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Influence of diffuse and chronic metal pollution in water and sediments onedible seafoods within Ondo oil-polluted coastal region, NigeriaIsaac A. Ololadea; Labunmi Lajideb; Victor O. Olumekunc; Olusola O. Ololaded; Benjamin C. Ejelonua

a Department of Chemistry and Industrial Chemistry, Adekunle Ajasin University, Akungba-Akoko,Ondo-State, Nigeria b Department of Chemistry, Federal University of Technology, Akure, Nigeria c

Department of Plant Science and Biotechnology, Adekunle Ajasin University, Akungba-Akoko, Ondo-State, Nigeria d Department of Geography, Environmental Management and Energy Studies, Faculty ofScience, University of Johannesburg, Johanesburg, South Africa

First published on: 16 June 2011

To cite this Article Ololade, Isaac A. , Lajide, Labunmi , Olumekun, Victor O. , Ololade, Olusola O. and Ejelonu, BenjaminC.(2011) 'Influence of diffuse and chronic metal pollution in water and sediments on edible seafoods within Ondo oil-polluted coastal region, Nigeria', Journal of Environmental Science and Health, Part A, 46: 8, 898 — 908, First publishedon: 16 June 2011 (iFirst)To link to this Article: DOI: 10.1080/10934529.2011.580208URL: http://dx.doi.org/10.1080/10934529.2011.580208

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Journal of Environmental Science and Health, Part A (2011) 46, 898–908Copyright C© Taylor & Francis Group, LLCISSN: 1093-4529 (Print); 1532-4117 (Online)DOI: 10.1080/10934529.2011.580208

Influence of diffuse and chronic metal pollution in waterand sediments on edible seafoods within Ondo oil-pollutedcoastal region, Nigeria

ISAAC A. OLOLADE1, LABUNMI LAJIDE2, VICTOR O. OLUMEKUN3, OLUSOLA O. OLOLADE4

and BENJAMIN C. EJELONU1

1Department of Chemistry and Industrial Chemistry, Adekunle Ajasin University, Akungba-Akoko, Ondo-State, Nigeria2Department of Chemistry, Federal University of Technology, Akure, Nigeria3Department of Plant Science and Biotechnology, Adekunle Ajasin University, Akungba-Akoko, Ondo-State, Nigeria4Department of Geography, Environmental Management and Energy Studies, Faculty of Science, University of Johannesburg,Auckland Park Campus, Johanesburg, South Africa

The bioconcentration levels of 3 non-essential elements (Pb, Cd and Ni) have been investigated in three different seafoods; Fish(Tilapia zilli), Crab (Callinectes sapidus) and periwinkle (Littorina littorea), to investigate the ecosystem health status in Ondo oil-polluted coastal region, Nigeria. The seafood samples were chosen based on their popularity as a food source and the potential of thespecies to contain high levels of metals based on past research results. Metal concentrations in the biota showed marked interspecificdifferences with C. sapidus recording the highest concentrations of all the metals. The bioconcentration factor (BCF) showed thatC. sapidus and T. zilli have the greatest potential to concentrate Cd (BCF = 3–10) and Pb (BCF = 11–84) respectively. Lead uptakefrom both water and sediment (BCF ≈ BSAF: 0.003–0.018) were abysmally low in L. littorea as compared with other organisms.The high concentrations of Pb in fish species, effective bioaccumulation of Cd in species of crab and periwinkles, as well as very highBSAF of Ni found in species of crab indicated a strong influence from anthropogenic pollutant source on the biotic community. Oilpollution appears to be a major source of bioavailable metal contaminants for the selected biota. The study shows that C. sapidus andL. littorea can effectively compartmentalize potentially toxic metals such as Cd, Pb and Ni within their tissues. In terms of toxicity,C. sapidus had Cd concentrations greater than the 3,000 ng/g limit set by the Commission of the European Communities while Pbconcentration exceeded their limits in both C. sapidus and T. zilli. All levels of Ni were below the U.S. Food and Drug Administrationaction levels for these metals in fish, crustaceans and shellfish. The study revealed anthropogenic enrichment of the metals studiedwhich can possibly pose potential threats to the ecology of the area.

Keywords: Heavy metals, contaminants, bioaccumulation, seafoods, bioconcentration factor, indicator species.

Introduction

Trace metals are both extremely toxic and ubiquitous innatural environments.[1] These metals can entire aquaticorganisms either from natural or through anthropogenicsources. Once trace metals enter the food chain, theymay accumulate to dangerous levels and be harmful tohuman health.[2] However, subsequent tissue and bodyconcentrations of accumulated trace metals can show enor-mous variability across metals and invertebrate taxa.[3–5]

Address correspondence to Isaac A. Ololade, Departmentof Chemistry and Industrial Chemistry, Adekunle AjasinUniversity, Akungba-Akoko, Ondo-State, Nigeria; E-mail:olisa 200@yahoo.comReceived December 1, 2010

Consequent upon the dangers associated with toxic metalsin food, several agencies and organizations throughout theworld such as the United State Food and Drug Admin-istration (US FDA) and the World Health Organization(WHO) have provided guidelines and recommendationsconcerning the risk for the intake of trace elements fromfood.[6,7]

Fish and shellfish are good bioindicators of trace ele-ment contamination in the marine environment since theyoccupy different trophic levels and can display large bioac-cumulation factors.[8] Bioconcentration factors (BCFs) andbiota to sediment accumulation factors (BSAFs) have beenemployed to quantify the bioaccumulation of environ-mental pollutants in aquatic biota with the assumptionthat organisms achieve a chemical equilibrium with re-spect to water and sediment as route of exposure, re-spectively.[9] The accumulation of trace metals in aquatic

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Chronic metal pollution in coastal Nigeria 899

organisms is a function of several independent variables,such as (a) the environmental concentrations of metals inwater and sediments; (b) the species of organisms; and(c) body size, age and feeding habits of organisms.[51011]

Some other studies have shown that seasonal variationmay affect accumulated trace metal concentrations.[12,13]

In the present study, attention was focused on the gen-eral trace metal burden using whole meat tissue and noton different organs as reported in some of the stud-ies stated above. However, some key physiological mea-surements were made in order to analyze the trend inconcentrations.

Aquatic organisms in the Ondo Coastal Region (OCR),Nigeria, are one of the most important sources of seafoodparticularly for people in the Oil Producing Delta (OPD)region and the nation in general. However, human activi-ties are indirectly causing the slow extermination of impor-tant, economic animal species within this region through oilpollution. Considering the unregulated and continuous oilspillage into the OCR and the dependence of human pop-ulation on aquatic resources from this region, it becamenecessary to investigate and determine sea foods suitabil-ity for human consumption. Unfortunately, scientific dataon important metals of priority pollutant list of UnitedState Environmental Protection Agency (US EPA) on biotafrom OCR are either non-existing or unreported despite thehuge and growing economy, especially in fishing in recenttime.

Our previous studies on the assessment and monitoringof oil pollution impact (heavy metals and hydrocarbons)within OCR have concentrated, so far, on surface waterand sediments.[14–17] The status of some essential elementswithin the aquatic biota has also been reported.[18]

To further substantiate possible damage the oil spillmight have caused, three important metals of prioritypollutant list of United States Environmental ProtectionAgency (US EPA) and petroleum related (Pb, Cd andNi) were investigated in the present study.[19] Cadmiumis highly toxic to the kidneys and has been found inseafood, with the highest concentrations in crustaceansand mollusks.[20] Lead is a neurotoxin that has beenresponsible for the lowering of children’s IQs; lead levelstend to be higher in large predatory fish, crustaceans, andmollusks.[20]

The present work aims to examine the potential of threemarine species: fish (T. zilli), crab (C. sapidus) and peri-winkle (L. littorea) as biomonitors of Pb, Cd and Ni inrelation to that of surrounding water and sediments as ear-lier reported.[14–16] The biological empirical approach inthe present study would be limited to metal levels in tissueswhile bioaccumulation tests and toxicity tests will formthe basis of future investigation.[19] In addition, the studyequally hopes to determine the extent of tissue damageand consequently the suitability of the species for humanconsumption.

Materials and method

Study area

The study area has been described in our previous re-ports.[14–17] Briefly OCR is one of the most productive areasin Nigeria for fishing, both commercially and recreationally.Ten villages of approximately 2km apart were consideredin this study as indicated in Figure 1.

Sampling

The samples were collected at two different seasons; dryseason (December in 2004) and wet season (April in 2005).A global positioning system (GPS) was used to establishthe exact location of each site. The fish, T. zilli, was con-sidered in this study for two reasons; being a common,migratory species that are consumed almost on daily basisand as a smaller resident specie with small home rangesthat are consumed by bigger fish. Two other shellfish, theblue crab, C. sapidus, and a mollusk periwinkle, L. littorea,were also obtained for tissue analysis. The fishes were ob-tained with nets, aided by local fishermen while others werepicked randomly from their various habitats along the riverbank. All the samples were thoroughly washed with the seawater, placed in labeled polythene bags using latex glovesto prevent contamination, and then covered with ice inan ice chest. All the samples were freeze dried on arrivalinto the laboratory. This freezing process euthanized thesamples and prevented spoilage until sample preparation.Water and sediment samples were also collected at eachsampling point during the two seasons. The results havebeen reported.[14–16]

Sample preparation

The lengths of the fishes and the shell lengths of the peri-winkles were individually measured before they are groupedand pooled for metal analysis. The fish were analyzed whole(excluding stomach content) while the soft part of theperiwinkles was obtained by cracking the shells. Severalsamples were pooled to provide the required weight for di-gestion in duplicate. Whole crab was used in the study with-out separating the tissues since people generally consumeevery part. The mean soft body weight for each samplewas determined while the water content (% moisture) wasobtained after drying at 80◦C for 24 h (for fish and periwin-kles) and 48 h (for crab) based on literature guidance.[10] Thedried samples were ground homogeneously and stored in adessicator prior to undergoing further chemical analyses.

Metal analysis

Lead, Cd and Ni were determined with 2.0 g of finelyground tissue samples homogenized with 25 mL of

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900 Ololade et al.

State and Local Govt Boundary

Local Govt. Headquarter

Major Towns

Major Roads

RiversSampling Locations

N I G E R I A

ABUJAOndoState

AFRICA

5 00 E4 30 E 4 45 E

OGUNSTATE

OKITIPUPA LGA

IRELE LGA

EDOSTATE

-Ayetoro

Awoye

Igbekoda

0 1 2 Km

6 30 N

6 15 N

6 00 N

5 45 N

GULFOF

GUINEA

S-5

∆∆--DD

∆-F

∆-C

∆-H∆-G

∆-E

∆-B

Fig. 1. Map of the sampling locations (Inserted is the area map of Nigeria and Africa showing the geographical locations). (colorfigure available online)

de-ionized water after 10 mL of concentrated HCl and2 mL of HNO3 (Merck, HNO3 65%, GR for analysis) insuccession. The mixture was heated and boiled off to neardryness, given a thick yellow liquid. However, for sam-ples of crab, additional 25 mL of H2O2 (Fisher Biotech,H2O2 30% in Water) was added before digestion was com-pleted. All digested samples were filtered through WhatmanNumber 42 filter papers into 50.0 mL volumetric flasksand rinsed thrice with de-ionized water. The solution wasthen transferred to a 60 mL sample bottle and stored at−4 ◦C until metal determination. Metals concentrationswere analyzed using flame AAS (Alpha 4AAS, ChemicalTech. Analytical, Euro). Detection limits in the digestedsamples were 0.002 µg/g for Cd, 0.004 µg/g for Pb and0.001 for Ni. All the metal concentrations were expressedon a dry weight basis. Results were determined in mg/L(parts per million) and converted into mg/kg as follows:mg/L × 50 mL/sample weight.

Quality control

All chemicals used were of analytical-reagent grade. Stocksolutions of 1000 µg/mL (ppm) were used to prepare cal-ibration standards. At the time of the study, there were nobiota reference materials available. Consequently, reagent

blanks and internal standardization were used as controlmeasure. Dilutions of standards were made where neces-sary to ensure it fitted the calibration curve. The recoveriesof the 3 metals spiked at 10 times the approximate detectionlimit gave recoveries from 90–96%. In addition, sedimentPAC-2 SRM was used during sediment analysis. The re-covery rates for the metals in the reference materials werearound 79.5 to 92.4%.[15]

Bioconcentration factors (BCF) and sediment biotaaccumulation factor (SBAF)

The surface waters and sediments were analyzed at eachsampling station for the three metals as determined in thebiota. These results have been reported,[14–16] and the datafor trace metals were used in this report to calculate BCFand BSAF.

Statistical analysis

All data analysis was carried out using SPSS for windows13.0 version with significance level p < 0.01 and 0.05. Forthe statistical analyses, two-way ANOVA was conducted to

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Chronic metal pollution in coastal Nigeria 901

Table 1. Biological data on Biota sampled from OCR, Nigeria∗.

Code Locations Species No of Samples MWW a (g) Moisturea (%) MLa

A Ayetoro C. sapidus 4 24.3 ± 1.7 59.8 ± 2.1 –T. zilli 6 118.7 ± 1.4 74.8 ± 4.3 8.1 ± 1.7L. littorea 10 9.5 ± 1.2 78.1 ± 2.4 2.4 ± 0.9

B Asumaga C. sapidus 4 29.3 ± 2.3 53.4 ± 2.6 –T. zilli 5 116.4 ± 2.4 71.1 ± 4.1 9.2 ± 1.3L. littorea 10 8.5 ± 1.7 71.4 ± 2.0 3.1 ± 1.7

C Ilepete C. sapidus 5 43.7 ± 2.4 59.1 ± 1.4 –T. zilli 5 126.7 ± 8.9 76.4 ± 2.8 11.8 ± 1.1L. littorea 10 8.8 ± 2.1 69.4 ± 1.6 2.8 ± 1.3

D Obe Nla C. sapidus 4 54.7 ± 0.9 60.3 ± 2.2 –T. zilli 6 110.2 ± 8.6 72.6 ± 3.9 7.0 ± 0.3L. littorea 10 9.2 ± 3.3 76.4 ± 2.5 2.8 ± 1.9

E Ikorigho C. sapidus 5 54.7 ± 10.3 57.8 ± 2.3 –T. zilli 6 93.7 ± 10.3 69.1 ± 3.2 11.9 ± 1.3L. littorea 10 8.1 ± 3.6 74.2 ± 3.3 3.2 ± 1.1

F Ojumole C. sapidus 4 54.1 ± 1.9 58.9 ± 2.2 –T. zilli 5 120.4 ± 2.4 76.1 ± 4.3 11.2 ± 1.8L. littorea 10 10.5 ± 1.5 78.4 ± 3.1 3.7 ± 1.2

H Otumara C. sapidus 4 52.4 ± 1.4 61.2 ± 3.2 –T. zilli 6 128.4 ± 4.7 80.2 ± 4.3 12.0 ± 2.1L. littorea 10 10.9 ± 2.2 78.2 ± 2.9 3.8 ± 1.1

J Odofado C. sapidus 4 50.9 ± 1.9 59.8 ± 2.4 –T. zilli 6 122.6 ± 4.8 76.3 ± 4.7 11.4 ± 1.5L. littorea 10 10.2 ± 2.4 79.1 ± 3.3 3.7 ± 0.9

K Awoye C. sapidus 5 52.7 ± 1.6 60.3 ± 2.6 –T. zilli 6 125.7 ± 7.4 78.4 ± 3.9 11.6 ± 1.9L. littorea 10 9.9 ± 1.8 79.2 ± 3.2 3.7 ± 1.2

∗Adapted from Ololade et al.[18]

amean ± standard deviation; C: crab; F: fish and P: periwinkles; ML: mean length.MWW: mean wet weight.

assess the differences in metal concentrations with regardto locations and species variability.

Results and Discussion

Biota characteristic features

Details of some characteristic features of the biota exam-ined are presented in Table 1. The mean wet weight (ing) across the study areas varied between 24.3 to 54.7 forC. sapidus; 93.7 to 126.7 for T. zilli and 8.1 to 10.5 forL.littorea. The percent moisture was very high ranging be-tween 53 to 61% in C. sapidus and approximately between69 to 80% for T. zilli and L. littorea. The hard nature of theshells of crab could probably be responsible for the leastpercent moisture reported in the study. The mean length(in cm) which was only possible for T. zilli and L. littoreashells showed a range between 7.0 to 12.0 for T. zilli and2.4 to 3.8 for L. littorea. The mean wet weight of the sam-ples was much higher in T. zilli compared with the otherorganisms. This may be attributed in parts to the habitatnature of the organisms. Fish in general spend all their

lives in water unlike periwinkles and crab that can survivetemporarily without water around them. Only Pb concen-trations in C. sapidus appears to be significantly correlatedwith mass (r = 0.843, p < 0.05) (Figs. 2a–2c). Weak cor-relations were also reported between Cd in C.sapidus (r =0.753) and L.littorea (r = 0.752). The data showed thatthe small amounts of variability attributable to mass arenot significant compared to overall inherent variability. Ina number of gastropod species, metal concentrations havebeen found to be statistically independent of mass.[21]

Trace metal concentrations of the aquatic organisms

The Pb, Cd and Ni concentrations of T. zilli, C. sapidusand L. littorea collected within the OCR are summa-rized in Table 2. Across the two seasons, Cd concentrationranged between 3.04 to 29.39 mg/kg in C. sapidus, 0.57 to2.54 mg/kg in T. zilli and 0.64 to 2.91 mg/kg in L.littorea.Average concentration in Ni, however, ranged between 0.10to 6.90 mg/kg in C. sapidus, 0.50 to 1.80 mg/kg in T. zilliand 0.20 to 4.10 mg/kg in L.littorea. The average level ofthe non-essential metal, Pb, in the tissues of C. sapidusand T. zilli were relatively close (28.71 ± 0.48 mg/kg) but

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902 Ololade et al.

T. zilli

0

10

20

30

40

50

200150100500Sample wet weight (g)

Co

nc

(mg

/kg

)

Ni

Cd

Pb

Pb: R 2=0.2247Ni: R 2=0.0671

Cd: R 2=0.3295

L. littorea

0

1

2

3

4

5

151050

Sample wet weight (g)

Co

nc.

(m

g/k

g) Cd

Ni

Pb

Pb:R 2=0.019

Ni:R 2=0.349

Cd:R 2=0.566

C. sapidus

0

10

20

30

40

50

1007550250Sample wet weight (g)

Co

nc.

(m

g/k

g)

Cd

Pb

NiNi:R 2=0.204Cd:R 2=0.567Pb:R 2=0.711

Fig. 2. Correlation plots of sample weight and tissue metal con-centrations using data from all sites and seasons (p = 0.05). (colorfigure available online)

about 260 fold greater than the mean concentration of Pbin L.littorea (0.11 ± 0.08 mg/kg). This demonstrates theirsuitability as better indicator for Pb than L. littorea.

Trace metal concentrations in species collected for thisstudy followed the general trend crab > periwinkle > fish.The interspecific differences in concentrations for the samemetals are expected trend as earlier noted. The differ-ences are attributable, at least in part, to assimilation andmetabolism differences among species.[22] Thus, except Pb,other metals concentrations in fish from OCR were lowerthan those in crab and periwinkle; being species with morerestricted geographic ranges and feeding habits.[23] In ad-dition, increased level of the metals in C. sapidus and L.littorea also suggests greater potential binding sites of thesemetals in the cells of the organisms.[24]

Although much of the Cd accumulated by aquatic inver-tebrates is bound to metallothioneins,[25,26] the residual Cdreported across all species in the study is reflective of re-duced level of metallothioneins which plays important rolein metal detoxification.[25–27] In essence, metallothioneinsdegrading substance may be present within the study area.This hypothesis should further be investigated in futureresearch within the area. These figures indicate that peo-ple in population groups consuming excessive amounts ofcrab, C. sapidus, have a much higher risk of Cd exposurecompared to other organism studied. Similarly, bioaccu-mulation patterns of the three metals in the three tissuesvaried, depending on the type of species. In both crab andfish, the order of metal concentrations was the same at bothseasons: Pb >> Cd > Ni; however, this order is Ni > Cd>>> Pb in L. littorea (Table 2).

The relatively low level of Cd and Ni in T. zilli and L.littorea (containing tissues) as compared with C. sapidus(with hard parts) agrees with previous work,[28] and in linewith the fact that Cd normally has low concentration intissues.[29] On the other hand, increased level of Pb in fishhas been associated with environmental concentrations.[30]

Surprisingly, Pb concentrations in fishes at remote locationsfar from possible significant influence of oil spill (locationsbefore Ojumole village) are much higher (Figs. 3a–3c). Thismight be due to migratory nature of fish and the diffuse na-ture of Pb. It also re-emphasizes the fact that, areas remotefrom pollutant point source should be monitored alongwith hot spots. It is noteworthy that the Cd and Pb concen-trations in all the species could be even higher than thoseof the essential elements like Mn and Zn from the samesource.[18] In the same study, Ni was also higher than Znin all species and Mn (only in periwinkle). Consequently,it is believed that the high residual Cd and Pb in these or-ganisms must have resulted from a specific anthropogenicsource.

Metal concentrations tend to decrease down stream fromAyetoro until Ojumole village (areas located very close tothe Atlantic Ocean through which oil residues flows intothe neighboring communities) where concentrations be-gin to rise again. This is indicative of different rates ofbioavailable metals contaminants to the adjacent coastalwater and sediment in addition to economic activities atsome locations (Ayetoro and Awoye). In general, the un-usual increase from Ojumole is indicative of inherent an-thropogenic source which can only be linked to oil spill,being the only noticeable recurrent event within the area.However, the metal patterns found in the study did not sig-nificantly exhibit a clear seasonal variation except in Ni inT. zilli (p = 0.0191) and Pb in L. littorea (p = 0.0260).

Trace metal bioconcentration factors (BCF/BSAF)

The BCF values (Table 3) were based on the mean of thetwo seasons, since the differences are not statistically signif-icant. The values were greatest for Cd in C. sapidus (range:

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Table 2. Summary statistics of Cd, Pb and Ni in soft tissues of T. zilli, C. sapidus and L. littorea from Ilaje River, Ondo State, Nigeria(mg kg−1, dry weight), and comparison with the residue limits on shellfish foods in relevant national standards (mg/kg, wet weight).

Concentrations

Species Variables Cd Pb Ni

T. zilli Mean 1.46 (1.09) 27.34 (29.38) 1.29 (0.87)n = 9 (9) Minimum 0.57 (0.72) 16.20 (19.20) 0.90 (0.50)

Maximum 2.54 (1.69) 39.49 (38.60) 1.86 (1.80)S.D 0.69 (0.32) 8.17 (7.67) 0.46 (0.38)

C. sapidus Mean 12.08 (10.80) 30.92 (27.18) 3.55 (1.87)n = 6 (8) Minimum 3.62 (3.04) 21.04 (17.01) 0.10 (0.30)

Maximum 29.39 (14.64) 47.61 (40.04) 6.90 (3.70)S.D 9.39 (4.76) 9.09 (9.50) 2.64 (0.72)

L. littorea Mean 1.79 (2.16) 0.05 (0.17) 1.95 (1.39)n = 9 (9) Minimum 0.64 (0.92) 0.02 (0.06) 0.30 (0.20)

Maximum 2.63 (2.91) 0.09 (0.52) 4.10 (3.60)S.D 0.69 (0.69) 0.02 (0.15) 1.62 (1.23)

USFDAa (µg g−1) 3.0 1.5 70.0

#Concentrations are mean of triplicate analysis. Values in parenthesis are results of the wet season S.D: Standard Deviation; n: sample numbers.aMaximum Levels of Contaminants in Foods: promulgated United State Food and Drug Administration, USFDA.

3.35–9.92 mg/kg) and the least, Pb in L. littorea (range:0.004–0.018 mg/kg). The BCF values for the three tracemetals were between 1.00 and 9.92 mg/kg (C. sapidus),<0.01 and 2.48 mg/kg (L. littorea) and 0.38–3.33 mg/kg(T. zilli). Similarly, all the organisms studied, including fish,were shown high BCF for Ni, which has been studied veryrarely in Nigeria. The high BCFs > 1 indicate that the rateof metal uptake (K1) is greater than the rate of elimination(K2) from the tissue.[9] Very high bioconcentration of Pbwere found in both T. zilli and C. sapidus, but not in L.littorea. This shows that the mode of Pb uptake is primar-ily from water, and not diet.[31,32] In addition, the abysmallylow level in L. littorea suggests the organism either containsa good binding site for the metal or the rate of eliminationfrom the body is very high.

To evaluate further the efficiency of metal bioaccumula-tion in the organism, BSAF (BSAF = CB/CS, where CBand CS are the total metal concentrations in biota andsediment, respectively, in mg/g) were calculated (Table 3),and using the results of sediment from the same locationreported in our previous studies.[14,15] Bioaccumulation isexpected to occur in organisms if the BSAF value is > 1.[9]

The study shows that BSAF were <1.0 in Ni across allspecies, seasons and sampling stations, suggesting almostthe independence of Ni uptake by the various species onsediment concentration of the metal. In contrast, Cd (ex-cept in T.zilli) showed BSAF values ranging from 0.72–1.80in L.littorea and much higher 3.73–8.96 in C. sapidus, whichsuggested that its bioaccumulation had obviously occurredin these species from the study area. These values are rea-sonably high especially for these two heavy metals that aresaid to have no biological function.[33]

To appropriately demonstrate the probable source(s) ofthe metals with respect to water and sediment, the BCFs

and BSAFs were plotted against respective concentrationsin water and sediment (data in previous studies) (Figs. 4a–f).The correlation plot showed that, in L. littorea, metal up-take were mainly from sediments with Cd displaying thehighest significant positive correlation (R2 = 0.960, p <

0.05) (Fig. 4f). In contrast, Ni and Pb uptake in C. sapidusresults from water while Cd find its way into the speciesmajorly through sediment (R2 = 0.902) and partly fromwater (R2 = 0.873) (Figs. 4c and 4d). Interestingly, in T.zilli(Figs. 4a and 4b), significantly high but negative correla-tions were observed between BCF in Pb (R2 = −0.864)and Ni (R2 = −0.889), suggesting high elimination rateof these metals from the tissues. It can be hypothesizedthat for Pb and Cd in crab (C. sapidus) and periwin-kle (L. littorea), the combined rates of detoxification andexcretion falls far below the rate of metal uptake (com-bined across all sources). Thus, the incoming metal canhave a toxic effect on the organism. The increase in theconcentration of metabolically available metal is a con-sequence of increased rate of uptake over the maximumcombined rate of detoxification and excretion. The con-centration may reach a threshold at which sublethal andfinally lethal toxic effects are manifested.[34] According toAbel,[35] the order of toxicity (measured by either BCF orBSAF) by some metals in aquatic organisms were givenas Cd > Pb > Ni (abstracted from a longer chain) andcrustaceans such as C. sapidus has been reported to followthis order.[36,37] Similar pattern was observed in the presentstudy.

Figures 4c and 4d further demonstrate that C. sapiduseffectively accumulate the Cd and Pb metals. Evidently,the BCFs and BSAFs for Cd and Pb, the two mosttoxic elements of anthropogenic origin, were very highindicating that C. sapidus can be utilized as suitable

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904 Ololade et al.

Fig. 3. Spatial seasonal distribution pattern of (a) Cd, Pb and Ni in T. zilli; (b) Spatial seasonal distribution pattern of Cd, Pb and Niin C. sapidus and (c) Spatial seasonal distribution pattern of Cd, Pb and Ni in L. littorea. (color figure available online)

indicator for Cd and a promising indicator for Ni andPb. The study shows that C. sapidus have a higher ac-cumulation potential than the other aquatic animals. Inaddition, the study showed that fish appear to be highlyinsensitive indicator of Cd but with pronounced sensitiv-ity for Pb. The results of most studies in the past sup-ported this conclusion and showed that metals such asCd bioaccumulated poorly in fish as compared to Pb.[38,39]

Generally, the bioaccumulation of the three metals indi-

cated dependence on the physiological accumulation pat-tern of the individual species concerned for a particularmetal.

The BSAF data is a reflection of the significant impactof disturbance, either through dredging or bioturbation byanimals, which results into metal redistribution from thecontaminated sediment base.[14,15] These data threatens thearea’s delicate ecological balance and potentially contami-nating the marine food chain. In general, the study showed

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Chronic metal pollution in coastal Nigeria 905

Table 3. Bioconcentration factor (BCF) and biosediment accumulation factor (BSAF) in T. zilli, C. sapidus and L. littorea fromOCR, Nigeriaa.

Locations Sample Cd Pb Ni

Ayetoro T. zilli 0.86 (0.45)b 35.50 (0.85)b 0.16 (0.40)b

C. sapidus 3.31 (1.73) 1.70 (2.09) 1.66 (0.35)L. littorea 1.75 (0.911) 0.016 (0.018) 2.140 (0.443)

Asumaga T. zilli 0.55 (0.60) 83.67 (0.75) 0.08 (0.21)C. sapidus 4.36 (4.75) 1.62 (1.76) 1.78 (0.10)L. littorea 0.66 (0.722) 0.005 (0.005) 0.671 (0.059)

Ilepete T. zilli 0.79 (0.750 51.92 (0.73) 0.13 (0.20)C. sapidusc 5.50 (7.00) 1.39 (2.79) 0.02 (0.01)L. littorea 1.22 (1.143) 0.005 (0.004) 0.542 (0.067)

Obe Nla T. zilli 0.66 (0.51) 20.80 (0.50) 0.09 (0.22)C. sapidus 6.76 (5.27) 1.99 (1.85) 1.86 (0.20)L. littorea 1.41 (1.091) 0.006 (0.006) 0.201 (0.054)

Ikorigho T. zilli 1.08 (0.71) 16.34 (0.42) 0.06 (0.20)C. sapidus na (na) na (na) na (na)L. littorea 0.89 (1.020) 0.004 (0.004) 0.340 (0.158)

Ojumole T. zilli 1.13 (0.69) 12.10 (0.61) 0.08 (0.22)C. sapidus 9.77 (6.04) 2.04 (1.71) 1.74 (0.61)L. littorea 1.87 (1.141) 0.009 (0.007) 0.661 (0.231)

Otumara T. zilli 0.54 (0.56) 11.19 (0.68) 0.04 (0.13)C. sapidus 8.51 (8.96) 1.66 (2.24) 2.51 (0.65)L. littorea 0.96 (1.420) 0.004 (0.005) 1.542 (0.231)

Odofado T. zilli 0.70 (0.99) 13.11 (0.74) 0.04 (0.12)C. sapidus 6.02 (8.65) 2.14 (1.77) 1.70 (0.41)L. littorea 1.25 (1.799) 0.004 (0.003) 2.332 (0.557)

Awoye T. zilli 0.91 (1.31) 32.54 (0.73) 0.06 (0.18)C. sapidusc 5.63 (7.93) 2.26 (0.66) 1.00 (0.14)L. littorea 1.12 (1.623) 0.018 (0.014) 3.921 (0.741)

aData from Ololade and Lajide[16] for water and Ololade et al.[14,15] for sediments.bdata in parenthesis are BSAF levels.conly wet season data used in calculation.na: sample not available.

that not all chemical elements and chemical compounds aresubject to bioaccumulation and among those that are; theextent of bioaccumulation varies considerably. This impliesthat inorganic contaminants such as heavy metals enteringcoastal waters may be concentrated by edible marine organ-isms to varying degrees from water, their food or sediments.

Comparison of metal concentration with other studies andregulatory guidelines

Table 4 compares average metal concentrations in this studywith those from ecologically related parts in Nigeria andother parts of the world. Generally, differences in concen-trations may probably be due to ecological factors. ThePb content in C.sapidus is far above the Pb level deter-mined in red king crabs (Paralithodes camtschanticus) fromnorth eastern Bering sea, Artic Alaska (0.04–0.12 µg/gwet wt) and those of Swan Lake, Texas.[40,41] The valueequally exceed the 1.5 µg/g wet wt US Food and Drug Ad-

ministration’s lead level of concern for crustacean.[6] Apartfrom samples of L.littorea, concentrations of all the metalsare greater than those obtained from Pearl River Estuary,China.[42] The average Pb and Cd in fish reported in thestudy are greater than the <0.25 µg/g in fish muscle re-ported in a field study in Vietnam.[43] However, a muchgreater concentrations of Cd (6.0–1.2 µg/g) and similarlevel of Pb (20.6–9.2 µg/g) in fish to those obtained inour study had been reported from North Pacific Ocean,USA.[44] However, in a similar and closely related ecologi-cal environment in Nigeria, levels of Cd and Pb similar tothose obtained in this study have been reported.[45,46–49]

The oral health guideline for Cd is based on a toxicoki-netic model that predicts that an adverse health effect wouldresult in people chronically exposed to 0.01 mg/kg/day ofCd in their food.[50] Therefore, with exposure frequency ofalmost 365days/year for a population that eat fish seven (7)times a week (fishing is a major occupation of inhabitants),the levels obtained in the study deserves monitoring. More-over, WHO has established a provisional tolerable weeklyintake (PTWI) for Cd at 7 µg/kg of body weight.[50] This

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906 Ololade et al.

C. sapidus

-2

-1.2

-0.4

0.4

1.2

-0.5 0 0.5 1 1.5log C s

log

BS

AF Cd

Ni

Pb

Cd: y = 0.950x + 0.575R 2 = 0.902

Pb: y = -0.309x + 0.602R 2 = 0.113

Ni: y = 7.309x - 6.17R 2 = 0.4341

(d) C. sapidus

0

0.4

0.8

1.2

-0.5 0 0.5 1 1.5 2

log C w

log

BC

F

Cd

Ni

Pb

Ni: y= 0.367x + 0.187R 2 = 0.704

Cd: y=1.215x + 0.563R 2 = 0.873

Pb: y=0.305x - 0.084R 2 = 0.654

( c )

L. littorea

-3

-2

-1

0

1

-0.5 0.5 1.5log C w

log

BC

F

Cd

Ni

Pb

Ni: y=-1.054x + 0.037R 2 = 0.328

Cd: y = -0.446x + 0.135R 2 = 0.185

Pb: y=-0.289x - 1.846R 2=0.023

(e)

L. littorea

-3

-2

-1

0

1

0 0.5 1 1.5log C s

log

BSA

F

Cd

Ni

Pb

Pb: y = 1.762x - 4.274

R 2= 0.694

Ni: y = 5.646x - 4.797

R 2 = 0.608

Cd: y = 0.954x - 0.134

R2 = 0.960

(f)

T. zilli

-0.6

-0.3

0

0.3

0.6

0.9

-0.5 0 0.5 1 1.5 2log C w

log

BC

F Cd

Ni

Pb

Pb: y= -1.633x + 2.159R 2 = 0.864

Cd: y= -0.537x - 0.027R 2 = 0.318

Ni: y= -1.162x + 0.029R 2 = 0.889

(a)T. zilli

-1.2

-0.9

-0.6

-0.3

0

0.3

0 0.5 1 1.5log C s

log

BSA

F

Cd

Ni

Pb

Pb: y = -0.240x + 0.097

R2

= 0.089

Cd: y = -0.287x - 0.098

R2

= 0.070

Ni: y =-0.975x + 0.001

R2 = 0.162

(b)

Fig. 4. Correlation plots of (a) BCF and (b) BSAF of Cd, Pb and Ni across all species and seasons. (color figure availableonline)

PTWI weekly value corresponds to a daily tolerable intakelevel of 70 µg of Cd for the average 70 kg man and 60 µgfor the average 60 kg woman. Based on the data in Ta-ble 2, the daily Cd intake through fish across both seasonsfor the general population (0.32–2.54 mg/kg) is well abovethe guidelines established by WHO. Unlike fish, crab andperiwinkles are eaten at least once in a week. Their level inthe present work still ranged above the 7 µg/kg of body

weight PTWI. Similarly, the average concentrations of Pbacross the biota exceed the 25 µg/kg body weight PTWIfor children.[48] Therefore, Cd and Pb residues in theseedible sea foods from OCR might cause latent health risksto consumers and must be of primary concern. The impactsare expected to less in adults due to higher rate of detoxifi-cation (≈99%) of the metal in adults through the urine andfeaces compared to 65 % being detoxified in children.[51]

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Chronic metal pollution in coastal Nigeria 907

Table 4. Comparisons of element concentrations (mg/kg, dry weight) in soft tissues of biota from various geographic areas in theworld.

Species Geographical area Cd Ni Pb

Fish Present study, Nigeria, n = 9 0.57–2.54 0.50–1.86 16.20–39.49(Pearl River Estuary, Chinaa, n = 35 0.01–0.13 0.17–2.08 0.09–30.7North Pacific Ocean, USAb, n = 1–4 for different species 1.2–6.3 nd 13.0–20.0Ipo River, Delta State, Nigeriac, n = 4 0.23–1.65 2.38–3.75 19.02–38.00Okumeshi River, Delta State, Nigeriad, n = 4 0.45–0.62 0.13–0.17 <0.01

Crab Present study, Nigeria, n = 6–8 3.04–29.39 0.10–6.90 17.01–47.61Pearl River Estuary, Chinaa, n = 7 0.20–1.61 0.26–1.39 0.09–0.29North Pacific Ocean, USAb, n = 3 1.9–3.4 nd 0.2–57Swan Lake, Texase, n > 20 0.01–0.51 0.04–1.61 1.80–23.7

Periwinkle Present study, Nigeria, n = 9 0.64–2.91 0.20–4.10 0.02–0.52Pearl River Estuary, Chinaa, n = 3 0.39–0.99 0.73–31.0 0.28–0.69Swan Lake, Texase, n > 20 1.78–8.37 1.46–5.11 2.40–34.1

n = number of samples.aIp et al.[42]

bMiao et al.[44]

cFriday et al.[48]

dEkeanyanwu et al.[49]

ePark and Presley.[41]

Conclusion

This field study provides useful information and a baselinefor future and continued studies on Cd, Pb and Ni metalconcentrations in species of crabs, fish, periwinkle and otherimportant marine foods in Nigeria and the World at large.The study demonstrates that these species can be used asa suitable bioindicator to monitor the environmental base-line levels of the metals examined. In particular, the studyshows that C. sapidus and L. littorea can effectively com-partmentalize potentially toxic metals such as Cd, Pb andNi within their tissues. This apparent ability to accumu-late high concentrations of metals was related to severalfactors, including the induction of metal-binding proteins.The high BCF and BSAF are indicative of potential threatto the entire ecosystem. All the organisms did not demon-strate any clear significant seasonal variation. The tracemetal residues are, in general, greater at locations with re-ported cases of oil spillage than other locations observed inthe study. Hence, initial indications are that oil spill fromChevron and Shell activities appear to be of major signif-icance as a local source of bioavailable contaminants (Pb,Cd and Ni).

This study may be insufficient as representative of otherlocations with similar oil pollution records due to varia-tion in water physical-chemical characteristics and otherecological factors. In addition, there are limited pub-lished data base on metals content in biota from oil pol-luted sites. Consequently, more environmental data areneeded from other locations so that effective hazard as-sessments and risk management decisions can be madethat would not only be on site-specific basis. This reportsuggests that these high concentrations are probably in-fluencing the diversity of intertidal animals within these

locations. This should however, form the basis of furtherstudies.

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