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Mercury concentrations in edible species harvested from Gresik coast, Indonesia and its health risk assessment

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A study to evaluate total mercury levels in common edible marine animals (the fishes Leiognathus equlus, Coilia dusumieri, Johnius belengerii, Mugil vaigiensis, Arius leptonotacanthus, Chanos chanos, and the shrimp Penaeus merguensis) harvested from
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  Reçu le 5 juin 2009 ; accepté après révision le 2 février 2010.Received 5 June 2009; accepted in revised form 2 February 2010. Cah. Biol. Mar. (2010) 51 : 1-8 Mercury concentrations in edible species harvested fromGresik coast, Indonesia and its health risk assessment Agoes SOEGIANTO 1 , Noer MOEHAMMADI 1 , Bambang IRAWAN 1 , Mochammad AFFANDI 1 and HAMAMI 2(1)  Department of Biology, Airlangga University, Kampus C, Jl. Mulyorejo, Surabaya 60115, Indonesia. (2)  Department of Chemistry, Airlangga University, Kampus C, Jl. Mulyorejo, Surabaya 60115, Indonesia.Tel.: 62-31-5936501. Fax: 62-31-5936502. E-mail: agoes_soegianto@unair.ac.id  Abstract: A study to evaluate total mercury levels in common edible marine animals (the fishes  Leiognathus equlus, Coiliadusumieri, Johnius belengerii, Mugil vaigiensis, Arius leptonotacanthus, Chanos chanos, and the shrimp  Penaeusmerguensis ) harvested from Gresik coastal waters, Indonesia, has been carried out during 2004-2008. Concentrations of mercury in edible species from Gresik coast were relatively low compared to those in marine animals from other regionsof the world. Mercury concentrations in marine animals from this area were below the current standards for humanconsumption (USA: !  1 mg.kg -1 wet weight (ww), Japan: !  0.4 mg.kg -1 ww, Europe: !  0.5 and !  1 mg.kg -1 ww (depending onspecies), and Indonesia: !  0.5 mg.kg -1 ww). Assuming per capita consumption of fish in Gresik region is 0.46 kg.week  -1 , itseems that the mercury level found in the present study does not represent any risk to health. Résumé : Concentrations de mercure dans les espèces comestibles récoltées sur la côte de Gresik en Indonésie et sonévaluation de risque pour la santé . Une étude pour évaluer les niveaux de mercure dans les animaux marins communscomestibles (les poissons  Leiognathus equlus, Coilia dusumieri, Johnius belengerii, Mugil vaigiensis, Arius leptonotacan-thus, Chanos chanos, et la crevette  Penaeus merguensis) récoltées dans les eaux côtières de Gresik, en Indonésie a étéeffectuée en 2004-2008. Les concentrations en mercure des espèces comestibles de la côte gresik étaient relativement bassecompares à celles des animaux marins d’autres régions du monde. Les concentrations de mercure des animaux marins dece secteur étaient au-dessous des normes actuelles pour la consommation humaine (USA : !  1 mg.kg -1  poids humide (ww),Japon : !  0.4 mg.kg -1 ww, Europe : !  0.5 et !  1 mg.kg -1 ww (selon les espèces) et Indonésie : !  0.5 mg.kg -1 ww). Ensupposant une consommation de poissons par personne dans la région Gresik de 0.46 kg.semaine -1 , il semble que le niveaude mercure trouvé dans la présente étude ne représente pas de risque pour la santé  Keywords: Mercury  ! Bioaccumulation  ! Seafood  ! Food safety  ! Gresik coast  ! Indonesia  2MERCURY CONCENTRATIONS IN EDIBLE SPECIES FROM INDONESIA Introduction Pollution of aquatic ecosystems by heavy metals is animportant environmental problem, as heavy metalsconstitute some of the most dangerous toxicants that can bioaccumulate (Ryams-Keller et al., 1998). Mercury, atoxic metallic element, has been shown to bioaccumulate infish tissue, and humans consuming fish can potentiallyconsume significant levels of mercury (Adams & Onorato,2005). Methylmercury is the form of mercury the mosttoxic to humans (NRC, 2000) and the majority of totalmercury in fish muscle tissue is in the monomethyl form(Bloom, 1992). This highly toxic metal is stringentlyregulated in waste discharges (Gress & Lord, 2002). It hasalready been documented that mercury caused the death of many people in Minamata Japan from intake of seafoodcontaminated with toxic level of mercury (Nitta, 1972). Gresik coastal waters receive waste waters that potentially contain trace metals from numbers of treatmentfacilities of industries. As one of the big industrial cities inIndonesia, this zone has been under constant urban pressureduring the last twenty years due to industrial development.The potential industries which contribute to the level of metals in these coastal waters are a superphosphate plant,an asphalt plant, a coal-fired electric power plant, copper and iron smelters and refineries, natural gas processing plant, etc. Local fishermen still catch edible aquatic animalsfrom this region for cheap sources of animal protein. Thesize of edible species in this area is relatively smaller compared to that from Java Sea. However, local people stillconsume these animals as protein source.Determining the levels of potential contaminants in ediblemarine animals from this region is important for humanhealth concerns. To our knowledge there are no previous dataavailable regarding mercury levels in marine animalsharvested from this area. Previous data presented theconcentration of As, Cd, Cr, Cu, Ni, Pb, Zn and Se in bananashrimp and some species of fish (Soegianto & Hamami, 2007; Figure 1. Sampling location of marine animals. Figure 1. Localisation d’échantillonnage des animaux marins.  A. SOEGIANTO, N. MOEHAMMADI, B. IRAWAN, M. AFFANDI, HAMAMI 3 Soegianto et al., 2008). The present study was carried out toevaluate total mercury levels in common edible marineanimals harvested from Gresik coastal waters, Indonesia inorder to assess the seafood consumption safety. The resultswere also evaluated according to current standards to identifyany potential health hazards from consuming mercurycontaminated seafood. Materials and Methods  Animal samples Six species of fishes, ponyfish (  Leiognathus equlus Weber & de Beaufort, 1931), anchovy ( Coilia dusumieri Weber &de Beaufort, 1913), drum (  Johnius belengerii Weber & deBeaufort, 1936), mullet (  Mugil vaigiensis Weber & deBeaufort, 1922), sea catfish (  Arius leptonotacanthus Weber & de Beaufort, 1913), and milkfish ( Chanos chanos Weber & de Beaufort, 1913), and one species of shrimp (  Penaeusmerguensis de Man, 1888) were chosen as samples for mercury analyses. The species selected was based ongeneral abundance in the area, similarity of their size andtheir potential to be consumed by local people. The animalswere caught by gillnets from Gresik coastal waters during2004 to 2008 (Fig. 1). The samples were then directly placed in a cool box and brought to the laboratory. Duringtransportation the temperature of ice box maintained near 4°C. The biological information of the specimens is shownin Table 1.  Mercury analysis Depending on availability, several animals of each specieswere processed for mercury analysis (Table 1). For fishspecies consumed in entirety (e.g., anchovies and pony-fish), whole body samples were homogenized and preparedfor mercury detection. For other fish and shrimp, onlyedible flesh was used for mercury detection. Before filleted,external water of each individual sample was absorbedusing tissue papers. The flesh was then pooled, weighed tothe nearest 0.1 g on an analytical balance, minced by knifeand added to a known amount of double de-ionized water,then pureed using a multi-speed blender. The anchovy and ponyfish were handled with the same method. Each pooledsample was divided into between two to four sub-samplesdepending on the quantity. The sub-samples were placedseparately into special flasks, weighted and frozen at -20°Cfor a period not less than 8 hours. The frozen samples werethen placed under vacuum on a freeze-dryer unit(Labconco) until they were completely dried. Dried samplewas weighed and approximately 1 g of each was digested in5 ml of high purity HNO 3 and 5 ml of high purity HCl usingMicrowave Digester (Ethos D) for approximately 25 min-utes. Digests are filtered through filter paper and made upto 50 ml with double de-ionized water.Mercury analyzer (Nippon Jarrell Ash) was used for determination of mercury (Hg) in the tissue of animals.Analytical blanks were run in the same way as the samplesand concentrations were determined using standardsolutions prepared in the same acid matrix. Validity of analytical methods was checked using standard referencematerial (dogfish muscle reference materials, DORM-2) provided by the National Research Council of Canada. Therecoveries for Hg in the tissue standard reference materialDORM-2 were between 97 to 108%. Mercuryconcentration was quoted as mg.kg -1 wet weight. Statistical analysis Data below limit of detection (< 0.0006 mg.kg -1 ) were notused in statistical analysis. All data were tested for fitnessto a normal distribution by Kolmogorov-Smirnov test. Thedata were not normally distributed, then transformed andsubjected to parametric statistics. Differences in totalmercury levels between species of each period wereexamined using a One Way ANOVA. When significantdifferences were detected (p < 0.05), a Duncan test was SpeciesType of tissueJune 2004June 2005July 2006July 2007July 2008analysedNTWNTWNTWNTWNTW  Penaeus merguensis Flesh25218.42625625214.314146.915142.8  Leiognathus equulus Whole Body27192.520212.82812128108.930186.8 Coilia dusumieri  Whole Body18142.318115.816274.615259.8-- Chanos chanos Flesh5159.2----4101.84130.1  Mugil vaigiensis Flesh3102.2476.8798--8136.6  Arius leptonotacanthus Flesh5150.8598.93102.65107.35118.3  Johnius belengeri  Flesh--683679.47101.2863.2 Table 1. Sample information on marine animals form Gresik coastal waters, Indonesia. N: number of animal; TW: total weight of animals (g); -: data non available. Tableau 1. Echantillonnage d’animaux marins des eaux côtières de Gresik, Indonésie. N : nombre d’animaux ; TW : poids total desanimaux (g) ; - : données non disponibles.  4MERCURY CONCENTRATIONS IN EDIBLE SPECIES FROM INDONESIA used to determine which species were different from each period. Results The concentrations of mercury in shrimp and fishes fromGresik coastal waters are presented in Table 2. Significantdifferences in Hg concentration between species were found (p< 0.05) at period of 2004, 2005, 2006 and 2007 respectively;whereas no significant difference between species was noted (p> 0.05) in 2008. In 2004, the highest Hg concentration wasnoted in sea catfish, whereas milkfish, shrimp and mullet hadrelatively similar values of Hg. In 2005, sea catfish had thehighest level of Hg, followed by drum, mullet, anchovy, shrimp,and ponyfish. In 2006, the highest concentration of Hg wasrecorded in sea catfish, followed by drum, mullet and the lowestone was noted in shrimp. In 2007, drum showed the highest Hgconcentration, followed by sea catfish; while ponyfish, anchovyand shrimp had similar values of Hg. In 2008, the levels of Hgin drum, milkfish, sea catfish and mullet were relatively similar. The present study indicated that the mercury levels in tissuesshowed a high variation among all species and periods. Valuesof mercury in same species were changed from one period toanother. The concentrations of mercury (mg.kg -1 wet weight) inshrimp, ponyfish, anchovy, mullet, milkfish, sea catfish anddrum ranged from < 0.0006 to 0.0082, < 0.0006 to 0.0083, <0.0006 to 0.009, 0.0008 to 0.0081, 0.0029 to 0.0118, 0.0039 to0.0619 and 0.014 to 0.0593 respectively during 2004-2008.Although variability of Hg concentrations was quite high fromspecies to species, the concentrations of Hg in sea catfish anddrum were however relatively higher than those in shrimp, ponyfish, anchovy, milkfish and mullet. The concentrations of mercury in sea catfish were relatively similar to those in drum.During 2004 to 2006, the highest mercury levels noted in seacatfish, and in 2007 and 2008 the highest mercuryconcentration recorded in drum. Discussion This study provides information regarding total mercury levelsin tissue of edible marine animals harvested from Gresik coastalwaters. Mercury levels in shrimp, ponyfish, and anchovy arelower than those in milkfish, mullet, sea catfish and drum,which could be due to a lower time spent in this area. Our results showed that during 2004 to 2008, the average size of  ponyfish, anchovy and shrimp collected from this area wasrelatively smaller compared to that from adjacent waters (JavaSea). This fact implies that populations of those animals onlyspend less time of their life cycle in this coast. Meanwhile milk-fish, mullet, sea catfish and drum collected from this areashowed relatively high level of Hg. This finding confirms thatthey spend more time and obtain much of their food in this area.    T  a   b   l  e   2 .    M  e  r  c  u  r  y  c  o  n  c  e  n   t  r  a   t   i  o  n  s   (  m  g .   k  g   -   1   w  e   t  w  e   i  g   h   t   )   i  n   t   h  e   t   i  s  s  u  e  o   f  a  q  u  a   t   i  c  a  n   i  m  a   l  s   f  o  r  m   G  r  e  s   i   k  c  o  a  s   t  a   l  w  a   t  e  r  s ,   I  n   d  o  n  e  s   i  a .  -  :   d  a   t  a  n  o  n  a  v  a   i   l  a   b   l  e  ;   M  :  m  e  a  n  ;   S   D  :   S   t  a  n   d  a  r   d   D  e  v   i  a   t   i  o  n  ;   M   i  n  :   M   i  n   i  m  u  m   V  a   l  u  e  ;   M  a  x  :   M  a  x   i  m  u  m   V  a   l  u  e  ;  n  :  n  u  m   b  e  r  o   f  s  u   b  s  a  m  p   l  e  a  n  a   l  y  s  e   d .    T  a   b   l  e  a  u   2 .    C  o  n  c  e  n   t  r  a   t   i  o  n  s  e  n  m  e  r  c  u  r  e   (  m  g .   k  g   -   1   p  o   i   d  s   f  r  a   i  s   )   d  a  n  s   l  e  s   t   i  s  s  u  s   d  e  s  a  n   i  m  a  u  x  m  a  r   i  n  s   d  e  s  e  a  u  x  c   ô   t   i   è  r  e  s   d  e   G  r  e  s   i   k ,   I  n   d  o  n   é  s   i  e .  -  :   d  o  n  n   é  e  s  n  o  n   d   i  s  p  o  n   i   b   l  e  s  ;   M  :  m  o  y  e  n  n  e  ;   S   D  :   é  c  a  r   t  -   t  y  p  e  ;   M   i  n  :  v  a   l  e  u  r  m   i  n   i  m  a   l  e  ;   M  a  x  :  v  a   l  e  u  r  m  a  x   i  m  a   l  e  ;  n  :  n  o  m   b  r  e   d  e  s  o  u  s  -   é  c   h  a  n   t   i   l   l  o  n  s  a  n  a   l  y  s   é  s .  A. SOEGIANTO, N. MOEHAMMADI, B. IRAWAN, M. AFFANDI, HAMAMI 5 Our findings are in accordance with Palmer & Presley(1993) who reported that natural population of shrimpcollected in the contaminated area of Lavaca Bay, Texaswere not contaminated with mercury, implying that theyspent less time (< 3 weeks) in this area. To determine the degree of mercury contamination in thestudy area, our results were compared with other works(Table 3). The concentrations of mercury in edible speciesfrom Gresik coast are relatively lower than those in marineanimals from Tyrrhenian Sea, Italy (Barghigiani et al,2000), from Florida Coast, USA (Adams, 2004; Adam &Onorato, 2005), from Irish waters, UK (Tyrrell et al., 2005),from coastal area in Malaysia (Agusa et al., 2005), fromSuez Canal in Port-Said Harbour (Soliman, 2006), fromGulf of Cambay, India (Reddy et al., 2007), and fromAlexandia region, Egypt (Ahdy et al., 2007). To our knowledge, the lower value of mercury in our finding is possibly due to the smaller size of marine animals collectedfrom Gresik coast compared to marine animals from other areas. Positive relationships between total mercury levelsand fish size and fish age were obtained in most areas,indicating that mercury levels tend to increase over time asfish grow (Adams & Onorato, 2005). These relationshipsare influenced by the relatively slow rate at which mercuryis eliminated compared to the rate at which it isaccumulated in fish tissues (Bryan, 1984). Mercuryelimination rates for some species of fish also tend todecrease with increasing fish body size (Trudel &Rasmunssen, 1997). For marine fishes, dietary exposure is also an importantsource of mercury (Trudel & Rasmunsen, 2001). Themercury content in diets of some fish species, especiallythose that consume fish as part of their diet, increases as thefish grows larger (Mathers & Johansen, 1985). Metalsincluding mercury can become more concentrated as theygo through various food chains and food webs in an Table 3. Concentrations of mercury (mg.kg -1 wet weight) in edible marine species from different regions. Tableau 3. Concentrations en mercure (mg.kg -1  poids frais) dans les espèces marines comestibles de différentes régions. LocationSpeciesHg (mg.kg -1 Referencewet weight) Gulf of Cambay, India  Harpodon nehereus (Hamilton, 1822), Teleostei0.24 ± 0.083Reddy et al. (2007)Suez Canal in Port-Said ,  Mugil cephalus (Linnaeus, 1758), Teleostei0.18-1.17Soliman (2006)Harbour Egypt Sardina pilchardus (Walbaum, 1792), Teleostei0.20-0.97  Metapenaeus monoceros (Fabricius, 1789), Crustacea - Decapoda0.01-0.54Estuarine and offshore waters Sciaenops ocellatus (Linnaeus, 1758), Teleostei0.02-3.6Adams & Onorato (2005)of Florida, USAFlorida Atlantic Coast, USA Thunus albacares (Bonnaterre, 1788), Teleostei0.068-0.65Adams (2004) Thunus atlanticus (Lesson, 1831), Teleostei0.16-2.0  Eutynnus alletteratus (Rafinesque, 1810, Teleostei0.11-3.4Alexandria region, Egypt  Mugil capito (Cuvier, 1829), Teleostei0.014-0.06Ahdy et al. (2007) Siganus rivulatus (Forsskal, 1775), Teleostei0.011-0.275 Sparus auratus (Linnaeus, 1758), Teleostei0.0125-0.0725Coastal area in Malaysia Selar crumenophthalmus (Bloch, 1793), Teleostei0.0175-0.1375Agusa et al. (2005)  Decapterus kurroides (Bleeker, 1855), Teleostei0.0275-0.0425  Rastrelliger kanagurta (Cuvier, 1816), Teleostei< 0.0125-0.0125  Pomadasys kaakan (Cuvier, 1830), Teleostei0.0150-0.0325 Scomberoides lysan (Forsskal, 1775), Teleostei0.0175-0.0325Tyrrhenian Sea, Italy  Nephrops norvegicus (Linnaeus, 1758), Crustacea – Decapoda0.2-4.4Barghigiani et al. (2000)  Parapanaeus longirostris (Lucas, 1846), Cruatacea – Decapoda0.1-1.7  Eledone cirrhosa (Lamark, 1798), Mollusca - Cephalopoda0.1-1.8Irish Waters, UK  Solea solea (Linnaeus, 1758), Teleostei0.04-0.09Tyrrell et al. (2005) Gadus morhua (Linnaeus, 1758), Teleostei0.08-0.1  Melanogrammus aeglefinus (Linnaeus, 1758), Teleostei0.06-0.18  Merluccius merluccius (Linnaeus, 1758), Teleostei< 0.03-0.07  Microstomus kitt (Walbaum, 1792), Teleostei0.04-0.06Gresik Coast, Indonesia  Penaeus merguensis (de Man, 1888), Crustacea – Decapoda< 0.0006-0.0082This study  Leiognathus equulus (Weber & de Beaufort, 1913), Teleostei< 0.0006-0.0083 Coilia dusumieri (Weber & de Beaufort, 1931), Teleostei< 0.0006-0.009 Chanos chanos (Weber & de Beaufort, 1913), Teleostei0.0029-0.0118  Mugil vaigiensis (Weber & de Beaufort, 1922), Teleostei0.0008-0.0081  Arius leptonotacanthus (Weber & de Beaufort, 1913), Teleostei0.0039-0.0619  Johnius belengerii (Weber & de Beaufort, 1936), Teleostei0.014-0.0593
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