Science of the Total Environment 502 (2015) 167–171

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Science of the Total Environment

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A combined whelk watch suggests repeated TBT desorption pulses

J.M. Ruiz ⁎, N. Albaina, B. Carro, R. Barreiro
Depto. BA, BV y Ecología, Universidade da Coruña, Rua da Fraga 10, 15008 Coruña, Spain

H I G H L I G H T S

• Tributyltin (TBT) and derivatives were monitored in 2 gastropods over N 10 years.

• Tissue TBT declined soon after the 2003 European ban but seem lately stabilized.
• The TBT share in the rock-snail shows an overall decreasing but oscillatory trend.
• The combined results are compatible with butyltins desorption from sediments.
• This natural phenomenon is now thought to be not a one-off event but a recurrent one.

a r t i c l e i n f o a b s t r a c t

Article history: Environmental quality in coastal Europe has improved since the complete 2003 ban on the use of tributyltin
Received 10 June 2014 (TBT) in antifouling paints. However, there is evidence that TBT is entering the water column, presumably
Received in revised form 8 September 2014 from illegal practices. We determined the concentration of butyltins (BTs: TBT and derivatives) in populations
Accepted 9 September 2014
of two gastropods, the rock snail Nucella lapillus (n = 17) and the mud snail Nassarius reticulatus (n = 18) at reg-
Available online 26 September 2014
ular intervals from pre-ban times until 2009 and 2011, respectively, in NW Spain. Although a substantial decline
Editor: Kevin V. Thomas in TBT occurred shortly after the ban, no significant changes were observed in either species over the last 3-year
period of study. In addition, the proportion of TBT relative to the sum of BTs (a marker of recent pollution) in the
Keywords: most recent rock snail samples unexpectedly increased; this proportion therefore showed a generally decreasing
Biomonitoring but oscillatory trend over time. The results are consistent with the theoretical expectation of BT desorption from
Butyltin sediments; however, this natural phenomenon is now interpreted as a recurrent episode rather than a unique,
Gastropods transient event. Evidence of this subtle input improves our understanding of TBT persistence in the environment
Nassarius reticulatus in Europe and worldwide.
Nucella lapillus
© 2014 Elsevier B.V. All rights reserved.
Tributyltin (TBT)

1. Introduction passive diffusion. This desorption is a natural phenomenon that tends

Tributyltin (TBT) is an organometallic compound formerly used as a
biocide in ship antifouling paints (e.g., Ruiz et al., 1996; Santillo et al.,
2001). In 2008, the International Maritime Organization (IMO) banned
TBT application and imposed the complete removal of TBT-based
paint from ship hulls (imo.org); in Europe and South Korea, these regu-
lations were established in 2003 (European Union –EU– Directive 2002/
62/EC and Choi et al., 2010, respectively). Recently, efforts have focused
on documenting the anticipated reduction of TBT in the environment;
however, there are concerns that this reduction will be deferred because
of sediments transitioning from pollution sink to source. The remobili-
zation of hydrophobic pollutants such as TBT is consistent with theory;
specifically, when the water concentration of a substance decreases,
some of the adsorbed contaminant is returned to the aquatic phase by
⁎ Corresponding author. Tel.: +34 981 167000.
E-mail address: jmruiz@udc.es (J.M. Ruiz).
to decrease over time (an “aging” effect) and is enhanced by sediment
disturbance (e.g., Eggleton and Thomas, 2004).
Previous theoretical studies indicate that such TBT desorption
should be much reduced in both quantity and duration relative to
the original inputs (Harris et al., 1996), and more recent laboratory
experiments have supported the occurrence of some aging in
organic-rich sediments (Burton et al., 2006). However, field studies
of the desorption of TBT into the aquatic environment are rare. An in-
crease of sediment–water partition coefficients in Poole Harbour was
reported after introduction of the UK legislation (Langston and Pope,
1995), and changes in the baseline butyltin (BT) bioaccumulation
pattern of two intertidal gastropod species in Spain (Ruiz et al.,
2008) have been documented. Continuation of the latter work
found that this distortion of tissue BT ratios appeared to be a tran-
sient event and thus was consistent with a generalized aging effect
(Ruiz et al., 2010). Here, we test our hypothesis with additional mon-
itoring of these two gastropod species.

http://dx.doi.org/10.1016/j.scitotenv.2014.09.019
0048-9697/© 2014 Elsevier B.V. All rights reserved.
168 J.M. Ruiz et al. / Science of the Total Environment 502 (2015) 167–171
2. Materials and methods
Two gastropod species commonly used in Atlantic Europe for pollu-
tion studies were investigated: the rock snail Nucella lapillus (L.), an in-
tertidal, rocky-shore carnivore in which tissue TBT is primarily derived
from water (Bryan et al., 1989); and the mud snail Nassarius reticulatus
(L.), a soft-bottom depositivore known to uptake considerable amounts
of BTs from sediments as well as from water (Pope, 1998). The sampling
localities are distributed across Galicia (NW Spain) and vary from ex-
posed sites to protected estuarine stretches. The collecting season for
both species (see below in this section) were not coincident, because
the surveys were designed to also assess population imposex, which re-
quires sampling within the respective reproductive periods. Surveys of
each species after the 2003 EU TBT ban were conducted every 3 years
per species; as a result, the sampling lag between species is 1.5 years.
As rock snail populations had last been monitored in 2006, a new
survey took place over the summer months (July-September) of 2009.
Detailed information on the location of intertidal sites, sample selection,
and laboratory procedures is provided in Ruiz et al. (1998). The original
sampling network consisted of 20 populations, but unknown factors
have reduced it to 17. The fourth survey of the mud snail, conducted
as part of the present study, occurred over February and March 2011;
the gastropods were collected and treated as detailed in Ruiz et al.
(2005). The number of sampling localities gradually decreased over
time, from 26 in 2000 to 24 in 2008. In addition, for the last 2011 cam-
paign, the number of sampling localities was reduced down to 18 due to
financial constraints.
The whole tissues of all sampled females (n ≥ 13) were pooled and
processed for BT (TBT and derivatives di- and mono-butyltin, DBT and
MBT) determination. Analyses of samples collected up to 2006 were per-
formed using a blind protocol by the Unité Mixte de Recherche 5034
(Pau, France). This protocol (Szpunar et al., 1996) progressively lowered
the MBT (the most problematic chemical species) quantification limit to
0.4 ng Sn g−1 Fresh Weight (a factor of 5 was used to convert this mea-
sure to Dry Weight, DW). Briefly, the analytical procedure included in-
ternal standards, solubilization, ethylation, and extraction to isooctane.
Detection was accomplished with a GC-AED (Gas Chromatograph -
Atomic Emission Detector) system equipped with a split/splitless injec-
tion port and an automatic sampler. From 2008 onward, samples were
analyzed using a new isotope dilution method we had employed previ-
ously (Díaz et al., 2007). In summary, using a blind protocol, samples
were subject to enrichment (82.4% 119Sn-enriched tin metal),
ethylation, derivatization, and extraction to hexane. Detection
was achieved with a GC-ICP-MS (Gas Chromatograph - Inductively
Coupled - Mass Spectrometer) system. The measured isotope ratios
(118/119 and 120/119) were corrected for mass bias, and the final con-
centrations of BTs were determined from the 120/119 isotope ratio and
verified using the 118 isotope results. For comparison, the MBT quantifi-
cation limit with this last GC-ICP-MS detection technique was 1.5 times
lower than with the previous GC-AED.
These two procedures have consistently yielded satisfactory recov-
ery of the different CRMs (Certified Reference Materials: PACS-2,
NIES11, and BCRs 477 and 710) employed through time. The concentra-
tions of each BT are reported here as ng Sn g−1 DW (or ppb Sn DW). The
values are analytical means, and their CVs (or relative standard
deviations) do not surpass 10% with the exception of MBT in several
samples from older surveys. The data were evaluated for normality
and homoscedasticity prior to statistical analysis and were log-
transformed and/or subject to non-parametric analyses as required
(see Section 3). The significance levels are depicted here as *, ** and
*** for p b 0.05, p b 0.01 and p b 0.001, respectively.
3. Results
The BT concentrations of the samples collected in the present study
are presented in Table 1. The complete datasets thus consist of 4 surveys
for both the rock snail (n = 17 populations sampled in 1996, 2003, 2006
and 2009) and the mud snail (n = 18 populations sampled in 2000,
2005, 2008 and 2011). TBT decreased substantially over time in both
species, such that average tissue concentrations in the most recent sur-
veys were nearly one order of magnitude lower than those measured a
decade before (Fig. 1A-B). Although some declines appear clear, ANOVA
(***) and post-hoc Tukey HSD tests found that the only significant differ-
ence in each dataset was that between the group formed by the first two
surveys and the group formed by the last two (i.e., 1996 + 2003 vs.
2006 + 2009 for the rock snail ***, and 2000 + 2005 vs. 2008 + 2011
for the mud snail *).
Fig. 1C-D plots the temporal change in the relative amount of TBT (as
a percentage of the aggregate of all three BTs) in both gastropods.
Heteroscedastic mud snail data series subject to Kruskal-Wallis (***)
and a posteriori Nemenyi tests revealed (q N 3.852) that the percentage
of TBT in this sediment dweller was reduced from a maximum value in
2000 to consistently lower levels in 2005 (**), 2008 (***) and 2011 (*);
pairwise differences among these last three surveys were not signifi-
cant. In contrast, ANOVA (***) and Tukey HSD tests revealed (**) an un-
expected oscillation in the proportion of TBT in rock snail tissues: it
significantly increased from 1996 to a maximum in 2003, then reached
a minimum in 2006, and increased again in 2009 to values not signifi-
cantly different than those observed 13 years before. A scarcity of data
prevented mathematical modeling, but the trend (fitted by eye to
mean values with a dotted line in Fig. 1C) resembles a chemical oscilla-
tor approaching equilibrium (see Epstein and Pojman, 1998).
Fig. 2 plots the sum of derivative BTs vs. the parent compound (TBT)
for all samples of each gastropod; for each species, only regression lines
(no data points) are shown for the first 3 surveys for clarity (in black,
red and blue for the 1st, 2nd and 3rd campaign, respectively). All rela-
tionships were significant for the previous datasets (Ruiz et al., 2010),
and similar results were found in the present study for the six regres-
sions calculated for the decimal logarithm of the tissue residues in a
number of data points, which were lower in the present study due to
reasons explained in Section 2 (n = 17 for the rock snail and n = 18
for the mud snail). The two most recent surveys of these same popula-
tions (in 2009 and 2011, represented by green diamonds and lines, re-
spectively, in Fig. 2) also yielded highly significant (***) relationships
between variables, particularly for the mud snail.
Except for the surveys shown in red (i. e. 2003 and 2005, see below in
the next section), the line Y intercepts in Fig. 2 are higher for the rock
snail than for the mud snail (1.00 and above vs. 0.60 and below,
respectively); this conforms with Bryan et al. (1993), who concluded
that the latter species has a more effective BT metabolism in agreement
with its well known tolerant, and therefore eurytopic, character. Howev-
er, over the last 3-year period, the mud snail showed little BT depuration
(Fig. 2B) that is significant for neither TBT (Fig. 1B) nor the sum of deriv-
atives (Tukey HSD test following ANOVA of differences between the 2008
and 2011 data). In contrast, while the rock snail similarly showed negli-
gible changes in TBT (no net horizontal displacement in Fig. 2A, see also
Fig. 1A and text above in this section), some considerable DBT + MBT
depuration is evident (note vertical drop in Fig. 2A) and significant
(Kruskal-Wallis *** and Nemenyi test for 2006 vs. 2009 *).
4. Discussion
It has been shown that TBT pollution has substantially decreased in
the study area over the last decade. Such a scenario of decreasing new
contaminant input should be associated with a change in individual
BT distributions, from a higher proportion of TBT (relative to the total
BT measured) to a lower one. This pattern has been more apparent in
quickly reacting environmental matrices (e.g., water and mussels, Choi
et al., 2010) than in less responsive ones (i.e., sediments, Harino et al.,
2009; Choi et al., 2010). Our results for the mud snail Nassarius
reticulatus agree with this pattern and also with the observations avail-
able for the same species in Portugal, where it was shown that both TBT
 J.M. Ruiz et al. / Science of the Total Environment 502 (2015) 167–171 169

Table 1
Concentration (mean ± SD, ng Sn g−1 DW) of butyltins (MBT, DBT and TBT for mono-, di- and tri-butyltin, respectively) in tissues of Nucella lapillus (rock snail) and Nassarius reticulatus
(mud snail).

Rock snail 2009 Mud snail 2011

Code a MBT DBT TBT Code b MBT DBT TBT

1 5.0 ± 0.4 34.7 ± 2.4 6.1 ± 0.3 1 61.6 ± 3.1 123.4 ± 6.2 125.8 ± 2.5
8 10.4 ± 0.6 31.4 ± 1.6 33.4 ± 0.7 2 26.8 ± 2.7 59.9 ± 4.2 48.7 ± 1.5
9 38.8 ± 3.5 124.0 ± 3.7 103.1 ± 2.1 3 127.2 ± 11.4 254.9 ± 17.8 341.3 ± 13.7
13 52.3 ± 4.2 124.5 ± 10.0 114.4 ± 3.4 4 13.5 ± 1.4 40.9 ± 2.5 23.1 ± 1.2
14 62.2 ± 5.6 177.6 ± 10.7 183.7 ± 5.5 5 12.3 ± 0.9 33.7 ± 2.7 33.2 ± 2.0
15 21.4 ± 1.3 153.4 ± 7.7 30.8 ± 1.5 6 26.1 ± 2.6 59.8 ± 3.6 65.9 ± 2.6
16 6.7 ± 0.5 47.1 ± 2.8 5.9 ± 0.1 8 95.1 ± 7.6 162.7 ± 11.4 177.3 ± 10.6
17 4.8 ± 0.5 9.5 ± 0.6 3.9 ± 0.1 9 5.6 ± 0.6 13.5 ± 0.5 10.7 ± 0.5
18 5.1 ± 0.3 11.0 ± 0.9 15.6 ± 0.9 11 16.1 ± 1.3 27.1 ± 2.2 19.8 ± 1.0
21 9.0 ± 0.4 43.9 ± 3.5 12.5 ± 0.5 13 6.6 ± 0.5 11.7 ± 0.9 4.0 ± 0.1
25 7.3 ± 0.6 28.6 ± 0.9 40.6 ± 0.8 14 8.0 ± 0.7 18.0 ± 0.5 8.2 ± 0.2
26 5.8 ± 0.6 22.3 ± 1.6 13.3 ± 0.4 16 6.0 ± 0.4 7.4 ± 0.5 10.5 ± 0.4
28 13.8 ± 1.4 47.2 ± 3.3 71.4 ± 4.3 17 7.9 ± 0.6 9.7 ± 0.6 10.1 ± 0.2
32 45.0 ± 4.1 131.0 ± 6.5 140.9 ± 5.6 18 10.8 ± 0.5 19.9 ± 1.0 29.1 ± 1.5
33 12.7 ± 0.8 45.7 ± 3.7 23.3 ± 1.2 20 10.7 ± 1.0 54.5 ± 2.7 29.7 ± 1.2
34 15.6 ± 0.9 189.4 ± 9.5 23.0 ± 0.5 21 16.5 ± 1.3 31.3 ± 2.5 30.5 ± 0.6
37 23.4 ± 2.3 139.8 ± 11.2 74.0 ± 1.5 23 16.6 ± 1.5 45.5 ± 1.8 42.2 ± 2.1
26 17.1 ± 1.7 22.8 ± 0.9 34.7 ± 1.7
a, b
as originally assigned in Ruiz et al. (1998 and 2005, respectively).

concentration and its proportion in tissues significantly decreased from
2003 to 2008 (n = 5, Sousa et al., 2009). More generally, their main
finding (i.e., of little recent decline in BT contamination after some sub-
stantial initial declines) is also consistent with the general view that fol-
lowing regulations on TBT use, levels of environmental pollution quickly
decreased but then stagnated. This was observed after both the earlier,
partial TBT restrictions (e.g., in France in 1982, see Michel and Averty,
1999) and the later total ban (2003 in some areas, see Section 1). In
the former case, the persistent levels have been ascribed to the continu-
ing legal use by bigger vessels; in the latter, they are usually attributed
to hotspot estuarine areas (such as bays, ports, and dry-docks) with sed-
iments that act as reservoirs, affecting the surrounding environment
through remobilization and diffusion (Kim et al., 2011; Verhaegen
et al., 2012). The biology of this infaunal species, with its close

Fig. 1. Long-term changes in tributyltin (TBT) levels in tissues of intertidal gastropods. Plot
of the decimal logarithm of TBT concentration (panels A and B) and its proportion
(percentage with respect to the aggregate TBT plus derivatives, panels C and D) in the
rock snail Nucella lapillus (n = 17) and the mud snail Nassarius reticulatus (n = 18).
Boxes represent values from the lower 25th to the upper 75th percentile; the mean is rep-
resented as a cross and the median as a horizontal line within the box. The tails represent
the minimum and maximum values that are not outliers. Outliers (points N 1.5 times the Fig. 2. Long-term changes in butyltin levels in tissues of intertidal gastropods. Plot of the
interquartile range) are denoted by small empty squares. The dotted line in panel C has sum of derivatives (the decimal logarithm of di- plus mono-butyltin, DBT and MBT)
been fitted by eye to highlight the trend.Years with different lower case letters exhibit against the decimal logarithm of the parent compound (tributyltin, TBT) in Nucella lapillus
significant differences, see text. (A, n = 17) and Nassarius reticulatus (B, n = 18).
170 J.M. Ruiz et al. / Science of the Total Environment 502 (2015) 167–171
interactions with sediments, likely explains the observed persistence of
old TBT inputs (as denoted by the lowered proportion of TBT in tissues,
see Fig. 1D) and predicts slow recovery in such turbid environments.
However, the changes in BT residues in the rock snail Nucella lapillus
are more challenging to explain. What environmental processes occur-
ring six years after the complete EU ban could account for the increase
in the tissue proportion of TBT to pre-ban levels? It has to be noted that
the consistent dependence of derivatives on TBT concentrations
(Fig. 2A-B) indicate the common origin of BT pollution in the area,
(i.e., the use of the parent compound in antifouling paints; e.g., Church
et al., 2006), potentially with minimal secondary sources (see Ruiz
et al., 2008). And ever since increasing TBT percentages are indicative
of increasing proximity to the source(s) (in time and/or space;
e.g., Seligman et al., 1996) and the spatial framework has not changed,
this increase from 2006 to 2009 is a clear signal of recent TBT input affect-
ing the rock snails (Fig. 1C) but not the related mud snails (Fig. 1D). Pre-
viously, we described how, under receding TBT pollution, passive
desorption from sediments shortly after the 2003 EU TBT ban could
yield the contrasting results in the two gastropods illustrated by the
abrupt change of slope of the respective red lines in Fig. 2 (years 2003
and 2005). Briefly, species such as the rock snail are most prone to
being affected by whatever TBT is released into the water column be-
cause this TBT tends to concentrate in the surface microlayer surrounding
intertidal organisms four times a day (Ruiz et al., 2008). Thus, an intense
desorption episode was deemed a credible mechanism explaining the
first observed rise in the proportion of TBT (1996–2003), a pulse that ap-
peared to end by the time of the following surveys (2006 for the rock
snail and 2008 for the mud snail, see the concomitant recovery of the
slopes of both blue lines in Fig. 2; Ruiz et al., 2010). Accordingly, could
the more recent rise in 2009 be interpreted as an additional but more
subtle desorption pulse, again manifested only in the rock snail?
Although there is a large literature on TBT, studies of BT residues are
unfortunately scarce, and only a few focus on the same gastropod species
across Europe. This information shortage is anticipated to wane, as the
imposex vigilance program, mandatory within OSPAR (the Convention
for the Protection of the Marine Environment of the NE Atlantic), has re-
cently recommended the quantification of TBT and derivatives in tissues
(see ospar.org). Continued monitoring in Ria de Aveiro (NW Portugal) by
Galante-Oliveira et al. (2009) found a decline in imposex in Nucella
lapillus after 2003, but a separate analyses in 2006 (n = 9 populations)
recorded a much higher proportion of TBT in relation to DBT (concentra-
tions varied from 10 to 134 and from b 10 to 18 ng Sn g−1 DW,
respectively); these were considered evidence of expected, fresh inputs,
considering that TBT legislation was not fully effective until September
2008. Coincidently, Oliveira et al. (2009) surveyed the North Wales
coast and showed that imposex in N. lapillus decreased significantly
from 1987 to 1994 and further to 2006, likely reflecting the partial UK leg-
islation in 1987 and subsequent total EU ban in 2003; additional analyses
of the same populations (n = 14) found primarily undetectable levels of
DBT (concentrations varied from b2.3 to 6.2 ng Sn g−1 DW) and MBT
(b5.1 ng Sn g−1 DW), such that TBT (0.8 – 39 ng Sn g−1 DW) represented
the highest BT fraction and suggested recent inputs in 2006. Lastly, during
a long, generally decreasing pattern of imposex in western Iceland,
Guomundsdóttir et al. (2011) conducted a one-off chemical assessment
of N. lapillus populations (n = 16) in 2009. Concurrent with alarmingly
increasing imposex levels in some small harbors, TBT (concentrations
varied from 2.07 to 70.38 ng Sn g−1 DW) was revealed as more predom-
inant and abundant than DBT and MBT (b1.5 – 24.66 and b 0.8 ng Sn g−1
DW, respectively), suggesting continuous inputs into coastal waters and
presumably the illegal use of these compounds.
Although these three studies are not fully comparable, spanning dif-
ferent countries and times relative to the observance of TBT regulations,
they encompass almost all of the rock snail latitudinal range and allow a
conclusion: under a scenario of decreasing TBT pollution (as evidenced
by the amelioration of specific biological effects), the finding of a pre-
ponderance of TBT several years after the 2003 EU total ban implies
fresh inputs into the water column. An analogous situation was ob-
served in Arcachon Bay (France) where, following the first restrictions
imposed in 1982 to protect aquaculture, the frequency of biological ef-
fects caused by TBT (specifically, oyster shell malformations) rapidly de-
creased but then increased several years later (see Fig. 3 in Alzieu, 1991
and Fig. 5 in Ruiz et al., 1996). Although commonly invoked anthropo-
genic factors, such as contemporary release from ship hulls via either
legal or illegal paints, may be important contributors to these instances
of recurrent pollution, others mechanisms may also be responsible. In
particular, desorption from sediments is a natural phenomenon, and it
is expected to occur in disparate geographical settings, its timing
governed by the onset and outcome of TBT regulations in each particular
area. Thus, even if new theoretical and/or laboratory developments re-
garding this important issue may be unlikely for a disappearing pollut-
ant, detailed BT monitoring is expected to augment the field database
and thus enhance our understanding of the long term fates and effects
of this paradigmatic pollutant.
Acknowledgements
Thanks are due to J. Díaz y A. Irabien (Depto. Ingeniería Química y
Química Inorgánica, Universidad de Cantabria) for performing the anal-
yses of butyltins in 2009 and 2011 samples. This work was partially sup-
ported by the Spanish Ministerio de Educación y Ciencia (MEC,
CTM2004-04496/MAR, co-funded by the European Fund for Regional
Development), the Xunta de Galicia (PGIDIT05PXIC10302PN), and
some cooperative agreements between the Universidade da Coruña
and the Instituto Español de Oceanografía. B.C. and N.A. received post-
graduate fellowships (Deputación da Coruña and FPU-MEC AP2006-
03231, respectively. The institutions had no other role than providing
funding.
Appendix A. Supplementary data
Supplementary data associated with this article can be found in the
online version, at http://dx.doi.org/10.1016/j.scitotenv.2014.09.019.
These data include Google maps of the most important areas described
in this article.
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