Ecological implications of heavy metal in fish from the Severn estuary

Ecological implications of heavy metal in fish from the Severn estuary

Abdullah, M. I., Royle, L. G. & Morris, A. W. (1972). Heavy metal concentrations in coastal waters. Nature, 235: 158-160. Black, W. A. P. & Mitchell, ...

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Abdullah, M. I., Royle, L. G. & Morris, A. W. (1972). Heavy metal concentrations in coastal waters. Nature, 235: 158-160. Black, W. A. P. & Mitchell, R. L. (1952). Trace elements in the common brown algae and in seawater. J. Mar. BioL Assoc. UK, 30: 575-583. Bryan, G. W. (1969). The absorption of zinc and other metals by the brown seaweed Laminaria digitata. J. Mar. BioL Assoc. UK, 49: 225-243. Butterworth, J., Lester, P. & Nickless, G. (1972). Distribution of heavy metals in the Severn Estuary. Mar. Poll. Bull., 3: 72-74. Fuge, R. & James, K. H. (1973). Trace metal concentrations in brown seaweeds, Cardigan Bay, Wales. Mar. Chem. (in press). Gutknecht, J. (1965). Uptake and retention of cesium 137 and zinc 65 by seaweeds. LimnoL Oceanogr., 10: 58--66. Nickless, G., Stenner, R. & Terrille, N. (1972). Distribution of cadmium, lead and zinc in the Bristol Channel. Mar. Poll. Bull., 3: 188-190. R. FUGE Preston, A., Jefferies, D. F., Dutton, J. W. R., Harvey, B. R. & K. H. JAMES Steele, A. K. (1972). British Isles coastal waters: the concentrations of selected heavy metals in seawater, suspended matter and biological indicators--a pilot survey. Environ. Poll., 3: 69-82. Young, E. G. & Langille, W. M. (1958). The occurrence of inorganic elements in marine algae of the Atlantic Provinces of Canada. Can. J. Bot., 36." 301-310.

are mcreaslng. For these data to be useful m individual and in compounded studies, every effort should be made to ensure a known, high level of quality. Trace element concentrations in seaweeds are subject to several sources of variation; consequently, publication of such data should contain sample sizes, mean values, a measure of variance (e.g., standard deviation), date of collection and methods of sample handling. We have tried to follow these requirements in presenting our data which are available in raw form upon request.

Department of Geology, University College o f Wales, Aberystwyth, Cards., Wales

Ecological Implications of Heavy Metal in Fish from the Severn Estuary Tissues and organs of the flounder collected from the Severn at Oldbury, in the course of a year long survey, have been analysed for lead, cadmium and zinc. Differences have been noted in the level of zinc deposition in the various age groups of this teleost, particularly in autumn and summer. In an attempt to explain these results, the feeding habits of the flounder have been studied and heavy metal analyses conducted on some of its principal foodstuffs and related animals. Recent reports (Butterworth et al., 1972; Nickless et aL, 1972; Peden et aL, 1973) have recorded relatively high levels of lead, cadmium and zinc in the tissues of several vertebrate and invertebrate species from the Bristol Channel and Severn estuary. Furthermore, the concentrations of these elements in the waters of this area have been shown to be much higher than in the open sea (Abdullah et al., 1972; Preston et al., 1972). In attempting to assess the ecological significance of the heavy metal burden in the tissues of certain key estuarine species, analyses of lead, cadmium and zinc have been made on fish collected from the intake screens of the Oldbury Nuclear Power Station, located in the middle reaches of the Severn estuary. Species have been selected which differ in their migratory patterns, feeding habits and life span in the hope that it might be possible to relate heavy metal levels to these and other aspects of their biology. In view of the significant part that the shrimp (Crangon vulgaris) plays in the food chain of many estuarine teleosts, similar determinations have been made on this species, collected from both Oldbury and Milford Haven.

Materials and Methods The majority of the species used in this study were obtained in the course of regular sampling from the intake screens of the nuclear power station at Oldburyon-Severn, where the cooling water is drawn from a tidal reservoir built out over the intertidal flats immediately in front of the station. In the course of the survey, over 1,250 flounders

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(Platiehthyes flesus) were examined in collections made during October, 1972 and in February and June, 1973. In addition to recording the lengths and weights of individual fish, gut analyses were made on representative specimens of various size groups. The approximate age composition of selected length classes was ascertained by otolith examination combined with analysis of length-frequency distributions. In addition to the flounder, heavy metal determinations were also made on the sand t o b y (Pomatoschistus minutus) and the sea snail (Liparis liparis) both of which occurred in considerable numbers in the power station samples. A limited number of gut analyses were also carried out on the latter species. Specimens of the anadromous river lamprey (Lampetra fluviatilis) were obtained in the course of their autumn and winter spawning migration through the Severn estuary, and samples of the nonmigratory and nonparasitic brook lamprey (Lampetra planeri) came from the river Honddu in Breconshire and the river Chew in Somerset. Animal tissues and organs were dried at 105°C to constant weight (normally 24 h). Samples (approximately I g) were weighed accurately and digested in a mixture of hot perchloric acid (6 ml) and nitric acid (2"5 ml), both of Aristar grade, until a clear colourless solution was obtained (20 min at 100°C). The cold solution was then diluted to 25 ml with deionized water and analyzed directly using an Hilger-Watt Atomspek atomic absorption spectrophotometer. In each case, two blank determinations were conducted. Standard readings were obtained by treating an aliquot of a solution containing known concentrations of metals in exactly the same manner as for the organic material. After acid treatment, the solution was made up to 25 ml with deionized water and analysed directly. Results were checked against analyses of the so-called 'standard kale', for which concensus readings were obtained (Bowen, 1967). In addition, some duplicate analyses were conducted at the laboratory of the Government Chemist, London; again, there was good correlation with ourresults.

TABLE 1 Lead, cadmium and zinc levels in the tissues of whole flounders (Platichthyesflesus) of different length and age classes. Length (cm) and age classes 7-9 14-17 18 20 27-29

(0÷)** (1+) (2+,3+) (3+,4+) (5+)

Oct. 72

Lead Feb. 73

13.94-1.1 23.24.2.3 18.7±1.3 15.7±1.4 22.44-1.1

16.5±1-3 27.44.1.1 25.1±0.9 27.44-1.1

*Mean concentrations (ppm) dry tissue ± S.D. Cadmium June 73 Oct. 72 Feb. 73 June 73 Oct. 72 19.7±1 '3 22-94.1.3 21.6±1.6 24-54.1.0 29.2±1.1

3.94.0.5 4.24.0.8 4.0±0-5 3.9±0.7 5.2±1.0

5.2±0-5 5.4±0.2 4.84-0.3 7-3i0'7

3.4±0.4 4.24-0.4 4.1±0.4 4-2±0.4 5.1±0.8

143.84-2.8 110.14-1.5 102.2±1.6 91.44-1.8 76.34-1-3

Zinc Feb. 73

June 73

139.44-0.8 144.94.1.3 132.8±0.6 175.64-1.3

173-15:1.4 156.34.1.4 124.7± 1.0 124-84-2.5 147.54-1.0

* Results based on twenty analyses for each group. ** Not represented in the February sample.

Results F o r comparative purposes, heavy metal concentrations have been expressed (Tables 1 and 2) as p p m dry weight based on digests of whole animals, but these concentrations may vary widely in different tissues. Thus, detailed analyses of different tissues or organs in the flounder have shown that lead muscle levels rarely exceed 20~o of the values recorded for liver, heart or kidney tissue (approximately 20-30 ppm) and the highest concentrations were observed in the brain (38-5-43-6 ppm). For cadmium, muscle values were again relatively low, varying from 2-11% of those observed in the liver or kidney (21.2-27.5 ppm). Maximum zinc concentrations occurred in kidney tissue (300-420 ppm) and these levels were about four times as high as in liver, heart or brain and five times greater than the muscle concentrations. In general, the highest zinc concentrations were those observed in the flounder, and, unlike the lead or cadmium levels, the concentrations of this element showed distinct seasonal and age variation (Table 1). Thus, both in autumn and summer samples, the highest zinc levels were recorded for the smallest flounders assigned to the 0 + year class and, in the remaining groups, there was a consistent decrease in zinc levels with increasing age and length. On the other hand, in the February samples (where the 0 + age class was not represented), the zinc values were higher than in autumn or summer and remained relatively constant over all length and age groups, apart from a higher value in the largest specimens. It is perhaps significant that the same length class in the June sample shows a similar departure from the otherwise downward trend of zinc levels with increasing length and age.

Neither the lead nor cadmium concentrations show a consistent decrease with increasing length or age and, indeed in the majority of cases, the largest flounders tend to exhibit the maximum levels of both elements. Furthermore, while the cadmium levels in the Oldbury fish are similar to those reported for flounders from Hinckley Point in the Bristol Channel (when recalculated in terms of dry weight), the zinc analyses from the latter area are much lower. As in the Ythan estuary (Healey, 1971), the goby is an autumn and winter resident at Oldbury, weekly samples showing a more or less consistent increase in numbers from July onwards, reaching a peak in midwinter and declining again in the early spring. In this species, lead and cadmium levels are of the same order as those of the flounder, but the zinc concentrations are distinctly lower and comparable only with those of the largest flounders in the sample of October, 1972 (Table 2). The most significant feature of the heavy metal determinations carried out on the sea snail (Table 2) are in the cadmium levels, which are from four to five times higher than those observed in the sand goby and three to four times as high as in the flounder. On the other hand, lead levels were similar to those of the latter species, but rather higher than in the goby. Zinc figures are of the same order as m a n y of the flounder samples and show a tendency to be somewhat reduced in the larger specimens. In the case of all three elements, the concentrations recorded for the Severn river lamprey are very much below those of the three teleost species, but it is note-

TABLE 2 Levels of lead, cadmium and zinc in some estuarine and freshwater species. Species Sand goby (Pomatoschistus minutus)* Sea snail (Liparis liparis)* 2-4 cm 5-9 cm River lamprey (Lampetra fluviatilis )* * Brook lamprey (Lampetra planeri)** Adults Ammocoetes Ammocoetes Shrimp (Crangon vulgaris)*

Location

No. of analyses

Mean concentrations (ppm) dry weight i S.D. Lead Cadmium Zinc

Oldbury-on-Severn

20

17.6±0.9

Oldbury-on-Severn Oldbury-on-Severn Oldbury-on-Severn

10 10 6

29.94-1.2 25.84-1"6 6.0±0'7

River Honddu River Honddu River Chew Oldbury-on-Severn Milford Haven

10 20 10 10 10

12"0+1 '13 8 "84.1 "08 8.64-1-0 34"04.1 "0 55-6±1 "6

3"24.0.5

75.6±2.0

13.74-0.5 16"84-0.9 0"54-0.3

107'9i1"5 86"54-3"2 47"1±1.0

0"75±0'3 0.23 4.0.2 1-25±0"3 124.84.1"5 4.94-0.6

117'0±3"3 93.6 4-3 "6 199"34-1-0 125"94.1"1 101"04-1.0

* Collected during the period July 1972-February 1973. ** Collected during the period November 1972-April 1973. 13

seems unlikely that the goby could be a significant factor in the heavy metal burden of the flounder, but the shrimp and other crustaceans may well be important factors. The contrast between the cadmium concentration of the sea snail and the goby is of special interest, suggesting that in spite of the apparent ecological parallels there may be basic differences in the diet of the two species. Gut analyses of the Oldbury sea snails indicate that the shrimp is an important element of the food of at least the larger animals. Thus, of 50 individuals examined, 45~o of the guts contained mainly shrimps, while in 16~ of cases they were the sole component. No gut analyses have been carried out on the Severn gobies, but detailed studies on this species in the Ythan estuary (Healey, 1971) have shown that the amphipod, Corophium volutator is the major constituent of the diet Discussion and that unlike the Severn sea snail, the shrimp is much Without a much more detailed study of the biology less important. In this connection therefore, the of the flounder population of the Severn estuary, it is exceptionally high cadmium concentrations of the difficult to advance more than a tentative explanation Oldbury shrimps is highly significant. The anadromous river lamprey, Larnpetra fluviatilis, of the observed seasonal and age variations in zinc concentrations. As can be judged from the power after a freshwater larval stage of about four and a half station samples, the relative abundance of the Oldbury years, undergoes metamorphosis from the ammocoete flounders has followed a broadly biphasic pattern, with and enters the estuary when about five years. For a maximum numbers in summer falling to minimum levels further period of about one and a half years, the adult in October (Hardisty & Huggins, unpublished observa- lamprey feeds parasitically on the blood and muscle tions). A second peak was reached at the beginning of tissues of teleost host species (Hardisty & Potter, 1971), January, 1973. These changes may well reflect seasonal probably within the area of the Bristol Channel, before movements in and out of the Oldbury region of the re-entering the estuary on its spawning migration. It estuary which could differentially affect the older animals. might therefore be anticipated that the heavy metal Since there is evidence that ingested zinc may be excreted figures for this species would reflect the levels prevalent by both marine vertebrates and invertebrates (Skidmore, in the muscle and body fluids of host fishes within its 1964; Bryan, 1968), the varying patterns of zinc feeding area. In fact, figures for all three elements are accumulation might well reflect the varying periods lower than for any other of the vertebrates studied; a which flounders of different age groups have spent within circumstance that may partly be related to the comparatively low levels of heavy metals in the muscle areas of higher or lower zinc concentrations. The general tendency for zinc levels to decrease with tissue and blood on which these animals feed. The figures for brook lampreys are particularly age and length which was observed in the October and June samples is probably based on metabolic factors. interesting in view of the fact that this species is entirely The absence of this trend in the February sample and confined to freshwater and feeds only during the larval the uniformly higher values observed at this time, could stage when the principal component of its diet is diatoms be attributable, either to a change of diet, to differences (Hardisty & Huggins, 1970). Thus, zinc values for in feeding intensity, or to movements into the area from ammocoetes of this species from the river Honddu in other regions. Gut analyses indicate that the diet of the Breconshire are more than twice as high as in the Severn youngest flounders appears to be relatively constant river lamprey, and specimens from the river Chew throughout the year, consisting primarily of polychaetes, (arising in the Mendip Hills) had concentrations more but there is considerable seasonal variation in the food than four times higher than those of the anadromous intake of larger fish. Thus, in October, 1972 the gut form (Table 2). These observations emphasize the need contents of flounders of the 1 ~ age class or above for caution when interpreting heavy metal concentrations showed the remains of gammarids, shrimps and gobies, without adequate information on background levels. Clearly, at this stage, it is impossible to comment on but in early spring the shrimp was the dominant food organism, despite the fact that shrimps are said to be the possible biological effects of heavy metal concentraless numerous in the estuary at this time of the year tions of the order of those observed in these estuarine (Lloyd & Yonge, 1947). Furthermore, it has been fish species. The view has been expressed that in the observed that the major food organism of the larger area of the Bristol Channel, the deterioration in the flounders in June, 1973 was the crustacean, Macome variety of fish species has been greater than in any other baltica, at a time when the shrimp was very abundant in region of the British coasts (Clark, 1971), although a the Oldbury area. In fact, very few individuals revealed more optimistic interpretation has been made on the the remains of shrimps in their gut contents during basis of comparisons of growth in river lampreys from this area (Hardisty & Huggins, 1973). Furthermore, this period. Bearing in mind that the goby population consists of although no quantitative assessments are possible, only two age classes, the rate of accumulation of lead comparisons of our fish samples from Oldbury intake or cadmium appears to be of a similar order to that of screens with the faunal lists compiled by Lloyd (1940) flounders of comparable age, although zinc concentra- for the same region, provide no evidence of deterioration tions were considerably lower. For these reasons, it in species variety over the last 30 years; and it is evident worthy that the zinc values for both the larval and adult stages of the purely freshwater species, Lampetra planeri, are in general as high as those observed in some of the flounder samples from the estuary of the Severn. Cadmium concentrations are again very low, but the lead values tend to be somewhat higher than in the adult of the river lamprey. Relatively high zinc levels were found in shrimps from both Milford Haven and Oldbury, and lead concentrations from both sites were generally rather higher than in Severn teleosts. The most significant feature of these analyses, however, is the high cadmium levels observed in the Oldbury shrimp samples.

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Abdullah, M. I., Royale, L. G. & Morris, A. W. (1972). Nature, 235: 158. Bowen, H. J. M. (1967). Analyst, 92: 124. Bryan, G. W. (1968). J. mar. BioL Ass. UK, 48: 303. Butterworth, J., Lester, P. & Nickless, G. (1972). Mar. Poll. Bull., 3(5): 72. Clark, R. B. (1971). Mar. Poll. Bull., 2: 153. The authors wish to express their gratitude to the CEGB for Hardisty, M. W. & Huggins, R. J. (1970). J. ZooL, Lond., 161: 549. their co-operation in making this study possible, to many local Hardisty, M. W. & Huggins, R. J. (1973). Nature. fishermen, and to Dr Raymond Ward of the Government Chemist Hardisty, M. W. & Potter, I. C. (1971). The General Biology of Laboratory, London for undertaking to duplicate some of our Adult Lampreys. In: The Biology of the Lamprey, Vol. 1, analyses. Academic Press. Healey, M. C. (1971). J. ZooL, Lond., 163: 177. M. W. HARDISTY Lloyd, A. J. (1940). Proc. Bristol Nat. Soc., 9: 202. R. J. HUGGINS Lloyd, A. J. & Yonge, C. M. (1947). J. mar. Biol. Ass, UK, 26: 626. S. KARTAR Nickless, G., Stenner, R. & Terrille, N. (1972). Mar. Poll. Bull., 3(12): 188. M, SAINSBtm¥ Peden, J. P., Crothers, J. H., Waterfall, C. E. & Beasley, J. (1973). Mar. Poll. Bull., 4(1): 7. University o f Bath, Preston, A., Jefferies, D. F., Dutton, J. R. W., Harvey, B. R. & Claverton Down, Steele, A. K. (1972). Environ. Pollution, 3: 69. Bath, B A 2 7.4 Y, U K Skidmore, J. F. (1964). Quart. Rev. BioL, 39: 227. that the Severn estuary still remains a satisfactory nursery ground for the juvenile stages of a number of marine teleosts as well as providing a migratory route for anadromous species.

Land-Derived Pollutant Hydrocarbons Evidence is given for the derivation of oH pollution from on-shore sources and for a possible relation between its concentration in estuurine sediment and in the Hpids of the sediment biomass. Microbial degradation of oil has been shown to take place in seawater and marine sediments if nutrients are present and readily available carbon sources absent. Floodgate (1972) has also pointed out that rates of degradation depend upon the chemical components of the oil, and that undigested oil residues m a y persist in the environment. Amongst the alkane components of oil, it is the normal alkanes which are preferentially degraded (Johnston, 1970; Blumer & Sass, 1972) and gas-liquid chromatographic analysis of the residual alkanes shows a chromatographic trace consisting of an envelope of unresolved peaks. This envelope represents overlapping homologous series of branched and cyclic alkanes containing between 15 and 35 carbon atoms. The observation of alkane patterns of this type during analysis of marine sediment would suggest derivation from oil spillage at sea, but Farrington & Quinn (1973) describe the same patterns for alkanes from sediments and clams of Narragansett Bay, which are unlikely to be derived from oil spills, but which, they adduce, must derive from land drainage and sewage effluent. After finding a similar alkane pattern in sediment from the estuary of the River Blyth (Northumberland, UK), we have also found it in non-tidal upstream sediments (Fig. 1) and also in the treated sewage sludge of a sewage works, the effluent from which flows into the river. Above the effluent input point, the pattern was much less pronounced. The amounts of alkane present and alkane-free lipid are given in Table 1. Lipid is taken as that part of a methanol-dichloromethane extract which is soluble in petroleum ether.

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Fig. 1 Gas chromatograms of alkanes from sediments A (top graph), and E (middle), and sewage sludge, S (bottom). 5% OV-1 on Varaport 30 in a~"× 10' stainless steel column, programmed 70-300°C at 4°C/rain. 15