the Science of the Total Environment An international Journal for Srfenltfk S taesrch Into the Environment and It' Relationship sslth Man

ELSEVIER The Science of the Total Environment 224 (1998) 181-188 " ' 1 ------

Mercury in the bivalveAnadara ( Senilia) senilis from Ghana and Nigeria

Claude R. Joiris*, Maureen I. Azokwu, Fred A. Otchere, Ishaque B. Ali

Laboratory for Ecotoxicology and Polar Ecology, Free University of Brussels (VUB), Pleinlaan2, B -l050 Brussels, Belgium

Received 4 June 1998; accepted 25 September 1998

Abstract

Samples of the bivalve Anadara (Senilia) senilis collected from a closed lagoon (Sakumo) and two open lagoons in Ghana (Benya and Ningo;n = 550), and the Bonny river estuary in Nigeria(n = 620), were analyzed for their total and organic mercury content. Total mercury concentration showed significant spatial differences, with median values of 0.1 /rg/g dry wt. in the closed lagoon, 0.2 in the estuary and 0.3 in the open lagoons. Concentration tended to be higher during the dry season in the lagoons, but lower in the estuary. The median relative organic concentration varied between 20 and 60% methyl Hg, depending on location and season. Age effects were detected in the lagoons, total Hg concentration decreasing with length. © 1998 Elsevier Science B.V. All rights reserved.

Keywords: Mercury; Bivalves; Ghana; Nigeria; West Africa

1. Introduction low level of industrial activity in the less devel­ oped regions, there is a growing awareness of the The occurrence of metal contaminants has be­ need for rational management of aquatic re­ come a problem of increasing concern. This situa­ sources including control of waste discharges into tion has arisen as a result of rapid population the environment. The uptake of contaminants in growth, increased urbanization, expansion of in­ an aquatic environment by living organisms de­ dustrial activities, exploration and exploitation of pends on their total concentration and their natural resources, extension of irrigation and chemical forms. Some aquatic biota, especially other modern agricultural practices, as well as the bivalves, are often used as bioindicators and thus lack of environmental regulations. Low concen­ considered to provide information on the con­ trations of heavy metals occur in West African tamination of the surrounding water or sedi­ aquatic systems compared to other areas of the ments, though it has not yet been proven that world (Biney et al., 1994). Despite the relatively direct dose-response relationships always exist between the contamination of such bioindicators and of the ecosystem they belong to (Morrison, * Corresponding author. Tel.: +32 2 6293414; fax: +32 2 1989). 6293438; e-mail: [email protected] This paper presents seasonal and spatial varia-

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tions of mercury concentration (total and organic), and soft tissue fresh weight were measured. Dry in the West African bloody cockle Anadara flesh weight was determined after dry freezing for (Senilia) senilis from the coasts of Ghana and 24 h. Condition index (Cl), defined as the ratio Nigeria. This cockle was formerly called Arca between soft tissues dry weight (mg dry wt.) and senilis by Linnaeus (1758). In 1842, Gray created shell length (cm) (Hawkins et al., 1987), was used the genus Senilia, a genus without species. By to characterize the ‘health’ of the cockles by subsequent designation of Gray (1847), Arca se­ summarizing their physiology in terms of growth, nilis became the type for the genus. Reinhart reproduction and secretion (Lucas and Beninger, (1935) classified the West African bloody cockle 1985). Size classes based on shells length were: into the subgenus Senilia of the genus Anadara; < 3 cm as small, 3 -4 cm as medium and > 4 cm his classification of the family Arcidae is now as large. widely accepted as is Anadara (Senilia) senilis for The method used to determine total mercury the West African bloody cockle (e.g. Yoloye, (2H g) concentration (Hatch and Ott, 1968) was 1974a). modified as described in detail by Joiris et al. (1991) by specific atomic absorption spectrometry 2. Materials and methods (AAS) performed with a Perkin-Elmer MAS-50 analyzer, wavelength 253.7 nm, with a detection Cockles were collected in October 1996 and limit of 0.04 ¡Xg /g dry wt. for an average 6-g February 1997 (wet and dry seasons, respectively) sample. from three lagoons in Ghana: Benya, Sakumo and Methyl mercury (MeHg) was determined by Ningo, between 5-6° N and 1°20' W and 0°20' E. liquid-gas chromatography with electron capture Benya and Ningo are ‘open lagoons’ (water tem­ detector (ECD) as described in detail in Joiris et perature: 24-32°C; salinity: 10-40%e, similar to al. (1991), with a detection limit 0.01 /xg/g dry wt. that of the sea except during the wet season. for an average 6-g sample. There is contact with the sea throughout the year Tests were conducted in order to detect a pos­ and partly under tidal influence, spring tide is 1 m sible matrix effect, and to establish the repro­ high), while Sakumo is a ‘closed lagoon’ (water ducibility of the measurements, for both total and temperature: 27-34°C, salinity: 27-70%c, varia­ organic Hg. Ten cockles were homogenized and tions being mainly due to dilution from direct divided into 10 equal parts; two parts were treated rainfall and small creeks during the wet season, as usual and to the other parts, known quantities and evaporation during the dry season. It is cut of MeHg were added before analysis. When mea­ off from adjacent sea by a sand bar, 40 m wide for sured MeHg was plotted as a function of the a greater part of the year). For the Bonny River added concentration, a linear regression was ob­ estuary, Nigeria, sampling covered two dry and tained. The slope (1.1) for the samples is close to two wet seasons between 1995 and 1997 from the ideal slope of one to consider any possible three stations: Okrika located towards the indus­ matrix effect negligible. Reproducibility for the trial city of Port Harcourt, while Andoni and method showed a standard error of 8%. Blanks Bonny are located towards the Atlantic Ocean, at and internal standard were included in each batch the mouth of the estuary. The Nigerian crude oil in addition to certified reference material (CRM). terminal with its allied services and a recent giant The certified value for MeHg was 0.731 /xg/g dry Nigerian Liquefied Natural Gas Project are lo­ wt. ± 0.06 and for SHg was 0.789 /ag/g dry wt. ± cated at the mouth of the estuary. Bonny river 0.074 (DORM-1, National Research Council of estuary is situated between 4°25' N to 4°45' N Canada, Marine Analytical Chemistry Standards and 7°05' E to 7°15' E. This area is covered by Program). In this study, a value of 0.77 ¡xg /g dry mangrove, freshwater, swamp and lowland rain wt. ± 0.03, i.e. 96% of the target value for XHg forests. All samples were collected during the (n = 8) and 0.62 /xg/g dry wt. ±0.07 or 85% of neap tide by local fishermen. the target value for MeHg (n = 12) were ob­ For each bivalve, total weight, length, width tained.

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Table 1 Mercury in West African cockles from Ghana and Nigeria

Closed Open Estuary0 lagoon3 lagoonsb

Dry season 2 H g 0.16 (3 0 ) 0.33 (81) 0.14 (311) (0.08-0.45) (0.14-0.89) (0.02-0.32)

M eHg 0.09 (19) 0.17(81) 0.06 (2 5 2 ) (0.07-0.24) (0.05-0.33) (0.22-0.14)

Inorg H g 0.07d 0.15 (81) 0 .0 9 (7 2 6 ) - (0.05-0.23) (0.02-0.27)

%MeHg 56 50 (81) 39 (1 2 6 ) - (3 2 -6 3 ) (1 1 -9 3 )

S H g load 0.06 (3 0 ) 0 .1 9 (8 7 ) 0.11 (377) (0.03-0.10) (0.04-0.66) (0.02-1.32)

Condition index 1 2 6 (3 0 ) 171(9 9 ) 183 (3 7 5 ) (77-176) (44 -6 5 8 ) (6 3 -1 1 5 0 )

Length 2.3 (49) 3 .6 (9 9 ) 4.1 (4 5 2 ) (2.1-3.2) (1.6 -5 .9 ) (2 .2 -8 .9 )

Wet season SH g 0.11 (3 8 ) 0.19 (45) 0.21 (1 8 8 ) (0.05-0.38) (0.10-0.35) (0.08-0.39)

MeHg 0.05 (3 6 ) 0.07(2 4 ) 0.05 (1 6 0 ) (0.03-0.11) (0.04-0.21) (0.02-0.16)

Inorg Hg 0.06d 0.12 (2 4 ) 0.15 (723) - (0.06-0.11) (0.03-0.36)

% M eHg 42 37(2 4 ) 25 (7 2 3 ) - (3 4 -4 2 ) (7 -8 4 )

S H g load 0.13 (38) 0.12 (4 5 ) 0.30 (1 8 8 ) (0.04-0.39) (0.05-0.53) (0.05-0.92)

Condition index 302 (5 0 ) 164 (45) 2 4 1 (2 8 5 ) (62-655) (79 -4 3 1 ) (5 5 -1 0 1 1 )

Length 4.1 (74) 4.0 (6 9 ) 4 .9 (2 8 5 ) (2.1—6.2) (1.9 -6 .4 ) (2 .6 -9 .3 )

Motes. Inorganic Hg concentration calculated as the difference between 2H g and MeHg. Median values (min.-max.); concentrations in fig /g dry wt.; load in /xg; length in cm; (n ) — number of samples. “Sakuno, Ghana. Benya and Ningo, Ghana. cOkrika, Andoni and Bonny, Bonny river, Nigeria. d Calcula te d as the difference of median values for SH g and MeHg.

The data were expressed as total and methyl 3. Results and discussion mercury on a dry weight base, and differences were tested using the Mann-Whitney [/-test of Total mercury concentration in the cockles from significance (Siegel, 1956), since results did not the lagoons, for both wet and dry seasons, de­ show a normal distribution. creased with length (i.e. with age), corresponding

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OD 00.25- 5 ° ® S |. ° o ■ 0 0 9% o • .15' w * * OO CD .05'

2.5 3.5 4.5 5.5 6.5 2.5 3.5 4.5 5.5 Length Length

Fig. 1. Relationship between SHg concentration (¿¿g H g/g dry wt.) and length (cm) of cockles. Dots: dry season, circles: wet season; (a) Benya lagoon; and (b) Andoni.

to an apparent growth dilution effect (Fig. la). as pH, temperature and salinity (e.g. Philips, This resulted in a significant difference between 1976). two of the three size classes (small and large In the lagoons, total mercury concentration was classes; 0.22 and 0.16 jxg Hg/g dry wt., respec­ higher in the dry season than in the wet season tively, P < 0.01), as described by Boyden (1974). (almost twice higher in the open lagoons); in the Such an effect was generally not detected in the estuary, on the contrary, dry season concentra­ estuary (Fig. lb), with the exception of Andoni, at tions were lower (Table 1). If these cockles were the mouth, where SHg tended to decrease with to be used as bioindicator, this suggests that the length during the 1997 wet season (Fig. 2). The lagoons become more contaminated in the dry differences in mercury content in the bivalve along season than in the wet season, and the reverse in the coasts of Ghana and Nigeria (Table 1) may be the estuary. These seasonal variations might, mainly due to the degree of urbanization and however, be due to seasonal variations in primary population density influencing the amount of do­ production: the higher the particulate matter mestic discharges in lagoons (Ntow and Khwaja, (phytoplankton) concentration, the lower its Hg 1989; Biney, 1991), as well as possible industrial concentration for a given Hg level in the water. influences in the estuary, even if other factors This phenomenon has been described for PCB also play a role such as organism physiology, contamination in the North Sea (Delbeke and particularly sexual cycle, and abiotic factors such Joiris, 1988; Delbeke et al., 1990), in the Barents and Greenland seas (Joiris et al., 1995,1997), and in the Antarctic, where low PCB contamination .4' of the ecosystem and low phytoplankton biomass .35' resulted in high PCB concentration on suspended .3' particulate matter (Joiris and Overloop, 1991). In .25' this study, the increase may be due to reduced ■ X .2' water and nutrients in-flow into the lagoons dur­ .15' ing the dry season causing important differences

. 1' in primary production and thus in suspended par­ .05 ticulate matter concentration. On the other hand, ifanoo S o 0 the decrease in concentration during the wet sea­ 6 7 10 Length son might be caused by dilution or transport out

Fig. 2. Relationship between Hg concentration and length of the area by increased surface run-offs. Similar (Andoni, wet season, 1997); blocks: SHg; open squares: MeHg. trends have been reported in fish and shellfish by

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Mearns et al. (1988) and in Californian mussels load of the river. Joseph and Srivastava (1993), for DDTs, PCBs and chlordanes by Stephenson et Mitra and Choudhury (1993) and Pillai and Val- al. (1995). The higher concentration observed in sala (1995) observed increased concentrations of the wet season in the estuary could be the result heavy metals during the monsoon season similar of increased run-off water influx into the river to the observation made in this study. Significant after rainfall with a possible increase in pollutant spatial differences in total mercury were observed,

Table 2 Mercury in cockles from Bonny river, Nigeria (see legend Table 1)

Station Okrika Okrika Andoni Andoni Bonny Year 1995 1996 1995 1996 1996

Dry season XHg 0.11 (25) 0.11 (7 0 ) 0 .1 6 (7 5 0 ) 0.12 (5 2 ) 0 .1 8 (7 6 ) (0.08-0.14) (0.03-0.28) (0.08-0.26) (0.02-0.32) (0.08-0.32)

MeHg 0.04 (2 0 ) 0.05 (5 9 ) 0 .0 6 (720) 0.06 (3 2 ) 0.06 (27) (0.04-0.16) (0.02-0.12) (0.03-0.14) (0.02-0.10) (0.03-0.12)

Inorg H g 0 .0 T 0.06 (4 3 ) 0.09 (4 0 ) 0 .0 8 (3 2 ) 0.09 (77) - (0.04-0.13) (0.02-0.15) (0.02-0.22) (0.03-0.27)

%MeHg 36 41 (4 3 ) 45 (4 0 ) 4 9 (3 2 ) 37 (77) - (1 1 -7 3 ) (2 3 -9 2 ) (1 6 -9 3 ) (1 4 -7 1 )

XHg load 0.28 ( 23) 0.21 (7 0 ) 0 .1 0 (7 5 0 ) 0.10 (5 2 ) 0.39 (76) (0.02-0.35) (0.02-0.08) (0.04-0.56) (0.04-0.38) (0.09-1.32)

Condition index 103 (2 0 ) 256 (9 3 ) 173 (763) 1 8 9 (6 0 ) 2 5 1 (3 9 ) (63-220) (9 3 -1 1 5 0 ) (7 0 -4 8 7 ) (8 4 -3 6 7 ) (7 9 -6 4 8 )

Length 2 .8 (2 0 ) 4.9 (9 3 ) 3.7(2 4 0 ) 4.2 (6 0 ) 4.4 (3 9 ) (2.2—4.6) (3 .2 -8 .9 ) (2.9—6.6) (3.5—5.3) (2 ,7 -6 .4 )

Station Okrika Okrika Andoni A ndoni Bonny Year 1996 1997 1996 1997 1997

Wet season XHg 0.29 (1 6 ) 0.17 (6 5 ) 0.23 (4 4 ) 0.18 (37) 0.22 (3 2 ) (0.16-0.39) (0.08-0.29) (0.16-0.37) (0.08-0.39) (0.11-0.31)

M eHg 0 .0 4 (7 6 ) 0.05 (4 7 ) 0.05 (43) 0.05 (2 0 ) 0.08 (3 4 ) (0.03-0.07) (0.03-0.15) (0.02-0.12) (0.02-0.13) (0.03-0.16)

Inorg H g 0.25 (7 6 ) 0.12 (4 4 ) 0.19 (43) 0 .1 2 (7 9 ) 0.13 (77) (0.13-0.36) (0.03-0.24) (0.12-0.31) (0.04-0.21) (0.03-0.13)

%MeHg 1 4 (7 6 ) 28 (4 4 ) 19 (4 3 ) 39 (79) 51 (77) (7 -2 7 ) (1 2 -8 4 ) (8 -4 1 ) (1 9 -6 4 ) (2 2 -8 1 )

XHg load 0 .3 9 (7 6 ) 0.20 (6 5 ) 0.44 (4 4 ) 0.21 (37) 0.13 (3 2 ) (0.23-0.76) (0.05-0.92) (0.11-0.90) (0.10-1.02) (0.06-0.23)

345 (4 4 ) 183 (5 0 ) 141 (100) Condition index 2 8 8 (7 6 ) 246 (75) (1 7 6 -3 9 5 ) (116-993) (146-683) (72-1011) (5 5 -3 0 6 ) 4.6 (4 4 ) 4.2 (50) 3.5 (100) Length 5.1 (7 6 ) 4 .6 (7 5 ) (4.7-6.7) (2.7-9.3) (2 .6 -4 .8 ) (4.5 -5 .6 ) (3 .7 -8 .3 )

Calculated as the difference of median values for XHg and MeHg.

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. 35 ' .18 .16 .25 00 .14 1

.15' .08 .06 .04 .05- .02

2.5 3.5 4.5 5.5 6.5 3.5 4.5 5.5 Length Length

Fig. 3. Relationship between MeHg concentration ( /u.g H g/g dry wt.) and length (cm) of cockles, (a) Benya lagoon; and (b) Andoni. See legend Fig. 1.

concentrations being higher in samples collected 1996, 315 in 1995 and 380 in 1997; IITA, 1997). from Andoni and Bonny (the mouth of the estu­ Methyl mercury (MeHg) concentration for both ary) than in Okrika. Presumably, the concentra­ dry and wet seasons was fairly stable (Table 1), tions obtained for the mouth of the estuary are and no trend was detected as a function of size accumulation of the quantity naturally generated (Fig. 3). The relative MeHg concentration as a from the ocean surface around the area and the function of length was stable during the wet sea­ portion still available after dilution as water flows son; during the dry season, however, it was towards the ocean. No significant difference was sometimes stable and sometimes decreasing (Fig. noted for each station between seasons, except 4). The percentage of organic mercury reflects the for the wet seasons in the estuary (Table 2): the flushing rate (i.e. resident time) of mercury in wet season 1996 provided higher values for XHg these lagoons (Philips, 1988). Hence the stagnant (0.3 and 0.2 /u.g/g dry wt., for Okrika and Andoni, lagoon had higher percentage (i.e. larger resi­ dence time and thus more time for méthylation) respectively), corresponding to a higher level of as compared to the open ones. inorganic Hg. This difference could be due to An important factor possibly explaining such lower precipitations in 1996, with deficit of ap­ seasonal differences could be spawning: varia­ proximately 100 mm of rain in comparison with tions in the weight of gonads during the repro- 1995 and 1997 (220 m m /m onth in June and July

100 60 90* 80 50 70 •• * o m 40 X ° 60 2 \ 50 • .V e* 30 40 o o» •• _ • • 20 30 •o » 20 « o 10 10 O o o o 0 0 1 2.5 3 3.5 4.5 3.5 4.5 5.5 Length Length

Fig. 4. Relative methylmercury concentration (%MeHg) as a function of length in cockles, (a) Ningo lagoon; and (b) Andoni. See legend Fig. 1.

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! CO oe “ o *

° «S«0*0 »°8m • » * ■ * g /• • •• 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 3.5 4.5 5.5 Length

Fig. 5. Relationship between load (/xg Hg) and length (cm) of Benya cockles. Dots: dry season; circles: wet season; (a) Benya lagoon; and (b) Andoni.

ductive cycle can be responsible for variations in the degree of urbanization and population density the pollutant content of molluscs, particularly for of the locations, but other biotic and abiotic fac­ organometals (Boyden and Philips, 1981; tors may be of importance as well. The existence Bouquegneau and Joiris, 1988). This could also of such differences, as well as the detection of an provide an explanation for geographical differ­ age effect in the lagoons, once more shows that ences, since the spawning period can be different, the link between the level of contamination of e.g. in open and closed lagoons (Yankson, 1981), aquatic ecosystems and concentrations in biota to and since variations in concentrations from one be used as bioindicators, is a complex one and locality to another could be due to differences in that many factors must be taken into account gonad development at different sites (Cossa et al., before allowing spatial and temporal compar­ 1979). In addition, the sex ratio in our Nigerian isons. samples was 44 females/15 males, corresponding to the 3:1 ratio reported by Yoloye (1974b), while References it was close to one in Ghana. Variations of the condition index (Cl) with season, however, did Biney C. A baseline study of trace metals in marine organisms not show any systematic trend, and there was no from Ghana, West Africa. In: Coastal zone ‘91’. Long- direct link between Cl and Hg concentration (Ta­ beach, California: ASCE, 1991:1155-1167. Biney C, Amuzu AT, Calamari D et al. Review of heavy bles 1 and 2). metals in the African aquatic environment. Ecotoxicol The total body load of Hg in the cockles was Environ Saf 1994;28:134-159. also calculated by multiplying Hg concentration Bouquegneau J-M, Joiris C. The fate of stable pollutants — by individual soft tissues weight. It showed a heavy metals and organochlorines. Adv Comp Environ positive relationship with length, and seasonal Physiol 1988;2:218-219. Boyden CR. Trace element content and body size in molluscs. differences were detected in load as in concentra­ Nature 1974;251:311-314. tion (Fig. 5). Boyden CR, Philips DJH. Seasonal variation and inherent variability of trace elements in oysters and their implica­ 4. Conclusions tions for indicator studies. Mar Ecol Prog Ser 1981;5:29-40. Cossa D, Bourget E, Piuze J. Sexual maturation as a source of variation in the relationship between cadmium concentra­ In the lagoons, median 2Hg concentration was tion and body weight of Mytilus edulis L. Mar Pollut Bull significantly higher in the dry season than the wet 1979;10:174-176. Delbeke K, Joiris CR. Accumulation mechanisms and geo­ season. In the estuary on the contrary, concentra­ graphic distribution of PCBs in the North Sea. Océanis tions were lower in the dry season. Spatial dif­ 1988;14:399-410. ferences in concentration (Benya > Ningo > Delbeke K, Joiris CR, Bossicart M. Organochlorines in dif­ Sakumo and Bonny river estuary) seem to reflect ferent fractions of sediments and in different compartment

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of the Belgian continental shelf and the Scheldt estuary. Mitra A, Choudhury A. Metal content in the gastropod Nerita Environ Pollut 1990;66:325-349. articulata (Gould). Ind J Environ Health 1993;35:31-35. Gray JE. Synopsis of the content of the British Museum. Morrison GMP. Trace element spéciation and its relationship London: Trustees of the British Museum, 1847. to bioavailability and toxicity in natural waters. In: Trace Hatch WR, Ott WL. Determination of sub-microgram quanti­ element spéciation: analytical methods and problems. CRC ties of mercury by atomic absorption spectrophotometry. Press, 1989:25-41. Anal Chem 1968;40:2085-2087. Ntow WJ, Khwaja AM. Mercury pollution in Ghana (West Hawkins CM, Rowell TW, Woo P. The importance of cleans­ Africa) coastal commercial fish. Environ Tech Lett ing in the calculation of condition index in the soft-shell 1989;10:109-116. clam, Maya arenaria (L.). J Shellfish Res 1987;6:29-36. Philips DJH. The common mussel Mytilus edulis as an indica­ IITA. High rainfall station, International Institute of Tropical tor of pollution by zinc, cadmium, lead and copper. I. Agriculture, O nne/ Port Harcourt, Nigeria, 1997. Effects of the environmental variables on uptake of metals. Joiris CR, Overloop W. PCBs and organochlorine pesticides Mar Biol 1976;38:59-69. in phytoplankton and Zooplankton in the Indian sector of the Southern Ocean. Ant Sei 1991;3:371-377. Philips DJH. California State Mussel watch: Ten-year data Joiris CR, Holsbeek L, Bouquegneau J-M, Bossicart M. Mer­ summary 1977-1987, Water Quality Monitoring Report cury contamination of the harbour porpoise Phocoena p h o ­ 87-3. California State Water Resources Control Board, coena and other cetaceans from the North Sea and the Sacramento, CA 1988:313. Kattegat. Water Air Soil Pollut 1991;56:283-293. Pillai VK, Valsala KK. Seasonal variations of some metals in Joiris CR, Ali IB, Holsbeek L, Bossicart M, Tapia G. Total bivalve molluscSunetta scripta from the Cochin coastal and organic mercury in Barents sea pelagic fish. Bull Envi­ waters. Ind J Mar Sei 1995;24:113-115. ron Contam Toxicol 1995;55:674-681. Reinhart P. Classification of the pelecypod family Arcidae. Joiris CR, Ali IB, Holsbeek L, Kanuya-Konoti M, Teleke MY. Bull Musée r Hist Natur Belg 1935;11:1-68. Total and organic mercury in Greenland and Barents seas Siegel S. Non parametric statistics for the behavioral sciences. demersal fish. Bull Environ Contam Toxicol 1997;58: New York: McGraw-Hill book Company, Inc., 1956:267. 101-107. Stephenson MD, Martin M, Tjeerdema RS. Long-term trends Joseph KO, Srivastava IP. Heavy metal load in edible oyster, in DDT, PCBs and chlordane in California mussels. Arch Crassostrea madrasensis (Preston) from the Ennore Estuary Environ Contam Toxicol 1995;28:443-450. in Madras (India). J Environ Biol 1993;14:121-127. Linnaeus C. Systema Naturae. Salvius, Stockholm, 1758. Yankson K. Gonad maturation and sexuality in the West Lucas A, Beninger PG. The use of physiological condition African bloody cockle, Anadara senilis (L.). J Moll Stud index in marine bivalve aquaculture. Aquaculture 1981;48:294-301. 1985;44:187-200. Yoloye V. The validity of the subgenus Senilia ( Bivalvia: Meams A, Matta M, Simeck-Beatty D, Buchman M, Shige- Arcidae Anadarinae, Anadara). Proc Maiae Soc Lond naka G, Wert W. PCB and chlorinated pesticide contami­ 1974a;41:21-24. nation in U.S. fish and shellfish: A historic assessment Yoloye V. The sexual phase of the West African bloody cockle report, NOAA Technical Memorandum NOS OMA 39, Anadara Senilia (L.) ( Bivalvia: Arcidae Anadarinae, Seattle, WA 1988:140. A nadara). Proc Maiae Soc Lond 1974b;41:25-27.

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