biomonitoring of heavy metals using mytilus galloprovincialis in safi coastal waters, morocco

Biomonitoring of Heavy Metals Using Mytilusgalloprovincialis in Safi Coastal Waters, Morocco

Mohamed Maanan

Geolittomer, LETG–UMR 6554, Universite de Nantes, B.P 81227–44312 NantesCedex 3, France

Received 14 December 2006; accepted 5 June 2007

ABSTRACT: Heavy metal concentrations of mercury, cadmium, lead, zinc, cooper, nickel, manganese,and chromium in Mytilus galloprovincialis were investigated to provide information on pollution of Saficoastal area, since these metals have the highest toxic potential. The concentration of Hg and Pb wasdetermined by AFS and ICP-MS methods, respectively, whilst the remaining metals (Cd, Cr, Cu, Mn, Zn,and Ni) were quantified by AAS. High lead, cadmium, chromium, and mercury levels were registered in tis-sue samples collected from two stations near the Jorf Lihoudi and Safi city, while elevated concentrationof manganese and zinc (14.70–25.30 mg kg21 and 570–650 mg kg21 dry wt, respectively) were found inmussel specimens from Cap Cantin. The high levels of nickel found respectively in the areas near theindustrial area being of concern in terms of environmental health need frequent monitoring. The metalconcentrations recorded at the clean stations may be considered as useful background levels to which torefer for comparison within the Atlantic coast. M. galloprovincialis are suitable biomonitors to investigatethe contamination levels of heavy metals pollution face a different human activity in this coastal area ofthe Atlantic coast. # 2007 Wiley Periodicals, Inc. Environ Toxicol 22: 525–531, 2007.

Keywords: Atlantic coast; heavy metals; mussel; anthropogenic input

INTRODUCTION

Metals are a group of the most important pollutants which

cause environmental degradation in coastal areas. Heavy

metals are deemed serious pollutants because of toxicity,

persistence, and nondegradability in the environment. The

importance of heavy metals in coastal environments derives

from both their potential toxic effects and excessive anthro-

pogenic sources which can equal or exceed natural input

(Hyun et al., 2006). Since the early works of Goldberg

(1975) and Phillips (1976), marine mussel are widely used

as bioindicators of heavy metals pollution in coastal areas

because they are known to concentrate these elements, pro-

viding a time integrated indication of environmental con-

tamination. Therefore, contaminants concentrations in the

tissues of bivalves more accurately reflect the magnitude of

environmental contamination. Monitoring programs and

research for metals in the environmental samples have

become widely established because of concerns over accu-

mulation and toxic effects, particularly in aquatic organ-

isms and to humans consuming these organisms (Rainbow,

2002).

Factors known to influence metal concentrations and

accumulation in these organisms include metal bioavaila-

bility, season of sampling, hydrodynamics of the environ-

ment, size, sex, changes in tissue composition, and repro-

ductive cycle (Szefer et al., 2004). Seasonal variations have

been related to a great extent to seasonal changes in flesh

weight during the development of gonadic tissues

(Rainbow, 2002; Szefer et al., 2004).

This study describes a preliminary investigation of the

suitability of the mussel ‘‘Mytilus galloprovincialis’’ as bio-monitors of spatial and temporal variation of heavy metals

in Safi coast.

Correspondence to: M. Maanan; e-mail: mohamed.maanan@univ-

nantes.fr

Published online in Wiley InterScience (www.interscience.wiley.com).

DOI 10.1002/tox.20301

�C 2007 Wiley Periodicals, Inc.

525

MATERIALS AND METHODS

Description of the Study Area

Morocco is one of the countries which give attention to

environmental problems. One aspect is to evaluate the

degree of pollution in the Safi coast, where no previous

studies have been carried out. The sources of heavy metals

are evident in Safi coastal area. The major anthropogenic

sources of heavy metals in Safi coast are industrial and

urban waste, wastewater discharges, and agricultural activ-

ity. This pollution has strong negative impacts on marine

life and on the fishery resources. There are the large indus-

trial complexes around Safi coast. Moreover, several

streams deliver more than 274 000 m3 of wastewater dis-

charges daily into Safi coast. Unfortunately, monitoring

data are lacking in most regions where anthropogenic activ-

ities are well developed. It is now well established that

heavy metals causes reproductive and developmental

adverse effects on a wide diversity of aquatic organisms,

especially on molluscs, at very low concentrations.

Mediterranean mussels (M. galloprovincialis) were col-

lected in the intertidal zone during low tide, from Cap Can-

tin to Tensift estuary at the seven stations (Figure 1):

Station Sa-1 is Cap Cantin. Specimens of M. gallopro-vincialis are attached to the bed rock. Seawater tempera-

ture, pH, and salinity varied between 14.6 and 20.88C, 8.1and 8.36, and 31.4 and 34.8%, respectively.

Station Sa-2 is located in the Lalla Fatna beach. There is

no anthropic activity near this station. In addition, during

summer this beach is the site of intense tourism activities.

Seawater temperature and salinity values were within the

ranges of 14.9–21.28C and 31.6–34.6%, respectively.

Station Sa-3 is situated in the Safi city, neighbour-

ing urban wastewater. Seawater temperature and salinity

values were between 15.4 and 21.48C, and 30.2–34.2%,

respectively.

Station Sa-4 is located is about 2 km North of the indus-

trial area. The water temperature and salinity values are

reported to be of 14.8–21.48C and 31.4–34.3%, respectively.

Station Sa-5 is located in the Jorf Lihoudi near industrial

complex area and wastewater treatment plant. The water

temperature and salinity values are reported to be of 15.4–

25.38C and 28.4–33.8%, respectively.

Station Sa-6 is about 4 km south of the industrial area.

The temperature of water ranged from 14.7 to 21.38C and

salinity values were between 31.1 and 34.3%.

Fig. 1. Study area and sampling locations in the Safi coast.

526 MAANAN

Environmental Toxicology DOI 10.1002/tox

Station Sa-7 is located in the Tensift estuary. There is

agricultural development near this station. Seawater tem-

perature and salinity values were within the ranges of 15.5–

22.68C and 31.1–34.5%, respectively.

Sampling and Chemical Analysis of Molluscs

Approximately, 175 intertidal specimens of M. gallopro-vincialis were gathered from the rocks at low tide in the

natural areas, between August 2004 and May 2005, at the

seven stations in Safi Coast (Sa-1, Sa-2, Sa-3, Sa-4, Sa-5,

Sa-6, and Sa-7). Shell size and shape play a role in indicat-

ing species, but this method is not completely accurate

(Innes and Bates, 1999). In this study, we examined Myti-

lus mussels of similar size, weight, and shape to minimize

species differences in our results (Duquesne et al., 2004).

The average length of mussels used in the study was 4.67

6 0.47 cm.

During mussel sampling, temperature, total salinity

(Model 33 YSI salinometer), and pH (ATC Piccolo HI

1280 pH-meter) were measured in situ.For each sampling, 10 molluscs were pooled together af-

ter a 24 h depuration of their gut content in clean seawater.

The soft parts were dried at 1208C for 24 h, and ground in

an agate mortar for homogenisation. Approximately 1 g of

freeze-dried mussel sample was placed in a Teflon reactor

fitted with a stainless steel carcass. After the addition of

1 mL of Milli-Q water and 6 mL of concentrated Merck

Suprapur nitric acid, the reactor was maintained at 908C for

2 h and at 1308C for other 4 h in an oven. Once the sample

is cold, the volume was adjusted to 25 mL with Milli-Q

water and then transferred to a glass flask. Cd, Cr, Cu, Mn,

Ni, and Zn were determined by atomic absorption spectro-

photometry with an HGA 400 graphite furnace (AAS sys-

tem Analyst 800 of Perkin-Elmer 5000, with Zeeman cor-

rection) and Pb was determined using an inductively

coupled plasma-mass spectrometer (Perkin Elmer). For the

determination of total mercury, the technique of cold

vapour was used, employing a Perkin-Elmer FIAS system

coupled to a spectrophotometer, using a reducing dissolu-

tion of SnCl2 in HCl. All the analyses have been performed

within the updated rigorous quality control system of the

laboratory, which guarantees the performance of all the

results produced (Hatch and Ott, 1968). Quality assurance

was assessed using lobster hepatopancreas TORT-2

(NRCC) as reference materials provided by the National

Research Council of Canada. These standards were treated

and analysed under the same conditions as the soft tissue

samples, and recoveries of mercury ranged from 97 to

102% and for other elements ranged from 92 to 108%. The

detection limits were (mg kg21 dry wt): 0.8 (Cd), 0.8 (Cu),

0.8 (Cr), 0.8 (Mn), 0.005 (Hg), 0.8 (Pb), 0.8 (Ni), and 1.7

(Zn). Heavy metal concentrations in soft tissue of mussel

are also reported in mg kg21 dry wt.

Statistical Analysis

Statistical analysis was carried out using STATISTICA

(StatSoft, 1995). ANOVA was used to test the influence of

season and location on element concentrations in mussel.

RESULTS

The interspatial and interseason concentrations of Cd, Pb,

Hg, Cu, Cr, Zn, Mn, and Ni in the soft tissue of M. gallo-provincialis are presented in Figure 2. Concentrations of all

the analysed metals are expressed in mg kg21 dry wt.

The soft tissue concentrations in the Safi coast mussels

were on average 9.92 (Cd), 10.75 (Pb), 0.70 (Hg), 17.04

(Cu), 11.53 (Cr), 249.25 (Zn), 15.54 (Mn), and 19.24 (Ni).

The highest values of tissue Cd, Pb, Hg, Cu, Cr, Zn, Mn,

and Ni concentrations were recorded near industrial area.

As can be seen in Figure 2, the soft tissue concentrations

of heavy metals such as Zn, Hg, Ni, Pb, Cr, Mn, and Cd in

Mytilus from Safi coast collected in spring were generally

higher than those collected in autumn. This was probably

connected with heavy rain in spring period and conse-

quently with higher load of eroded material from the land

enriched in heavy metals.

DISCUSSION

Safi coast characterized by the highest levels of almost all

metals analyzed is located in a heavily industrialised and

populated area. For a long period it has received heavy met-

als from industry located within the catchments area. Metal

bioaccumulation in this study, showed that bioavailability

highly depends on seasonal, meteorological, oceanographic

characteristics, and anthropic inputs (industrial, urban, and

agricultural) (Rainbow et al., 2000; Casas and Bacher,

2006).

As regards geographical variation in the bioaccumula-

tion of heavy metals in the Safi coast in 2004–2005, the

mussel data showed up variation between seven stations for

Cd, Cr, Hg, Cu, Zn, Ni, and Pb, but not for Mn.

Although variability was quite high from mussel to mus-

sel, the highest concentrations of Cd, Cu, Cr, Mn, and Pb

were consistently found at the station Sa-6 (4 km in the

south of phosphate industry effluents). In addition, higher

Hg levels were found in mussels at the Safi urbane sewages,

and higher Ni levels were found near the phosphates indus-

try effluents. Spatial distribution of bioaccumulation of

metals is in the accordance with the prevailing circulation

of water mass in the Atlantic Moroccan coast where the

main swell direction is north-south.

The concentrations of Ni in M. galloprovincialis variedamong the sampling sites with the ratios of the highest to

the lowest values being 11.7–31.7. Higher concentrations

527BIOMONITORING OF HEAVY METALS USING M. GALLOPROVINCIALIS


of Ni were mainly recorded near the phosphates industry

effluents (16.3–31.7 mg kg21) and Safi city station (17.4–

27.3 mg kg21); significantly lower values were obtained

from Lalla Fatna beach (14.1–18.5 mg kg21).

The concentrations of Cr ranged from 1.9 to 28.9

mg kg21 for all sites during the study period. Both the high-

est (16.58–28.9 mg kg21) and the lowest (1.9–4.2 mg kg21)

Cr concentrations were recorded at 4 km in the south of

phosphates industry effluents and Lalla Fatna beach,

respectively.

M. galloprovincialis from different sampling sites

showed a wide range of accumulated Cu concentrations

with the ratios of the highest to the lowest values being

4.1–43.1. Higher levels of Cu were mainly recorded at Safi

station (14.5–43.1 mg kg21), 4 km in the Southern waters

of industrial area (18.5–38.86) and Cap Cantin station

Fig. 2. Seasonal variations in trace metal concentrations (mg kg21 dry wt) inMytilus gallo-provincialis from Safi coast in the period from August 2004 to May 2005.

528 MAANAN


(14.2–30.4 mg kg21) during the study period. The anthro-

pogenic sources of copper include its use as an antifouling

agent in paints, agriculture, and animal and human excreta

(animal manure and human sewage sludge).

The concentrations of Zn in M. galloprovincialis variedslightly among the study sites with the ratios of the highest

to the lowest values being 107.4–365.78 during the study

period. This indicates that the spatial distribution of this

metal in Safi coastal waters was fairly uniform. Slightly

higher concentrations of Zn were found at Essaouira Laq-

dima (265.6–318.2 mg kg21) and Cap Cantin station

(210.7–350.4 mg kg21) in relation with development of ag-

ricultural activity, whereas lower values were recorded at

Lalla Fatna beach (107.4–221.5 mg kg21). Levels of Zn in

the sediments were high, but Zn occurs naturally in the

environment and may come from background levels in the

sediments.

The concentrations of cadmium in M. galloprovincialisvaried among sites with the ratios of the highest to the low-

est values being 2.12–34.71 mg kg21. Higher values were

recorded at 4 km southern of industrial area (12.68–34.71

mg kg21); whereas lower values were obtained from Lalla

Fatna beach (2.3–3.2 mg kg21). Cadmium is a natural con-

stituent of rock phosphates and deposits from some regions

of the world contain markedly elevated levels of the metal.

The manufacture of phosphate fertilizer in Jorf Lihoudi

results in a redistribution of the cadmium in the rock phos-

phate between the phosphoric acid product and the gypsum

waste (Cheggour et al., 1999). The other sources of cad-

mium are industries that employ thermal processes, e.g.,

cement manufacture; all release airborne cadmium, the

metal being a natural constituent of the raw materials.

The concentrations of lead recorded at all sites ranged

from 0.1 to 26.45 mg kg21 during the study period. The

major sources of lead in the environment, of significance to

living organisms, arise from lead mining and the refining

and smelting of lead and other metals. Besada et al. (2002)

proved that the anthropogenic emissions in Spanish North-

Atlantic coast of this metal are due to the consumption of

leaded gasoline, as well as to the low or nonexistent treat-

ment of urban and industrial sewage. Although large

amounts are probably also discharged into soil and water,

lead tends to localize near the points of such sewage dis-

charge ‘‘Jorf Lihoudi and Safi’’.

The mercury concentrations varied among sites with the

ratios of the highest to the lowest values being 0.01–2.31

mg kg21. Significantly higher values of mercury were

recorded at Safi city station (0.58–2.31 mg kg21) and at 4

km southern of industrial area (0.97–2.12 mg kg21) during

the study period; whereas the lower concentrations were

recorded at Lalla Fatna beach (0.01–0.12 mg kg21). The

high-pH water as well as the low organic matter content of

the sediment does not favour the methylation of mercury.

In addition, bioconcentration and bioaccumulation factors

are relatively low compared to other aquatic systems

(Nguyen et al., 2004). Many parameters may affect the

mercury accumulation: such as specimen size, sexual matu-

rity, sensitivity to seasonal, feeding habits, trophic position,

water quality, and environmental contamination (Szefer

et al., 2004).

The concentrations of Manganese in M. galloprovincia-lis varied among sites with significant differences between

sites. The ratios of the highest to the lowest values among

sites were 7.2–27.5 during the study period. Significantly

higher concentrations of Manganese in were obtained from

Cap Cantin (14.7–25.3 mg kg21); whereas lower values

were recorded at 3 km north of industrial area (7.2–10.5 mg

kg21). A crustal origin was more apparent for Mn; a rough

estimate of the average concentration of manganese in the

earth’s crust is about 1000 mg kg21 (NAS/NRC, 1973).

The tissue concentrations of this metal in mussels were

quite elevated in stations close to the mouths of estuaries

and remarkably low in typical urban areas distant from

these points. These results are in close agreement with other

Moroccan studies indicating that Mn is an excellent tracer

of continental inputs into aquatic systems produced by the

breaking up of rocks and soils of surrounding watersheds

(Maanan et al., 2004).

Metal concentrations in mussel tissue showed seasonal

cycles, with minima in winter. Depending on the station,

these cycles were more or less developed and regular. This

is in agreement with the results of Mubiana et al. (2005)

where a marked spring peak was observed for several met-

als in soft tissues.

The seasonal distribution of heavy metal accumulation

explicitly reveals that the organisms are differentially selec-

tive. Seasonal variation in heavy metal concentrations

showed that there was a rise in these metals concentrations

during the spring period which is probably connected with

drainage of the soil. Statistical analysis (one-way ANOVA)

indicated that for all heavy metal, the station effect is more

significant than season effect. These results show the strong

of pollution impact in the sampling stations what decreases

the seasonal effect.

The present results are concordant with those of other

studies performed for areas along the Atlantic coast (Chafik

et al., 2001; Banaoui et al., 2004), in El Jadida coast

(Maanan, in press) Casablanca-Mohamedia (Bouthir et al.,

2003), in Agadir bay (Moukrim et al., 2000). Heavy metal

concentrations from this study were compared with those of

other open and coastal areas of the world ocean. The values

obtained here are comparable to those attributed to the

most industrialized areas.

Table I shows that the levels of Cd and Pb in the mussels

collected from Safi coastal waters (9.92, and 10.75 mg

kg21, respectively) were lower than Baltic Sea coastal

waters (33 and 13.4, respectively); whereas the levels of Hg

(0.7) and Cu (17.04) were found to be higher than those

obtained from Spanish Atlantic coast (0.11–0.61 and 5.33–

7.2, respectively).



TABLEI.

Comparisontracemetalconcentrationsin

marinebivalvesobtainedin

this

studywithliterature

data

from

theMoroccanand

otherregionalloverworld(m

gkg21dry

wt)

Region

Year

Zn

Cu

Cd

Mn

Ni

Hg

Cr

Pb

Reference

Safi

coastalwaters,Morocco

(M.ga

llop

rovincialis)

2004–2005

107.4–365.7

4.1–43.1

2.12–34.71

7.2–27.5

11.7–31.7

0.01–2.31

1.9–28.9

0.1–26.45

Presentstudy

ElJadidacoast,Morocco

(M.ga

llop

rovincialis)

2004–2005

112.6–612.3

4.35–142.2

1.33–25.3

8.74–34.8

12.70–94.3

0.02–2.3

3.97–20.6

0.50–34.2

Maanan,in

press

HongKongwaters

(Perna

Viridis)

1998–2003

67–170

8.9–130

0.17–2.9

0.3–63

2.0–20.0

Liu

andKueh,2005

Korean

waters

(M.ga

llop

rovincialis)

1998–1999

70.3–157

3.93–13.6

0.06–2.36

6.8–227

0.02–0.07

3.62–52.7

Szeferetal.,2004

Goro

Bay,Italy

(M.ga

llop

rovincialis)

62.9–154.7

9.4–21.2

3.7–4.3

3.5–9.7

0.167–0.231

2.3–10.5

15.8–29

Locatelli,2003

Macau,Brazilcoast

(Crassostrea

rhizop

horae)

1998

233–1400

21.3–281

2.5–5.0

13–56.7

0.9–5.7

Silvaetal.,2003

SpanishNorthAtlanticcoast

(M.ga

llop

rovincialis)

1991–1999

176–316

5.33–7.2

0.46–1.40

0.11–0.61

0.9–3.0

Besadaetal.,2002

Western

Anatolia,Turkey

(M.ga

llop

rovincialis)

1999–2000

117–423

7.4–52

17–63

Uguretal.,2002

Moroccan

Atlanticcoastalwaters

(M.ga

llop

rovincialis)

1993–1999

117–379

6.6–73.5

0.4–8.0

Chafiketal.,2001

MuguLagoon,LosAngeles,USA

(M.ga

llop

rovincialis)

1995

756

23

5.8

61.8

0.906

0.4

116

3.3

176

5.5

0.86

0.4

Cohen

etal.,2001

Balticsea(M

.trossulus)

1998

1846

45

336

7.2

22.2

60.8

2.96

0.6

13.46

2.2

Rainbowetal.,2000

530 MAANAN


Author gratefully acknowledges two reviewers for their critical

scientific suggestions and comments; I appreciate their effort in

bringing the text to a publishable state.

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biomonitoring of heavy metals using mytilus galloprovincialis in safi coastal waters, morocco

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