Environmental Pollution 106 (1999) 183±192

www.elsevier.com/locate/envpol

The recovery of populations of dogwhelks su€ering from imposex in

the Firth of Forth 1987±1997/98
K.L. Miller, T.F. Fernandes*, P.A. Read
Department of Biological Sciences, Napier University, 10 Colinton Road, Edinburgh EH10 5DT, Scotland, UK

Received 10 December 1998; accepted 9 March 1999

Abstract
The impact of tributyltin (TBT) contamination on dogwhelk (Nucella lapillus) populations was assessed at 33 sites in the Firth of
Forth, UK, during spring 1997 and summer 1998. The sex ratio of the animals; the ratio of juveniles to adults; the degree of
imposex, as determined by the relative penis size index (RPSI); and the total tin concentration in a sample of dogwhelk tissue were
used as measurements of TBT impact on dogwhelk populations. These data were compared with data from a similar survey carried
out at the same sites in the Firth of Forth in 1987 (Bailey, S.K., Davies, I.M., 1988. Tributyltin contamination in the Firth of Forth
(1975±1987). Science of the Total Environment 76, 185±192.) before restrictions were introduced on the use of TBT. The results
demonstrate a general recovery in dogwhelk populations from the impact of TBT at the majority of the sites studied, although at six
of the sites, the RPSI value remains high enough to suggest breeding problems in the population. It is suggested that large vessels
are responsible for localised cases of imposex within the Firth of Forth. # 1999 Elsevier Science Ltd. All rights reserved.
Keywords: Dogwhelk; Imposex; Firth of Forth; Population recovery; Tributyltin

1. Introduction time and rate of dispersion of TBT in the water column,

Tributyltin (TBT) has been described as one of the
most toxic compounds ever deliberately introduced into
the aquatic environment (e.g. Bailey et al., 1995). Dur-
ing the 1970s and the early 1980s, TBT was the principal
active biocide in antifouling paints which were applied
to the hulls of boats (de Mora and Pelletier, 1997). Due
to the `self-polishing' nature of the paint, it easily lea-
ched into the water column contaminating water, sedi-
ments and biota in areas of high boat use (e.g. Dowson
et al., 1993). More recent lines of research have sug-
gested additional sources of TBT to the aquatic envir-
onment. Bailey et al. (1995) and Evans et al. (1996) have
suggested that activities associated with the operation
of oil terminals are sources of TBT contamination. In
addition, Fent and Muller (1991) and Bailey et al.
(1997) have detected TBT in sewage and wastewaters.
Dowson et al. (1992) and Minchin et al. (1996) have
proposed that water movements a€ect the retention
* Corresponding author. Tel.: +44-131-455-2526; fax: +44-131-
455-2291.
E-mail address: t.fernandes@napier.ac.uk (T.F. Fernandes)
0269-7491/99/$ - see front matter # 1999 Elsevier Science Ltd. All rights reserved.
PII: S0269-7491(99)00076-7
whilst the biological, chemical and physical properties
of the sediment to which TBT adsorbs in¯uences the
resuspension and redeposition of this compound.
The dogwhelk, Nucella lapillus, has been shown to
be particularly sensitive to TBT, even at very low con-
centrations in the water (below 1.25 ng TBT lÿ1, Bryan
et al., 1986). This has resulted in the use of the dog-
whelk as a reliable bioindicator of TBT pollution. The
availability of a reliable bioindicator is of particular
importance since the water concentrations of TBT are
frequently below chemical detection limits (Bryan et al.,
1988). TBT induces a condition known as imposex in
certain molluscs, namely Nucella lapillus, whereby male
reproductive characters are superimposed on females'
genitalia (Oehlmann et al., 1991). Imposex in the dog-
whelk has been measured using the relative penis size
index (RPSI) which describes the mean bulk of the penis
in females as a percentage of the mean bulk of the penis
in males from the same population (Gibbs et al., 1987).
Several hypotheses have been proposed as to how
TBT bioaccumulation alters the normal hormonal bal-
ance of Nucella lapillus (Matthiessen and Gibbs, 1998).
FeÂrall and LeGall (1983) suggested that TBT acts on the
184 K.L. Miller et al. / Environmental Pollution 106 (1999) 183±192
neurohormones which control sexual di€erentiation in
molluscs. Ronis and Mason (1996) suggested that TBT
causes imposex by blocking the sulphur conjugation,
and hence excretion, of testosterone and its metabolites.
This hypothesis is supported by the work of OberdoÈr-
ster et al (1998) who suggested that TBT targets the
steroid metabolism pathway in molluscs. Finally, Spoo-
ner et al. (1991) suggested that TBT inhibits the cyto-
chrome P-450 dependent aromatase responsible for the
conversion of testosterone to estradiol-17b, causing a
signi®cant increase in testosterone accumulation which
results in the masculinisation of females. There is a
considerable weight of evidence in favour of this
hypothesis, but it has not been proved unequivocally.
Numerous studies have shown that the severity of
imposex can generally be related to the concentration of
TBT in the water column (e.g. Gibbs et al., 1988). In
brief, it has been observed that when the TBT con-
centration is less than 1.25 ng TBT lÿ1, the RPSI is less
than 5%. At this level the subsequent e€ect on the
reproductive system is penis development in females
with no apparent e€ect on breeding. At TBT con-
centrations of 2.5±5 ng TBT lÿ1, the RPSI tends to be
greater than 40% and many females become sterilised
due to scaling of the vagina and the overgrowth of a vas
deferens which blocks the vagina. Since these females
are unable to reproduce, the dogwhelk populations in
a€ected areas are likely to decline in numbers (Gibbs et
al., 1988; Hawkins et al., 1994). More recently, Evans et
al. (1995) proposed that a dogwhelk population can be
considered to be relatively healthy if the RPSI value
is less than 25% because at this level, there is little
impairment of breeding in the population.
Following the discovery of the acute toxic e€ects of
TBT-based antifouling paints in France, the UK Gov-
ernment introduced a series of measures to reduce the
environmental impact of TBT in UK coastal waters
(Douglas et al., 1993). The main outcomes of these
measures have been: the prohibited use of TBT paints
on boats less than 25 m in length (1987), the establish-
ment of an Environmental Quality Target (EQT) of 2
ng TBT lÿ1 in sea water (1988) and the categorisation of
TBT by the Department of the Environment as a List II
substance (1991). More recently, Minchin and Minchin
(1997) have suggested that the prohibited use of TBT
paints should be extended to include boats less than 50
m in length and the International Maritime Organisa-
tion (IMO) have suggested further restrictions to vessels
greater than 50 m in length.
In response to these regulations, numerous surveys
have been undertaken to assess their e€ectiveness (e.g.
Spence et al., 1987; Evans et al., 1991, 1994, 1995, 1996;
Dowson et al., 1993; Scott et al., 1994; MPMMG,
1998). These studies have shown con¯icting evidence as
to the extent of the recovery of dogwhelk populations,
implying that the current policies for antifouling may
not have been e€ective in reducing the input of TBT to
UK coastal waters and thus suggesting that further
restrictions may be required (Ten Hallers-Tjabbes,
1997).
The aim of the research described here was to assess
the current status of dogwhelk populations in the Firth
of Forth and to compare the results with those obtained
by Bailey and Davies (1988) in order to determine whe-
ther or not the health of the sampled populations are
improving 10 years after the use of TBT was restricted
by the UK government.
2. Materials and methods
Thirty-three rocky shore sites which had been studied
by Bailey and Davies in 1987 were re-examined in 1997±
1998. These sites in the Firth of Forth are limited to
areas east of South Queensferry because further
upstream, salinity is reduced and there is a lack of rocky
substrate, making conditions unsuitable for the occur-
rence of dogwhelks (Bailey and Davies, 1988). The
locations of the surveyed sites are shown in Fig. 1 and
the corresponding site numbers and grid references are
listed in Table 1.
Sampling was carried out in March and April 1997
and July and August 1998. Sampling of the dogwhelk
populations took place during low tide at the highest
shore level within the barnacle zone at which dogwhelks
were observed. The area was searched for 15 min
simultaneously by two samplers, paying attention to
rock faces, crevices and pools. All accessible dogwhelks
in sight were collected and the presence or absence of
egg capsules at each site was recorded.
The length of each dogwhelk was measured using
callipers, and the animal was classi®ed as an adult or
juvenile according to the presence or absence of teeth
(Feare, 1970). The relative proportions of adults and
juveniles (as a percentage of the total sample) were used
as an indication of the breeding success of the popula-
tions. Although the number of dogwhelks at each site
was recorded (Table 1), abundance could not be used as
a parameter to determine the status of dogwhelk popu-
lations since abiotic and biotic factors such as the degree
of exposure and the availability of food resources
determine the abundance of dogwhelks at a site (e.g.
Spence et al., 1990).
Sub-samples of 30 adult dogwhelks from each site
were retained for the determination of sex ratios and
RPSI values, whilst the remainder of the dogwhelk
sample was randomly distributed within the sampled
area of the shore. Following the methodology employed
by Bailey and Davies (1988), the sub-sample of dog-
whelks was immersed in nearly boiling water in order to
kill the animals quickly (Evans et al, 1991). The dog-
whelks were remeasured and then removed from their
 K.L. Miller et al. / Environmental Pollution 106 (1999) 183±192
Fig. 1. Firth of Forth showing the location of the survey sites and an indication of the degree of imposex at each of the sites [relative penis size index
(RPSI)<5%; 5%<RPSI<25%; RPSI>25%].
shells using a vice. Females were identi®ed from the
presence of a sperm-ingesting gland (Gibbs et al., 1987).
The penis (if present) was measured using a graticule in
the eyepiece of a binocular microscope. The sex ratios
were used as an estimate of the health of the popula-
tions. The RPSI values were determined and calculated
according to the methods of Gibbs et al. (1987) and
used to estimate the degree of imposex within the
populations, according to the following formula:
RPSI ˆ ‰Mean length of female penis3 =
1†
Mean length of male penis3 Š  100
The tissue concentration of total tin in six dogwhelks
from each site was measured by graphite furnace atomic
absorption spectroscopy (GFAAS) at the Fisheries
Research Services Marine Laboratory (FRSML) in
Aberdeen, following the protocol detailed in Harding et
al. (1998). The method has a precision of 13% and a
lower detection limit of 30 ppb in solution (Grewar,
personal communication). This provided an estimate of
background concentrations of total tin and permitted
further comparison with the data from 1987 (Bailey and
Davies, 1988).
3. Results
Juveniles (untoothed individuals) dominated the
population at the majority of the sites (Table 1 and Figs.
185
2 and 3). Similar proportions of adults and juveniles
were recorded at Barnsness, Dirleton, Earlsferry, Pans-
goat, West of Anstruther, Caiplie, Crail Harbour and
Fifeness (Table 1 and Figs. 2 and 3). Adult-dominated
populations were recorded at North Queensferry, Bil-
lowness and Anstruther Harbour (Table 1 and Figs. 2
and 3).
Table 1 shows that the sex ratios (males: females)
were generally male biased in all the samples ( p < 0:01,
Chi-squared test), ranging from 1.14 at Skateraw, Dun-
bar and North Queensferry to nine males:females at
Gosford. However, female-biased sex ratios occurred at
three sitesÐDirleton (0.87), Anstruther Harbour (0.87)
and Crail Harbour (0.67) ( p<0.01, Chi-squared test).
All the populations sampled had a very high propor-
tion of females showing imposex (71.4±100%), with over
half of the sites studied yielding samples in which all the
females showed penis development (Table 1). However,
populations were relatively healthy (RPSI values less
than 25%) at most of the sites with the exception of six
sites which had RPSI values greater than 25%ÐDunbar
(39.0%), South Queensferry (38.0%), North Queen-
sferry (51.1%), Aberdour (31.7%), Pettycur (28.6%) and
Buckhaven (35.0%) (Table 1, Fig. 1). It should be noted
that the full sub-sample of adults was not collected at
Prestonpans, Sea®eld Mine and West Wemyss (Table 1).
However, Gibbs et al. (1987) have stated that repro-
ducible RPSI results can be obtained with samples of 10±
40 dogwhelks.
There are no signi®cant correlations between any of
the variables recorded at each site. In other words, a
 186
Table 1
Results of the surveys showing information concerning site details, relative proportions of adults and juveniles in a known sample size, occurrence of egg capsules, sex ratio, percentage of females
showing imposex in 1997±98 and the relative penis size index (RPSI) value of a sub-sample of adults in 1987 and 1997±98 and the total tin concentration in tissue samples from 1987 and 1997±98
(mg tin/kg wet wt)

Site No. Site Grid Abundance Relative proportions Egg Sex %Imposexed RPSI (%) RPSI (%) Tissue total Tissue total
reference of sample (%) capsules ratio (M:F) females in 1987 in 1997±98 tin concentration tin concentration
in 1987 in 1997±98
(mg/kg wet wt) (mg/kg wet wt)
Adults Juveniles
(toothed) (untoothed)

1 Skateraw NT750750 559 27.37 72.63 No 1.14 71.43 4.4 2.6 ± 0.0007
2 Barnsness NT725774 582 54.81 45.19 No 2.75 87.5 2.9 4.6 <0.02 0.0031
3 Dunbar NT682794 446 40.36 59.64 No 1.14 100 19.2 39.0 0.06 0.001

K.L. Miller et al. / Environmental Pollution 106 (1999) 183±192

4 Seacli€ NT609846 386 14.77 85.23 Yes 2.33 88.89 10 1.0 0.02 0.0035
5 North Berwick NT555855 313 25.24 74.76 Yes 2.33 77.78 21.1 3.7 0.03 0.0023
6 Dirleton NT515862 607 52.22 47.78 Yes 0.875 81.25 15.9 1.8 ± 0.0026
7 Gullane NT473833 382 27.75 72.75 No 2.33 100 15.1 16.4 0.03 0.0011
8 Kilspindie NT456805 327 39.76 60.24 Yes 1.5 100 17 13.6 0.07 0.0003
9 Gosford NT440776 404 14.36 85.64 Yes 9 100 22.8 3.1 0.02 0.0016
10 Long Craigs NT413763 448 9.37 90.63 Yes 2.75 87.5 31.2 11.4 0.05 0.0021
11 Cockenzie (Inner) NT405759 348 24.43 75.57 Yes 3.29 100 11 18.7 0.26 0.0012
12 Cockenzie (Outer) NT401757 545 20 80 Yes 1.73 100 39.1 16.7 0.06 0.0022
13 Prestonpansa NT387747 183 11.48 88.52 Yes 1.63 100 21.7 4.2 0.02 0.0018
14 Joppa NT320736 337 11.57 88.43 No 2.75 87.5 16.5 4.1 0.03 0.001
15 South Queensferry NT137787 145 33.1 66.9 Yes 2.33 100 34.8 38.0 0.11 0.0042
16 North Queensferry NT135803 316 67.09 32.91 No 1.14 100 32.5 51.1 0.05 0.004
17 Aberdour NT194850 489 34.36 65.64 No 1.73 100 31.7 31.7 0.06 0.001
18 Burntisland NT239858 754 11.01 88.99 Yes 1.31 100 18.3 11.4 0.06 0.0007
19 Pettycur NT265861 660 11.36 88.64 Yes 1.5 100 36.5 28.6 0.05 0.0017
20 Sea®eld Mineb NT279895 90 21.11 78.89 Yes 1.375 75 12.7 11.5 0.06 0.0007
21 West Wemyssb NT327946 377 5.04 94.96 No 2.8 80 11.1 17.2 0.04 0.0008
22 Buckhaven NT356976 674 4.75 95.25 Yes 2.33 100 8.2 35.0 0.04 0.0016
23 Largo Bay NO412024 526 8.17 91.83 Yes 2 80 14.4 11.0 0.07 0.0027
24 Earlsferry NT483995 748 48.93 51.07 Yes 1.73 100 14.9 4.1 0.03 0.0015
25 Pansgoat NO539022 344 38.66 61.34 No 2 80 35.4 13.5 0.03 0.0045
26 Pittenweem NO549024 598 34.62 65.38 No 1.5 100 54.8 21.4 0.09 0.0006
27 Billowness NO564028 589 67.74 32.26 No 3.29 100 33.7 14.2 0.05 0.0008
28 West of Anstruther NO566033 728 50.96 49.04 Yes 1.73 90.91 33.7 11.3 0.08 0.00014
29 Anstruther Harbour NO573034 645 64.03 35.97 Yes 0.87 100 27.7 6.8 0.05 0.0009
30 Caiplie NO591052 784 44.13 55.87 No 1.73 90.91 14.1 21.1 0.05 0
31 Crail Harbour NO612073 695 55.25 44.75 No 0.67 94.44 64.1 12.6 0.18 0.0022
32 Roome Rocks NO622078 896 30.26 69.75 No 1.31 100 17.4 8.4 0.05 0
33 Fifeness NO636094 794 53.9 46.1 Yes 1.31 84.62 8.3 2.0 0.02 0.0007
a
Only 23 adults in sub-sample.
b
Only 19 adults in sub-sample.
 K.L. Miller et al. / Environmental Pollution 106 (1999) 183±192
Fig. 2. Relative proportions of adults (toothed) and juveniles (untoothed) at sites 1±15 on the south coast of the Firth of Forth.
high RPSI value in 1997±98 does not imply a large
proportion of adults, an absence of egg capsules, a high
sex ratio and a high percentage of imposexed females or
vice versa. Bailey and Davies (1988) showed that there
was a correlation between RPSI value and total tin
concentration in the Firth of Forth in 1987. However,
there is no correlation between RPSI value and total tin
in this study, probably due to the wide range of RPSI
values which can be found at various concentrations of
total tin in dogwhelk tissue (Bailey and Davies, 1988).
Comparison of the 1997±98 data with those obtained
in 1987 (Bailey and Davies, 1988) indicates that there
has been a signi®cant general decrease in RPSI values
( p<0.05, Wilcoxon's test for matched pairs) (Table 1,
Fig. 4). This general decrease in RPSI value is supported
by the fact that there has also been a signi®cant general
decrease in the total tin concentration of body tissue
over the 10-year period ( p<0.05, Wilcoxon's test for
matched pairs) (Table 1). At several sites, namely
Skateraw, Barnsness, Gullane, Kilspindie, Cockenzie
187
(inner), Burntisland, Sea®eld Mine, West Wemyss and
Largo Bay, the RPSI value has remained at a similar
low level to that of 1987 (Table 1, Fig. 4). An increase in
RPSI value was recorded at Caiplie (Table 1, Fig. 4).
Dunbar, North Queensferry and Buckhaven showed an
increase in RPSI value over the ten year period (Table 1,
Fig. 4). South Queensferry and Aberdour remained at a
high RPSI value similar to that of 1987, whilst at Pet-
tycur there was a decrease in RPSI value from 36.5 to
28.6% (Table 1, Fig. 4).
4. Discussion
4.1. Current status of dogwhelk populations in the Firth
of Forth
In general, dogwhelk populations in the Firth of
Forth appear to be breeding successfully since the
majority of the populations are juvenile dominated
188 K.L. Miller et al. / Environmental Pollution 106 (1999) 183±192

Fig. 3. Relative proportions of adults (toothed) and juveniles (untoothed) at sites 16±33 on the north coast of the Firth of Forth.

which indicates recent successful breeding. However, at
three sites the populations were dominated by adults,
suggesting that breeding may be impaired in localised
areas. The results concerning the breeding success of the
dogwhelk populations should be treated with caution
since the available food resource in¯uences the number
of juveniles produced in a season (Spence et al., 1987).
In addition, seasonality may in¯uence the proportion of
adults and juveniles. In spring, adults tend to aggregate
in crevices to mate and lay egg capsules (Feare, 1970);
thus they may be inaccessible. Likewise, the new recruits
may be unobtainable if they remain in these crevices.
However, adults and juveniles were obtained from cre-
vices during both sampling periods.
There was no correlation between the presence or
absence of egg capsules and the proportion of adults
and juveniles, thus the presence of egg capsules could
not be used as an indication of breeding success and so
could not be used to compare sites. Seasonality is not
thought to in¯uence the presence or absence of egg
capsules in this study since they were observed during
both sampling periods.
In general, the sex ratio of dogwhelk populations in
the Firth of Forth was male biased, suggesting that the
populations are relatively unhealthy. Since the sex ratio
of healthy populations of the dogwhelk is normally
expected to be slightly female biased due to di€erential
mortality of the sexes (Feare, 1970), a male-biased sex
 K.L. Miller et al. / Environmental Pollution 106 (1999) 183±192
Fig. 4. Di€erence in relative penis size index (RPSI) values in the
Firth of Forth between 1987 and 1997±98. Decreases in RPSI value
are shown by positive values and increases in RPSI value are shown by
negative values.
ratio could be an indication of higher female mortality.
This is most likely caused by ruptured capsule glands as
a result of the accumulation of aborted egg capsules
which cannot be expelled due to the advanced stages of
imposex (Gibbs et al., 1987).
Seasonality can in¯uence RPSI values since male and
female penes vary in length according to the season.
However, seasonality is not thought to in¯uence the
RPSI values obtained in this study since sampling was
carried out within the same season. The relatively small
number of adults collected at three of the sites for RPSI
value determination suggests that localised extinctions
may have occurred in the recent past, thus implying that
TBT contamination within the Firth of Forth has been
relatively high in localised areas.
The lack of any signi®cant correlations between any
of the variables recorded at each site suggests that these
parameters cannot be used individually, or in combina-
tion, to evaluate or compare the status of dogwhelk
populations at di€erent sites. However, the data could
be used as baseline data for monitoring purposes,
allowing a temporal comparison to be made. Dogwhelk
RPSI values are a known reliable indicator of TBT
pollution (Bryan et al., 1988) thus this parameter is
extremely important when assessing the status of a
population, indicating recent pollution. Data concern-
ing population structure are also very important, espe-
cially in the absence of vas deferens sequence index
(VDSI) data, re¯ecting the breeding success of a popu-
lation over time.
189
4.2. Causes of continued imposex in the Firth of Forth
Dogwhelk populations appear on the whole to have
recovered from the hormonal e€ects of TBT in the Firth
of Forth, with the exception of Dunbar, South Queen-
sferry, North Queensferry, Aberdour, Pettycur and
Buckhaven. The general recovery is best attributed to
the restrictions concerning the use of TBT-based anti-
fouling paints which were established in 1987 (Dowson
et al., 1993). Since imposex does not regress, it is sug-
gested here that the restrictions have been e€ective in
reducing the amount of TBT entering the Firth of Forth
as indicated by the reduction in the degree of imposex in
dogwhelk populations in the area and the decrease in
the total tin concentration of dogwhelk body tissue.
This is especially true for sites 1±14 on the south coast
of the Firth of Forth, with the exception of Dunbar and
South Queensferry, and for sites 24±33 in the East Neuk
of Fife on the north coast (Figs. 1 and 4).
It has been shown that dogwhelks can live for over
10 years under laboratory conditions and in sheltered
rocky shore areas (Gibbs, personal communication).
However, dogwhelks normally live for 5±6 years (Gibbs,
personal communication); thus it is unlikely that the
imposexed individuals were a€ected by TBT con-
tamination before the restrictions were enforced. Sev-
eral explanations can be o€ered as to why imposex is
still occurring in localised areas in the Firth of Forth 10
years after the use of TBT was severely limited. Mar-
inas, boatyards and harbours are areas with which a
high degree of imposex has been associated in previous
studies (e.g. Huet et al., 1996). Privately owned boats
are moored at the marina at South Queensferry and, if
the hulls of these boats were coated with old supplies of
TBT-based antifoulings, the TBT could leach into the
water column accounting for the high degree of imposex
at South Queensferry. This explanation can also be
applied to Dunbar where ®shing boats are moored.
Minchin and Minchin (1997) have reported that ®shing
vessels can be over 25 m in length and, therefore, con-
tinue to be a signi®cant source of TBT contamination.
An alternative explanation is required for the rela-
tively high degree of imposex at the other sites with an
RPSI value greater than 25%. Davies and Bailey (1991)
have reported that TBT leaches from the hulls of large
vessels, but that since they spend a large proportion of
time o€shore, the concentration of TBT leached from
the anti-fouling paint is quickly diluted and dispersed to
levels which cause no measurable imposex e€ects. Large
vessels use the Firth of Forth as a passage to Grange-
mouth and Rosyth, situated west of the Forth Bridges
(Bailey and Davies, 1988). Studies have shown that
currents are weak in the Firth of Forth (Dyke, 1987;
Webb and Metcalfe, 1987); thus the retention time of
TBT in the water column will be relatively long and TBT
is likely to accumulate in localised areas of TBT input
190 K.L. Miller et al. / Environmental Pollution 106 (1999) 183±192
Fig. 5. Sewage discharges in the Firth of Forth and the six sites with a relative penis size index (RPSI) value greater than 25% (?).
with dogwhelk populations showing diminishing impo-
sex e€ects downstream of the input (Dowson et al.,
1992). This could o€er an explanation for the high
degree of imposex at North Queensferry and South
Queensferry since this is the narrowest area in the Firth.
In addition, the Firth of Forth `shipping lanes' pass
closer to the north coast of the Firth and large vessels
are constantly in dock at Hound Point and Braefoot
Bay, acting as ®xed point sources of TBT in these areas.
Therefore, it is likely that the high degree of imposex at
Aberdour could also be caused by leaching from large
vessels. It is suggested here that large vessels are
responsible for the increase or small change in RPSI
values at sites 15±22 (Figs. 1 and 4).
A ®nal suggestion as to the source of TBT in the Firth
of Forth is sewage and wastewater. Fent and Muller
(1991) have described the various ways in which TBT
can be present in domestic and industrial sewage and
wastewater, whilst Harding (1996) has shown that cer-
tain timber treatment processes can be responsible for
discharging TBT into the Firth of Forth. Fig. 5 shows
the numerous points of sewage discharge in the Firth of
Forth (Johnson, 1996). TBT is not measured in dis-
charges (Judy Dobson, SEPA, personal communica-
tion), thus there is no direct evidence which correlates
high RPSI values with sewage discharge points, but it is
a distinct possibility which must be considered in view
of the localised areas of concern. It is possible that the
high RPSI values at North Queensferry and Aberdour
result from the discharge from the paper mill at In-
verkeithing which is not dispersed rapidly due to the
relatively weak currents. In addition, Minchin et al.
(1997) have reported that organic-rich sediments have a
high anity for organotins; thus domestic sewage dis-
charge may contribute to the maintenance of back-
ground levels of TBT in sediments. It is also likely that
in localised areas, sewage discharge could cause high
levels of TBT in sediments, resulting in the high level of
imposex at six of the sites in this study (Figs. 1 and 5).
Stewart and Thompson (1997) have reported that
TBT accumulates in ®ne sediments and degrades slowly
over a number of years. The desorption of TBT from
the sediment, caused by disturbance of the sediment acts
as an indirect source of TBT contamination to the water
column (Clark et al., 1988; Unger et al., 1988). Harding
(1996) has reported that the dominant substrate type of
the Firth of Forth is mud which, according to Webb
and Metcalfe (1987), is regularly resuspended and rede-
posited over a tidal cycle as the current strengthens and
weakens. Such a disturbance could, therefore, cause
TBT desorption. In addition, Dowson et al (1993) have
mentioned that dredging activities can result in TBT
desorption from sediments. It is likely that sediment
resuspension and redistribution contributes to the
background level of TBT in the Firth of Forth. In areas
of high disturbance, high RPSI values would be expec-
ted, especially if the current action was weak. This could
explain the high degree of imposex (>25%) recorded in
this work at Dunbar, South Queensferry, North
Queensferry, Aberdour, Pettycur and Buckhaven.
In summary, dogwhelk populations in the Firth of
Forth have shown a general recovery from the e€ects
 K.L. Miller et al. / Environmental Pollution 106 (1999) 183±192
of TBT, with the exception of Dunbar, South Queen-
sferry, North Queensferry, Aberdour, Pettycur and Buc-
khaven which are likely to show breeding impairment
since the RPSI values were greater than 25% (Evans et
al., 1995). Background levels of TBT arising from the
leachate from the hulls of large boats, sediment resus-
pension and redeposition and sewage and wastewater
discharge remain high enough to cause a slight imposex
in all of the dogwhelk populations sampled within the
Firth of Forth. However, the level is not high enough to
cause a widespread breeding impairment (Evans et al.,
1995) and imposex is a localised problem within the Firth
of Forth. It is suggested that large vessels, in conjunction
with localised currents and disturbances, are responsible
for the high degree of imposex in the six problem areas
within the Firth of Forth.
Acknowledgements
The authors would like to thank Dr. Ian Davies and
Professor Paul Tett for their comments on the manu-
script. The authors also wish to extend thanks to Gavin
Grewar for carrying out GFAAS, Fiona Crouch for
demonstrating the methodology and to all the techni-
cians and post-graduate research students at Napier
University who volunteered to help with sampling.
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