Marine Pollution Bulletin 46 (2003) 1150–1155

www.elsevier.com/locate/marpolbul

Imposex in the indigenous Nassarius kraussianus

(Mollusca: Neogastropoda) from South African harbours
David J. Marshall *, Anisha Rajkumar
School of Life and Environmental Sciences, University of Durban-Westville, Private Bag X54001, Durban 4000, South Africa

Abstract

Nassarius kraussianus populations in the Durban and Richards Bay harbours (along the eastern seaboard of southern Africa) and
in the Knysna lagoon (southern Cape coast) showed imposex development, confirming bioavailability of tributyltin (TBT) in these
waterways. Incidence of imposex (which ranged from 29% to 100%) and relative penis length of females (RPL; which ranged from
1.3% to 55.2%) were markedly variable among populations from different sites in each waterway, indicative of localised effects of
TBT contamination. Shell length of the snails was apparently not correlated with contamination level, as assessed from imposex
measurements. While population imposex features are easy to determine and often provide a sensitive biomarker of TBT exposure,
the discussion outlines reservations when extrapolating these to general ecological situations. Additionally, this study represents the
first published report on the topic for sub-Saharan, African harbours, some of which seem remarkably less affected than suggested
for other world regions.
Ó 2003 Elsevier Ltd. All rights reserved.

Keywords: Tributyltin; Organotin; Antifouling paints; South Africa; Nassarius kraussianus; Biomarker

1. Introduction trated in the northern latitudinal regions, including East

Asia (Horiguchi et al., 1994; Blackmore, 2000; Bech
Imposex is characterized by the development of male et al., 2002), Korea (Hong et al., 2002), Mediterranean
morphological features (penis and vas deferens) in fe- (Michel et al., 2001; Ramon and Amor, 2001; D
ıez et al.,
male individuals of gastropod molluscs. It is exclusively 2002), Spain (Barreiro et al., 2001), Portugal (Barroso
related to exposure to organotin antifouling paint et al., 2002a), United Kingdom (Gibbs and Bryan, 1986,
compounds, and thus serves as a useful morphological 1996; Bryan et al., 1986–1988, 1993; Gibbs et al., 1987,
biomarker of contamination of these compounds in 1988), the Netherlands (De Wolf et al., 2001), and the
marine systems (Gibbs and Bryan, 1986; Bryan et al., North Sea (Birchenough et al., 2002). Different oceanic,
1987; Gibbs et al., 1988; Barreiro et al., 2001; Barroso climatic and biotic conditions pertain to different world
et al., 2002a,b). Although various organotin species regions, and in spite of the need for comprehensive
(monobutyltin, MBT; dibutyltin, DBT; tributyltin, global maritime initiatives (such as Globallast which
TBT; and triphenyltin, TPhT) may accumulate in the focuses on species introductions), conspicuously less is
tissues of marine invertebrates, TBT shows the greatest known about TBT contamination and its effects in
accumulation, and is the primary cause of imposex southern hemisphere harbours. Relevant investigations
(Bryan et al., 1988; Barreiro et al., 2001). have been undertaken in Chile, Brazil and Argentina
Despite international efforts, including a shipping (see Penchaszadeh et al., 2001 and references therein),
moratorium on the use of TBT, its continued occurrence but no published reports of TBT contamination are
in natural systems has prompted a proliferation of re- known for any sub-Saharan, African harbours.
cent investigations. These have, however, been concen- Southern Africa is positioned along a primary ship-
ping route between Europe, the Americas, and Asia. Its
harbours provide infra-structural support to a global
*
Corresponding author. Tel.: +27-31-2044-410/+27-31-2044-460; shipping industry, with some of the largest and busiest
fax: +27-31-2044-790. African harbours being located on the eastern sea-
E-mail address: [email protected] (D.J. Marshall). board of South Africa, at Durban and Richards Bay
0025-326X/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/S0025-326X(03)00191-7
 D.J. Marshall, A. Rajkumar / Marine Pollution Bulletin 46 (2003) 1150–1155 1151

(province of KwaZulu-Natal; KZN). These harbours 2. Materials and methods

were constructed within extensive and pristine natural
estuarine systems which support mud banks provid- Specimens of Nassarius kraussianus (n ¼ 412) were
ing habitat for the indigenous neogastropod mollusc, collected from mud banks in Durban and Richards Bay
Nassarius kraussianus (Dunker, 1846), a species com- harbours, and from the Knysna lagoon between April
monly occurring in estuarine and salt-marsh systems and October 2002 (Fig. 1). Sample sites (two at Richards
from Namaqualand on the west coast, to Mozambique Bay, four at Durban and three at Knysna) were selected
on the east coast of southern Africa (Kilburn and Rip- on the basis of mud bank availability and in order to
pey, 1982). Considering the attention given to its con- include good spatial coverage within each waterway.
generic, N. reticulatus (Bryan et al., 1993; Barreiro et al., One of the sites at Richards Bay was in close proximity
2001; Barroso et al., 2002a,b), it seemed a potential to a major coal terminal (R2), while the other (R1) ap-
candidate for examining the condition of imposex. proximately 10 000 m away, supports a few small craft
Knysna lagoon, in the southern Cape Province, was piers (Fig. 1). Sampling sites at Durban harbour were
considered as a useful comparator to the relatively either adjacent to a small craft mooring area (D4 and
similar KZN harbours, in that it is geographically re- D5) or, along the Bayhead lagoon (D3 and D6), an area
moved and lacks maritime activity. fringed with mangroves and removed from primary
We report here the novel occurrence of imposex in shipping activity (Fig. 1). Unsuccessful attempts were
N. kraussianus, and provide the first information on made to collect N. kraussianus from estuaries near
TBT bioavailability in sub-Saharan, African harbours. Durban and Richards Bay, at Mtunzini, Tugela River,
TBT contamination, as inferred from imposex devel- Umgeni River, and Isipingo. Knysna lagoon is sur-
opment, was found to vary within and between the rounded by a residential and tourist town (Knysna) and
waterways examined, being highly localised around is distinct from the two KZN harbours in not being
docking areas. Additionally, and with reservation associated with shipping or heavy industry. At Knysna,
considering the sample size, overall TBT effects seemed specimens were collected from a small craft harbour
less severe than those suggested for other world re- (approximately 50 vessels; K1), and from other sites at
gions. 100 m (K2) and 3000 m (K3) away from this.

Fig. 1. Map of southern Africa showing Knysna, Durban and Richards Bay, and the details of Durban and Richards Bay harbours. The symbols
given in the harbour maps are as follows: asterisk––harbour entrance; triangles––coal and container terminals at Richards Bay and Durban re-
spectively; squares––small craft; closed circles––general shipping; open circles––natural area.
1152 D.J. Marshall, A. Rajkumar / Marine Pollution Bulletin 46 (2003) 1150–1155

Live individuals were returned to the laboratory in ANOVAs, multiple comparison tests, and regression
Durban. After measuring the shell length of each snail analyses) were performed on log-transformed data using
(using a digital vernier calipers;
0.01 mm), the shell SPSS ver. 11 for Windows.
was removed by boiling and cracking in a bench vice, a
procedure that apparently had no effect on penis length.
Penis length was determined for both sexes using a 3. Results
dissecting microscope (64 magnification), with sex
determination based on gonadal characteristics. Gen- Gross penis enlargement in female specimens of
der-specific mean values for shell length and penis length Nassarius kraussianus confirms imposex for this species.
were calculated for each population from each water- The incidence of imposex varied among populations in
way. These means were used to calculate penis to shell each of the three waterways, ranging from 29% at D6 to
length ratios, as well as the more commonly used rela- 100% at R1, R2 and D4 (Table 1). Relative penis length
tive penis length index (RPL: female penis length as a (RPL) varied from 1.3 (K3) to 55.2 (R2) (Tables 1 and
percentage of male penis length; see Bryan et al., 1993; 2). Although incidence of penis development in females
Barreiro et al., 2001). Statistical comparisons (one-way in K3 was relatively high, penes were always vestigial,

Table 1
Measurements of shell length and penis length of Nassarius kraussianus individuals from Durban and Richards Bay
N Shell length (mm) Penis length (mm) Penis length/ RPL % Imposex
(mean
1SE) (mean
1SE) shell length
Females
Richards Bay
R1 11 7.16
0.21 AB 1.63
0.30 A 0.23 24.5 100
R2 10 6.55
0.11 A 4.14
0.13 B 0.63 55.2 100
Durban
D3 21 8.18
0.08 C 0.20
0.07 C 0.02 2.8 38
D4 33 8.31
0.17 C 3.80
0.26 B 0.46 48.2 100
D5 18 8.43
0.13 C 3.31
0.17 B 0.39 51.2 94
D6 24 7.30
0.13 B 0.29
0.12 C 0.04 3.7 29

Males
Richards Bay
R1 9 7.05
0.15 A 6.65
0.17 AC 0.95
R2 15 7.52
0.09 AB 7.50
0.18 BC 0.99
Durban
D3 23 7.80
0.08 C 6.96
0.19 A 0.84
D4 11 8.29
0.09 CD 7.87
0.29 B 0.95
D5 23 8.52
0.09 D 6.47
0.12 A 0.76
D6 21 7.62
0.13 B 7.76
0.15 B 1.02

Significant differences are indicated by different letters associated with means in columns (ANOVA; P < 0:05; Tukey). N ¼ sample size for each
population.

Table 2
Measurements of shell length, and penis length of Nassarius kraussianus individuals for Knysna
N Shell length (mm) Penis length (mm) Penis length/ RPL index % Imposex
(mean
1SE) (mean
1SE) shell length
Females
K1 33 7.36
0.07 A 4.00
0.37 A 0.54 44.8 84.8
K2 15 7.25
0.15 A 1.38
1.62 B 0.19 18.4 46.7
K3 49 7.37
0.08 A 0.12
0.02 C 0.02 1.3 40.8

Males
K1 48 7.14
0.05 A 8.92
0.09 A 1.23
K2 15 7.05
0.15 A 7.47
0.25 B 1.06
K3 31 7.06
0.10 A 9.00
0.16 A 1.27

Significant differences are indicated by different letters associated with means in gender-specific columns (ANOVA; P < 0:05; Tukey). N ¼ sample size
for each population.
 D.J. Marshall, A. Rajkumar / Marine Pollution Bulletin 46 (2003) 1150–1155 1153

questioning whether the effect in this case was artefac- TBT within the harbours, and suggest lesser severity of
tual. RPL varied in a similar manner to the ratio of contamination than that reported for many northern
female penis length to shell length, and differed among hemisphere harbours.
the populations in the following order (from highest to Both female penis length (relative to male penis
lowest): R2 > D5 > D4 > R1 > D6 > D3 for the KZN length––RPL) and vas deferens development are po-
harbours, and K1 > K2 > K3 for Knysna (Tables 1 tentially useful biomarkers of TBT exposure (Bryan
and 2). et al., 1993; Philips and Rainbow, 1994; Blackmore,
Although mean shell length differed significantly 2000), but data for these parameters should be inter-
among the populations at Richards Bay and Durban preted with reservation. For instance, imposex devel-
(the former contained smaller individuals), there was no opment provides limited information on exposure time
pattern to suggest any relationship between female im- frame; adult snails living in uncontaminated conditions
posex development and male or female body size for the have been shown to display imposex features derived
populations (Table 1). For example, although the shell from TBT exposure during their juvenile stages (Gibbs
lengths of females in populations D3, D4 and D5 were and Bryan, 1996). Additionally, comparisons between
the same, imposex was much less pronounced in D3 populations and species are invalid in cases where life-
than in D4 and D5. Also, male shell length was the same history traits, such as longevity and female recruitment,
in populations exhibiting either high (R2) or low levels differ (see Bryan et al., 1993). Finally, species size dif-
of imposex (D6; Table 1). Male penis length was not ferences could invalidate species comparisons through
correlated with shell length (F ¼ 1:486; P ¼ 0:23) nor inequality in relative penis size variances (females to
imposex development of females in the same population. males), assuming an allometric relationship for male
As an example, mean male penis length for R2 and D4 penis length. These may explain why many studies
(showing high imposex development) was not signifi- measure TBT tissue concentrations in addition to de-
cantly different from D6 (which showed low imposex termining imposex parameters.
development; Table 1). Other than the above theoretical constraints in in-
Gender-specific weight and size parameters of the terpreting relationships between imposex development
Knysna populations were not significantly different from and TBT exposure, discrepancies exist for comparable
each other. These parameters also appeared similar investigations. Separately performed studies on Nassa-
across the sexes, and fell into the ranges recorded for rius reticulatus showed that, for the same RPL of more
populations from the KZN harbours (Tables 1 and 2). than 80%, minimum TBT tissue concentrations vary
between 100 and 500 ng Sn g1 dry wt. (Bryan et al.,
1993; Barreiro et al., 2001). Although TBT tissue con-
4. Discussion centrations in N. reticulatus were higher than 2200 ng
Sn g1 dry wt. at RPL values above 80%, the reliability
Numerous investigations have considered the rela- of these values is thwarted by the asymptotic nature of
tionship between imposex development in neogastropod the relationship (see Barreiro et al., 2001). The highest
molluscs and TBT concentration in their tissues, or in RPL value for N. reticulatus was much greater than the
the marine environment (sediments and water bodies) below 60% determined here for N. kraussianus. Not-
(Gibbs and Bryan, 1986; Bryan et al., 1986–1988, 1993; withstanding interspecific differences in sensitivity, the
Barroso et al., 2002a,b). These investigations provide relatively low RPL values of N. kraussianus suggest less
resounding evidence in support of the exclusive link severe TBT contamination in southern African harbours
between imposex development and exposure to TBT in than elsewhere.
natural marine systems. Although details are available Despite the above mentioned limitations and the
for relatively few species, in particular Nucella lapillus variable persistence of TBT in sediments (from 1.8 years
and Nassarius reticulatus (Gibbs and Bryan, 1986; Bryan to decades; see Ramon and Amor, 2001; Anderson et al.,
et al., 1986–1988, 1993; Barreiro et al., 2001; Barroso 2002), population imposex frequencies and RPLs of N.
et al., 2002a,b), imposex development has been reported kraussianus suggest remarkable spatial variability of
for numerous neogastropod species (>50 species in TBT contamination in the harbours studied (Tables 1
Bryan et al., 1986 and >120 species in Penchaszadeh and 2). This seemingly relates to proximity of the con-
et al., 2001). While the relationship between imposex tamination source, as well as current directions and tidal
and TBT is thought to generalise across neogastropod prisms within the waterways. Assuming that the lesser
taxa, sensitivity to TBT is variable from one taxon to the contaminated sites are affected by sources R2 at Rich-
next (Bryan et al., 1993). The findings of the present ards Bay, D4 and D5 at Durban, and K1 at Knysna,
study, that imposex is prevalent in southern African then it may be inferred that contamination decreases
harbour populations of Nassarius kraussianus, thus in- among the waterways in the above-listed order. Con-
dicates TBT bioavailability in these harbours. The data tamination declines moderately within 10 000 m at
further indicate spatial limitations on the distribution of Richards Bay (between R1 and R2), and acutely within
1154 D.J. Marshall, A. Rajkumar / Marine Pollution Bulletin 46 (2003) 1150–1155

approximately 3000 m at Durban (D3 and D5), and Barreiro, R., Gonz
alez, R., Quintela, M., Ruiz, J.M., 2001. Imposex,
within 100 m at Knysna (K1 and K2). Relatively strong organotin bioaccumulation and sterility of female Nassarius
reticulatus in polluted areas of NW Spain. Marine Ecology
ocean current systems along the coastline (Field and Progress Series 218, 203–212.
Griffths, 1991) are expected to limit the occurrence of Barroso, C.M., Moreira, M.H., Bebianno, M.J., 2002a. Imposex,
biologically significant TBT contamination outside the females sterility and organotin contamination of the prosobranch
KZN harbours. Nassarius reticulatus from the Portuguese coast. Marine Ecology
The absence of any relationship between imposex and Progress Series 230, 127–135.
Barroso, C.M., ReisHenriques, M.A., Ferreira, M.S., Moreira, M.H.,
shell size of differently affected populations of N. kra- 2002b. The effectiveness of some compounds derived from
ussianus compares favourably with the results for other antifouling paints in promoting imposex in Nassarius reticulatus.
studies. At least one study shows that TBT exposure in Journal of Marine Biology Association UK 82, 249–255.
bivalve molluscs is not correlated with scope for growth Bech, M., Strand, J., Jacobsen, J.A., 2002. Development of imposex
(Widdows et al., 2002). Although the development of a and accumulation of butyltin in the tropical muricid Thais
distinguenda transplanted to a TBT contaminated site. Environ-
vas deferens in females of N. kraussianus was not de- mental Pollution 119, 253–260.
termined, populations showing a high incidence of im- Birchenough, A.C., Barnes, N., Evans, S.M., Hinz, H., Kr€ onke, I.,
posex (R2, D4 and D5) were characterized by either Moss, C., 2002. A review and assessment of tributyltin contami-
lower snail abundances (DJM; pers. obs.) or lower fe- nation in the North Sea, based on surveys of butyltin tissue
male to male ratios (see Table 2), suggesting TBT- burdens and imposex/intersex in four species of neogastropods.
Marine Pollution Bulletin 44, 534–543.
related sterility and female mortality. Any systemic Blackmore, G., 2000. Imposex in Thais clavigera (Neogastropoda) as
effect arising from the local extinction of N. kraussianus an indicator of TBT (tributyltin) bioavailability in coastal waters of
remains unclear, as the functional role of this snail in Hong Kong. Journal of Molluscan Studies 66, 1–8.
these benthic systems is unknown. Bryan, G.W., Gibbs, P.E., Hummerstone, L.G., Burt, G.R., 1986. The
TBT has been shown to accumulate in the tissues of a decline of the gastropod Nucella lapillus around south–west
England: evidence for the effect of tributyltin from antifoul-
variety of marine animals, including nematodes, mus- ing paints. Journal of Marine Biology Association UK 66, 611–
sels, amphipods and fishes (Schratzberger et al., 2002; 640.
Albalat et al., 2002; Chien et al., 2002; Shim et al., 2002; Bryan, G.W., Gibbs, P.E., Burt, G.R., Hummerstone, L.G., 1987. The
Hong et al., 2002; Ohji et al., 2002). Given the potential effects of tributyltin (TBT) accumulation on adult dog-whelks,
toxicity of TBT (Hunziker et al., 2002), its effects on Nucella lapillus: long-term field and laboratory experiments.
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functionally important benthic taxa, such as nematodes, Bryan, G.W., Gibbs, P.E., Burt, G.R., 1988. A comparison of the
deserve further investigation. The Durban and Richards effectiveness of tri-n-butyltin chloride and five other organotin
Bay harbour systems constitute extensive nursery compounds in promoting the development of imposex in the dog-
grounds for pelagic fishes (Harris and Cyrus, 1999), and whelk, Nucella lapillus. Journal of Marine Biology Association UK
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Bryan, G.W., Burt, G.R., Gibbs, P.E., Pascoe, P.L., 1993. Nassarius
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