花蓮師院學報 民 92,17 期 35-44 頁 Accumulations of Heavy Metals in Fish Wen-Bin Huang a , Tzong-Huei Lee b , Chih-Yu Chen c,* a Department of Science Education, National Hualien Teachers College, Hualien, Taiwan 970, R.O.C. b Graduate Institute of Pharmacognosy science, Taipei Medical University, Taipei, Taiwan 110, R.O.C. c Department of Tourism, Hsing Wu College, Taipei, Taiwan 244, R.O.C. (Received May 15, 2003; Accepted October 6, 2003) Abstract High level accumulation of heavy metals in tissues from environment is considered toxic for the marine organisms. In this review, we primarily compared the accumulations of the two essential metals, copper and zinc, and three non-essential metals, cadmium, lead and mercury, in the fish tissues of liver, gonad, gill, intestine and muscle. In general, the order of the metal concentrations in the tissues of fish is liver and gonad > gill and intestine > muscle. The accumulation levels of the essential metals are generally higher and more homeostatic than the non-essential metals in fish. The differences of the metal accumulation levels influenced by the feeding, habitat, sex and age (size) of fish in the tissues were discussed. Effects of the seasonal change and the salinity in the environment were also reviewed. Keywords: zinc, copper, lead, cadmium, mercury, fish, tissue, pollution increased in fish may pose a threat to human Introduction health through consumption of the fish (Chen and Chen, 1999), though some metals, for Heavy metals are considered the important example zinc and copper, are essential trace pollutants of aquatic environment because of minerals for metabolic regulation at cellular and their toxicity and accumulation by marine tissue levels (Vallee and Faclchul, 1993). The organisms (Zyadah and Chouikhi, 1999). The concentrations of heavy metals in tissues of fish concentrations of the metals, such as cadmium, are determined primarily by the level of pollution of the water and food. * Corresponding author The concentrations 36 花蓮師院學報第十七期 themselves are the result of uptake and release than any other organs in fish (Al-Yousuf et al., processes 2000). elements with and characteristic their biological kinetics half for time, Fish may accumulate heavy metals by influenced by the age (size) of individuals, the absorption through gills or by consumption of feeding habits of these species, and by the season, contaminated food and sediments (Wong et al., as well as the biochemical characteristics of the 2001). tissues (Farkas et al., 2000). In this review, we heavy metals are higher in gills than in intestines primarily concentrated on the accumulations of in fishes (Table 1). However, the accumulation the two common essential metals, copper and patterns of metals in tissues of fishes are varied zinc, and three non-essential metals, cadmium, with the kind of metals. With the exception of lead and mercury, in fish tissues of liver, gonad, zinc gill, intestine and muscle. gastrointestinal absorption and gill uptake, the In general, the concentration of the which cadmium Accumulation of heavy metals in tissues significantly and copper showed demonstrate both more significant uptake through gill than through digestive tract (Chen and Chen, 1999). Gonad is another organ with high metal concentration in Recently metals tissues of fishes (Table 1). Kidney is the major accumulated in fish tissues are shown in Table 1. organ of cadmium accumulation in rainbow trout Liver is the tissue accumulated the highest level Oncorhynchus mykiss (McGeer et al., 2000). of the reported essential and heavy non-essential metal Muscle is the tissue that usually has the concentrations. It is a storage and detoxification lowest organ for the metals (Avenant- Oldewage and concentrations in fishes (Table 1). Marx, 2000) and an organ where the specific concentrations in skin, as well as in muscle, were metabolism enzyme-catalyzed generally lower than in gills, liver, intestines and reaction related to these metals take place (Jaffar gonads (Wong et al., 2001). However, opposite and Pervais Shahid, 1989). In addition, it plays cases could be found usually in contaminant area. an important role in contaminant storage, For example, the mercury concentrations in redistribution, detoxification or transformation, muscle were higher than those in livers of smelt and also acts as an active site of pathological Osmerus eperlanus and perch Perca fluviatilis in effects induced by contaminants (Evans et al., the Vaike Vain Strait, western Estonia, due to the 1993). characteristics of the Strait and the fish habitat process and The liver tissues are more often recommended as an indicator of water pollution essential (Voigt, 2000). and non-essential metal Metal 重金屬在魚體之累積 37 compared to plankton feeders and pelagic Regulation of essential and non-essential metals in tissues carnivores (Krishnamurti and Nair, 1999). The concentrations of mercury in muscle tissue of the metals predatory fishes (Esox lucios, Alburnus alburnus, accumulated in various tissues depend on the Gymnocephalus cernua, Perca fluvatilis, Belone biochemical characteristics of the metal (Farkas belone) et al., 2000). Accumulation of zinc and copper non-predatory are generally higher than lead and cadmium in membras, Sprattus sprattus baltius, Osmerus the tissues of Epinephelus areolatus, Lutjanus eperlanus, russelli and Sparus sarba (Wong et al., 2001). Except of mercury, the concentrations of the The small range of the bioaccumulation factors heavy metals (ex. Cadmium, copper and zinc) in of zinc in various fish tissues indicates that zinc tissues generally appear to be inversely related to is regulated to maintain a homeostatic status in the trophic level of the fish species (Amundsen et fish (Chen and Chen, 1999). al., 1997). The different degrees of the Lead has no biological function or requirement and its are higher than species Rutilus those (Clupea rutilus) (Voigt, of the harengus 2000). The eco-geographic habitat of the fishes fish tissues are may be another factor related to the metals generally low (< 1 μg/g) (Thompson, 1990). accumulated in tissues. The levels of mercury Accumulation of zinc and copper, if occurred, is concentrations in the coastal inshore species are rapid but quantitatively low. For cadmium, higher than those in open-sea fishes, but for time to half saturation is long and saturation copper the opposite is observed (Voigt, 2000). concentrations are high (McGeer et al., 2000). Higher concentrations of cadmium apparently concentrations in marine are encountered in livers of the benthic fishes, as Feeding and habitat relevance compared to that of the pelagic fish (Roméo et al., 1999). Metal accumulations in tissues are found to By contrast, Zyadah and Chouikhi (1999) reported that the pelagic Boops boops The observed differences accumulated the heavy metals in the organs more between the metal concentration in fishes may be than the benthic Mullus barbatus and Merluccius related primarily to their feeding habits, as well merliccius, as the accumulation trends of the essential and bio-concentration capacity of each species non-essential metals in fish were attributed to the (Farkas et al., 2000). Maximum concentrations ecology and physiology of the fishes (Zyadah of the metals are found in benthic feeders as and Chouikhi, 1999). be species specific. the metal content in food and especially for copper. The However, it must be 38 花蓮師院學報第十七期 noted that high variability of the metal waters (Schuhmacher et al., 1992). The concentrations among individuals of fish within accumulation of the metals in livers showed the same species should be considerable (Wong good correlation for zinc and cadmium with the et al., 2001). fish size (Al-Yousuf et al., 2000). An age dependency has been described in analyzing the Seasonal variation correlation between metal concentrations and fish age (Ward and Neumann, 1999). In most Marked Seasonal differences are found for cases, negative relationships were reported in cadmium and lead concentrations which are cadmium, copper, lead and zinc, but positive elevated in autumn as compared to spring, but correlations were often found in mercury (Farkas less pronounced for copper and zinc (Farkas et et al., 2000). The negative correlations between al., 2000). The highest metal concentrations in the concentration of metals and fish age is caused muscle appear between November and February, by the variation of feeding rate with age of during the periods of lower salinity, at the end of individuals, the dilution by growth, and the food the rainy season, and at the beginning of the dry preference of certain age classes. season (Campos-C, 1992). Increase of salinity which has positive correlation with age is in the environment would significantly reduced possibly the accumulation of copper in the tissues of biomagnification (Amundsen et al., 1997). the only metal Mercury related to Oreochromis niloticus (Karakoc, 1999). These results showed that the salinity in environment Sex effects might interfere the accumulation of heavy metals In addition, seasonal changes in Metal levels in tissues differ between males feeding rate, in gaining or losing weight, or in and females, and the greatest differences are synthesis of metal binding proteins, are all found in gonads (Latkovskaya, 2000). responsible for storage of the metals (Farkas et concentrations of the essential metals of zinc and al., 2000). copper are higher in the female gonads, while the in fishes. The male gonads have higher contents of the Age and size dependent non-essential metals of cadmium and lead. The average metal concentrations in liver, skin and The age and size of fish affect the metal muscle of female fish are higher than those of accumulation in themselves, as well as their male fish (Al-Yousuf et al., 2000). Different feeding habits and retention time in polluted concentrations of heavy metals accumulated in 重金屬在魚體之累積 39 different tissues between males and females For example, the gills of the Liza macrolepis probably of can be used as a good bio-indicator of metal physiological processes in different sexes and the pollution in coastal area because of the feeding specificity of biochemical composition of tissues habit and life style of the fish with a significant during the periods of growth and gonad bioaccumulation (Chen and Chen, 1999). reflect the specific nature formation in fish (Latkovskaya, 2000). Conclusions Bio-indicator of monitoring pollution In fish tissues, accumulation of the essential metals are generally higher and more Some behavioural changes in fish are observed after exposure to homeostatic than the non-essential metals. sub-lethal The distribution patterns of the accumulations concentration of metals due to stress, and such of the heavy metals in the fish tissues are changes can be used as biological indicators or similar. as biological early warning system in water and lowest metal concentrations are liver and quality assessment (Khunyakari et al., 2001). muscle, respectively. Copper concentrations in gills and livers metal concentrations and fish ages were changed during the detoxification period, generally negative in zinc, copper and cadmium, indicating that histology is a successful tool but positive in mercury. capable of revealing sensitively the effects of accumulated trends and mechanisms between heavy metals on the environment and aquatic the essential and non-essential metals are biota (Arellano et al., 1999). significantly different in fishes on their habitats In addition, McGeer et al. (2000) noticed that the initial In general, the tissues of the highest The relationships of the However, the and sex, seasons, and regulation patterns. patterns of accumulation for each metal were generally consistent with the damage, repair and acclimation pattern from physiological measurements. Acknowledgements concurrent In monitoring The author would like to express his hearty metal pollution with fish, these specificities and appreciation differences should be considered. Therefore, Department of Marine Resources, National Sun the specific fish species used, as well as the fish Yat-sen University for his comments and tissues selected, may be good metal pollution suggestions on the manuscript, and Mr. Craig indicators (Catsiki and Strogyloudi, 1999). Deardoff for his help with English writing. to Prof. C.-t. Shih of the I 40 花蓮師院學報第十七期 also wish to thank the two anonymous concentrations in Ariopsis bonillai (Pisces: reviewers for their constructive comments on Siluriformes) the manuscript. Colombian from Santa Caribbean. Marta, Revista de Biologia Tropical, 40(2), 179-183. Catsiki, V. -A. and Strogyloudi, E. (1999). References Survey of metal levels in common fish Al-Yousuf, M. H., El-Shahawi, M. S. and Al-Ghais, S. M. (2000). 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Heavy metal Relative high concentration tissue Liver 1, 2, 3, 4, 5, 8, 9, 10, 11, 12, Intestine 7 Gill 1, 3, 10 Muscle 4, 6, 8, 9, 10 Zinc Liver 3, 4, 5, 9, 10, Gonad 2 Gill 3, 10, Intestine 5 Muscle 4, 6, 9, 10 Liver 3, 4, 9, 10, 12, 13, Gonad 12, Kidney 11 Gill 3, 10, 13, Intestine 13 Muscle 6, 9, 10 Liver 3, 9, 10, 12 Gill 6, 10, 12 Muscle 9 Lead Mercury Liver 6, Muscle 14 - Avenant-Oldewage and Marx (2000), fish Otolithoides biaritus, Pellona felligera, Wong et al. (2001), fish species: Epinephelus Eleutheronema tetradactyla, Coilia areolatus, Lutjanus russelli, Sparus sarba. 3 4 Farkas et al. (2000), fish species: Anguilla 10 Amundsen et al. (1997), fish species: Coregonus lavaretus, Perca fluviatilis, Esox lucioperca. lucius, Lota lota, Salmo trutta, Coregonus Al-Yousuf et al. (2000), fish species: Lethrinus albula. 11 Chen and Chen (1999), fish species: Liza macrolepis. 6 dussumieri, Harpodon nehereus. anguilla, Abramis brama, Stizostedion lentjan. 5 Muscle 6, 10 seheli, Johnius glaucus, Lates calcarifera, species: Claries gariepinus. 2 Relative low concentration tissue Copper Cadmium 1 Relative highest concentration tissue Oncorhynchus mykiss. 12 Roméo et al. (1999), fish species: Sardinella Boops boops. 13 costae, Cephalophlis nigri, Pseudupeneus prayensis. Zyadah and Chouikhi (1999), fish species: Mullus barbatus, Merluccius mercluccius, aurita, Scomber japonicus, Trachurus trachurus, Serranus scriba, Epinephlus McGeer et al. (2000), fish species: Lundebye et al. (1999), fish species: Salmo salar. 14 Voigt (2000), fish species: Clupea harengus 7 Wong et al. (1999), fish species: Sparus sarba. membras, Sprattus sprattus baltius, 8 Karakoc (1999), fish species: Oreochromis Osmerus eperlanus, Esox lucios, Alburnus niloticus. 9 Krishnamurti and Nair (1999) , fish species: Arius tenuispinis, A. coelatus, Valamugil alburnus, Rutilus rutilus, Gymnocephalus cernua, Perca fluvatilis, Belone belone. 44 花蓮師院學報第十七期 重金屬在魚體之累積 黃文彬 a a 國立花蓮師範學院自然科學教育學系 李宗徽 b b 陳治宇 c,* 台北醫學大學生藥學研究所 c 醒吾技術學院觀光系 摘要 對海洋生物來說,由環境累積高濃度的重金屬在組織內通常被認為是有毒的。在本文中, 我們比較二種必需金屬(鋅與銅)與三種非必需金屬(鎘、鉛與汞),在魚類體內肝臟、性腺、鰓、 腸及肌肉等組織中之累積情形。一般而言,重金屬在魚類組織中所累積濃度的高低順序通常是: 肝臟與性腺 > 鰓與腸 > 肌肉。必需金屬在魚體內所累積之濃度,通常比非必需金屬之濃度, 來得較高且穩定。因魚類本身攝食、棲地、性別與年齡大小,以及受環境季節變動與鹽度等因 子影響,造成魚體各組織內重金屬累積濃度差異或變動等現象,本文亦均有論述。 關鍵詞: 鋅、銅、鉛、鎘、汞、魚類、組織、污染