface microlayer (SMIC) and sub-surface waters (0-5m) in south-west England. Samples collected during the summer in 1986, 1987 and 1988.
217
Organotin in the waters o f south-west England
TABLE I Lethal and Sub-lethal Toxicity Threshold Values for Various Life Stages of a Number of Marine Organisms in Relation to the U K EQS Value for Seawater of 2 ng TBT/litre (Equivalent to 0.8 ng Sn/litre) Organism
Toxicity threshold (ng Sn/litre)
Biological effect
Reference
Mussel adult Mussel juvenile Mussel larvae Copepod Oyster spat Oyster adult Dogwhelk Mud Snail
94 82 40 35 4 1 1 1
Reduced growth Reduced growth 15 day LCso value 6 day 21% survival Compensation for hypoxia Gel-formation-shell-chambering Induction of imposex Induction of imposex
Stephenson et al. (1986) Salazar & Salazar (1988) Beaumont & Budd (1984) Hall (1988) Lawler & Aldrich (1987) Alzieu et aL (1989) Bryan et al. (1989) Bryan et al. (1989)
EQS
0.8
UK value for TBT in seawater
In 1987, concentrations were greater than in 1986 at about half the sites, possibly due to a surge of anti-fouling activity by owners of small boats in anticipation of the ban. In 1988, however, the trend was reversed and organotin levels declined in the majority of the microlayer samples, although this was not consistently reflected in the sub-surface samples (Fig. 2). It is clear that the concentrations of organotins in both surface microlayer and sub-surface waters in 1988 were still greater than toxicity threshold values for a number of organisms (Table 1). A more detailed analysis of the 1988 data indicates that both TBT and DBT were detected at all the sampling sites and that enhancement of both species occurs in the surface microlayer (Fig. 3). Most of the organotin is m
TBT 0.5rn
~
DBT 0.5m
TBT SMIC
m
DBT 8MIC
ng Sn/L 350 I
350 I J300
300 i
t 250 i
~200 150~
/'150
100[~
~100
50 0 1
2
3
4
5
6
7
8
9
10
11 12 13 14 15
0
S a m p l e site
Fig. 3.
Concentrations of TBT and DBT in surface microlayer (SMIC) and sub-surface waters (0"5 m) in samples taken in July 1988.
218
John J. Cleary l
1988 bottom
I
1989 bottom
~
1988 0.5m
1989 0.5m
~
1988 SMIC
~
1989 SMIC
ng Sn/L
..........
350
~350
300 250
t 300 I -j 250
200
_i 200
150
-! 150
100
100
50 0
50 1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
0
Sample site Fig. 4.
Decline of TBT concentrations in the surface microlayer (SMIC) and sub-surface waters (0-5m) in 1989 compared with 1988.
present as TBT, and although DBT is detected at all locations, concentrations are much lower in both the microlayer and sub-surface. The minimum TBT concentrations are 18 ng Sn/litre in sub-surface waters and 38 ng Sn/litre in the surface microlayer. In the most polluted sites bulk water TBT concentrations are greater than 100 ng Sn/litre and in the microlayer more than 300 ng/litre TBT. Vertical profiles of TBT in seawater for 1988 and 1989 show clearly that in 1989 concentrations were reduced at all the locations sampled in both the surface microlayer and sub-surface waters (Fig. 4). The pattern of distribution was the same for both sets of samples with maximum concentrations occurring in areas of high boating activity, and minimum values at open water locations. The decline in concentration in 1989 was greater in the surface microlayer than in sub-surface waters and was most marked in marina samples. In sub-surface waters, concentration changes were similar in 0"5 m and bottom samples at both open water sites and marina sites. It is clear also that maximum TBT values occur in the surface microlayer and minimum values in bottom waters. There is no evidence that sediments act as a source of TBT to bottom waters but this may be because samples which are taken 10 cm off the bottom are not close enough to the sedimentwater interface to reflect such an input.
Tidal study cycle Results from tidal cycle samples taken over a 48 h period at Sutton marina, Plymouth (site 7), showed that maximum TBT concentrations occurred at low water and minimum values at high water. Mean TBT values for
Organotin in the waters of south-west England
219
successive tides were 51 and 21 ng Sn/litre at low water and high water respectively in samples taken 0"5 m sub-surface. A calculated high water concentration of 16ng Sn/litre, based on dilution of marina water with typical Plymouth Hoe water, was in good agreement with the measured value of 21 ng Sn/litre. The influence of tidal change on seawater TBT levels in Sutton marina therefore was much closer in magnitude to the two-fold changes found by Waldock et al. (1987) in the River Crouch than it was to the 20-fold changes found by Clavell et al. (1986) in San Diego Bay. Surface microlayer samples did not show a similar relationship with tidal state, but this is not surprising since enhancement or depletion of the microlayer by exchange with sub-surface waters is unlikely to occur quickly unless conditions are particularly turbulent.
DISCUSSION Although the concentrations of organotin in seawater have declined significantly since the introduction of legislation in 1987, TBT concentrations at all sites in 1989 were still greater than values known to cause chronic toxic effects in a variety of marine species, some of which have recently been shown to occur at very low levels (Table 1). The concentrations of TBT in sub-surface waters in 1989 ranged from below detection limits to 30ng Sn/litre, and even in the majority of non-marina sites exceeded threshold values known to cause sub-lethal effects on Crassostrea gigas Spat (LaMer & Aldrich, 1987). In addition, TBT levels in the majority of samples were greater than 1 ng Sn/litre, a concentration which causes gel formation and shell chambering in Crassostrea gigas (Alzieu et al., 1989), initiates imposex in Nucella lapillus and Ilyanassa obsoleta (Bryan et al., 1989) and also exceeds the EQS value for seawater. Concentrations of TBT in the surface microlayer were even greater than in sub-surface waters ranging from 4 to 75 ng Sn/litre in the 1989 survey. Typical inhabitants of the microlayer are the microneuston such as bacteria, ciliates and algae which serve as a food source for copepods and larger organisms (Zaitsev, 1971). In addition, eggs and larvae of many fish and invertebrate species, some of commercial importance (Hardy, 1982), are temporary inhabitants of the surface microlayer. Therefore TBT enrichment in the microlayer may be biologically significant to the organisms which reside there, either temporarily or permanently. For example, in 1989 concentrations were high enough to be potentially biologically significant to the neuston at some locations, since TBT values of 35 ng Sn/litre which are toxic to copepods (Hall, 1988) and 40 ng Sn/litre which are toxic to mussel larvae (Beaumont & Budd, 1984), arewell within the range of concentrations measured.
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The existence of toxicity threshold data does not in itself imply that similar toxic effects will occur in environmental samples of the same or greater toxicant concentration since many factors such as bioavailability, degradation, partitioning, etc. will influence effects. The biological significance of microlayer TBT concentrations also depends on whether the neuston take up and are stressed by the TBT that occurs there. Our primary concern is whether the occurrence of toxic concentrations of contaminants such as TBT in the microlayer leads to actual toxicity of ecologically or economically important microlayer species. A number of studies elsewhere have demonstrated that contaminated microlayers can be toxic to neustonic eggs and larvae (Cross et al., 1987; Hardy et al., 1987). Thus, the existence of high environmental TBT levels does give cause for concern. The high organotin concentration in the surface microlayer may also affect organisms resident in the littoral zone, since they will be exposed to the microlayer deposited on the littoral sub-strata as the tide recedes. The nature of exposure for littoral organisms is therefore different and potentially much greater than for other communities that dwell in sub-surface waters. Since TBT readily adsorbs to surfaces, organisms that live and graze on them may be exposed to even higher concentrations than those in water would suggest. The tidal cycle study showed that marina concentrations of TBT are not affected greatly by tidal state, and in contrast to the 20-fold increases described by Clavell et al. (1986), nearby receiving waters are not strongly influenced by high marina concentrations and vary only by a factor of two over a tidal cycle (G. Bryan, 1990, pers. comm.). Therefore, variations in TBT concentrations over a tidal cycle are small enough not to invalidate samples taken at varying states of the tide. CONCLUSION It is clear that the legislation is becoming effective in south-west England and that environmental concentrations of organotins are declining. Nevertheless, TBT seawater values in 1989 are sufficiently high to continue to be a cause for concern, since throughout the water column they exceed the EQS and toxicity threshold values for a variety of organisms. Concentrations found in the surface microlayer are great enough to pose a serious threat to neustonic and littoral organisms. ACKNOWLEDGEMENTS The author would like to thank Dr A. R. D. Stebbing for his helpful comments on this paper and Mrs M. Brinsley and Miss H. Vine for their
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assistance in various aspects o f the work. Part of the work was carried out under D e p a r t m e n t of the E n v i r o n m e n t contracts nos 7/8/76 and 7/8/103.
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