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Environmental Pollution 152 (2008) 636e643 www.elsevier.com/locate/envpol

Heavy metal accumulation in Littoraria scabra along polluted and pristine mangrove areas of Tanzania
H. De Wolf*, R. Rashid
Ecophysiology, Biochemistry and Toxicology Group, University of Antwerp, Groenenborgerlaan 171, B-2020 Antwerp, Belgium Received 21 March 2007; received in revised form 19 June 2007; accepted 24 June 2007

Anthropogenic activities result in heavy metal accumulation and adverse morphological effects in the mangrove gastropod Littoraria scabra.
Abstract The periwinkle Littoraria scabra was collected at polluted and pristine mangrove sites along the Tanzanian coastline, including Msimbazi, Mbweni (i.e. Dar es Salaam) and Kisakasaka, Nyamanzi and Maruhubi (i.e. Zanzibar). Periwinkles were morphologically characterized, sexed and their heavy metal content was determined using ICP-MS. Analysis revealed that L. scabra from polluted areas contained higher soft tissue heavy metal levels, were signicantly smaller and weighed less compared to their conspecics from the unpolluted mangroves. The current morphological observations may be explained in terms of growth and/or mortality rate differences between the polluted and non-polluted sites. Although a variety of stressors may account for these adverse morphological patterns, our data suggest a close relationship with the soft tissue heavy metal content. Compared to soft tissue heavy metal levels that were measured in L. scabra along the same area in 1998, most metals, except for arsenic, chromium and iron have decreased dramatically. 2007 Elsevier Ltd. All rights reserved.
Keywords: Dar es Salaam; Heavy metals; Littoraria scabra; Mangrove; Zanzibar

1. Introduction Intense anthropogenic activities have recently led to the contamination of marine ecosystems (e.g. Langston, 1990; De Kock and Kramer, 1994; Galloway et al., 2002). The occurrence of pollutants in excess of natural loads has become a problem of increasing concern. Indeed, the development of coastal zones throughout the world has put immense pressures on biological communities that inhabit these areas (e.g. Ferletta et al., 1996; Temu, 2001). In Africa this situation has arisen as a result of rapid population growth, increased urbanisation, expansion of industrial activities, exploration and exploitation of natural resources, extension of irrigation and

* Corresponding author. Tel.: 32 3 218 03 47; fax: 32 3 218 04 97. E-mail address: hans.dewolf@ua.ac.be (H. De Wolf). 0269-7491/$ - see front matter 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2007.06.064

lack of nancial resources and environmental regulations (e.g. Mwaguni and Munga, 1997; Temu, 2001). For instance, Tanzania, a developing country on the Western Coast of the Indian Ocean, is experiencing increasing impacts of environmental degradation due to an increased urbanisation and industrialization (e.g. Semesi, 1992; Silima et al., 1994; Mgana and Mahongo, 1997). Its population density and level of industrial activities have markedly increased during the past three decades, converting vast open, once pristine forests and ecosystems into residential or industrial areas (Machiwa, 1992). The latter has resulted in an uncontrolled disposal of domestic and industrial wastes (Machiwa, 1992). Msimbazi river, located in Dar es Salaam, receives for instance untreated wastes from industrial and anthropogenic efuents with average efuent rates of 256 m3/h with peak values of 606 m3/h (Akhabuhaya and Lodenius, 1988; Mgana and Mahongo, 1997). All pollutants such as PAHs, PCBs and heavy metals are taken by the river and accumulate

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in the coastal and mangrove sediments where they pose a threat to the intertidal communities (e.g. Van Brugen, 1990; Machiwa, 1992). The Western Indian Ocean Marine Science Association (WIOMSA) surveys have shown that coastal waters in all major coastal town and cities in Tanzania and the island of Zanzibar are polluted (Van Brugen, 1990; Machiwa, 1992; Ferletta et al., 1996; Engdahl et al., 1998). Mangrove sediments have been shown to have a high capacity to accumulate materials discharged to the near shore marine environment (Harbison, 1986). This is mainly due to the anaerobic as well as rich sulphide and organic matter content that favours the retention of water-borne heavy metals. Subsequent oxidation of sulphides between tides mobilizes the previously trapped metals, increasing their bioavailability (e.g. Silva et al., 1990; Clark et al., 1998; Tam and Wong, 2000). As a result elevated concentrations of heavy metals have been recorded in mangrove sediments, which often reect the long-term pollution caused by human activities (e.g. Lacerda et al., 1992; Perdomo et al., 1999; Harris and Santos, 2000; Tam and Wong, 2000; MacFarlane, 2002; Preda and Cox, 2002). Despite efforts undertaken to evaluate pollution levels in and around Dar es Salaam and the East African coastline in general, very few studies have considered the accumulation of pollutants in and the effect they have on the local marine fauna and ora. Recently, De Wolf et al. (2001) have measured heavy metals in the soft tissue of the gastropod Littoraria scabra along the mangroves of Dar es Salaam. The authors showed that this gastropod accumulated considerable amounts of heavy metals, reecting the pollution sources in the study area. Against this background we want to re-assess the soft tissue heavy metal content in L. scabra along the mangroves of Dar es Salaam and Zanzibar and compare the current metal levels with those that were published in 2001 (De Wolf et al., 2001). In addition we want to investigate the shell morphology of L. scabra and assess potential environmental related adverse morphological effects.
2. Material and methods
L. scabra samples were taken between 10/09/2005 and 12/09/2005 at polluted (i.e. Msimbazi, Maruhubi) and relatively pristine mangrove areas (i.e. Mbweni, Kisakasaka, Nyamanzi) (i.e. Akhabuhaya and Lodenius, 1988; Machiwa, 1992; Basha and Kombo, 1994; Mgana and Mahongo, 1997; Mohammed, 1997; Sesabo et al., 2006) along the coastline of Dar es Salaam and Zanzibar (Fig. 1). From each site 20 specimens were morphologically characterized. Shell height (HS) and width (WS) were measured to the nearest 0.05 mm using calipers, while the total weight (TW) and soft tissues body weight (BW) were determined to the nearest 0.01 mg. The shells of the periwinkles were subsequently broken and the sex was determined based on the presence/absence of a penis using a binocular microscope. Individual soft tissue samples were digested in a microwave oven, adding a mixture (5:1) of nitric acid (70%) and peroxic acid (30%). The digested samples were stored at 4  C until further analysis. Aluminium, arsenic, cadmium, chromium, copper, iron, manganese, lead and zinc were measured in the soft tissue samples by means of inductively coupled plasma mass spectroscopy (ICP-MS), using a Varian spectrophotometer. Analytical efciency was checked using standard reference material (Mytilus edulis, CRM 278R), digested and analysed in the same way as the soft tissue samples. Recovery percentages are given in Table 2.

Fig. 1. Sampling area and sampling sites.

The morphometric characteristics (i.e. TW, BW, HS, WS) were analysed by means of a two way multivariate analysis of variance (2-MANOVA), comparing the xed factor sex and the random factor site and subsequent post hoc sheffe tests. Because of the unbalanced nature of the design (i.e. factor sex, Fig. 1), the type III SS was considered. Means and standard deviations of the morphological data set were used to plot the different sites. Interpopulational differences in metal content, expressed as mg/g dry weight were analysed using individual two way analysis of variance (2-ANOVA) tests, contrasting the xed factor sex and the random factor site. Mean values and standard deviations were plotted and graphically compared to the metal data obtained from 1998 (De Wolf et al., 2001). Finally, the morphological and metal data sets were combined in a canonical discriminant analysis (CDA). The mean values of the rst two canonical roots were subsequently used to plot the study sites in a 2-dimensional graph. The dependent variables that were responsible for the observed patterning among the sites were superimposed as vectors on the 2-dimensional CDA plot. All statistical analyses were performed using the software package, Statistica v. 5.0 and a signicance level of 5% was used throughout.

3. Results The results of a 2-MANOVA for shell height, shell width, total weight and body weight, contrasting the xed factor sex and random factor site are presented in Table 1. Signicant morphological differences were only observed among the sampling sites (Table 1; psite < 0.001). Post hoc testing revealed that L. scabra specimens from Nyamanzi, Kisakasaka

Table 1 Summary of the 2-MANOVA, contrasting the xed effect sex and the random effect site for possible differences in shell morphology Effect Site Sex Site sex Wilks l 0.194 0.913 0.802 F 11.83 2.06 1.25 df1 16 4 16 df2 266.4 87 266.4 P <0.001* 0.093 0.233

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Fig. 2. Mean shell height (SH), shell width (SW), total weight (TW), body weight (BW) and standard deviations for male and female Littoraria scabra collected at the ve mangrove sampling sites.

and Mbweni (i.e. unpolluted sites) were heavier and had on average more elongated and wider shells compared to the specimens that were collected from Msimbazi and Maruhubi (i.e. polluted sites) (Fig. 2). At all sites, female periwinkles were heavier and had more elongated and wider shells compared to the males. Irrespective of the sex, the biggest and heaviest animals were found in the mangroves of Nyamanzi (Fig. 2). The results of the 2-ANOVAs for heavy metal analysis are presented in Table 2. All elements differed signicantly among the sampling sites (Table 2). Of these elements, only chromium and manganese revealed a signicant sex related effect (Table 2). In general no interaction existed between the sites that were analysed and the sex of the individuals. The maximum average levels of aluminium, copper, iron, manganese, lead and zinc were recorded in the soft tissues of the periwinkles that were collected at both polluted mangrove sampling sites (Fig. 3). Indeed, soft tissue levels of these elements differed by a factor 2 (i.e. iron, lead) up to a factor 10 (i.e. copper, manganese) when periwinkles from polluted and

Table 2 Summary of the 2-ANOVA, contrasting the xed effect sex and the random effect site for possible differences in soft tissue heavy metal content (increments and decrements of soft tissue metal levels are visualized by means of increasing or decreasing arrows) and recovery percentages of some elements, obtained by comparison with available standard reference material concentrations Element Site Al As Cd Cr Cu Fe Mn Pb Zn 0.000000* 0.000747* 0.000000* 0.000007* 0.000000* 0.000000* 0.000000* 0.000000* 0.000000* Sex 0.945457 0.858097 0.474941 0.012604* 0.238295 0.921815 0.017145* 0.392165 0.514932 Site sex Msimbazi, Mbweni, % Recovery 1998 1998 0.339936 0.921085 0.775200 0.172883 0.756674 0.640713 0.115316 0.775093 0.494462 n.a. Y Y [ Y Y Y Y n.a. n.a. [ Y Y Y [ Y Y n.a.

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ya

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102.82 89.25 93.53 110.32 92.15

n.a., Data not available.

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Fig. 3. Mean heavy metal tissue levels and standard deviations, expressed as mg/g dry weight.

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unpolluted mangroves were compared (Fig. 3). In contrast, arsenic did not reveal a clear geographical pattern between the mangrove sites, but generally the average soft tissue concentration of this element was very low at all sites (ranging

from 0.69 mg/g to 1.31 mg/g in females and 0.63 mg/g to 1.32 mg/g in males) with Nyamanzi animals showing the maximum concentration of 1.31 mg/g in females and 1.32 mg/g in males. Finally, soft tissue cadmium levels peaked in Maruhubi

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Fig. 3 (continued).

only, while chromium levels were relatively high at all sampling sites (Fig. 3). Compared to 1998, arsenic, cadmium, copper, iron, manganese and lead decreased in the soft tissues of L. scabra that were collected at the polluted mangrove site of Msimbazi, while chromium increased (Fig. 3). A relatively similar pattern emerged at the pristine mangrove site of Mbweni, as all elements, except for arsenic and iron, including chromium decreased as well, compared to the results of 1998 (Fig. 3). The results of the CDA are summarized in Fig. 4. With 69.78% of the variation explained, CV1 is the most important canonical root and is mainly an expression of SH (0.7393), Zn (0.5667), Cu (0.4847), SW (0.3799), Pb (0.3196), Al (0.2204), Mn (0.0779), Cd (0.0276) and Fe (0.0219). Both polluted sites (i.e. Msimbazi and Maruhubi) are discriminated along this root from the remaining unpolluted mangrove areas (i.e. Nyamanzi, Mbweni and Kisakasaka). Hence, periwinkles from the polluted sites are smaller and contain on average higher levels of Cu, Fe, Mn, Cd, Al, Zn and Pb compared to their conspecics from the unpolluted mangroves

(Fig. 4). The second canonical root is far less important, explaining only 17% of the remaining variation and reveals a geographical pattern, discriminating the Zanzibar periwinkles from those that were collected at Dar es Salaam. Unfortunately, since this root reveals so little variation, it is not straightforward to explain the observed geographical patterning in terms of the variables that were included in the CDA. 4. Discussion We clearly noted a signicant shell size difference among the periwinkles from the ve mangrove sites. Indeed, specimens that were collected at unpolluted mangroves had more elongated, broader shells and weighed more, compared to the periwinkles that were collected at the polluted sites. In addition periwinkle densities were clearly smaller at both polluted mangroves compared to the densities that were observed at the pristine sites (pers. obs.). Both observations suggest that living conditions are less favourable in the polluted mangroves, resulting in higher stress levels, compared

en

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1,0 Maruhubi 0,8 TW Cd Fe Zanzibar Dar es Salaam polluted site

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Mn BW As HS

-0,8 -4 -2 0 2 4

CV1 (69.78%)
Fig. 4. Mean values for the rst two canonical variables discriminating the ve mangrove sampling sites based on metal and morphological data.

to the pristine sites. Elevated stress levels and poor living conditions may, indeed, increase the mortality rate in the affected L. scabra populations and may decrease growth rates as well. Hence, periwinkles could die at a younger age or could grow slowly as a result of stress resisting energy allocation effects that limit resource acquisition rates of organisms in the polluted sites (e.g. Koehn and Bayne, 1989; Grime, 1989). The sexual dimorphism that has been detected in this study has previously also been found in other littorinid species (Reid, 1986, 1996). Indeed a statistically signicant dimorphism in shell height has been found in 10 of the 11 species of the genus Littorina in which it has been investigated whereby females were always slightly larger (Reid, 1996). The larger size of females is probably related to their faster growth (Moore, 1937), although greater longevity (Daguzan, 1977) and sexual selection have also been claimed (Erlandson and Johannesson, 1994). Periwinkles can accumulate substantial amounts of metals from their surrounding water or their diet without showing any distinct physiological effect (Bryan et al., 1983; Krolak, 1998). In this study, soft tissue metal levels reected ambient metal levels, as the highest metal concentrations were detected in periwinkles from the polluted mangrove sites. These observations are in line with previous toxicological research that has been performed in the same area in which Msimbazi and Maruhubi came out as heavily metal polluted sites (e.g. Van Brugen, 1990; Machiwa, 1992; Mgana and Mahongo, 1997; Mohammed, 1997; De Wolf et al., 2001) and coincide with the morphological patterns as well. Indeed, periwinkles from polluted mangrove sites are not only smaller and do not only occur a lower densities, but in general contain also higher soft tissue metal levels. Hence, circumstantial evidence suggests a relationship among the pollution status of a mangrove

site, the amount of accumulated metals and shell morphology of L. scabra that inhabits these polluted areas. Although it is difcult to compare the metal concentrations over time, since information on possible intra-annual variation is missing in this species, most tissue metal levels are markedly lower since the last time they were measured in 1998 (De Wolf et al., 2001). This decrease may be due to the realization of (1) a better waste water treatment system, (2) an industrial discharge reduction and (3) an improved industrial solid waste treatment (Whitney et al., 2003; DAWASA, 2000). In specic, improvements have been realized in the water stabilization ponds of Vingunguti, Mabibo, Ubungo, Pugu, Msasani and Mikocheni which are used for the treatment of industrial and domestic wastes before being disposed through the streams into the ocean (DAWASA, 2000; Kjellen, 2006). These actions were imposed as a result of the Tanzanian Governments involvement in the reduction of environmental degradation through the Environmental Management Act (EMA) which is responsible for undertaking environmental enforcement, compliance, monitor environmental impact statements, research and awareness rising. Despite the overall decreasing metal trends, some metals remain high or have even increased in the soft tissues of L. scabra. At Msimbazi this was the case for chromium, while at Mbweni arsenic and iron levels have increased. Although toxicological data from Mbweni are scant, the increase of arsenic and iron, might be related to the dispersal of (1) sediments via currents from Msimbazi (De Wolf et al., 2001) and/or (2) heavy dusts produced by a cement factory located in the direct vicinity (i.e. Wazo Hill) (UNEP/IMS/UDSM/FAO/SIDA, 1998). With respect to chromium, it has to be noted that soft tissue levels of this metal are relatively high at all sites, including the unpolluted mangrove areas of Kisakasaka and Nyamanzi. Hence, it is difcult

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to pinpoint possible sources and explain the current observations. 5. Conclusion In conclusion, metal levels have dropped markedly in the soft tissues of L. scabra, since 1998, possibly reecting governmental actions that were undertaken to protect the environment. Nevertheless, this decreasing trend needs to be conrmed in the future, possible seasonal levels of soft tissue metal variability must be investigated, while the adverse morphological observations and their potential relation with environmental pollution need to be addressed in detail in the future as well.

Acknowledgements This work was supported by a BOF-NOI grant FA070400/ 3/41 of the University of Antwerp. HDW is a Postdoctoral Fellow of the Fund for Scientic Research e Flanders (Belgium) (F.W.O.).

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