Possible effects of organotins on scallop recruitment

Marine Pollution Bulletin Marine Pollution Bulletin. Volume 18, Number 11, pp. 604-608, 1987,

~x~25-326x/87S3.00"~H~O O 1987 PergamonJournalsLtd.

Printed in GreatBritain.

Possible Effects of Organotins on Scallop Recruitment DAN MINCHIN*, COLM B. DUGGAN* and WILLIAM KINGt *Fisheries Research Centre, Department of the Marine, Abbotstown, Dublin 15, Ireland t State Laboratory, Department of Finance, Abbotstown, Dublin 15, Ireland

The adult populations of the scallop (Pecten maximus) and of flame shells (Lima hians) have declined in the North Water of Mulroy Bay on the north coast of Ireland. Settlements of these and some other bivalve species either failed or were reduced. These events relate well to the first introduction and subsequent increased use of organotin net-dips on salmonid farms in this Bay. The last use of these net-dips was during the spring of 1985. In 1986 there was a good settlement of scallops, and settlements of other bivalves were recorded except for flame shells. Levels of TBT in adult scallop tissue in the North Water are high, 0.7 lag g-t wet wt; levels determined in other species were much lower. Pacific oyster (Crassostrea gigas) shell thickening was used to monitor the presence of organotins in a number of areas including Muiroy Bay. In Kilkieran Bay, an area having a scallop fishery, this was greatest at the innermost station, suggesting higher levels there. Shell thickening and organotins in Pacific oysters were also measured in Cork Harbour.

There is evidence of organotin contamination in areas where scallop populations exist about the Irish coast. One population, in Mulroy Bay, has been studied prior to, during and after the extensive use of organotins, in particular, b/s-(tri-n-butyltin)-oxide (TBTO), used in net-dips for salmonid cage netting (Minchin & Duggan, 1986). Since 1979 a production system for the ongrowing of scallops was developed, based on intense settlements from the years 1979 to 1982 (Minchin, 1983). Some of these scallops were exported to France and Spain for experimental ongrowing. Since 1983 various bivalves have had either reduced settlements or settlement failures in the North Water of Mulroy Bay. The use of tributyltin compounds (TBT) in net-dips was discontinued in the Bay in the spring of 1985 and since that time there have been signs of recovery. This paper outlines events in Mulroy Bay with particular reference to the Pectinacea, and includes observations in areas adjacent to other scallop populations. Methods

Scallops and flame shells were sampled by diving, except in Cork Harbour where scallops were dredged 604

Deployment and examination of monitor collectors for procuring scallops are outlined by Minchin (1983). Scallops were aged by counting the rings laid down on both valves. Bivalve larvae were collected from 20 m vertical tows using a 90 gm mesh net. Pacific oysters were either ongrown suspended from the surface in lantern nets or in bags on trestles, and those exposed to low levels of organotins developed thickened shells (Alzieu et al., 1982). A shell index of length/thickness was calculated for these oysters from selected sites about the Irish coast (Fig. 1). TBT residues in mollusc tissues were determined using an atomic absorption procedure based on M & T Chemicals Ltd. Standard Test Methods briefly outlined in Waldock & Miller (1983). Observations

Mulroy Bay Bivalves which settled out on scallop collectors were recorded for each of the years 1979 to 1986, and these demonstrate great variation of settlement intensity (Table 1). The species most sensitive to organotins appear to be among the Pectinacea, three of which, Lima hians, Chlamys varia and Pecten maximus, are found in Mulroy Bay. Lima hians The flame shell is distributed in varying abundance throughout the North Water and Broad Water of Mulroy Bay, from low water spring tide to depths of about 20 m, in areas free of silt and mud. In the Moross Channel Lima were abundant, their byssal threads TABLE 1 Relative extent of bivalve settlements in Mulroy Bay. Year 1979 1980 1981 1982 1983 1984 1985 1986

Pecten > 1000 209 151 37 0 0 0 c.200

Musculus

Lima

Cardium

Hiatella

++ ++ ++ ++ + 0 + ++

++ ++ ++ +++ 0 0 0 0

++ ++ ++ + 0 0 0 ++

++ ++ ++ + 0 0 0 ++

Settlement of scallops as recorded on .settlement panels; the mean number per panel per array of panels is shown for the area of greatest concentration: 0 -- no settlement + -- poor settlement + + -- moderate settlement + + + - - intense settlement

Volume 18/Number ll/November 1987

forming an interwoven carpet in shallow water covering large areas of sediment. This community has been observed each year by diving, and data were collected during 1980 (Hobson, 1981), 1985, and 1986. In 1982 there was an intense settlement of Lima, which fouled spat collectors and equipment used for ongrowing bivalves. Since 1982 no Lima spat were found on scallop collectors (Table 2). In 1983 early umbonate larvae were observed, but no late umbonate or eyed stages were seen. No Lima larvae were seen in plankton tow samples after 1983. There has been a noticeable decline of the population of Lima in the Moross Channel. This was estimated in 1986 to be less than 2% of its 1980 level (Table 3). By 1985 this resulted in a great reduction of the expanse of the byssal carpet on the sea floor, with areas of exposed and unstable sand burying some of this carpet to depths of 18 cm. Sand ripples of up to 60 cm amplitude were noticed in areas previously level and carpeted by Lima. In 1980, the kelps, Laminaria and Saccorhiza, were attached to the carpet. In 1985 drifts of kelp of up to 10 mX 3 m were found in sheltered hollows in the Channel, having torn away from remaining patches of carpet. Seastars (Marthasterias, Asterias, and Solaster) fed on Lima exposed in the uprooted undersides of the carpet. In 1986 there were smaller drifts of kelp, but larger expanses of unstable sand.

TABLE 2 Observations on larvae and settlement of Lima hians in Mulroy Bay. Year

Abundance of Lima larvae

Observations of settlement on collectors

1979 1980

present 7 July- 14 August, common

1981 1982

4 July- 18 August, common 9 July-18 August, common

1983

July, only early umbonate none seen

Settlement recorded Moderate settlement, 7-13 mm in September Settlement recorded Intense settlement, 2-8 mm in October No settlement No settlement No settlement No settlement

1984 1985 1986

none seen

no plankton study

TABLE 3 Relative abundance of Lima recorded per 100 man-minutes diving.

Age

1980

1985

1986

0

1520 920 440 20 0 0 145 c.5 2900 100%

0 3 30 141 6 2 190 105 182 6.3%

0 0 5 22 13 5 55 120 45 1.6%

1 2 43 5 samplesize

dive duration(min.) sample per 100 min.

relativeabundance

Chlamys varia This species of scallop is not naturally abundant in ,u.._.~.-,~,, -,,, the Bay. It is normally associated with kelp holdfasts, stones and boulders, from low water to about 10 m 6~ depth; and has only been found in small numbers on _ ~ - ~ ¢ collectors during 1979 to 1982.

BAY

°i

IRELAND

BALLINAKILL B A Y ~ ARDBEAR BAY BERTRABOUY BAY~ KILKIERAN B A Y

GALWAY

~.a..

~

DUBLIN

K" NEW HARBOUR

MUCKINISH LOUGH

DINGLE

CORK

HARBOUR TERHAVEN CASTLETOWNBERE ~ Fig. 1 Distribution of study localities around the Irish coast.

605

Marine Pollution Bulletin

Pecten maximus

Apart from reduced settlements in 1981 and 1982, the first indication of possible environmental deterioration was noticed during July 1983. No scallop larvae were observed after mid-July, at which time 'D' veligers of many bivalve species were abundant. However, there were few eyed larvae (Minchin, internal report) and these were identified as the bean mussel, Musculus marmoratus. Only one scallop spat settled on collectors in the North Water in 1983, although there was some settlement in the Broadwater. In 1984 and 1985 settlements also failed in the North Water, yet again small numbers settled on marine algae and aquaculture structures in the northern part of the Broadwater. In 1986 however, over 1500 scallop spat were taken per commercial collector bag. This was comparable to the numbers collected before the use of organotins commenced. Spat survival to date has been good. The population of scallops declined from an estimated 554 000 in 1980, 222 000 in 1984 to 171 000 in 1985, a decline to 28% of the 1980 population (Table 4). The 1983 year class was represented by one individual in the 1984 sampling (by diving); none of the 1983 or 1984 year classes were present in 1985. These results agree well with collectors used for monitoring settlement (Table 1). Frozen samples of scallop tissue were sent (1984) to MAFF, Fisheries Laboratory, Burnham-on-Crouch, for organotin analysis. Levels of TBT (expressed as TBTO) ranged from 1.60 to 2.08 p.g g-~ wet wt of tissue of scallops ongrown in cages in the North Water from 1982 to 1984. More recently (1986) levels of 0.75 p.g g-i have been found in scallops in the North Water (Table 5). Ongrown scallops sampled in the autunm 1986 from an area in the Broadwater, which is well ventilated with sea water from outside the Lough, had levels of 0.25 p.g g-~ TBT. These scallops had an estimated mortality of 10% over the winter of 1985-86.

TABLE 4 Estimated numbers of scallops in the North Water, Mulroy Bay. Age

1980

1984

1985

Year Class

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

40* 3 19 38 75 126 69 64 29 40 18 13 2 2

< 1 7 24 21 12" 1 24 35 31 31 17 12 4 1 < 1 -

4 26 18 4* 1 16 20 26 21 12 7 3 1 < 1 < 1

1984 1983 1982 1981 1980 1979 1978 1977 1976 1975 1974 1973 1972 1971 1970 1969 1968

554

222

171

Populationsize estimates Xl000

These figures are based on diver sampling. *Indicates the year class of the intense 1979 settlement. The poor 1978 year class for all years gives some confidence to the aging technique. TABLE 5

Concentrations of tributyltin (expressed as TBTO ttg g-~ wet wt) in molluscan tissue. Year

Crassostrea gigas

1986

North Water (1)

Mytii'us eduli's' Limahians

1986 1985 1985

Moross S. Broadwater (6) NorthWater (1)

Pecten maximus

1985

Deegagh Point (cultivated) (3) North Water

. . . .

5).

1986

Crassostrea gigas . . . .

. . . .

. . . .

. . . .

. . . . . . .

. . . . . . .

. . . . . . .

. . . . . . .

,,

Shell distortion in Crassostrea gigas Hatchery reared Crassostrea gigas of 23.8 m m + 4.5

S.D., from a TBT free area, were ongrown at Mulroy Bay in 1985 (Fig. 2). Shell distortion was noticeable after 70 days and most shells had a pit at the point of adductor insertion and a transparent gel between the shell lamellae of the fiat valve. Levels of TBT in tissues from four stations are shown in Table 6. Shell distortion was also noticed in ongrown oysters in 1986, and TBT was found in this and other species at this time (Table

Mulmy Bay Locality

Species

Mytilus edulis ....

Ostrea edulis

Tissue TBTO 0.3 0.1 0.15 0.2 0.25 0.75

Other localities Clew Bay 1986 Ardbear Lough

1986

1986 1985 1986 1985 1986 1986 1985 1986 1986 1986 1986 1986 1985

1985

0.15 0.2 .... (Salt Lake) < 0.1 Ardfry, Galway Bay 0.2 .... (oyster pond) ND Baltimore 0.3 Lough Hyne ND Oysterhaven ND Drakes Pool, Cork Harbour (1) 0.35 ,, (1) 0.7 aoste;ian, Cork Harbour (2) 0.1 . . . . (S. side) (3) < 0.1 N. Channel, C o r k H a r b o u r (N. side) (4) < 0.1 New Harbour, Galway Bay ND Inner Harbour, Bantry Bay ND Tralee Bay ND

Limit of detection 0.05 p.g g-t. ND = not detected in sample. For Irish localities see Fig. 1 and for Cork Harbour station numbers see Fig. 3. TABLE 6

Shell distortion and TBT levels in Pacific oyster tissue, Mulroy Bay, 1985.

Other Localities There are indications of organotin contamination in some other inlets about the Irish coast, where scallops also exist (Fig. 1, Tables 5, 7). This evidence is based on the analysis of organotins in tissue and shell distortion in Pacific oysters. Oysters from Cork Harbour (Fig. 3) were found to have high levels (0.7 Ixg g-I TBT) near Crosshaven (Owenboy Estuary), a major yachting centre. Lower levels were found in oysters at other sites

606

Station

Shell index

Mean size

TBT (as TBTO o.gg-~)

1. 2. 3. 4. 5. 6.

North Water N. Broadwater

Deegagh Point Cranford Bay Carlan Bay S. Broadwater

7.2 :t: 1.9 7.0 + 1.4 7.7 + 1.5 7.7:1:1.5 5.9 :t: 1.5 6.0± 1.4

Station numbers are shown in Fig. 2.

42.7 :i: 7.1 41.8 ± 7.8 44.5 + 7.6 40.9-t- 7.7 42.7 + 6.8 37.4± 6.1

0.2 0.35 0.45 1.3

Volume 18/Number l 1/November 1987 within the Harbour

(< 0.1-0.1

~tg g-~). T h e r e w a s a

five f i s h - f a r m s , a n d h e r e P a c i f i c o y s t e r s h e l l d i s t o r t i o n

in

w a s f o u n d t o b e g r e a t e s t at t h e i n n e r m o s t p a r t o f t h e

1 9 8 0 . T h e p o p u l a t i o n a g e c l a s s s t r u c t u r e at t h a t t i m e

B a y (Fig. 4). F i s h - f a r m s in t h i s B a y d i s c o n t i n u e d t h e u s e

(Fig. 3) s h o w s f e w i n d i v i d u a l s l e s s t h a n 7 y e a r s o f a g e

of organotin net-dips during 1985.

small fishery for scallops, within Cork

(1974+

year

classes).

In

1986

this

Harbour,

area

was

re-

CORK

examined and only a single two year old scallop was

HARBOUR

captured. I n K i l k i e r a n B a y t h e r e is a s c a l l o p f i s h e r y , a n d a l s o

NORTH WATER

MOROSS CHANNEL

BROADWATER

•

~=

•

MULROY

N 1

=

km

Fig. 2 Mulroy Bay. Stars indicate position of fish farms. Ongrowing of Pacific oysters took place at stations I-6.

Fig. 3 Cork Harbour. Distribution of the scallop population in April 1980. Inset shows the age distribution of landed scallops at this time. Pacific oyster growing stations are numbered. Open squares are sites where ongrown oysters were not recovered.

TABLE 7 Shell distortion and TBT levels in Pacific oysters at Irish localities. Locality

1 2 3 4 5

1 2 3 4 5 6

Killybegs Harbour Richies Bay, near Killybegs Bellacragher, North of Clew Bay Clew Bay, yacht moorings Clew Bay BaUinakiU Bay Ardbear Bay Bertraghbouy Bay Kilkieran Bay, Upper Camus .... Gurraig Sound .... Ardmore .... Lettercallow Coonawilleen Ardfry Pond, Galway Bay New Harbour . . . . . Muckinish Lough Dingle Castletownbere Oysterhaven Cork Harbour, Drakes Pool .... Rostellan S. North Channel .... N. North Channel ,, Oyster Pond .... Brick Island

Shell index

S.D.

4.7 4.8 14.0 7.6 12.1 3.9 6.9 12.5 7.2 10.1 11.5 11.2 13.5 19.6 9.6 18.4 18.2 5.9 18.9 5.2 14.1 12.9 10.0 13.9 12.5

1.0 0.5 5.2 0.9 3.1 1.4 1.2 4.4 0.8 3.3 3.3 2.6 1.8 6.6 2.2 3.8 4.8 1.2 5.0 1.3 5.7 4.5 2.3 7.6 4.6

TBT (as-'TBTO ttg g- ~) 0.15 0.2 ND 0.7 0.1 < 0.1 < 0.1 -

=

Source FB SC Y SC SC, Y SC Y FB Y -

Oysters were ongrown at each locality from April 1986 and were examined at the end of the growing season (October 1986). Oysters examined at Lough Hyne demonstrated normal shell growth. Likely sources of TBT: Fishing Boats (FB), Salmon Cages (SC), Yachts (Y). N D - TBT not detected in sample. Station numbers for Kilkieran Bay and Cork Harbour appear in Figs 3, 4. 607

Marine Pollution Bulletin

Fig. 4 Kilkieran Bay. Distribution of scallops (hatched), fish farms (stars) and Pacific oyster ongrowing stations (numbered). One fish farm close to station 4 is known not to have used organotin net-dips.

Discussion TBT was found in molluscan tissues at various localities about the Irish coast. The levels varied within bays, being greatest near known sources. Pacific oysters provided an inexpensive means of identifying the presence of organotins, using the flat shell length/thickness index. C. gigas ongrown in Mulroy Bay during 1980 however, did not show any indication of shell thickening, whereas those grown during 1985 and 1986 did. Organotins are thought to have been first introduced in small amounts as a net-dip on fish-farms in 1981. This usage increased until the end of 1984. However, by the summer of 1985 no further treated nets were being used, on the advice of the Fisheries Research Centre. The re-appearance of scallop settlements, and those of most other species, in the North Water of Mulroy Bay in 1986, may well reflect the discontinuation of the use of organotin net-dips. In Archachon Bay (Alzieu et aL, 1986), following a ban on organotin antifouling paints in 1982, there has been a continued decline of organotin levels; a similar trend may be expected in Mulroy Bay. In spite of the discontinued use of TBT, in net-dips, in Mulroy Bay since the spring of 1985, relatively high levels of TBT (0.75 ~tg g-l) were found in adult scallop tissues within the North Water, and (0.25 p.g g-l) in the Broadwater. Davies et aL (1986) have shown that scallops, in one experiment, retain approximately 80% of the accumulated TBT, even after a removal of ten weeks from a source. A gradual build up of TBT in the adductor tissue takes place, being transferred from other organs. The high levels of 1.60 to 2.08 ~g g-t found in Mulroy Bay in 1984 are comparable with the levels of 1.86 Ixg g-i found by Davies et aL (1986) in scallops after sixteen weeks exposure to organotin paints. 608

It is not clear whether the levels found in scallops are a result of a continued bioaccumulation or residual from years of former contamination when higher levels were probably present in the water. TBT levels ranging from 0.002 to 0.006 p.g 1-1 (concentration expressed as tin) were found in October 1986 in water samples from the North Water and Broad Water of the Bay. This represents levels in terms of TBTO of 0.005-0.015 Ixg 1-1. In Cork Harbour there has been little or no scallop recruitment since 1974; it is possible that this may be due to the presence of TBT. Organotin antifouling paints were thought to have been first available at about the time of this poor recruitment. However, turbidity arising out of industrial development of the perimeter of the Harbour may also have influenced settlement. In the innermost part of Kilkieran Bay the degree of shell thickening in Pacific oysters was found to be similar to those from Mulroy Bay in 1985. There is however little information on scallop settlement from this region in Kilkieran Bay. Elsewhere levels of TBT in Pacific oysters were lower than those for scallops; Pacific oysters have an ability to purge or detoxify almost 90% of the accumulated levels (Davies et aL, 1986). Levels in mussels and flame shells are comparatively low, and some mussel settlement has occurred in every year of study in Mulroy Bay since 1978, whereas flame shells have failed to settle since 1983. Unless settlements of flame shells take place over the next few years the resident population may be endangered. It would appear that pectinids, and particularly flame shells, are more susceptible to the presence of organotins than other bivalves but it is not known whether the reproductive process and larval development are affected. A bye-law banning the use of organotin antifouling compounds on boats and other aquatic structures has been in force since 9 April 1987 in the Republic of Ireland. We would like to thank Dr M. J. Waldock of the Fisheries Laboratory, MAFF in Burnham-on-Crouch and Dr. G. Topping of the Marine Laboratory, DAFS in Aberdeen for determining levels of TBT in tissues and sea water respectively. TBT levels in tissues were also determined at the State Laboratory in Dublin with the assistance of P. Bonnet, B. McDonald and D. O'Gara. We acknowledge the assistance of the Fisheries Research Centre diving unit for sampling scallops. Alzieu, CI., Heral, M., ThJbaud, Y., Dardignac, K. J. & Feuillet, M. (1982). Influence des peintures antisalissures a base dbrganostanniques sur la calcification de la coquille de l'huitre. R ~ Trav. Inst. Peches Marit. 45,101-106. Alzieu, CI., Sanjuan, J., Deltreil, J. P. & Bovel, M. (1986). Tin contamination in Archachon Bay: effects on oyster shell abnormalities. Mar. Pollut. Bull. 17,494-498. Davies, I. M., McKie, J. C. & Paul, J. D. (1986). Accumulation of tin and tributyltin from anti-fouling paint by cultivated scallops (Pecten maximus) and Pacific oysters (Crassostrea gigas) Aquaculture 55, 103-114. Hobson, D. (1981). On the biology of Lima hians in Mulroy Bay. B.A. Moderatorship Thesis, University of Dublin. Minchin, D. (1983). Pecten maximus in Mulroy Bay. Part 2. 4th International pectihid workshop 10-13 May 1983, Aberdeen, Scotland. Minchin, D. & Duggan, C. B. (1986). Organotin contamination in Irish waters. ICES CM 1986/F:48. Waldock, M. J. & Miller, D. (1983). The determination of total and tributyl tin in sea water and oysters in areas of high pleasure craft activity. ICES CM 1983/E:12.