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Environmental impact of TBT: the French experience
The Science of the Total Environment 258 Ž2000. 99᎐102
Environmental impact of TBT: the French experience Claude Alzieu IFREMER ᎏ BP 171, 34203 sete ´ cedex, France Accepted 14 April 2000
Abstract The deleterious effects of TBT released by antifouling paints were first documented in Arcachon Bay ŽFrance. at the end of the 1970s. As a result of the high level of water contamination, the production of Pacific oysters was severely affected by a complete lack of reproduction and the appearance of calcification anomalies which were responsible for a strong decline in the marketable value of the remaining stock. Regulations that had been successively adopted from January 1982 had positive effects on the recovery of the oyster grounds by reducing ambient water concentrations. Most antifouling paints act by releasing toxicants into the water which avoid the fixation of the organisms responsible for fouling. The use of these paints results in significant inputs of biocides in the waters. The harmful effects on non-target organisms were first evidenced in the bay of Arcachon ŽFrance. where the most acute disturbances were recorded following tributyltin ŽTBT. contamination. 䊚 2000 Elsevier Science B.V. All rights reserved. Keywords: Tributyltin ŽTBT.; Biological effects; Regulations
1. Arcachon bay The bay of Arcachon, located on the French Atlantic coast, is a triangle-shaped enclosed bay, opening onto the Atlantic Ocean through a narrow channel. Crassostrea gigas oyster beds occupy the central portion of the bay and, in an average year, produce 10 000᎐15 000 tons of commercial oysters. The particular sensitivity of the bay to antifouling inputs is due to fact that the harvest
E-mail address: [email protected] ŽC. Alzieu..
areas are surrounded by marinas and numerous seasonal moorings, representing a total accommodation capacity of 7800 pleasure craft. From 1975 to 1982, oyster production was severely affected as a result of stunted growth problems, followed by a complete lack of reproduction and appearance of shell calcification anomalies ŽAlzieu, 1991.. His and Robert Ž1983r1985. demonstrated that the absence of spatfall was not due to any fecundity problems of the mother oyster, but that the TBT concentrations in the bay waters was the cause. Laboratory and in situ experiments revealed the extreme
0048-9697r00r$ - see front matter 䊚 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 8 - 9 6 9 7 Ž 0 0 . 0 0 5 1 0 - 6
100
C. Alzieu r The Science of the Total En¨ ironment 258 (2000) 99᎐102
Table 1 Effects of TBT acetate on C. gigas embryogenesis and larval development ŽHis and Robert, 1983r1985. TBT acetate Effects on reproduction Žg ly1 . 100 50 25 10 3᎐5 1 0.5 0.2 0.1 0.05 0.02
Inhibition of fecundity Inhibition of segmentation Partial reduction of segmentation Absence of the formation of trocophore Absence of veligers-malformation of trocophore Abnormal veligers-malformation of trocophore 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
toxicity of TBT towards the embryogenesis and larval development of oysters, and the toxicity scale, defined by the same authors, shows that TBT significantly affects larval growth from a concentration level of approximately 20 ng ly1 , and embryogenesis from a level of 1 g ly1 ŽTable 1.. Concurrent with the spatfall recovery failure, cases of stunted growth and shell calcification anomalies were observed as early as 1974. These anomalies consisted of stacked ‘chambers’ filled with a gelatinous substance, giving the shell a ball-like shape. The role of TBT in the calcification anomalies was established experimentally ŽAlzieu et al., 1981᎐1982. from the study of batches of anomaly-free oysters kept in a marina and in experimental tanks, in which plates coated with TBT-based paint were placed. Control batches were placed in experimental tanks, and on oyster beds known to be free of any malformations. Observations showed that the formation of jelly, and later of gelatinous pockets Žchambers., developed concurrently, both in the marina and in the TBT-contaminated tanks, whereas it was non-existent in the control batches placed in uncontaminated experimental tanks and in the TBT-free natural environment. The effect of low levels of TBT on the Pacific oyster shell calcification was confirmed by Thain and Waldock Ž1983.,
and furthermore, Chagot et al. Ž1990. showed that TBT levels below 2 ng ly1 may inhibit calcification, resulting in gelatinous pockets inside the shell. Toxicological data regarding the impact of TBT on marine organisms provide, in certain cases, an estimate of maximum acceptable TBT concentrations, i.e. levels that should not exceed those in order to ensure the reproduction and survival of the most sensitive species. The ‘no observed effect levels’ ŽNOEL. proposed by Alzieu Ž1989. show the extreme sensitivity of planktonic organisms and of molluscs to TBT effects: - 1 ng ly1 1 ng ly1 - 2 ng ly1 20 ng ly1 1᎐10 g ly1 1᎐100 g l - 500 g ly1
Gastropod sexuality Žimposex. Phyto- and zooplankton growth Oyster calcification anomalies Ž C. gigas. Oyster C. gigas reproduction Fish reproduction Fish behaviour Shellfish moult
Results derived from monitoring programs carried out along the Atlantic ŽAlzieu, 1989; Alzieu et al., 1990. and Mediterranean coasts ŽGabrielides et al., 1990., found that these thresholds were frequently exceeded.
2. Regulations The losses incurred in spat sales to other French oyster farms, as well as in the sales of marketable-size oysters, were considerable. A rough estimate by Alzieu Ž1991. suggests that, from 1977 to 1983, the lost revenue for the Arcachon oyster culture industry amounted to approximately US $147 million. Due to the impact on the exploitation of marine biological resources generated by chronic TBT contamination, the question of the feasibility of having the oyster culture inside the bay was addressed to the authorities. As a consequence, France was the first country to regulate the use of organotin-based antifouling paints. The ordinance passed by the Ministry of the Environment on 19 January 1982 prohibited the use of paints containing over 3% organotins on the hulls of boats less than 25 m long, in areas of extensive oyster cultures along the English channel and the
C. Alzieu r The Science of the Total En¨ ironment 258 (2000) 99᎐102
Atlantic coast. This ordinance taken for a period of 3 months, was extended and later enacted into the decree of 14 September 1982, introducing new restrictions: 1. a ban on all organotin paints for boats less than 25 m long to all French coast-weavers was granted, up to the 1 October 1982 for paints containing less than 3% of organotins, and without any limited period for light alloy boats, in consideration of the lack of any tin-free paint compatible with alloys; and 2. ordinance-defining labelling requirements for organotin paints, in order to inform on their limited uses. A new decree, taking into account the provisions of the European Directive, was published in October 1992. The ban was extended to the sale and use of organotin paints for boats less than 25 m long, without any weaver for light alloys, and to all immersed equipment including nets. Sales of organotin paints are only allowed in containers of 20 l for dock maintenance. In addition, the sale and use of paints containing compounds of mercury, arsenic, aldrin, dieldrin, endrin, pentachlorophenol and their derivatives, chlordane, heptachlor, hexachlorobenzene, camphechlor and DDT, are prohibited.
3. Efficiency of the regulations The ban on TBT paints, for boats less than 25 m long, resulted in a progressive decrease of TBT water concentrations, and the subsequent return of normal oyster farming in Arcachon Bay: as early as 1983 for spatfall, and 1984᎐1985 for shell anomalies ŽAlzieu, 1991.. Concurrently, the TBT contamination decreased rapidly: on analysing the total organotin content in the waters and the flesh of oysters, Alzieu et al. Ž1986. estimated that the concentrations were 5᎐10 times lower in 1985 compared to 1982. This decrease was confirmed by the results of monitoring conducted between 1986 and 1992 ŽAlzieu, 1989; Michel, P., personal communication. and shown in Table 2. Sea water TBT levels in marinas were
101
Table 2 TBT sea water contamination Žng ly1 . in Arcachon bay Sampling area
Arcachon Marina La Vigne Marina La Hillion
TBT ng ly1 1986 a
1987 a
1992 b
8᎐57 2᎐89 - 2᎐51
10᎐50 - 2᎐30 2᎐5
7 3 - 0.2
a
Alzieu, 1989. Michel Žunpublished..
b
below the NOEL for oyster reproduction, and below the detection limit in the central part of the bay ŽLa Hillion.. Conversely, and as a consequence of the TBT ban, the use of traditional copper-based paints increased sharply, resulting in a significant increase of copper inputs into marine coastal waters. The long-term monitoring of data between 1979 and 1991 showed an increase in copper content in the flesh of oysters harvested in the vicinity of marinas and mooring areas ŽClaisse and Alzieu, 1993.. This increase, particularly perceptible from 1982, was statistically confirmed by trend analysis.
4. Conclusion TBT contamination in France represented the first instance of dispersion-induced chemical contamination to have produced a major impact on oyster production. In Arcachon Bay, the consequences have been comparable to certain epizootic diseases caused by parasites which had occurred in the past, and in 1981, the cessation of all oyster culture activities was officially considered. The January 1982 ban is one of the rare examples where legislators responded quickly to a critical situation: less than 3 months were necessary to pass of the ordinance after the scientific demonstration of TBT effects. Nevertheless, if the efficiency ban appears undoubted, the TBT trace levels still remaining in coastal waters are sufficient to produce adverse effects on non-target organisms Ži.e. imposex on gastropods.; as a result, local actions are taken in order to reduce
102
C. Alzieu r The Science of the Total En¨ ironment 258 (2000) 99᎐102
TBT inputs from boats of more than 25 m long, as in the Brest roadstead ŽAtlantic coast., where a pilot experiment is being carried out by the French Navy. The objectives are to reduce, by a factor of four, the TBT inputs from coatings operations. This goal will be achieved through the voluntary application of the TBT ban to all ships having a surface hull of less than 1500 m2. In addition, the ban is applied to all roadstead ships. The preliminary results of the survey, conducted to control the efficiency of Navy action, seems encouraging. Nevertheless, there is an urgent need for nondangerous antifouling paints. References Alzieu Cl, Heral ´ M, Thibaud Y, Dardignac MJ, Feuillet M. Influence des peintures antisalissures ` a base d’organostanniques sur la calcification de la coquille de l’huıtre ˆ Crassostrea gigas. Rev Trav Int Peches Marit 1981᎐1982; ˆ 45Ž2.:101᎐116. Alzieu Cl, Sanjuan J, Deltreil JP, Borel M. Tin contamination in Arcachon bay: Effects on oyster shell anomalies. Mar Pollut Bull 1986;17Ž11.:494᎐498.
Alzieu Cl. L’etain et les organoetains en milieu marin: ´ ´ biogeochimie et ´ ecotoxicologie. Rapports scient et tech de ´ l’IFREMER 1989;17:1᎐93. Alzieu Cl, Michel P, Sanjuan J, Averty B. Tributyltin levels in French Mediterranean coastal waters. Appl Organomet Chem 1990;4:55᎐61. Alzieu Cl. Environmental problems caused by TBT in France: assessment, regulations, prospects. Mar Environ Res 1991;32:7᎐17. Chagot D, Alzieu Cl, Sanjuan J, Grizel H. Sublethal and histopathological effects of trace levels of tributyltin fluoride on adult oysters Crassostrea gigas. Aquat Living Resour 1990;3:121᎐130. Claisse D, Alzieu Cl. Copper contamination as a result of antifouling paint regulations? Mar Pollut Bull 1993;26 Ž7.:395᎐397. Gabrielides GP, Alzieu Cl, Readman JW, Bacci E, Aboul Dahab O, Salihoglu I. MED POL survey of organotins in the Mediterranean. Mar Pollut Bull 1990;21Ž5.:233᎐237. His E, Robert R. Developpement des veligeres ´ ´ ` de Crassostrea gigas dans le bassin d’Arcachon. Etudes sur les mortalites ´ larvaires. Rev Trav Inst Peches Marit 1985;47Ž1r2.:63᎐88. ˆ Thain J.E., Waldock M.J. The effect of suspended sediment and bis, tributyltin oxide on the growth of Crassostrea gigas spat. ICES, CM 1983rE:10.
Environmental impact of TBT: the French experience Claude Alzieu IFREMER ᎏ BP 171, 34203 sete ´ cedex, France Accepted 14 April 2000
Abstract The deleterious effects of TBT released by antifouling paints were first documented in Arcachon Bay ŽFrance. at the end of the 1970s. As a result of the high level of water contamination, the production of Pacific oysters was severely affected by a complete lack of reproduction and the appearance of calcification anomalies which were responsible for a strong decline in the marketable value of the remaining stock. Regulations that had been successively adopted from January 1982 had positive effects on the recovery of the oyster grounds by reducing ambient water concentrations. Most antifouling paints act by releasing toxicants into the water which avoid the fixation of the organisms responsible for fouling. The use of these paints results in significant inputs of biocides in the waters. The harmful effects on non-target organisms were first evidenced in the bay of Arcachon ŽFrance. where the most acute disturbances were recorded following tributyltin ŽTBT. contamination. 䊚 2000 Elsevier Science B.V. All rights reserved. Keywords: Tributyltin ŽTBT.; Biological effects; Regulations
1. Arcachon bay The bay of Arcachon, located on the French Atlantic coast, is a triangle-shaped enclosed bay, opening onto the Atlantic Ocean through a narrow channel. Crassostrea gigas oyster beds occupy the central portion of the bay and, in an average year, produce 10 000᎐15 000 tons of commercial oysters. The particular sensitivity of the bay to antifouling inputs is due to fact that the harvest
E-mail address: [email protected] ŽC. Alzieu..
areas are surrounded by marinas and numerous seasonal moorings, representing a total accommodation capacity of 7800 pleasure craft. From 1975 to 1982, oyster production was severely affected as a result of stunted growth problems, followed by a complete lack of reproduction and appearance of shell calcification anomalies ŽAlzieu, 1991.. His and Robert Ž1983r1985. demonstrated that the absence of spatfall was not due to any fecundity problems of the mother oyster, but that the TBT concentrations in the bay waters was the cause. Laboratory and in situ experiments revealed the extreme
0048-9697r00r$ - see front matter 䊚 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 8 - 9 6 9 7 Ž 0 0 . 0 0 5 1 0 - 6
100
C. Alzieu r The Science of the Total En¨ ironment 258 (2000) 99᎐102
Table 1 Effects of TBT acetate on C. gigas embryogenesis and larval development ŽHis and Robert, 1983r1985. TBT acetate Effects on reproduction Žg ly1 . 100 50 25 10 3᎐5 1 0.5 0.2 0.1 0.05 0.02
Inhibition of fecundity Inhibition of segmentation Partial reduction of segmentation Absence of the formation of trocophore Absence of veligers-malformation of trocophore Abnormal veligers-malformation of trocophore 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
toxicity of TBT towards the embryogenesis and larval development of oysters, and the toxicity scale, defined by the same authors, shows that TBT significantly affects larval growth from a concentration level of approximately 20 ng ly1 , and embryogenesis from a level of 1 g ly1 ŽTable 1.. Concurrent with the spatfall recovery failure, cases of stunted growth and shell calcification anomalies were observed as early as 1974. These anomalies consisted of stacked ‘chambers’ filled with a gelatinous substance, giving the shell a ball-like shape. The role of TBT in the calcification anomalies was established experimentally ŽAlzieu et al., 1981᎐1982. from the study of batches of anomaly-free oysters kept in a marina and in experimental tanks, in which plates coated with TBT-based paint were placed. Control batches were placed in experimental tanks, and on oyster beds known to be free of any malformations. Observations showed that the formation of jelly, and later of gelatinous pockets Žchambers., developed concurrently, both in the marina and in the TBT-contaminated tanks, whereas it was non-existent in the control batches placed in uncontaminated experimental tanks and in the TBT-free natural environment. The effect of low levels of TBT on the Pacific oyster shell calcification was confirmed by Thain and Waldock Ž1983.,
and furthermore, Chagot et al. Ž1990. showed that TBT levels below 2 ng ly1 may inhibit calcification, resulting in gelatinous pockets inside the shell. Toxicological data regarding the impact of TBT on marine organisms provide, in certain cases, an estimate of maximum acceptable TBT concentrations, i.e. levels that should not exceed those in order to ensure the reproduction and survival of the most sensitive species. The ‘no observed effect levels’ ŽNOEL. proposed by Alzieu Ž1989. show the extreme sensitivity of planktonic organisms and of molluscs to TBT effects: - 1 ng ly1 1 ng ly1 - 2 ng ly1 20 ng ly1 1᎐10 g ly1 1᎐100 g l - 500 g ly1
Gastropod sexuality Žimposex. Phyto- and zooplankton growth Oyster calcification anomalies Ž C. gigas. Oyster C. gigas reproduction Fish reproduction Fish behaviour Shellfish moult
Results derived from monitoring programs carried out along the Atlantic ŽAlzieu, 1989; Alzieu et al., 1990. and Mediterranean coasts ŽGabrielides et al., 1990., found that these thresholds were frequently exceeded.
2. Regulations The losses incurred in spat sales to other French oyster farms, as well as in the sales of marketable-size oysters, were considerable. A rough estimate by Alzieu Ž1991. suggests that, from 1977 to 1983, the lost revenue for the Arcachon oyster culture industry amounted to approximately US $147 million. Due to the impact on the exploitation of marine biological resources generated by chronic TBT contamination, the question of the feasibility of having the oyster culture inside the bay was addressed to the authorities. As a consequence, France was the first country to regulate the use of organotin-based antifouling paints. The ordinance passed by the Ministry of the Environment on 19 January 1982 prohibited the use of paints containing over 3% organotins on the hulls of boats less than 25 m long, in areas of extensive oyster cultures along the English channel and the
C. Alzieu r The Science of the Total En¨ ironment 258 (2000) 99᎐102
Atlantic coast. This ordinance taken for a period of 3 months, was extended and later enacted into the decree of 14 September 1982, introducing new restrictions: 1. a ban on all organotin paints for boats less than 25 m long to all French coast-weavers was granted, up to the 1 October 1982 for paints containing less than 3% of organotins, and without any limited period for light alloy boats, in consideration of the lack of any tin-free paint compatible with alloys; and 2. ordinance-defining labelling requirements for organotin paints, in order to inform on their limited uses. A new decree, taking into account the provisions of the European Directive, was published in October 1992. The ban was extended to the sale and use of organotin paints for boats less than 25 m long, without any weaver for light alloys, and to all immersed equipment including nets. Sales of organotin paints are only allowed in containers of 20 l for dock maintenance. In addition, the sale and use of paints containing compounds of mercury, arsenic, aldrin, dieldrin, endrin, pentachlorophenol and their derivatives, chlordane, heptachlor, hexachlorobenzene, camphechlor and DDT, are prohibited.
3. Efficiency of the regulations The ban on TBT paints, for boats less than 25 m long, resulted in a progressive decrease of TBT water concentrations, and the subsequent return of normal oyster farming in Arcachon Bay: as early as 1983 for spatfall, and 1984᎐1985 for shell anomalies ŽAlzieu, 1991.. Concurrently, the TBT contamination decreased rapidly: on analysing the total organotin content in the waters and the flesh of oysters, Alzieu et al. Ž1986. estimated that the concentrations were 5᎐10 times lower in 1985 compared to 1982. This decrease was confirmed by the results of monitoring conducted between 1986 and 1992 ŽAlzieu, 1989; Michel, P., personal communication. and shown in Table 2. Sea water TBT levels in marinas were
101
Table 2 TBT sea water contamination Žng ly1 . in Arcachon bay Sampling area
Arcachon Marina La Vigne Marina La Hillion
TBT ng ly1 1986 a
1987 a
1992 b
8᎐57 2᎐89 - 2᎐51
10᎐50 - 2᎐30 2᎐5
7 3 - 0.2
a
Alzieu, 1989. Michel Žunpublished..
b
below the NOEL for oyster reproduction, and below the detection limit in the central part of the bay ŽLa Hillion.. Conversely, and as a consequence of the TBT ban, the use of traditional copper-based paints increased sharply, resulting in a significant increase of copper inputs into marine coastal waters. The long-term monitoring of data between 1979 and 1991 showed an increase in copper content in the flesh of oysters harvested in the vicinity of marinas and mooring areas ŽClaisse and Alzieu, 1993.. This increase, particularly perceptible from 1982, was statistically confirmed by trend analysis.
4. Conclusion TBT contamination in France represented the first instance of dispersion-induced chemical contamination to have produced a major impact on oyster production. In Arcachon Bay, the consequences have been comparable to certain epizootic diseases caused by parasites which had occurred in the past, and in 1981, the cessation of all oyster culture activities was officially considered. The January 1982 ban is one of the rare examples where legislators responded quickly to a critical situation: less than 3 months were necessary to pass of the ordinance after the scientific demonstration of TBT effects. Nevertheless, if the efficiency ban appears undoubted, the TBT trace levels still remaining in coastal waters are sufficient to produce adverse effects on non-target organisms Ži.e. imposex on gastropods.; as a result, local actions are taken in order to reduce
102
C. Alzieu r The Science of the Total En¨ ironment 258 (2000) 99᎐102
TBT inputs from boats of more than 25 m long, as in the Brest roadstead ŽAtlantic coast., where a pilot experiment is being carried out by the French Navy. The objectives are to reduce, by a factor of four, the TBT inputs from coatings operations. This goal will be achieved through the voluntary application of the TBT ban to all ships having a surface hull of less than 1500 m2. In addition, the ban is applied to all roadstead ships. The preliminary results of the survey, conducted to control the efficiency of Navy action, seems encouraging. Nevertheless, there is an urgent need for nondangerous antifouling paints. References Alzieu Cl, Heral ´ M, Thibaud Y, Dardignac MJ, Feuillet M. Influence des peintures antisalissures ` a base d’organostanniques sur la calcification de la coquille de l’huıtre ˆ Crassostrea gigas. Rev Trav Int Peches Marit 1981᎐1982; ˆ 45Ž2.:101᎐116. Alzieu Cl, Sanjuan J, Deltreil JP, Borel M. Tin contamination in Arcachon bay: Effects on oyster shell anomalies. Mar Pollut Bull 1986;17Ž11.:494᎐498.
Alzieu Cl. L’etain et les organoetains en milieu marin: ´ ´ biogeochimie et ´ ecotoxicologie. Rapports scient et tech de ´ l’IFREMER 1989;17:1᎐93. Alzieu Cl, Michel P, Sanjuan J, Averty B. Tributyltin levels in French Mediterranean coastal waters. Appl Organomet Chem 1990;4:55᎐61. Alzieu Cl. Environmental problems caused by TBT in France: assessment, regulations, prospects. Mar Environ Res 1991;32:7᎐17. Chagot D, Alzieu Cl, Sanjuan J, Grizel H. Sublethal and histopathological effects of trace levels of tributyltin fluoride on adult oysters Crassostrea gigas. Aquat Living Resour 1990;3:121᎐130. Claisse D, Alzieu Cl. Copper contamination as a result of antifouling paint regulations? Mar Pollut Bull 1993;26 Ž7.:395᎐397. Gabrielides GP, Alzieu Cl, Readman JW, Bacci E, Aboul Dahab O, Salihoglu I. MED POL survey of organotins in the Mediterranean. Mar Pollut Bull 1990;21Ž5.:233᎐237. His E, Robert R. Developpement des veligeres ´ ´ ` de Crassostrea gigas dans le bassin d’Arcachon. Etudes sur les mortalites ´ larvaires. Rev Trav Inst Peches Marit 1985;47Ž1r2.:63᎐88. ˆ Thain J.E., Waldock M.J. The effect of suspended sediment and bis, tributyltin oxide on the growth of Crassostrea gigas spat. ICES, CM 1983rE:10.