Abstract: Background: The release of metals is increasing in industrial and urban areas and the impacts thereof are poorly understood. In an attempt to protect areas from anthropogenic impacts, certain areas are declared protected. The assumption thus could be that protected areas are free from the effects of pollutants. The Helderberg Marine Protected Area (HMPA) is situated in an urbanised region of False Bay, Cape Town, South Africa. Although considered a protected area, the question is raised whether metals from the surrounding area are affecting the coastal environment of the MPA. Materials and Methods: The study assessed the concentrations of 8 metals (Al, Mn, As, Mo, Cd, Fe, Cu and Zn) in the water, sediment and mussel Mytilus galloprovincialis. Samples were collected from within the HMPA, at its border (Lourens river) and adjacent to the HMPA (Strand) in August, 2012. Results: The results showed that metal concentrations were higher in the sediment than ambient coastal waters. Furthermore, metal concentrations were higher in mussels than the sediment for As, Mo, Cd, Cu and Fe. Conclusion: The most important result was that mussel Al, Mn, Cd, Cu and Fe concentrations were similar in and adjacent to the HMPA. The results suggested that the environment of the HMPA was exposed to contaminants (such as metals sampled in this study) from areas outside the MPA and management authorities should consider the effects of these and other contaminants in management plans of MPA’s.
INTRODUCTION
Coastal environments are under considerable threat due to the increased pressures of urbanization and industrialization. In southern Africa, the marine environment is considered to be relatively pristine in terms of global standards1,2. However, taking into account the multiple use of areas and increased population growth and development, localised anthropogenic activities in coastal areas may be increasing the habitat destruction and loss of vulnerable ecosystems. To ameliorate these effects, coastal areas are closed and declared marine protected areas. Although closed to the general public, a key question is whether declaration of protected areas are indeed protecting the ecosystems and organisms that are intended to be protected.
The long term release of metals into the coastal and aquatic environment may have negative impacts on the physical and chemical composition of biota, productivity, diversity and abundance3. Metals have different impacts on the environment and species, depending on organismal and system sensitivity to the metals4,5. Therefore, each study site might be influenced differently by metal contamination, based on the sites’ proximity to the sources of contamination and its level of exposure6.
To ascertain the level of metal contamination in the environment is a challenging task to undertake. Not only do metals occur naturally in the environment and integral to biochemical function, they can also occur in various forms of ionic speciation, depending on a host of chemical and physical factors7. Despite these challenges, biomonitoring is used to asses and monitor the levels of contamination in the environment that may be used as an indicator of accumulation and bioconcentration5. The use of biota to assess the quality of a habitat is based on the assumption that some species are more tolerant to chemicals than others and therefore can provide information on the types and level of contamination in the environment4,8,9.
Biomonitoring studies are based on the assumptions that organisms reflect the environmental conditions they live in6,9. Mussels have the ability to accumulate metals directly from the surrounding environment and absorb these into the tissue at levels much higher than that of the existing water and sediment10,11. The mussel, Mytilus galloprovincialis species has been the preferred indicator species for most biomonitoring programmes along coastal environments10-16. Mussels are suitable biomonitor species as they provide important information relating to the levels of heavy metal contamination in the environment through the analysis of the mussel soft tissue (or whole mussel)12. Analysing mussels to indicate areas of elevated metal concentration in mussel soft tissue, water and sediment17 can be useful in identifying and describing the relationship between the concentrations in mussels and the environment18,19.
Coastal and terrestrial based sources of pollution in False Bay and surrounding areas of the bay are the major contributors of contamination in the area20 with coastal ecosystems under considerable stress caused by non-point (maritime transportation) and point source contamination (treated sewage effluent, agricultural, commercial and urban development)21,22. Anthropogenic activities contribute largely to the poor water quality and the loss of sensitive invertebrate species along False Bay23-25.
Contamination discharged into river systems find their way into estuaries and coastal zones, which may result in the accumulation of contamination in the sediment and the bioaccumulation of contaminants in living organisms26,27. A high sensitivity to heavy metal bioaccumulation has been observed in the development stages of bivalves and the increase of metals concentrations at levels above the threshold are often toxic to the organisms28,29. Heavy metal contamination in areas of high anthropogenic activity is increasing to levels much higher than the levels found in the earth crust7. The Cd, Cu, Co, Zn, V and Mn occur naturally in the environment and are important to plant and animal health and the increase in non-essential metals released by anthropogenic activity are polluting the environment at alarming rates7,30.
The HMPA in False Bay, Cape Town (South Africa) was proclaimed in 2000 as a strategy to rehabilitate, conserve and protect a relatively small marine and coastal environment in Cape Town27. The MPA consists of 4 km of sandy beaches on the northern shore of False Bay and is situated between the Eerste river and Lourens river mouth. There are three potential land based pollution sources in and close to the HMPA, namely the Macassar Waste Water Treatment Works (WWTW), SOMCHEM national defence testing facility and the Lourens River and catchment area (urban run-off)31. Little to no information regarding the environmental history of HMPA and the impacts of contaminants from pollution sources and these are inhibiting effective management of the HMPA32,33.
Mytilus galloprovincialis are being used in Mussel Watch Programmes (MWP) by Department of Environmental Affairs (DEA)22 to assess the metal concentrations in False Bay. However, metal contamination in the HMPA has never been monitored33,34. Therefore, establishing a baseline of the metal contamination in and outside the HMPA will assist management authorities in developing a monitoring system to mitigate potential risk of toxic levels of contamination in and outside the MPA. The objectives of the study were to determine the level of metal concentration in the intertidal water, sediment and mussels (Mytilus galloprovincialis) in and outside the Helderberg Marine Protected Area.
MATERIALS AND METHODS
Study area: False Bay (34°06’21.29"S and 18°46’31.27"E) is one of the largest true bays in South Africa31 (Fig. 1). The bay formation is almost square with an approximate dimension of about 35×30 km in length31. The False Bay coastline is largely occupied by human settlement and commercial development activities with numerous small storm water outlets that drain into the bay22,35,36.
Three study sites along False Bay were chosen for the study: the Helderberg Marine Protected Area (HMPA), Lourens river mouth (Lourens) situated at the Eastern border of the HMPA and Strand situated in an urban coastal area approximately 2 km from the HMPA (Fig. 1). The land used at the three sites range from light industrial, agricultural, commercial and residential developments, waste water treatment works and solid waste dumpsites22.
Sampling: Specimens of the mussel Mytilus galloprovincialis (n = 5) were collected at low tide from the three sites in August, 2012. Mytilus galloprovincialis of similar sizes were collected from the three sites at low tide when mussels beds were exposed. On collection the mussels were stored in cooler boxes at the site and transported to the laboratory mussels where the mussels were depurated for 24 h, before being stored in a freezer at -20°C until further analysis. The mussel samples were treated by washing with deionized water, the wet weight, length and width of each mussel sample was measured before the mussels were dried in the oven for 48 h at 60°C37.
| Fig. 1: | Study area and location of sampling sites at the Helderberg Marine Protected Area (HMPA), Lourens river and Strand |
Sediment and water samples (n = 5) were collected simultaneously as the mussels at the three sites. Surface sediment samples were taken at low tide in the intertidal zone, using a pre-cleaned 500 mL plastic sample jar. Water samples were collected at a depth of 30 cm above the sediment, using a 500 mL pre-cleaned plastic sample jars. Water, temperature and pH was measured using an Hanna portable meter. Samples were transported to the laboratory where these were stored at -20°C until further analysis.
Frozen sediment samples were defrosted, where after they were oven dried for 48 h at 60°C in a Memmert drying oven. Sediment was ground with a mortar and pestle and subsamples (±0.2 g) used for metal analysis. Ground sediment aliquots and defrosted water samples (5 mL water) were digested using 10 mL of nitric acid (analar grade 60% HNO3). Samples were then heated to 40°C in a grant UBD heating block for one hour, thereafter to 120°C for 3 h. The digestates were allowed to cool and then filtered through Whatman No. 6 filter paper and then through 0.45 μm membrane micro-filter (Millipore) paper using a syringe. Samples were then placed in plastic centrifuge tubes containing 5 mL digestate and 10 mL distilled water and stored in a refrigerator until further analysis was done.
A blank accompanied all samples when analysis of samples took place. The concentrations of the metals were analysed with 5 replicates being done for each metal using an Inductively Coupled Plasma-Mass Spectrophotometer (ICP-MS), according to the methods of Mdzeke37 and the concentrations of Al, Mn, As, Mo, Cd, Fe, Cu and Fe analysed. Water concentrations of metals are presented as μg L–1 and sediment and mussel tissue as μg L–1 dry weight. Analytical standards (quality control standards) were used for all metals to determine the analytical variation. All metal concentrations were within 2% Relative Standard Deviation (RSD) of the certified concentrations (except for Al which 9% RSD).
The level of metal contamination in sediment is expressed in terms of a Contamination Factor (CF). An equation previously used by Varol38 was used to calculate the contamination factors for each heavy metal at each site39, CF = Metal concentration in sediment/background levels for marine sediment. The background concentrations for the sediment were from concentrations recorded by Hennig40.
The extent of pollution at each site was evaluated using methods based on Pollution Load Index (PLI). The pollution load index is an equation that makes use of the contamination factor39:
PLI = (CFmetal 1×CFmetal 2×CFmetal 3…. ×CFnth metal)1/nth metal
Statistical analysis: Statistical analyses were performed using SPSS 19.0 programme. Metal concentrations in water, sediment and soft tissue of mussels were tested for normality using the Levene’s test and for variance using the Shapiro-Wilke test. Variability of mean data was represented using the Standard Error of the Mean (SEM). Statistical significance differences were assumed at p<0.05.
RESULTS AND DISCUSSION
The coastal water temperatures ranged between 13.80 and 14.10°C with an overall mean of 13.91°C (SEM±0.12°C), with no significant differences recorded between the three sites. These measurements are similar to that previously reported in the study area34. The pH ranged between 6.93 and 7.83 with pH decreasing from Helderberg Marine Protected Area (HMPA) towards Strand. The mean pH at Strand (6.93±0.09) was significantly lower than the HMPA (7.83±0.03) and Lourens river (7.5±0.15), respectively (p<0.05). These pH levels were similar to that measured by Taljaard et al.31 where the average water pH at Lourens river, between 1990 and 1999, ranged between 7.4 and 7.7.
Metal concentrations in the water sampled from all three sites were lower than sediment and mussels (Table 1). Of the three sites, the highest concentrations of metals within the water of the HMPA were reported for 50% of the metals measured: Mn, As, Cu and Zn. The Zn concentrations were 3 times higher than the other two sites sampled with a maximum of 15.31 μg L–1 recorded at HMPA. According to Taljaard22 the waste water treatment and sewage out fall from the urban-industrial areas that discharge directly into False Bay, carry with it a wide range of chemical effluents and pollutants that increase the heavy metal contamination in the bay and may thus be potential sources of metal contamination at the sites sampled.
According to Taljaard et al.31 the monthly inflows from the Lourens river estuary into False Bay increases between May and October with an inflow peak reached between June and August. The high flow rate from the Lourens river into the bay suggests that there is a higher flushing and distribution rate of metals into the bay during these periods of the year. This could account for the relatively lower metals concentrations measured and the Lourens river as sampling took place during August.
Except for Cd, sediment metal concentrations increased from HMPA towards Strand. Concentrations of Mn, As, Cd, Fe, Cu and Zn were lower at the Lourens river than the HMPA (Table 2). Significantly higher (p<0.05) Al, Mn and Fe concentrations were recorded in the sediment than mussels at all the sites sampled (Fig. 2).
| Table 1: | Metal concentrations (μg L–1, n = 5) in coastal water samples collected at the HMPA, Lourens river and Strand |
| <l.d: Below level of detection | |
| Table 2: | Metal concentrations (μg g–1 dry weight, n = 5) in coastal sediment samples collected at the Helderberg Marine Protected Area (HMPA), Lourens river and Strand |
| <l.d: Below level of detection | |
When comparing differences between sites, concentrations of sediment Al, Mn and Fe were significantly lower (p<0.05) at the HMPA than Strand. Both water and sediment metal concentrations were below the sediment quality guidelines proposed for the Benguela region22, indicating that all the sites sampled were not heavily polluted. The elevated Mn and Zn concentrations could be related to the intensity of urban development and the run-off related contamination from surrounding agricultural and urban-industrial activities22,34.
Sediment plays an important role in the transportation of metals across the bay as it influences the amount of metals that are available in the water column and ultimately the bioavailability to filter-feeding organisms34. According to Taljaard et al.31 the hydrodynamics in False Bay is influenced by the shape of the bay and this could have accounted for similar metal concentrations at the HMPA, Lourens river and Strand.
The high coastal water Mn concentrations in the HMPA and Lourens river may be due to the industrial discharge from industrial activities to the north of the HMPA and the Macassar waste water works located to the west of the HMPA37. Due to the constant movement and fluctuation of water currents, majority of the metal concentrations in the water ranged from very low and undetectable levels31. The elevated sediment Mn concentrations at the HMPA may be due to the circular movement of longshore coastal currents along the three sites.
Concentrations of As, Mo, Cd, Cu and Zn were significantly higher (p<0.05) in the mussel M. galloprovincialis than sediment (Fig. 2). As filter feeding organisms, these mussels have the potential to accumulate a significant amount of metals from the ambient environment (water and sediment) as metals are bioavailable to accumulate in mussels30. Of the metals measured in mussels, Cd was higher in the HMPA than the other two sites sampled. The uptake of Cd in the soft tissue of mussels is influenced by the physio-chemical factors such as pH, temperature and the bioavailability of Cd in the environment28.
| Fig. 2(a-h): | Mean (a) Al, (b) Mn, (c) As, (d) Mo, (e) Cd, (f) Fe, (g) Cu and (h) Zn concentrations (μg g–1 dry weight) (M±SEM, n = 5) measured in water, sediment and Mytilus galloprovincialis (soft tissue) at the Helderberg Marine Protected Area (HMPA) Lourens river (Lourens) and Strand, *Indicates that sediment metal concentrations are significantly different from HMPA and #Indicates that mussel tissue metal concentrations are significantly different from HMPA |
| Table 3: | Metal concentrations (μg g–1 dry weight, n = 5) in the mussel Mytilus galloprovincialis collected at the Helderberg Marine Protected Area (HMPA), Lourens river and Strand |
| Table 4: | Sediment Contamination Factors (CF) and Pollution Load Index (PLI) of metals at the Helderberg Marine Protected Area (HMPA), Lourens river and Strand |
| ND: Not determined, Background concentrations based on values from Hennig40 | |
Although the Cd concentrations in mussels were lower than that reported by Sparks et al.2 for the region, the results suggests that anthropogenic sources of Cd could be the cause of elevated Cd concentrations reported in the HMPA and requires further investigation, even though the concentrations were below the recommended limit for shellfish41.
The As, Mo and Cu metals in mussels increased from HMPA to Strand with Cd and Zn decreasing from the HMPA to the Lourens river and then increasing to Strand (Table 3). The Mn concentrations increased from the HMPA to the Lourens river and then decreased towards Strand. The As with the sediment metal concentrations recorded, the increase in metals in mussel (As, Mo and Cu) may be attributed to the coastal dynamics of False Bay31.
Contamination Factor (CF) of metal concentrations in the sediment (except for Al, As and Mo) were calculated at each site (Table 4), using the background levels of metals recorded in False Bay by Hennig40. Contamination factors were highest at Strand for all metals analysed, followed by the HMPA and the Lourens river. Pollution Load Indices (PLI) calculated for the sediment for the three sites is illustrated in Table 4. Categorization of PLI from highest to lowest per site was: Strand>HMPA>Lourens river. The mean PLI results reported here are lower than that reported by El-Sammak and Aboul-Kassim42 where an average of 1.279 was recorded for all the sites sampled. The mean PLI recorded for the three sites sampled in False Bay was 0.99. El-Sammak and Aboul-Kassim42 reported that sites that had PLI’s>1.2 were considered to be affected by pollutants. Given that none of the site PLI values were greater than 1.2, it is suggested that none of the sites samples were negatively affected by exposure to metals and should not be considered polluted based on PLI values. Furthermore, the PLI values are similar to other sites in Cape Town. Relatively though, the PLI of HMPA is higher than the Lourens river, suggesting that, comparatively the HMPA is not protected from coastal metal contaminants. The relatively higher PLI level in the HMPA may be due to the release of industrial effluent to the north of the MPA and domestic sewage from the adjacent Macassar waste water treatment facility31. This postulation however, needs further investigation as the degree of metal released into the environment is influenced by the type, source and quantity of these metals.
CONCLUSION
The research provided an account of metal concentrations in and outside a marine protected in South Africa. The main findings of this study were that metal concentrations were generally not lower inside the MPA as would have been expected, suggesting that coastal dynamics and long shore movement may be responsible for the metal concentrations in the HMPA. Furthermore, metal concentrations in sediment may be related to the settling rates of sediment from surrounding industrial catchment areas and domestic effluent released into False Bay. The elevated metal concentrations in mussels in the HMPA (relative to sediment) suggests bioaccumulation of the metals and requires further investigation.
ACKNOWLEDGMENTS
The research was funded by the Cape Peninsula University of Technology (CPUT) (University Research Fund). We thank the technical staff at CPUT for assistance with collecting samples and laboratory analysis as well as the support from the City of Cape Town and Denel for granting access to the HMPA.