Toxins in the red Whelk

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Fig. 2 Summerchlorophyll--Firth of Clyde.

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those normally found in inshore waters. Although these levels indicate the effects of general nutrient enrichment in this area, they may not be deleterious and could be beneficial if the increased phytoplankton production is utilized by higher levels in the food chain. To test this, zooplankton feeding experiments were carried out in summer 1972. Filtering rates of the copepod Calanus on the particulate matter in water from different positions in the Clyde was measured using a particle counter. The results (Fig. 3) show that filtering rates in the coastal strip were about one quarter of those in the rest of the area. These experiments suggest that lower grazing rates may be an explanation of the higher chlorophylls but do not define the actual cause and for this more experimental work is needed. There are three main conclusions that can already be drawn from this study. (1) There is evidence of enhanced levels of contaminants in the Clyde. (2) This evidence is found most obviously at intermediate trophic levels (Tellina and zooplankton), rather than in the water or the fish. (3) Experiments show direct effects on organisms from this area which are comparable to effects found by contaminated additions to unpolluted waters, but the exact cause or causes remain to be determined. J. H. STEELE A. D. MCINTYRE R. JOHNSTON I. G. BAXTER G. TOPPING H. D. DOOLEY Marine Laboratory, Department o f Agriculture and Fisheries .for Scotland, Aberdeen, Scotland.

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Fig. 3 Zooplankton filtering rates (ml/animal/day) at inshore and offshore stations in Firth of Clyde.

Anonymous (1972). Baseline studies of pollutants in the marine environment and research recommendations. The IDOE Baseline Conference, May 24-26, 1972, New York. Barnett, P. R. O. (1971). Some changes in intertidal sand communities due to thermal pollution. Proc. R. Soc. Lond. B., 177: 353-364. Johnston, R., Adams, J. A. & Dooley, H. D. (1971). Some observations on the hydrography, chemistry and plankton of the Firth of Clyde in relation to nitrate-rich effluents. DAFS IR Report No. IR29-71. Marshall, S. M. & Orr, A. P. (1927). The relation of the plankton to some chemical and physical factors in the Clyde Sea area. J. mar. biol. Ass. UK, 14: 837-868. Preston, A. (1973). Heavy metals in British waters. Nature, 242: 5393, 95-97. Saward, D., Stirling, A. & Topping, G. (1972). Experimental studies with effects of copper on a marine food chain. 1CES/CM 1972/E:24. Stephen, A. C. (1929). Studies on the Scottish marine fauna: the fauna of the sandy and muddy areas of the tidal zone. Trans. roy. soc. Edin., 56: 291-306. Williams, R. & Holden, A. V. (1973). Organochlorine residues from plankton taken from Gourock in the Firth of Clyde to the International Ocean Weather Station India (59°00'N, 19°00'W). Mar. Poll. Bull., 4(7): 109-111.

Toxins in the Red Whelk A case of poisoning following consumption of Neptunea occurred in Scotland in 1970. The organism is caught in traps with the Edible Whelk where it constitutes less than 0 - 5 ~ of the catch. Toxin in the salivary gland demon-

strated by mouse bioassay could be distinguished from P S P toxin• It is concluded that the public health risk from consumption of the Edible Whelk is negligible. In contrast to other parts of the world, the seas of t57

north-west Europe harbour only a few naturally toxic marine molluscs. The acquired toxicity of filter-feeding molluscs as the result of their ingestion of toxic phytoplankton has been observed in many areas, including the North Sea (Wood, 1968). In the Pacific (Halstead, 1965), illnesses following the consumption of gastropods are well known, but to our knowledge there has been only one occasion when an incident has occurred in north European waters. In 1970, a case of poisoning was reported in Scotland following consumption of the gastropod Neptunea antiqua (Fleming, 1971); the object of this communication is to report certain of the toxicological and fishery aspects of this incident.

Poison in Whelks Neptunea antiqua is widely distributed in the waters of northern Europe, where it is often taken with catches of the edible whelk (Buccinum undatum) and more frequently in the by-catch of trawlers. N. antiqua is known by a variety of local names, including red or almond whelk, buckie or mutlog (Isle of Man), barnagh (Ireland), trompeten schnecke or Kinkhorn (Germany). In Britain, small numbers of Neptunea are eaten incidentally, because it forms part of the normal whelk catch and the meats are of similar appearance. It has been reported that fishermen in certain areas may select Neptunea for consumption in preference to the edible whelk Buccinum undatum; in the past a meal of red whelks was often taken in order to produce a deep and agreeable state of intoxication. Red whelks do not normally cause illness, probably because they form only a small proportion of the catch taken in whelk pots. Our observations made at one port on the east coast of England showed that the red whelk constituted less than 0.5~ of the catch, and it is concluded that the dose of red whelks taken in a meal of this composition does not contain sufficient toxin to cause even mild intoxication. In the incident reported in 1970 (Fleming, 1971), a young male consumed 6 large (13-15 cm long) red whelks (equivalent to about 100 g of flesh), and suffered from blurred vision, muscular twitching, tingling of hands and feet, weakness, paralysis and collapse, but recovered after 24 hours. In Japan, incidents of toxicity have been associated with N. arthritica (Asano, 1952) and N. intersculpta ( K a n n a & Hirai, 1956); the toxic principle was shown to be tetramine (tetramethyl ammonium hydroxide), present in the salivary glands (Asano, 1952; Asano & Ito, 1959, 1960). In Norway, F/inge and his co-workers (F/inge, 1957; Emmelin & F~inge, 1958) established the presence of the toxin in the salivary glands of N. antiqua and demonstrated the toxic effect of salivary gland extract on mice. Following the 1970 incident, we determined the quantity of toxin in red whelks taken with commercial whelk catches from the English east coast. Dilutions of aqueous (1:1) extracts of the salivary gland, and of the whole animal, both before and after boiling for 15 min (as used commercially for cooking whelks), were injected intraperitoneally into mice weighing 18-22 g. Similar tests were carried out with extracts prepared from tissues of the edible whelk. Raw and cooked extracts 158

of the salivary glands and of the whole edible whelk produced no observable response in the mice after injection. Extracts of the raw salivary gland of the red whelk containing the equivalent of 0.15 ml of the tissue killed mice in 7 and 7¼ min; an extract containing the equivalent of 0.25 ml of cooked salivary gland killed a mouse in 10~ min. In contrast to the PSP (Paralytic Shellfish Poisoning) toxin (Wood, 1968; McFarren, 1959) identified in mussels in north-east Britain in 1968, mice receiving whelk extract did not exhibit sudden neurotoxic movements prior to death, but remained inactive until they died. Death was characterized by swelling and bluish coloration of the mouth and nasal region. The tests suggested that about 30~ of the toxin was removed or destroyed by the cooking process. The 1970 incident occurred during the summer months when investigations were being made to determine the distribution of PSP toxins in molluscs from the north-east coast. It was considered at that time that the illness following consumption of Neptunea might be due to the gastropods feeding on filter-feeding molluscs which had accumulated PSP toxin. Such a route of accumulation has been demonstrated experimentally (Ingham, Mason & Wood, 1968), and illness resulting from the consumption of edible whelks which had acquired PSP toxin has been reported in Canada (Caddy & Chandler, 1968). The 1970 incident differs in one important respect from similar cases reported from Japan (Asano & Ito, 1959), in that paralysis has not been recorded as a symptom in the Japanese work. Corm (personal communication, 1970) reported low levels of PSP toxin in mussels taken from the Forth during the summer of 1970 (267 to 471 units/100 g of tissue) and it is possible that the case of Neptunea poisoning recorded from this area was due to PSP toxin, or to Neptunea toxin or to a combination of both. However, Neptunea taken from the Firth of Forth in October, outside the season when PSP toxin was expected, showed only the salivary gland to be toxic. It has been suggested that salivary gland toxin plays an important role in the capture of molluscs as food by Neptunea and there is evidence that it can affect a wide range of invertebrates taken as food (Pearce & Thorson, 1967). We found that the salivary glands of Neptunea antiqua constituted about 8~ of the wet weight of the flesh of the animal, but only about 1~ of Buccinum. Whittaker (1960) reported the production of an acetylcholine-like compound (identified as senecicylcholine) by Buccinum, but it is possible that our bioassay technique was not sensitive enough to detect this substance in the small glands.

Public Health Risk Whilst it is clear that the consumption of commercially caught whelks carries no inherent public health risk, there is evident danger when a substantial meal of selected red whelks is eaten. This is not likely to occur with any frequency, since the organisms are sublittoral and are usually taken with the edible whelk by professional fishermen. However, the activities of skin divers could lead to an increase in this type of incident, particularly as the attractive shape and colour of the

shells, together with their large size, might encourage collection. P. A. AYRES P. C. WOOD Ministry o f Agriculture, Fisheries and Food, Fisheries Laboratory, Burnham-on-Crouch, Essex CMO 8 H A , UK. Asano, M. (1952). Bull. ,lap. Soc. Sci. Fish., 17(8-9): 73-77. Asano, M. & Ito, M. (1959). Tohoku. J. Agri. Res., 10(2): 209-227.

Asano, M. & Ito, M. (1960). Ann. N Y Acad. Sci., 90(3): 674-688. Caddy, J. F. & Chandler, R. A. (1968). Proc. natn. Shellfish Assoc., 58: 46-50. Emmelin, N. & F~inge, H. (1958). Acta. zool., Stockh., 39: 47-52. F/inge, R. (1957). Nature, Lond., 180: 196-197. Fleming, C. (1971). Br. Med. J. (Brit.), 3: 250-251. Halstead, B. W. (1965). In: Poisonous and venomous marine animals, Vol. 1. US Gov. Printing Office, Washington DC. Ingham, H. R., Mason, J. & Wood, P. C. (1968). Nature, Lond., 220: 25-27. Karma, U. & Hirai, M. Lecture at Annual Meeting Japan. Soc. Fish. Tokyo (unpublished 1956). McFarren, E. F. (1959). J. Ass. off. agric. Chem., 42: 263-271. Pearce, J. B. & Thorson, G. (1967). Ophelia, 4: 277-314. Whittaker, V. P. (1960). Ann. N Y Aead. Sci., 90(3): 695-705. Wood, P. C. (1968). Nature, Lond., 220: 21.

Effect of Chelation on Toxicity of Copper Metals in the sea may form complexes with organic compounds, a process known as chelation, and this may modify their properties very greatly. Here the effect of chelation on the toxicity of copper to algae has been studied in the laboratory using the powerful chelating agent EDTA. Similar phenomena in the sea have implications both for anti-fouling paints, which usually contain copper, and for metal pollution in waters with a high organic content. Habitat-linked copper tolerance has been demonstrated in populations of the brown alga Ectocarpus siliculosus (Dillw.) Lyngb. (Russell & Morris, 1970; 1972), highly tolerant plants often being associated with copper-treated ships' hulls. However, a sample of Ectocarpus taken from a population occupying a muddy dock retaining wall exhibited a surprisingly low tolerance to copper, despite continual contact with fouled and painted vessels which might be expected to be a continuous source of highly tolerant material (Russell & Morris, 1972). Several workers (e.g. Erickson, Lackie & Maloney, 1970; Nielsen & Wium-Andersen, 1970) have shown that the effective toxicity of copper to some unicellular algae is considerably reduced in the presence of chelating agents. As chelation is likely to be an important factor operating in a muddy dock environment and in polluted habitats in general, its effect on the toxicity of copper to Ectocarpus siliculosus has been assessed.

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i M a t e r i a l and M e t h o d s A slightly copper-tolerant strain of E. siliculosus was selected as the test material. This strain had been isolated from a collection taken from the hull of a cargo vessel in April 1970 and maintained in culture at Liverpool. The basic growth medium was made as inorganic as possible by the exclusion of Na2 E D T A from Von Stosch's (1964) formulation. A second medium consisted of the basic formulation plus 3.7 mg E D T A per litre, and the third test medium employed was 'Erd Schreiber' medium (F~yn, 1934) which contains soil extract. A series of copper concentrations was prepared in each medium, these giving 0.00, 0.01, 0.03, 0.05, 0.10,

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Fig, 1 Effect of chelation on the toxicity of copper to E. siliculosus. (a) Mean growth of plants over a range of copper concentrations in three medium formulations. (b) Mean indices of tolerance calculated over a range of copper concentrations in three media. Media: e~--basic medium; A--basic medium÷EDTA; I1--Erd-Schreiber medium. 159