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Organotin compounds, fouling and the marine environment
Ocean & Shoreline Management 12 (1989) 285-294
Organotin Compounds, Fouling and the Marine Environment E. O. Oyewo Nigerian Institute for Oceanography and Marine Research, P. M. B. 12729, Lagos, Nigeria (Received 14 September 1988; accepted 11 November 1988)
ABSTRACT Routine shipping, boating and ocean engineering activities present surfaces on which fouling organisms can settle and create economic, operational and aesthetic problems. Tri-organotin-based anti-fouling preparations are often applied to these surfaces, leading to the inevitable introduction of tri-organotins into the marine environment. After critically considering several aspects of the behaviour, toxicity, toxicology, known and potential interactions of tri-organotins with biotic and abiotic components of the marine environment, it is concluded that tri-organotins are potentially hazardous. The need for more studies, and for caution in their application, is proposed.
INTRODUCTION The fouling of ships and other structures subjected to sea water is a long established, economic, operational and aesthetic problem. Anti-fouling strategies often involve chemical control, thus raising the vexed issue of the introduction of chemicals into the marine environment. This review, which is biased towards tri-organotins in relation to anti-fouling measures, summarises and discusses the fouling problem, as well as the behaviour and effects of tri-organotin compounds--especially in the marine environment. The principal aim is to give advance warning about, and focus world attention on, a potential marine pollution problem--thus avoiding 285 Ocean & Shoreline Management 0951-8312/89/$3-50 © 1989 Elsevier Science Publishers Ltd, England. Printed in Northern Ireland
286
E. O. Oyewo
another 'minimata' disaster. The article also gives some information on the fouling problem and some aspects of organotin chemistry.
HISTORICAL ASPECTS Tin is one of the earliest metals known to man, and although the pure metal was not used until 600 Bc, it was used in bronze implements as early as 3500 BC.1 Over a period of time, there has been a phenomenal growth in the tin industry; perhaps because tin can improve the characteristics of other materials, it has an extremely wide diversity of application in the chemical market classification. However, most of the growth in tin chemicals has resulted from increased demand for organotin compounds. Between 1965 and 1975, annual world production of organotin compounds rose from 2000 to 25 000 tons (2.03 x 1062.54 x 107 kg). 2 By 1980, annual production was estimated at more than 30000 tons (3.05 x 10~°kg). 3 Paralleling this increased production, there has been growing interest and development in organotin chemistry. The application of organotin chemicals broadly divides between the use of di-organotins in association with plastics, and the use of tri-organotins as biocides in varying circumstances. 4,5 Some of the latter uses lead to their introduction into the marine environment. In fact, the most significant routes of tri-organotin compounds into the sea is through their use in anti-fouling preparations and also from industrial discharges. For anti-fouling paints only, about 3000 tons (3"05 × 106 kg) of tri-organotins are used annually. 3 THE FOULING PROBLEM Generally, fouling results from the settlement and growth (usually unwanted) of algae and invertebrates on surfaces and structures immersed in sea water. These surfaces include the hulls of ships, oil platforms, jetties, buoys, marine pipes and cables, desalination and power plants. 6"7 Microfouling on anti-fouling coatings is also known. 8 About 5000 species of fouling organisms have already been identified, and, with some exceptions, fouling by algae is generally associated with mobile structures, while animal fouling is associated with stationary structures.4'6 The commonest fouling alga belongs to the genus Enteromorpha. According to Christie & Shaw, 9 its dominance is due to its ability to withstand wide fluctuations in environmental conditions, and to an effective spore attachment mechanism and a high regenerative capacity. Other fouling algae include species from the following genera:
Organotin compounds in the marine environment
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Ectocarpus, Cladophora, Chaetomorpha, Ulothrix and Polysiphonia. Animal foulers are mainly barnacles, molluscs, tube worms, sponges and hydroids. 4 One of the best known effects of fouling is the increased frictional resistance to ship movement, leading to increased fuel consumption. With large ships, an increase in cost of about 0.5% (sterling £80 000 per year in 1972) would result from a loss of only 0.1 knots (0.19 km/h) on a service speed of 16knots (29.65 km/h). ~° One estimate puts worldwide costs to shipping concerns, due to marine fouling, at $1000 million per year." Fouling also leads to the need for frequent dry docking, and hampers inspection, repair and maintenance of marine platforms. Tenacious attachment by fouling organisms can cause paint damage, while some fouling organisms can accelerate localised corrosion. H A thick growth of fouling organisms on oil platforms can create engineering problems by increasing the loading forces on the platform caused by waves and currents, and leading to design specifications being exceeded. 7 Aesthetically, fouling is unsightly and can be a nuisance to shippers and engineers. One logical way of preventing fouling is to protect a structure with an anti-fouling coating. Copper compounds were for many years the toxic agents in anti-fouling compositions, while compounds of mercury, tin, lead or zinc were sometimes used as boosters in these preparations. 6 However, the contemporary anti-fouling systems of choice are those that are based on tri-organotin compounds. THE REASONS FOR P R E F E R E N T I A L USE OF TRIORGANOTIN-BASED SYSTEMS According to Smith & Smith 2 and Craig, 3 tri-organotin compounds are effectively biocidal to a wide range of fouling organisms at low concentrations. They constitute only a minimum toxid hazard during application, and their terminal breakdown products are apparently innocuous and pose no serious long-term environmental problems. 2:,12 After application, they degrade to the less toxic di-organotins. Furthermore, they may be converted into tetra-organotins which are volatile and should therefore not accumulate in the marine environment. ~3 The mechanism for such a conversion involving naturally occurring iodomethane has been demonstrated. 14 Also, low mammalian toxicity and the reversibility of the poisonous effects of tri-organotins have been reported. 15-17 With such a unique combination of seemingly ideal properties, it is little surprise that they enjoy preferential usage which leads to their introduction in large amounts into the marine environment.
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IS T H E R E ANY NEED FOR CONCERN? In order to put this question in the proper perspective, it is necessary to examine the environmental behaviour, toxicity, toxicology and some specific effects of tri-organotins on some living organisms. To start with, the efficacy of tri-organotins as anti-fouling biocides logically implies that they are potent poisons. The argument that tri-organotins can break down into less toxic species or be converted into volatile and easily lost ones fails to take cognisance of the various inter-specific conversions that may occur in the environment. Besides, any of the organotin compounds can be picked up by a living organism and once ingested it may directly exercise some toxic effects, bio-magnified into toxic levels or in any case become incorporated into the food web. It is also necessary to recognise that the hazards posed by any chemical in the marine environment cannot be positively appreciated if its chemical properties are considered in isolation without reference to its established or potential interactions with biotic and abiotic components of the environment.
Speciation of tri-organotins It has been postulated that the degradation of tri-organotins in the environment starts with the absorption of UV light, or by biological or chemical means. 3 The decay then continues by tlhe stepwise loss of the organic groups. According to Poller, 18 the change from tri- to diorganotin involves the homolytic cleavage of the tin-carbon bond. The decay continues through to mono-organotin, and the final product may be the inorganic tin species. 3 Most of the evidence for speciation is from in-vitro studies. When decay studies are carried out under conditions that better simulate the environment, a greater stability for organotin species is suggested. 3 It also has to be pointed out that there are uncertainties in the terminal stages of the aforementioned scheme, and the end-product may not be inorganic tin. It has been reported, for example, that triphenyltin hydroxide in an aqueous environment degrades via photolysis to diphenyltin oxide accompanied by further degradation into a water-soluble, non-extractable polymeric species. 19
Some specific deleterious effects of tri-organotins Van der Kerk & Luitjen 5 established that growth is completely inhibited in some fungi by low concentrations (0-2-5 ppm) of triphenyltin chloride. Inhibition of carbon fixation by triphenyltin chloride has also been demonstrated in the diatom A c h n a n t h e s subsessilis. 2°
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It has also been shown that photosynthesis and respiration are inhibited in the algae Enteromorpha intestinalis and Ulothrix psendoflaca by triphenyltin chloride. 11 In the same paper, it was shown that photosynthesis is more sensitive to this biocide. Stuart 22 also reports that the 144-h ECso of bis(tributyltin) oxide (TBTO) for the copepod Acartia tonsa was 0-4 mg litre -1, a value which is close to that measured in San Diego bay. Ward et a1.,23 working with TBTO and a saltwater fish Cyprinodon variegatus, found the LCs0 to be 0-96 ppb (billion = 109). Even though the fish were metabolising the TBTO to the lower and less toxic alkyl moieties, a biocide that kills 50% of test animals at concentrations less than i ppb. should be regarded as hazardous in the environment. Further studies have associated shell deformations in Crassostrea gigas with the presence of TBTO and tributyltin fluoride (TBTF) in water. 24'25 As a result of this research, the French Government imposed a series of bans on anti-fouling preparations containing these compounds and prohibited their use on small boats. Perhaps the most disturbing aspect of some of these ill-effects is that organisms close to or at the centre of primary production are involved. Furthermore, it is known that methyl metals (which are more toxic than the inorganic forms) are more readily taken up by algae than other metal forms. 26 It is also interesting to note the indication that some organisms may develop resistance to tri-organotins. 12 Although this is not widespread at present, the implication of this finding is that if resistance becomes prevalent, larger quantities of the chemicals will be needed, or more potent ones will have to be developed.
Aikylation Since organometals are generally more toxic than their inorganic form, 3 alkylation is a relevant environmental issue. It has been shown that methylation can occur in sediments, and may be brought about by biotic as well as abiotic means. 27'37 An abiotic pathway for alkylation involving the redistribution of trimethyltin hydroxide has been demonstrated. Naturally occurring sulphides, iodomethane and alkylcobalamins can mediate alkylation, x3'14'28'29 It has also been reported 3° that these transformations can occur both within and without the bodies of organisms, while Kimmel et al. 31 have reported dealkylation mechanisms in relation to the mammalian metabolism of the miticide cyhexatin (tricyclohexyltin hydroxide). These possible interconversions suggests that environmentalists should be concerned about the presence of any organotin species in the environment. In this respect, even those triorganotins used in agriculture, ~5'32 as well as their breakdown products, may get into estuarine systems and should therefore be of concern.
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Toxicology of organotin compounds In general, the biological effects of tetra-organotins (ILSn) in mammals appears to be caused principally by the tri-organotin (R3Sn) compounds which are formed by their in-vivo and in-vitro conversions, especially in liver t i s s u e ) 6'17'33 This is probably why, compared to the tri-compound, there is a delay in the onset of poisoning. 34 As toxicological hazards therefore, tetra-organotins should be regarded as the equivalent trisubstituted compounds. From the toxicological viewpoint, tri-organotins are the most important organotin species; according to Craig 3 and Smith, ~7 the toxicity of organotin compounds is at a maximum when three organic groups are present (R3SnX). Maximum toxicity usually occurs for R = methylbutyl. Further increase in the length of the n-alkyl chain produces a sharp drop in toxicity. The mode of acute tri-organotin toxicity has been linked with their disruption of various mitochondrial functions through membrane damage, disruption of ionic transport and inhibition of ATP synthesis. 35 Triphenyltin iodide has powerful sternutatory effects. 16 The toxicology of di-organotins is different. The toxic action of the lower di-alkyltins is due to their ability to combine with enzymes containing two thiol groups in the correct formation. According to Smith, 17 the toxic effect of lower di-alkyltin compounds are similar to those of trivalent arsenicals in the inhibition of alpha-keto oxidases containing dithiol groups. The trend of decreasing toxicity with increase in length of the alkyl chain is also true for di-organotins.17 Mono-organotin compounds also show the trend of decreasing toxicity with increasing length of the alkyl chain but do not seen to have any important toxic action in mammals. The oral LDs0 for some mono-ethyltin compounds to the rat is between 70 and 700 mg/kg. ~6'17 Inorganic tin has very low mammalian toxicity. The acceptable level of tin in canned food is 250 times that of lead.~7 A R E THERE ANY A L T E R N A T I V E MEASURES? Currently, alternatives to chemical anti-fouling measures are receiving very little attention. The reason is probably because of the claims that tri-organotins, for example, are innocuous in the marine environment. Thus, it is necessary to examine a few alternatives, even if their application is futuristic. In the North Sea, a metal-protection system which depends on artificially cancelling out the natural ionic currents
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established between different structural members of submarine platforms appears to prevent the settling of fouling organisms. 7 There have also been speculations on the inhibitory effects of cathodic protection on marine growth by sacrificial anodism. The effect is, however, not yet very clear. 7 There is also the vexed question of biological control. In 1977, divers of the Chevron Oil Corporation successfully cleared paths on oil platforms through sea anemones thus allowing star fish access to climb and graze on fouling organisms. 7 This is a pointer to the possibility of biological control.
DISCUSSION From the ecological viewpoint only, a biological alternative is preferable even if impracticable in some circumstances. However, no matter what anti-fouling measures are contemplated, there is a need for more investigations into marine chemistry, organotin chemistry and the biology of fouling organisms. This need has in fact been stressed in the past. 6 The patterns of colonisation of fouling organisms, their zonation with depth, growth rate, succession pattern and even physiology must be well understood in attempting to rationally solve the problems of fouling. There should also be a careful balance between economic and environmental considerations. The former should not be at the expense of the latter. It is particularly noteworthy that the release of tri-organotins is more prevalent and more environmentally significant in harbours rather than the open sea. 3 Harbours are usually estuarine, and estuaries are complex ecosystems. Estuaries also have multiple uses which can be impaired by pollution. These uses are perhaps epitomised by the Lagos Harbour Complex in Nigeria. Apart from being a shipping lane, it is a nursery ground for some fish species and actually supports an artisanal fishery. It is an amenity for the Lagos Boat Club but also a recipient of domestic and industrial waste. Although tri-organotins and their breakdown products are generally less toxic than other organometallic equivalents, this should be seen in a relative context only. Low toxicity does not mean no toxicity, neither is low mammalian toxicity synonymous with low biological toxicity in general. A lot of data on organotin toxicity relates to mammals and this could be misleading; The LDs0 of vendex (bis(triphenyltin) oxide) to rats is 2630mg/kg. 15 The 96-h LDs0 of the same compound for blue-gill, fathead minnow and rainbow trout is 0.0048, 0.0019 and 0-0017 ppm respectively. It is also known that some other tri-organotin
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compounds with low mammalian toxicity are highly toxic to other forms of life. 4 It is also necessary to emphasise that, even where a chemical does not produce an acute effect, it may have insidious sub-lethal effects which may be important in the long run. Moreover, in the marine environment, living organisms are simultaneously exposed to a myriad of environmental stresses. Not only could the introduction of tri-organotins constitute an additional stress, it could, in combination with other factors, have a synergistic effect on or render some organisms susceptible to stresses to which they otherwise would not succumb. It has to be recognised that the marine environment is a very complex one in which nature maintains a delicate and dynamic equilibrium. The role that any particular biotic or abiotic species plays in this equilibrium is sometimes not well understood. Even where the environmental behaviour of a substance is predictable on the basis of its properties or similarity to a c o m p o u n d whose environmental behaviour is known, a surprise factor is often present in such considerations. 36 Against this background, the introduction of anything foreign, particularly chemicals, into the marine environment clearly needs to be done with caution and ideally with a sound understanding of both the shortand long-term effects of such introduction. ACKNOWLEDGEMENT A literature review carried out by the author as part of the MSc Pollution Control programme of the University of Leeds in 1984 formed the basis of this paper. The author is grateful to Dr L. V. Evans of the Plant Sciences D e p a r t m e n t for his helpful comments and suggestions. REFERENCES 1. Carlin, Jr, J. F., Mineral facts and problems. US Department of Interior, Burean of Mines Bulletin 671, 1980. 2. Smith, P. & Smith, L., Organotin compounds and applications. Chem. Brit., U (1975) 208-13. 3. Craig, P. J., Organometallic compounds in the environment. In Pollution: Causes, Effects and Control, ed. R. M. Harrison. Royal Society of Chem-, istry London, 1983, pp. 277-322. 4. Evans, C. J. & Smith, P. J., Organotin based anti-fouling systems. J. Oil Col. Chem. Assoc., 58 (1975) 160-8. 5. Van der Kerk, G. J. M. & Luitjen, J. G. A., Organotin compounds. III: The biocidal properties of organotin compounds. J. Appl. Chem., 4 (1954) 314-9. 6. Evans, L. V., Marine algae and fouling: A review with particular reference to ship fouling. Bot. Mar. xxxiv (1981) 177-83.
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7. Ralph, R. & Goodman, K., Foulplay beneath the waves: biology of North Sea platforms. New Scientist, 82 (1160) (1979) 1018-21. 8. Bishop, J. H., Silva, S. R. & Silva, V. M., A study of microfouling on anti-fouling coating using electron microscopy. J. Oil Col. Chem. Assoc., 57 (1974) 30-5. 9. Christie, A. O. & Shaw, M., Settlement experiments with zoospores of Enteromorpha intestinalis (L.) Link. Brit. Phycol. Bull., 3 (1968) 529-34. 10. Banfield, T. A., Antifouling compositions for large tankers. Pigment Resin Technol., 1(4) (1972) 33-7. 11. Terry, L. A. & Edyvean, R. G. J., Micro-algae and corrosion. Bot. Mar., xxiv (1981) 177-83. 12. Evans, C. J., Developments in the organotin industry. Part 1: Triorganotin chemicals. Tin and its Uses, (100) (1970) 3-6. 13. Guard, H. F., Cobet, A. B. & Coleman, W. M., Methylation of trimethyltin compounds by estuarine sediments. Science, 213 (4509) (1981) 770-1. 14. Craig, P. J. & Rapsomanikis, S. A new route to tris(dimethyltin sulphide) with tetramethyltin as co-product. J. Chem. Soc., Chem. Commun., (2) (1982) 114. 15. Evans, C. J., A new organotin miticide. Tin and its Uses, (110) (1976) 6-7. 16. Barnes, J. M. & Margos, L., The toxicology of organometallic compounds. Organomet. Chem. Rev., 3 (1968) 137-50. 17. Smith, P. J.~ Toxicological data on organotin compounds. In International Tin Research Council Publications, 1978 No. 538 pp. 3-10 and following Appendix D to p. 18. 18. Poller, R. C., Cleavage of tin-carbon bonds. In Organotin Chemistry Ed. R. C. Pollen. Logos Press, London, 1970, pp. 53-63. 19. Soderquist, C. J. & Crosby, D. G., Degradation of triphenyltin hydroxide in water. J. Agric. Food Chem., 28 (1982) 110-17. 20. Callow, M. E. & Evans, L. V., Some effects of triphenyltin chloride on Achnanthes subsessilis. Bot. Mar., xxiv (1981) 201-5. 21. Milner, P. A. & Evans, L. V., The effects of triphenyltin chloride on respiration and photosynthesis in the green algae: Enteromorpha intestinalis and Ulothrix Pseudoflacca. Plant, Cell Environ., 3 (1980) 339-48. 22. Stuart, C. U., Acute toxicity of bis(tributyltin) oxide to a marine copepod. Mar. Pollut. Bull., 14(8) (1983) 303-6. 23. Ward, G. S., Cramm, G. C., Parrish, P. R., Trachman, H. & Slesinger, A., Bioaccumulation and chronic toxicity of bis(tributyltin) oxide (TBTO): Tests with a saltwater fish. In Aquatic Toxicology and hazard assessment: Fourth Conference, ed. D. R. Branson & K. L. Dickson. American Society for Testing and Materials Special Publication No. 737, 1981, pp. 183-200. 24. Alzieu, et al., Influence des peintures anti-salissures dans les zones cochylicoles. Rev. Tray. Inst. Pech. Marit., 44 (1982) 301-49. 25. Waldock, M. J. & Thain, J. E., Shell thickening in Crassostrea gigas: Organotin anti-fouling or sediment induced. Mar. Pollut. Bull., 14(11) (1983) 411-5. 26. Laxen, D. P. H., The chemistry of metal pollution in water. In Pollution: Causes, Effects and Control, ed. R. M. Harrison. Royal Society of Chemistry, London, 1983.
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27. Hallas, L. E., Means, J. C. & Cooney, J. J., Methylation of tin by estuarine organisms. Science, 215(4539) (1982) 1505-7. 28. Thayer, J. S. & Brinckman, F. E., The biological methylation of metals and metalloids. In Advances in Organometallic Chemistry, Vol. 20, ed. F. S. A. Stone & R. West. Academic Press, New York, 1982, pp. 314-48. 29. Fanchiag, Y. T. & Wood, J. M., Alkylation of tin by alkylcobalamins. J. A. Chem. Soc., 103 (117) (1981) 5100-3. 30. Fish, R. H., Kimmel, E. C. & Casida, J. E., Bio-organotin Chemistry: Reactions of tributyltin derivatives with a cytochrome P-450 dependent mono-oxygenase enzyme system. J. Organomet. Chem., 118 (1976) 4-54. 31. Kimmel, E. C., Casida, J. E. & Fish, R. A., Bio-organotin Chemistry: Microsomal monooxygenase and mammalian metabolism of cyclohexyl compounds. J. Agric. Food Chem. 28 (1980) 117-22. 32. Evans, C. J., Plictran: A new organotin acaricide. Tin and its Uses, (86) (1970) 7-10. 33. Davies, A. G. & Smith, P. J., Recent advances in organotin chemistry. Adv. Inorg. Radiochem., 23 (1980) 1-77. 34. Cremer, J. E., The conversion of tetraethyltin into triethyltin in mammals. Biochem. J., 68 (1958) 685-92. 35. Stockdale, M., Dawson, A. P. & Selwyn, M. J., Effects of trialkyltin and triphenyltin compounds on mitochondrial respiration. Eur. J. Biochem., 15 (1970) 342-51. 36. Goldberg, E. D., Marine pollution. In Chemical Oceanography, Vol. 3, 2nd edn, ed. J. P. Riley & G. Skirrow. Academic Press, London, 1975, pp. 39-89. 37. Jewett, K. L., Brinckman, F. E. & Bellama, J. M., Chemical factors influencing metal alkylation in water. In Marine Chemistry in the Coastal Environment, ACS Symposium Series 18. American Chemical Society, Washington DC, 1975, pp. 304-18.
Organotin Compounds, Fouling and the Marine Environment E. O. Oyewo Nigerian Institute for Oceanography and Marine Research, P. M. B. 12729, Lagos, Nigeria (Received 14 September 1988; accepted 11 November 1988)
ABSTRACT Routine shipping, boating and ocean engineering activities present surfaces on which fouling organisms can settle and create economic, operational and aesthetic problems. Tri-organotin-based anti-fouling preparations are often applied to these surfaces, leading to the inevitable introduction of tri-organotins into the marine environment. After critically considering several aspects of the behaviour, toxicity, toxicology, known and potential interactions of tri-organotins with biotic and abiotic components of the marine environment, it is concluded that tri-organotins are potentially hazardous. The need for more studies, and for caution in their application, is proposed.
INTRODUCTION The fouling of ships and other structures subjected to sea water is a long established, economic, operational and aesthetic problem. Anti-fouling strategies often involve chemical control, thus raising the vexed issue of the introduction of chemicals into the marine environment. This review, which is biased towards tri-organotins in relation to anti-fouling measures, summarises and discusses the fouling problem, as well as the behaviour and effects of tri-organotin compounds--especially in the marine environment. The principal aim is to give advance warning about, and focus world attention on, a potential marine pollution problem--thus avoiding 285 Ocean & Shoreline Management 0951-8312/89/$3-50 © 1989 Elsevier Science Publishers Ltd, England. Printed in Northern Ireland
286
E. O. Oyewo
another 'minimata' disaster. The article also gives some information on the fouling problem and some aspects of organotin chemistry.
HISTORICAL ASPECTS Tin is one of the earliest metals known to man, and although the pure metal was not used until 600 Bc, it was used in bronze implements as early as 3500 BC.1 Over a period of time, there has been a phenomenal growth in the tin industry; perhaps because tin can improve the characteristics of other materials, it has an extremely wide diversity of application in the chemical market classification. However, most of the growth in tin chemicals has resulted from increased demand for organotin compounds. Between 1965 and 1975, annual world production of organotin compounds rose from 2000 to 25 000 tons (2.03 x 1062.54 x 107 kg). 2 By 1980, annual production was estimated at more than 30000 tons (3.05 x 10~°kg). 3 Paralleling this increased production, there has been growing interest and development in organotin chemistry. The application of organotin chemicals broadly divides between the use of di-organotins in association with plastics, and the use of tri-organotins as biocides in varying circumstances. 4,5 Some of the latter uses lead to their introduction into the marine environment. In fact, the most significant routes of tri-organotin compounds into the sea is through their use in anti-fouling preparations and also from industrial discharges. For anti-fouling paints only, about 3000 tons (3"05 × 106 kg) of tri-organotins are used annually. 3 THE FOULING PROBLEM Generally, fouling results from the settlement and growth (usually unwanted) of algae and invertebrates on surfaces and structures immersed in sea water. These surfaces include the hulls of ships, oil platforms, jetties, buoys, marine pipes and cables, desalination and power plants. 6"7 Microfouling on anti-fouling coatings is also known. 8 About 5000 species of fouling organisms have already been identified, and, with some exceptions, fouling by algae is generally associated with mobile structures, while animal fouling is associated with stationary structures.4'6 The commonest fouling alga belongs to the genus Enteromorpha. According to Christie & Shaw, 9 its dominance is due to its ability to withstand wide fluctuations in environmental conditions, and to an effective spore attachment mechanism and a high regenerative capacity. Other fouling algae include species from the following genera:
Organotin compounds in the marine environment
287
Ectocarpus, Cladophora, Chaetomorpha, Ulothrix and Polysiphonia. Animal foulers are mainly barnacles, molluscs, tube worms, sponges and hydroids. 4 One of the best known effects of fouling is the increased frictional resistance to ship movement, leading to increased fuel consumption. With large ships, an increase in cost of about 0.5% (sterling £80 000 per year in 1972) would result from a loss of only 0.1 knots (0.19 km/h) on a service speed of 16knots (29.65 km/h). ~° One estimate puts worldwide costs to shipping concerns, due to marine fouling, at $1000 million per year." Fouling also leads to the need for frequent dry docking, and hampers inspection, repair and maintenance of marine platforms. Tenacious attachment by fouling organisms can cause paint damage, while some fouling organisms can accelerate localised corrosion. H A thick growth of fouling organisms on oil platforms can create engineering problems by increasing the loading forces on the platform caused by waves and currents, and leading to design specifications being exceeded. 7 Aesthetically, fouling is unsightly and can be a nuisance to shippers and engineers. One logical way of preventing fouling is to protect a structure with an anti-fouling coating. Copper compounds were for many years the toxic agents in anti-fouling compositions, while compounds of mercury, tin, lead or zinc were sometimes used as boosters in these preparations. 6 However, the contemporary anti-fouling systems of choice are those that are based on tri-organotin compounds. THE REASONS FOR P R E F E R E N T I A L USE OF TRIORGANOTIN-BASED SYSTEMS According to Smith & Smith 2 and Craig, 3 tri-organotin compounds are effectively biocidal to a wide range of fouling organisms at low concentrations. They constitute only a minimum toxid hazard during application, and their terminal breakdown products are apparently innocuous and pose no serious long-term environmental problems. 2:,12 After application, they degrade to the less toxic di-organotins. Furthermore, they may be converted into tetra-organotins which are volatile and should therefore not accumulate in the marine environment. ~3 The mechanism for such a conversion involving naturally occurring iodomethane has been demonstrated. 14 Also, low mammalian toxicity and the reversibility of the poisonous effects of tri-organotins have been reported. 15-17 With such a unique combination of seemingly ideal properties, it is little surprise that they enjoy preferential usage which leads to their introduction in large amounts into the marine environment.
288
E. O. Oyewo
IS T H E R E ANY NEED FOR CONCERN? In order to put this question in the proper perspective, it is necessary to examine the environmental behaviour, toxicity, toxicology and some specific effects of tri-organotins on some living organisms. To start with, the efficacy of tri-organotins as anti-fouling biocides logically implies that they are potent poisons. The argument that tri-organotins can break down into less toxic species or be converted into volatile and easily lost ones fails to take cognisance of the various inter-specific conversions that may occur in the environment. Besides, any of the organotin compounds can be picked up by a living organism and once ingested it may directly exercise some toxic effects, bio-magnified into toxic levels or in any case become incorporated into the food web. It is also necessary to recognise that the hazards posed by any chemical in the marine environment cannot be positively appreciated if its chemical properties are considered in isolation without reference to its established or potential interactions with biotic and abiotic components of the environment.
Speciation of tri-organotins It has been postulated that the degradation of tri-organotins in the environment starts with the absorption of UV light, or by biological or chemical means. 3 The decay then continues by tlhe stepwise loss of the organic groups. According to Poller, 18 the change from tri- to diorganotin involves the homolytic cleavage of the tin-carbon bond. The decay continues through to mono-organotin, and the final product may be the inorganic tin species. 3 Most of the evidence for speciation is from in-vitro studies. When decay studies are carried out under conditions that better simulate the environment, a greater stability for organotin species is suggested. 3 It also has to be pointed out that there are uncertainties in the terminal stages of the aforementioned scheme, and the end-product may not be inorganic tin. It has been reported, for example, that triphenyltin hydroxide in an aqueous environment degrades via photolysis to diphenyltin oxide accompanied by further degradation into a water-soluble, non-extractable polymeric species. 19
Some specific deleterious effects of tri-organotins Van der Kerk & Luitjen 5 established that growth is completely inhibited in some fungi by low concentrations (0-2-5 ppm) of triphenyltin chloride. Inhibition of carbon fixation by triphenyltin chloride has also been demonstrated in the diatom A c h n a n t h e s subsessilis. 2°
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It has also been shown that photosynthesis and respiration are inhibited in the algae Enteromorpha intestinalis and Ulothrix psendoflaca by triphenyltin chloride. 11 In the same paper, it was shown that photosynthesis is more sensitive to this biocide. Stuart 22 also reports that the 144-h ECso of bis(tributyltin) oxide (TBTO) for the copepod Acartia tonsa was 0-4 mg litre -1, a value which is close to that measured in San Diego bay. Ward et a1.,23 working with TBTO and a saltwater fish Cyprinodon variegatus, found the LCs0 to be 0-96 ppb (billion = 109). Even though the fish were metabolising the TBTO to the lower and less toxic alkyl moieties, a biocide that kills 50% of test animals at concentrations less than i ppb. should be regarded as hazardous in the environment. Further studies have associated shell deformations in Crassostrea gigas with the presence of TBTO and tributyltin fluoride (TBTF) in water. 24'25 As a result of this research, the French Government imposed a series of bans on anti-fouling preparations containing these compounds and prohibited their use on small boats. Perhaps the most disturbing aspect of some of these ill-effects is that organisms close to or at the centre of primary production are involved. Furthermore, it is known that methyl metals (which are more toxic than the inorganic forms) are more readily taken up by algae than other metal forms. 26 It is also interesting to note the indication that some organisms may develop resistance to tri-organotins. 12 Although this is not widespread at present, the implication of this finding is that if resistance becomes prevalent, larger quantities of the chemicals will be needed, or more potent ones will have to be developed.
Aikylation Since organometals are generally more toxic than their inorganic form, 3 alkylation is a relevant environmental issue. It has been shown that methylation can occur in sediments, and may be brought about by biotic as well as abiotic means. 27'37 An abiotic pathway for alkylation involving the redistribution of trimethyltin hydroxide has been demonstrated. Naturally occurring sulphides, iodomethane and alkylcobalamins can mediate alkylation, x3'14'28'29 It has also been reported 3° that these transformations can occur both within and without the bodies of organisms, while Kimmel et al. 31 have reported dealkylation mechanisms in relation to the mammalian metabolism of the miticide cyhexatin (tricyclohexyltin hydroxide). These possible interconversions suggests that environmentalists should be concerned about the presence of any organotin species in the environment. In this respect, even those triorganotins used in agriculture, ~5'32 as well as their breakdown products, may get into estuarine systems and should therefore be of concern.
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Toxicology of organotin compounds In general, the biological effects of tetra-organotins (ILSn) in mammals appears to be caused principally by the tri-organotin (R3Sn) compounds which are formed by their in-vivo and in-vitro conversions, especially in liver t i s s u e ) 6'17'33 This is probably why, compared to the tri-compound, there is a delay in the onset of poisoning. 34 As toxicological hazards therefore, tetra-organotins should be regarded as the equivalent trisubstituted compounds. From the toxicological viewpoint, tri-organotins are the most important organotin species; according to Craig 3 and Smith, ~7 the toxicity of organotin compounds is at a maximum when three organic groups are present (R3SnX). Maximum toxicity usually occurs for R = methylbutyl. Further increase in the length of the n-alkyl chain produces a sharp drop in toxicity. The mode of acute tri-organotin toxicity has been linked with their disruption of various mitochondrial functions through membrane damage, disruption of ionic transport and inhibition of ATP synthesis. 35 Triphenyltin iodide has powerful sternutatory effects. 16 The toxicology of di-organotins is different. The toxic action of the lower di-alkyltins is due to their ability to combine with enzymes containing two thiol groups in the correct formation. According to Smith, 17 the toxic effect of lower di-alkyltin compounds are similar to those of trivalent arsenicals in the inhibition of alpha-keto oxidases containing dithiol groups. The trend of decreasing toxicity with increase in length of the alkyl chain is also true for di-organotins.17 Mono-organotin compounds also show the trend of decreasing toxicity with increasing length of the alkyl chain but do not seen to have any important toxic action in mammals. The oral LDs0 for some mono-ethyltin compounds to the rat is between 70 and 700 mg/kg. ~6'17 Inorganic tin has very low mammalian toxicity. The acceptable level of tin in canned food is 250 times that of lead.~7 A R E THERE ANY A L T E R N A T I V E MEASURES? Currently, alternatives to chemical anti-fouling measures are receiving very little attention. The reason is probably because of the claims that tri-organotins, for example, are innocuous in the marine environment. Thus, it is necessary to examine a few alternatives, even if their application is futuristic. In the North Sea, a metal-protection system which depends on artificially cancelling out the natural ionic currents
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established between different structural members of submarine platforms appears to prevent the settling of fouling organisms. 7 There have also been speculations on the inhibitory effects of cathodic protection on marine growth by sacrificial anodism. The effect is, however, not yet very clear. 7 There is also the vexed question of biological control. In 1977, divers of the Chevron Oil Corporation successfully cleared paths on oil platforms through sea anemones thus allowing star fish access to climb and graze on fouling organisms. 7 This is a pointer to the possibility of biological control.
DISCUSSION From the ecological viewpoint only, a biological alternative is preferable even if impracticable in some circumstances. However, no matter what anti-fouling measures are contemplated, there is a need for more investigations into marine chemistry, organotin chemistry and the biology of fouling organisms. This need has in fact been stressed in the past. 6 The patterns of colonisation of fouling organisms, their zonation with depth, growth rate, succession pattern and even physiology must be well understood in attempting to rationally solve the problems of fouling. There should also be a careful balance between economic and environmental considerations. The former should not be at the expense of the latter. It is particularly noteworthy that the release of tri-organotins is more prevalent and more environmentally significant in harbours rather than the open sea. 3 Harbours are usually estuarine, and estuaries are complex ecosystems. Estuaries also have multiple uses which can be impaired by pollution. These uses are perhaps epitomised by the Lagos Harbour Complex in Nigeria. Apart from being a shipping lane, it is a nursery ground for some fish species and actually supports an artisanal fishery. It is an amenity for the Lagos Boat Club but also a recipient of domestic and industrial waste. Although tri-organotins and their breakdown products are generally less toxic than other organometallic equivalents, this should be seen in a relative context only. Low toxicity does not mean no toxicity, neither is low mammalian toxicity synonymous with low biological toxicity in general. A lot of data on organotin toxicity relates to mammals and this could be misleading; The LDs0 of vendex (bis(triphenyltin) oxide) to rats is 2630mg/kg. 15 The 96-h LDs0 of the same compound for blue-gill, fathead minnow and rainbow trout is 0.0048, 0.0019 and 0-0017 ppm respectively. It is also known that some other tri-organotin
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compounds with low mammalian toxicity are highly toxic to other forms of life. 4 It is also necessary to emphasise that, even where a chemical does not produce an acute effect, it may have insidious sub-lethal effects which may be important in the long run. Moreover, in the marine environment, living organisms are simultaneously exposed to a myriad of environmental stresses. Not only could the introduction of tri-organotins constitute an additional stress, it could, in combination with other factors, have a synergistic effect on or render some organisms susceptible to stresses to which they otherwise would not succumb. It has to be recognised that the marine environment is a very complex one in which nature maintains a delicate and dynamic equilibrium. The role that any particular biotic or abiotic species plays in this equilibrium is sometimes not well understood. Even where the environmental behaviour of a substance is predictable on the basis of its properties or similarity to a c o m p o u n d whose environmental behaviour is known, a surprise factor is often present in such considerations. 36 Against this background, the introduction of anything foreign, particularly chemicals, into the marine environment clearly needs to be done with caution and ideally with a sound understanding of both the shortand long-term effects of such introduction. ACKNOWLEDGEMENT A literature review carried out by the author as part of the MSc Pollution Control programme of the University of Leeds in 1984 formed the basis of this paper. The author is grateful to Dr L. V. Evans of the Plant Sciences D e p a r t m e n t for his helpful comments and suggestions. REFERENCES 1. Carlin, Jr, J. F., Mineral facts and problems. US Department of Interior, Burean of Mines Bulletin 671, 1980. 2. Smith, P. & Smith, L., Organotin compounds and applications. Chem. Brit., U (1975) 208-13. 3. Craig, P. J., Organometallic compounds in the environment. In Pollution: Causes, Effects and Control, ed. R. M. Harrison. Royal Society of Chem-, istry London, 1983, pp. 277-322. 4. Evans, C. J. & Smith, P. J., Organotin based anti-fouling systems. J. Oil Col. Chem. Assoc., 58 (1975) 160-8. 5. Van der Kerk, G. J. M. & Luitjen, J. G. A., Organotin compounds. III: The biocidal properties of organotin compounds. J. Appl. Chem., 4 (1954) 314-9. 6. Evans, L. V., Marine algae and fouling: A review with particular reference to ship fouling. Bot. Mar. xxxiv (1981) 177-83.
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7. Ralph, R. & Goodman, K., Foulplay beneath the waves: biology of North Sea platforms. New Scientist, 82 (1160) (1979) 1018-21. 8. Bishop, J. H., Silva, S. R. & Silva, V. M., A study of microfouling on anti-fouling coating using electron microscopy. J. Oil Col. Chem. Assoc., 57 (1974) 30-5. 9. Christie, A. O. & Shaw, M., Settlement experiments with zoospores of Enteromorpha intestinalis (L.) Link. Brit. Phycol. Bull., 3 (1968) 529-34. 10. Banfield, T. A., Antifouling compositions for large tankers. Pigment Resin Technol., 1(4) (1972) 33-7. 11. Terry, L. A. & Edyvean, R. G. J., Micro-algae and corrosion. Bot. Mar., xxiv (1981) 177-83. 12. Evans, C. J., Developments in the organotin industry. Part 1: Triorganotin chemicals. Tin and its Uses, (100) (1970) 3-6. 13. Guard, H. F., Cobet, A. B. & Coleman, W. M., Methylation of trimethyltin compounds by estuarine sediments. Science, 213 (4509) (1981) 770-1. 14. Craig, P. J. & Rapsomanikis, S. A new route to tris(dimethyltin sulphide) with tetramethyltin as co-product. J. Chem. Soc., Chem. Commun., (2) (1982) 114. 15. Evans, C. J., A new organotin miticide. Tin and its Uses, (110) (1976) 6-7. 16. Barnes, J. M. & Margos, L., The toxicology of organometallic compounds. Organomet. Chem. Rev., 3 (1968) 137-50. 17. Smith, P. J.~ Toxicological data on organotin compounds. In International Tin Research Council Publications, 1978 No. 538 pp. 3-10 and following Appendix D to p. 18. 18. Poller, R. C., Cleavage of tin-carbon bonds. In Organotin Chemistry Ed. R. C. Pollen. Logos Press, London, 1970, pp. 53-63. 19. Soderquist, C. J. & Crosby, D. G., Degradation of triphenyltin hydroxide in water. J. Agric. Food Chem., 28 (1982) 110-17. 20. Callow, M. E. & Evans, L. V., Some effects of triphenyltin chloride on Achnanthes subsessilis. Bot. Mar., xxiv (1981) 201-5. 21. Milner, P. A. & Evans, L. V., The effects of triphenyltin chloride on respiration and photosynthesis in the green algae: Enteromorpha intestinalis and Ulothrix Pseudoflacca. Plant, Cell Environ., 3 (1980) 339-48. 22. Stuart, C. U., Acute toxicity of bis(tributyltin) oxide to a marine copepod. Mar. Pollut. Bull., 14(8) (1983) 303-6. 23. Ward, G. S., Cramm, G. C., Parrish, P. R., Trachman, H. & Slesinger, A., Bioaccumulation and chronic toxicity of bis(tributyltin) oxide (TBTO): Tests with a saltwater fish. In Aquatic Toxicology and hazard assessment: Fourth Conference, ed. D. R. Branson & K. L. Dickson. American Society for Testing and Materials Special Publication No. 737, 1981, pp. 183-200. 24. Alzieu, et al., Influence des peintures anti-salissures dans les zones cochylicoles. Rev. Tray. Inst. Pech. Marit., 44 (1982) 301-49. 25. Waldock, M. J. & Thain, J. E., Shell thickening in Crassostrea gigas: Organotin anti-fouling or sediment induced. Mar. Pollut. Bull., 14(11) (1983) 411-5. 26. Laxen, D. P. H., The chemistry of metal pollution in water. In Pollution: Causes, Effects and Control, ed. R. M. Harrison. Royal Society of Chemistry, London, 1983.
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27. Hallas, L. E., Means, J. C. & Cooney, J. J., Methylation of tin by estuarine organisms. Science, 215(4539) (1982) 1505-7. 28. Thayer, J. S. & Brinckman, F. E., The biological methylation of metals and metalloids. In Advances in Organometallic Chemistry, Vol. 20, ed. F. S. A. Stone & R. West. Academic Press, New York, 1982, pp. 314-48. 29. Fanchiag, Y. T. & Wood, J. M., Alkylation of tin by alkylcobalamins. J. A. Chem. Soc., 103 (117) (1981) 5100-3. 30. Fish, R. H., Kimmel, E. C. & Casida, J. E., Bio-organotin Chemistry: Reactions of tributyltin derivatives with a cytochrome P-450 dependent mono-oxygenase enzyme system. J. Organomet. Chem., 118 (1976) 4-54. 31. Kimmel, E. C., Casida, J. E. & Fish, R. A., Bio-organotin Chemistry: Microsomal monooxygenase and mammalian metabolism of cyclohexyl compounds. J. Agric. Food Chem. 28 (1980) 117-22. 32. Evans, C. J., Plictran: A new organotin acaricide. Tin and its Uses, (86) (1970) 7-10. 33. Davies, A. G. & Smith, P. J., Recent advances in organotin chemistry. Adv. Inorg. Radiochem., 23 (1980) 1-77. 34. Cremer, J. E., The conversion of tetraethyltin into triethyltin in mammals. Biochem. J., 68 (1958) 685-92. 35. Stockdale, M., Dawson, A. P. & Selwyn, M. J., Effects of trialkyltin and triphenyltin compounds on mitochondrial respiration. Eur. J. Biochem., 15 (1970) 342-51. 36. Goldberg, E. D., Marine pollution. In Chemical Oceanography, Vol. 3, 2nd edn, ed. J. P. Riley & G. Skirrow. Academic Press, London, 1975, pp. 39-89. 37. Jewett, K. L., Brinckman, F. E. & Bellama, J. M., Chemical factors influencing metal alkylation in water. In Marine Chemistry in the Coastal Environment, ACS Symposium Series 18. American Chemical Society, Washington DC, 1975, pp. 304-18.