Environmental problems caused by TBT in France: Assessment, regulations, prospects

Marine Environmental Research 32 (1991) 7-17

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Environmental Problems caused by TBT in France: Assessment, Regulations, Prospects

C l a u d e Alzieu IFREMER, Centre de Nantes, B.P. 1049, 44037 Nantes Cedex 01, France

A BSTRA CT The sea water pollution resulting from the tributyltin (TBT) released by antifouling paints has had serious consequences on the oyster production in a number of bays along the French coastline. Effects of this pollution on oyster growth and reproduction, as well as its economic impact in the Bay t~f Arcachon are reviewed. The influence of the ban on TBT use in antifouling paints on the recover), of the oyster stock is discussed in an attempt to reflect on the strategy required to protect the marine environment.

INTRODUCTION On 17 January 1982, the French Minister of Environment passed an ordinance restricting the use of antifouling paints containing organotin compounds on boats under 25m long. This decision, taken on the recommendation of the Evaluation Commission on Ecotoxicity of Chemical Substances following a review of recent findings on tributyltin (TBT) toxicity to oysters, was intended to protect French oyster culture farms. These measures which were adopted just a few months after the harmful effects of organotins on marine molluscs were demonstrated, have made it possible to save oyster culture in some particularly sensitive areas. Furthermore, they have led to the development of international awareness of the ecological risks connected with the fight against marine biofouling. 7

Marine Environ. Res. 0141-1136/91/$03.50 © 1991 Elsevier Science Publishers Ltd, England. Printed in Great Britain

8

Claude Alzieu

EFFECTS IN OYSTER C U L T U R E AREAS: CASE OF A R C A C H O N BAY French oyster culture areas are located in bays, lagoons and estuaries which are also the site of a large flotilla of pleasure craft representing a source of considerable TBT input. The harmful effects of TBT on the environment were first detected in Arcachon Bay. Located between the Gironde estuary and the Spanish border (Fig. 1), Arcachon Bay constitutes a triangle-shaped enclave with coastlines stretching approximately 18 km to the west, 19 km to the east and 20 km to the south. Water circulation inside the bay takes place through a network of channels the upstream sections of which tend to silt up increasingly. Despite the considerable volumes evacuated at ebb tide (130-420 million m3), water renewal is poor in the eastern part of the bay. Oyster production in Arcachon Bay dates back to the 18th century. In a normal production year, the culture areas stretching over approximately 1000 ha yield roughly ! 0 to 15 000 tons of Crassostrea gigas oysters, 600 tons of mussels, 100 tons of clams and 50 tons of cockles. Production areas (Fig. I) are surrounded by 10 marinas, representing 3140 permanent berths plus 4520 seasonal mooring berths. Pleasure craft navigation throughout the bay

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Oyster grounds, marinas and mooring areas in Arcachon Bay.

T B T pollution in France

9

is intense and the traffic ranges, according to estimates, between 10 000 and 15 000 boats during the summer season. From 1975 to 1982, oyster production was severely disrupted by a crisis presenting the following major symptoms. There was complete absence of any spatfall, preventing any direct replenishment of breeding stocks and eliminating a traditional source of revenue: the sale of spat for breeding purposes in areas where hydroclimatic conditions do not permit reproduction. Anomalies in the calcic growth of shells were seen; the shells took on a ball shape owing to the formation of numerous chambers.

EFFECTS ON REPRODUCTION From 1975 to 1982, spatfall in Arcachon Bay was very low and in certain years failed completely, whereas it remained satisfactory in neighbouring areas. Observations showed that larvae were surviving only a few days in the waters of the bay while their growth under laboratory conditions remained normal in clean water. His and Robert (1983-1985) showed that these anomalies were not tied to the fecundity of the breeding stock since parent oysters having reached sexual maturity, whether within the bay or outside, generated viable larvae with a normal growth under laboratory conditions. Once the water pollution in the bay was established as a cause, the same TABLE 1 Effects of T B T Acetate on C. gigas Embryogenesis and Larval Development T B T acetate (~tg 1- 1) 100 50 25 10 3-5

1 0.5 0.2 0-1 0-05 0.02

Effects on reproduction

Inhibition of fecundity Inhibition of segmentation Partial reduction of segmentation Absence of the formation of trocophores Absence of veligers malformation of trocophores Abnormal veligers-malformation of trocophores Numerous anomalies Total mortality in 8 days Perturbation in food assimilation Total mortality after 12 days Normal D-larvae; slow growth Almost total mortality after 12 days Slow growth; high mortality rate after 10 days No observable effect

From His & Robert, 1983-1985.

1o

Claude Alzieu

authors demonstrated that very low concentrations of tributyltin acetate were highly toxic and extremely harmful to the survival and growth of C. gigas oyster larvae. From various correlations between TBT contents and their effects on larvae (Table l), we observe that there is a very small difference between the no-effect level (NOEL) (20ng1-1) and the level causing considerable mortality as early as the second day (50 rig l-1). Comparatively, the NOEL for copper chloride is roughly 10/~g 1-i, i.e. five hundred times higher than for TBT. Although no evaluation of TBT levels in the waters of Arcachon Bay is available for the period concerned (1975-1982), certain indications seem to suggest that the concentrations at that time were higher than the NOEL for oyster larvae, which would explain the absence of spatfall. Among such assumptions, we find the significant TBT input, estimated at 8 kg day-1 during the summer season, and the high contamination by total tin (0"5-7 mg kg-1 dry weight) found in the digestive gland of oysters bred in the Bay (Alzieu et al., 1981-1982).

EFFECTS ON CALCIFICATION MECHANISMS Abnormalities, consisting of wafer-like chambering of the shell with formation of an interlamellar jelly (Fig. 2), were first observed in 1974 in Arcachon Bay. They progressively spread to all of the oyster culture areas along the Atlantic coast. At that time, H+ral e t al. (1981) described the three successive phases of the phenomenon as follows: (1) hypersecretion of a jelly appearing suddenly at the beginning of July and synchronously across populations of various ages; (2) deposition of a fine calcic layer completely

Fig. 2. Longitudinalsectionthrough an oyster shell showingchambersin both valves.

TBT pollution in France

11

enclosing the jelly within 15 days after its appearance, thus forming a gelatinous pocket; (3) disappearance of the jelly around the end of October or beginning of November, leaving a cavity called the 'chamber'. In addition, Krampitz et al. (1983) have shown that the gelatinous substance contained in the 'chambers' was a protein which differed from the calcification protein (conchyolin) in that its threonine content was higher and it showed a lower proportion of those amino acids providing the link with calcium: aspartic acid, glycine and serine. The determination of the role of TBT in the anomalies described above was established experimentally in the bay of Marennes-O16ron, from the study of batches of anomaly free oysters kept in: (1) a 300 boat marina; and (2) experimental tanks supplied with seawater by tidal input in which plates coated with TBT-base paint were placed. Control batches were placed on one hand in experimental tanks, and on the other hand in a natural environment on oyster beds known to be free of any malformations (Alzieu et al., 1981). Observations showed that the formation of jelly and later of gelatinous pockets developed concurrently both in the marina and in the TBT-contaminated tanks, whereas it was nonexistent in the control batches placed in experimental tanks and in the natural environment. The influence of TBT on the calcification of C. gigas was confirmed by Thain and Waldock (1983). The mechanism of TBT action on calcification remains unknown today. However, recent indications would suggest that TBT may inhibit calcification of C. gigas (formation of gelatinous pockets) at concentrations below 2 ng 1-1 (the lowest concentration tested by Chagot et al. 1990). Furthermore, Okoshi et al. (1987) have shown that sensitivity to chambering was not identical for two stocks of C. gigas bred in Japan. This behaviour could be explained by the presence of different genetic characters. This would tend to confirm the observations made on stocks bred in Arcachon Bay (Deltreil, J. P., 1983, pers. comm.) or the behaviour of hybrids obtained from various morphotypes (Bougrier, S., 1985, pers. comm.).

ECONOMIC IMPACT TBT contamination in the waters of Arcachon Bay coincided with an economic crisis in oyster culture which was so severe that for a while local public authorities considered discontinuing this activity. Losses incurred both in spat sales to other French oyster farms as well as in sales of marketable-size oysters were considerable. Trade professionals have estimated their losses due to the absence of spatfall, which in a normal year represents a production of 12 tons, as amounting to around 600 million

12

Claude Alzieu TABLE 2 Annual C. gigas Oyster Production in Arcachon Bay (ref. SRC Arcachon) Year

Production (tons)

1979 1980 1981 1982 1983 1984 1985

10000 6000 3000 5000 8000 12 000 12000

French francs (aboutUS $100 million). In terms of oyster production for the consumer market, Table 2 shows a decrease of approximately 9000 tons in 1981 as compared with a normal year (1984), which corresponds to a further 90 million French francs (US$15 million) in lost revenue. Between 1979 and 1983, total losses represented 28 000 tons, corresponding to a value of approximately 280 million French francs (US$47 million). This rough estimate shows that, from 1977 to 1983, lost revenues for the Arcachon oyster culture industry, as determined from data compiled by trade professionals, amounted to approximately 880 million francs (US$147 million). Even though it is difficult to attribute all variations in oyster production to the effects of TBT alone, it remains undeniable that the magnitude of the losses claimed by the oyster trade is out of proportion to the market for TBT-based paints which was estimated at 2 million francs (US$0.3 million) in 1981 (13 tons of paint), representing the requirements of the pleasure craft flotilla navigating in Arcachon Bay. However, these estimates do not take into account any indirect economic effects, such as: (1) depreciation in the quality and marketable value, leading to losses of markets controlled by the distribution channels: approximately 90% of the production appears to have been distributed through direct sales during the crisis due to the loss of public image of the product, an image which still has not fully recovered today; (2) reduction in the culture areas and indebtedness of the trade; (3) disaffection of young oyster farmers for a trade whose profitability had become uncertain; and (4) impact of the losses incurred by the oyster industry on the local economic structure. Nonetheless, these estimates alone provide a concrete image of the severe crisis suffered by the Arcachon oyster culture and of the potential dangers facing other bays in the long term. Furthermore, they have more than justified the regulatory measures taken to limit the use of organotins in antifouling paints.

T B T pollution in France

13

FRENCH REGULATIONS France was the first country to regulate the use of organotin-based antifouling paints. The 19 January 1982 ordinance passed by the Ministry of Environment prohibited the use of protective paints containing over 3% organotins on the hull of boats with a gross registered tonnage under 25 tons, in areas with intensive oyster culture, along the English Channel and the Atlantic coasts. These measures, taken initially for a period of 3 months (because of technical regulatory requirements) were extended and later enacted into the Decree of 14 September 1982. This Decree introduced new measures: (1) a ban of all organotin-based paints for boats under 25 m long; a waiver was granted up to 1 October 1982 for paints containing less than 3% organotin; (2) application of the above provisions to the entire coastline; (3) introduction of a waiver for light-alloy boats (taking into account the lack of any tin-free paints compatible with alloys); (4) ordinance defining labelling requirements: packaging of organotin-based paints must bear the statement: 'Caution--Use of this product is prohibited on the hulls, other than light-alloy hulls, of all boats and marine craft having an overall length under 25 m'; (5) enforcement term of the Decree set for 2 years and renewable for the same term. The provisions of the 14 September 1982 Decree were extended without any application deadline as of 10 March 1987. A new decree, integrating the provisions of European Directive No. 89/677/EEC dated 21 December 1989, is currently pending interministerial approval. This new decree considers banning the sale and use of organotinbased antifouling paints on hulls of boats under 25 m, as well as on traps, floats, nets and all immersed equipment, apparatus or constructions. Organotin-based paints would only be sold to maintenance sites in containers of at least 201. In shellfish culture areas, local authorities would be entitled, if needed, to prohibit navigation of all ships protected with organotin-based paints as well as any works on the hulls involving coating or removing of these paints. In addition, the sale and use of paints containing compounds with mercury, arsenic, aldrin, dieldrin, endrin, pentachlorophenol and its derivatives, chlordane, heptachlor, hexachlorobenzene, camphechlor and DDT are prohibited.

C U R R E N T STATUS A N D F U T U R E PROSPECTS The evolution of TBT contamination was initially monitored, from 1982 to 1985, by studying total tin and total organotin contents in the waters and in the flesh of oysters from Arcachon Bay. By the end of this period,

Claude Alzieu

14

INDEX A z~ INDEX B

~

100-

80-

60

40

2O

o 1980

Fig. 3.

81

82

83

84

85

86

87

88

89

Malformation indices between 1980 and 1989 at Cap Ferret Station: A, malformation on upper valve only; B, malformation on both valves.

concentrations were from five to ten times lower than those recorded in 1982 (Alzieu et al. 1986). Concurrently a decrease in shell malformations, both in terms of importance and spread, was observed. From 1985 onwards, monitoring of TBT contents and of TBT degradation products was extended to the input areas along the Atlantic and Mediterranean coastlines. Along the Atlantic coast, TBT contents are close to or below 100 ng i - 1 in marinas, and they do no~t exceed 5 ng i - ~ in oyster culture areas (Alzieu et al., 1989). These findings were confirmed by in situ observations showing that spatfall is taking place normally (NOEL for larvae is 20 ng 1- 1). A small percentage of oysters still exhibit calcification anomalies. Figure 3 shows that acute and subacute malformations have considerably decreased in Arcachon since 1982 and that there was a recurrence of anomalies in 1986-1987 owing to insufficient compliance with regulations. It should be emphasized that, concurrently, copper levels in oyster tissues have not increased in any statistically significant way, although the substitution of TBT-based paints has resulted in a ten-fold increase of copper inputs (Alzieu et al., 1987). Conversely, along the Mediterranean coast, very high contents have been recorded in large harbour areas (2-833 n g l - 1), in marinas (18-736 ngl -~) and in shellfish culture areas ( < 2-111 ng 1- 1) (Alzieu et al., 1990). These high values may be explained by inputs from boats not subject to the regulations ( > 25 m) and by poor water circulation due to the lack of any significant tidal currents. Locally, the concentrations recorded are likely to have harmful impacts on mussel culture.

TBT pollution in France

15

CONCLUSION Table 3 is a reminder highlighting some of the major events in the TBT pollution story and leads to a few final thoughts. TBT pollution in France represents the first instance of dispersioninduced chemical contamination to have produced a major impact on oyster production. In Arcachon Bay, the consequences of TBT have been comparable to certain epizootic diseases caused by parasites which had occurred in the past. In 1981, the cessation of all oyster culture activities was officially considered. The use of TBT in antifouling paints back in 1970 may have been legitimate at that time, in view of the lack of any preventive regulation on the impact of chemicals introduced on the market. A European Directive, passed in 1976, filled that legal void. It is unlikely that this directive would have prevented TBT contamination of coastal waters if it had existed earlier because the ecotoxicological bioassays recommended by the directive are not sufficient to assess the chronic toxicity risks in the aquatic environment. The synthesis of highly toxic molecules should incite us to take into closer consideration the sensitivity of aquatic organisms when laying down regulations. TABLE 3

Major Tributyltin Events 1974 1977 1978-1980 1980-4981

Calcification anomalies "~ Arcachon ) Spatfall failure Anomalies in all oyster grounds in France Search Paint input--larval toxicity Contamination levels Anomalies of calcification

January1982

French temporary ban

1982 1983

Paint-makers studies confirm previous results UK studies confirm larval toxicity and anomalies Spatfall normal in Arcachon Bay Oyster production becomes normal in Arcachon Bay Regulation passed in UK First International Organotin Symposium (Washington DC)

1984 1986 March 1987

French ban definitive

1987 1988 1989

Second International Organotin Symposium (Halifax, Canada) FAO UNEP pilot survey in Mediterranean waters EEC Directive OECD Workshops Management monitoring biological effects WHO Health criteria Convention for the protection of the Mediterranean Sea: adoption of recommendations Third International Organotin Symposium (Monaco)

17 April 1990

16

Claude Alzieu

The January 1982 ban on TBT in antifouling paints is one of those few rare examples where legislators responded quickly in a critical situation. Less than 3 months elapsed between the first scientific evidence and the publication of the first ordinance. Meanwhile, the Commission for Ecotoxicity Assessment of Chemical Substances had recommended banning measures to the Ministry of Environment. At the time this efficiency was greeted with strong criticism, not only from paint manufacturers who wished to have more time to conduct their own studies, but from some scientists who would have liked more data and less pragmatism. Today no one can deny that the strong presumptions on the extreme toxicity of TBT have since been substantiated by research work carried out in many countries. It is now acknowledged that the ban on the use of TBT-based paints on boats under 25 m has considerably reduced the contamination of coastal waters and limited their impact on oyster production, particularly in the Bay of Arcachon. This regulatory approach has since then been duplicated and improved by various national regulations and by the European directive. However, the fact remains that filter-feeder molluscs are not the only species sensitive to TBT trace levels and that, outside of shellfish production areas, high levels of TBT have been measured in the water. The question emerging now is whether current regulations are sufficient to protect coastal ecosystems. REFERENCES Alzieu, CI., H6ral, M., Thibaud, Y., Dardignac, M. J. 8z Feuillet, M. (1981-1982). Influence des peintures antisalissures ~ base d'organostanniques sur la calcification de la coquille de l'hu~tre Crassostrea gigas. Rev. Tray. Int. P~ches Marit., 45, 101-16. Alzieu, CI., Sanjuan, J., Deltreil, J. P. & Borel, M. (1986). Tin contamination in Arcachon bay: effects on oyster shell anomalies. Mar. Pollut. Bull., 17, 494-8. Alzieu, CI., Barbier, G. & Sanjuan, J. (1987). Evolution des teneurs en cuivre deis huitres du bassin d'Arcachon: influence de la 16gislation sur les peintures antisalissures. Oceanol. Acta, 10, 463-8. Alzieu, CI, Sanjuan, J., Michel, P., Borel, M. & Dr6no, J. P. (1989). Monitoring and assessment of butyltins in Atlantic coastal waters. Mar. Pollut. Bull, 20, 22-6. Alzieu, CI., Michel, P., Sanjuan, J. & Averty, B. (1990). Tributyltin levels in French Mediterranean coastal waters. Appl. Organomet. Chem., 4, 55-61. Chagot, D., Alzieu, CI., Sanjuan, J. & Grizel, H. (1990). Sublethal and histopathologicai effects of trace levels of tributyitin fluoride on adult oysters Crassostrea gigas. Aquat. Living Resour., 3, 121-30. H6ral, M., Berthom6, J. P., Polanco-Torr6s, E., Alzieu, CI., Deslou-Paoli, J. M., Razet, D. & de Garnier, J. (1981). Anomalies de croissance de la coquille de Crassostrea gigas.dans le bassin de Marennes-Ol6ron. Bilan de trois ann6es d'observation. CIEM. CM 1981/K, 31 pp.

TBT pollution in France

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His, E. & Robert, R. (1983-1985). D+veloppement des v61ig~res de Crassostrea gigas dans le bassin d'Arcachon. Etudes sur les mortalit6s larvaires. Rev. Tray. Inst. P~ches Marit, 47, 63-88. Krampitz, G., Drolshagen, H. & Deltreil, J. P. (1983). Soluble matrix components in malformed oyster shells. Experientia, 39, 1105-6. Okoshi, K., Mori, K. & Nomura, T. (1987). Characteristics of shell chamber formation between the two local races in the Japanese oyster, Crassostrea gigas. Aquaculture, 67, 313-20. Thain, J. E. & Waldock, M. J. (1983). The effect of suspended sediment and bis, tributyltin oxide on the growth of Crassostrea gigas spat. ICES, CM 1983/E, 10 pp.