- Email: [email protected]
Accumulation of Hg and other heavy metals in the Javan mongoose (Herpestes javanicus) captured on Amamioshima Island, Japan
Chemosphere 65 (2006) 657–665 www.elsevier.com/locate/chemosphere
Accumulation of Hg and other heavy metals in the Javan mongoose (Herpestes javanicus) captured on Amamioshima Island, Japan Sawako Horai a,d, Mikiko Minagawa b, Hirokazu Ozaki c, Izumi Watanabe b,*, Yasuo Takeda d, Katsushi Yamada d, Tetsuo Ando d, Suminori Akiba d, Shintaro Abe e, Katsuji Kuno b a
Department of Environmental Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo 183-8509, Japan b Department of Environmental and Natural Resource Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo 183-8509, Japan c Ocean Research Institute, The University of Tokyo, 1-15-1 Minamidai, Nakano, Tokyo 164-8639, Japan d Graduate School of Medical and Dental Sciences, Kagoshima University, 8-35-1 Sakuragaoka, Kagoshima 890-8520, Japan e Amami Wildlife Conservation Center, Ministry of the Environment, 551 Onsyojikosinohata, Yamato-son, Oshima-gun, Kagoshima 894-3104, Japan Received 5 September 2005; received in revised form 6 January 2006; accepted 26 January 2006 Available online 23 March 2006
Abstract Concentrations of 22 elements (Mg, V, Cr, Mn, Fe, Co, Ni, Cu, Zn, As, Se, Rb, Sr, Mo, Ag, Cd, Sb, Cs, Ba, Tl, total Hg (T-Hg), Pb) and organic Hg (O-Hg) were examined in the liver, kidney and brain of the Javan mongoose (Herpestes javanicus) and in liver of the Amami rabbit (Pentalagus furnessi) from Amamioshima Island in Japan. Relatively high levels of T-Hg levels (from 1.75 to 55.5 lg g 1 wet wt.) were found in the Javan mongoose. As for a comparison of hepatic T-Hg concentrations between the two areas, there was no significant difference between the Javan mongoose in Amamioshima and those in the Okinawa islands. In addition, T-Hg levels in the livers of the Amami rabbit were the same as in the livers of other herbivorous mammals. Taken together, it suggested that T-Hg accumulation in the livers of the Javan mongoose was not affected by the environment but by a specific physiological mechanism. The comparison of Hg and other heavy metal accumulations between terrestrial mammals (13 species, 61 individuals) including the Javan mongoose and marine mammals (18 species, 508 individuals) were also discussed. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Mercury; Organic mercury; Selenium; Javan mongoose; Terrestrial mammals; Marine mammals
1. Introduction As animals are at higher trophic levels, toxic effects of bioaccumulative contaminants such as some heavy metals through biomagnification are more severe (Burger et al., *
Corresponding author. Tel./fax: +81 42 367 5736. E-mail addresses: [email protected] (S. Horai), [email protected] (I. Watanabe). 0045-6535/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2006.01.078
2000). While toxic heavy metals such as Cd and Hg cause weight loss, organ damage, metabolic disorders and behavioral disorders (Takekawa et al., 2002), high specific accumulations of these metals have been found in sea turtles (Anan et al., 2001), marine mammals (Wagemann et al., 1998; Cardellicchio et al., 2000, 2002; Fant et al., 2001; Woshner et al., 2001; Chen et al., 2002; Monteiro-Neto et al., 2003; Ikemoto et al., 2004a,b) and sea birds (Elliott et al., 1992; Kim et al., 1996a,b; Kim et al., 1998; Wayland
658
S. Horai et al. / Chemosphere 65 (2006) 657–665
et al., 2001). Hence, although bioaccumulation of metals via aquatic food webs has been extensively studied, there is much less information regarding terrestrial systems. A database for heavy metal concentrations in some organs of various animals from Japan, is need to allow an analysis of heavy metal accumulation in the species and an understanding of heavy metal pollution in the country. The Javan mongoose lives in Amamioshima and the Okinawa islands in Japan. Amamioshima Island is almost 570 km in circumference and an area of approximately 719 km2. The area of this island is third largest island next to Okinawa and Sado. Because an island is isolated, there are endemic and rare organisms, which have formed peculiar biota in Amamioshima and Okinawa. The Javan mongoose could be useful as an indicator for heavy metal monitoring in a terrestrial system because it is a carnivorous terrestrial mammal and a top predator on Amamioshima Island. In this study, the heavy metal concentrations in Javan mongooses and Amami rabbits from Amamioshima Island were determined. 2. Material and methods 2.1. Samples Fifty four Javan mongooses, Herpestes javanicus, were collected from Amamioshima Island during 2004 and 2005 as part of a control of harmful wildlife. The specimens of 54 livers, 47 kidneys and 10 brains were analyzed in this study. Two Amami rabbits, Pentalagus furnessi, were collected from the same area in 2004. The deaths of the Amami rabbits were road accidents. Ten Javan mongooses were collected from Okinawa Island as part of a control of harmful wildlife in 2004. The 10 hepatic samples were used to compare the Hg level in livers with those from Amamioshima Island. All samples in this study were frozen at 80 °C until chemical analysis. Around 1979, Javan mongooses were introduced to Amamioshima Island from Okinawa Island, where the species was introduced from India as a countermeasure against bites by the habu, a species of very poisonous snake inhabiting the Amamioshima and Okinawa Islands, and also to prevent crop damage due to rodents. However, the danger of bites by the habu has been already decreasing remarkably before the Javan mongooses were introduced. This decrease has been a result of the capture of habu by human and the maintenance of the surroundings, for what the introduction of the Javan mongoose has contributed very little to the decrease in the problems (Japan Wild Research Center, 2000). In addition, excrement analysis of the Javan mongoose demonstrated that Javan mongooses have killed endemic rare species on Amamioshima Island such as the Amami rabbit, Pentalagus furnessi, and the Ryukyu robin, Erithacus komadori (Japan Wild Research Center, 2000). Extermination and control of invasive alien species are needed to protect the rare species
in the areas where unique ecosystems remain (Japan Wild Research Center, 2000). 2.2. Chemical analysis The livers, kidneys and brains were dried for 16 h at 90 °C. About 0.10 g of powdered samples were digested with 2.0 ml of nitric acid in a microwave. The concentrations of 20 elements (Mg, V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Rb, Sr, Mo, Ag, Cd, Sb, Cs, Ba, Tl, Pb) were determined by inductively coupled plasma-mass spectrometry (ICP-MS; Hewlett-Packard, HP-4500) (Watanabe et al., 2003). Iron concentrations were measured by atomic absorption spectrometry (AAS; Hitachi, Z-5310). Mercury levels were determined by cold vapor technique using a mercury analyzer (Hiranuma, Model HG-300). Concentration of organic Hg (O-Hg) was determined with CV-AAS with the modifying Uthe et al. (1972) method. Briefly, powdered samples were mixed with CuSO4 and acidic sodium bromide to release O-Hg followed by extraction of O-Hg into the toluene phase. Part of the toluene phase was removed, and sodium thiosulfate solution was added to it. A sample of the thiosulfate solution was removed and digested with a mixture of acids (HNO3:H2SO4:HClO4 = 2 ml:2.5 ml:2 ml). The accuracy of the methods was assessed using standard reference materials DORM2 (National Research Council Canada) and SRM1577b (National Institute of Standards and Technology). The recoveries of the metals ranged from 85% to 106%. In this study, all metal concentrations were expressed on a wet wt. basis (lg g 1 wet weight [wet wt.]). Conversion of concentrations from wet weight to dry weight basis using percent of water content in the tissues was done as to requirement. 2.3. Statistical analysis Correlation between the metal concentrations in tissues was examined using the Spearman rank test. The different sets of data were compared regarding location and species using the Mann–Whitney U-test. A p-value < 0.05 was considered statistically significant. All of the statistical analyses were executed by the Statcel2 program (Yanai, 2004). 3. Results and discussion 3.1. Heavy metal concentrations in tissues Heavy metal concentrations in the tissues of the Javan mongoose collected from Amamioshima Island are shown in Table 1. Most elements were highest in the livers, the Cd concentration was highest in the kidneys and the Cr concentration was highest in the brains. Mean T-Hg concentration was 12.7 lg g 1 wet wt. in livers of the Javan mongoose and the maximum was 55.5 lg g 1 wet weight. This level was the highest compared with some terrestrial mammals studied by Wren (1986).
0.339 ± 0.235 (0.0612–1.32) n = 53 0.121 ± 0.0890 (0.0138–0.435) n = 47 0.0126 ± 0.00521 (0.00814–0.0226) n = 10 0.0141 ± 0.0107 0.000872–0.0691 n = 53 0.00615 ± 0.00327 (0.00125–0.0202) n = 47 0.00241 ± 0.00238 (0.000392–0.00673) n = 10 ND; not detected. Minimum and maximum values are in parentheses. T-Hg; Total mercury. O-Hg; Organic mercury.
Brain
Kidney
Tl O-Hg
2.45 ± 1.61 (0.610–8.61) n = 53 2.00 ± 0.872 (0.667–4.64) n = 47 0.864 ± 0.448 (0.309–1.73) n = 10 12.7 ± 10.6 (1.75–55.5) n = 53 5.12 ± 2.68 (1.26–12.6) n = 47 1.27 ± 0.807 (0.383–2.90) n = 10
T-Hg Ba
0.0183 ± 0.0130 (ND–0.0610) n = 51 0.0163 ± 0.0126 (ND–0.0507) n = 27 0.00613 ± 0.00459 (ND–0.0160) n=9 0.0540 ± 0.0279 (0.0139–0.134) n = 53 0.0501 ± 0.0274 (0.0111–0.121) n = 47 0.0346 ± 0.0181 (0.0177–0.0734) n = 10
Cs Sb
0.0186 ± 0.0125 (ND–0.0673) n = 52 0.00532 ± 0.000951 (ND–0.00685) n=5 0.00309 ± 0.00135 (ND–0.00442) n=4 0.477 ± 0.416 (0.103–2.04) n = 53 1.10 ± 1.38 (0.176–9.14) n = 47 0.00532 ± 0.00278 (ND–0.00850) n=7
Cd Ag
0.143 ± 0.194 (0.0128–1.29) n = 53 0.00156 ± 0.00168 (ND–0.00761) n = 30 0.0108 ± 0.00283 (ND–0.0139) n=4 0.409 ± 0.0848 (0.277–0.657) n = 53 0.121 ± 0.0439 (0.0315–0.326) n = 47 0.0118 ± 0.00288 (ND–0.0145) n=4
Mo Sr
Brain
Kidney
0.0759 ± 0.0252 (0.0318–0.125) n = 53 0.0809 ± 0.0432 (0.0325–0.220) n = 47 0.0899 ± 0.0394 (0.0403–0.151) n = 10
Pb
8.32 ± 3.43 (3.00–18.8) n = 53 5.87 ± 2.63 (1.01–12.8) n = 47 3.56 ± 1.04 (2.30–5.55) n = 10
Liver
Se
4.60 ± 3.27 (1.07–18.5) n = 53 1.63 ± 0.485 (0.466–3.62) n = 47 0.249 ± 0.0586 (0.184–0.377) n = 10 0.0510 ± 0.0512 (0.0129–0.385) n = 53 0.0283 ± 0.0232 (0.00740–0.105) n = 47 0.0162 ± 0.0124 (ND–0.0359) n=7
As Zn
79.1 ± 41.4 (35.3–211) n = 53 21.4 ± 7.67 (4.94–42.5) n = 47 12.8 ± 2.59 (9.82–17.1) n = 10 10.3 ± 3.25 (4.77–19.5) n = 53 3.14 ± 0.871 (0.950–6.84) n = 47 3.44 ± 0.609 (2.56–4.28) n = 10
Cu Ni
0.0201 ± 0.0217 (ND–0.0862) n = 47 0.0121 ± 0.0185 (ND–0.116) n = 42 0.00674 ± 0.00148 (ND–0.00569) n=2 0.0493 ± 0.0209 (0.0184–0.109) n = 53 0.0205 ± 0.00675 (0.00559–0.0380) n = 47 0.00832 ± 0.00425 (0.00238–0.0142) n = 10
Co Fe
216 ± 86.4 (77.5–476) n = 53 131 ± 38.0 (62.8–210) n = 47 34.4 ± 7.95 (25.3–46.2) n = 10 4.38 ± 1.72 (2.23–10.4) n = 53 0.794 ± 0.218 (0.230–1.70) n = 47 0.392 ± 0.0748 (0.288–0.507) n = 10
wet wt.) in the three organs of Javan mongoose captured at Amamioshima Island
Mn
0.0275 ± 0.0193 (ND–0.00808) n = 52 0.0118 ± 0.00610 (ND–0.0343) n = 46 0.00602 ± 0.00210 (ND–0.00742) n=4 170 ± 41.3 (101–257) n = 53 110 ± 30.5 (38.4–258) n = 47 143 ± 11.6 (133–168) n = 10 Liver
V Mg Organs
Cr
1
Table 1 Heavy metal concentrations (mean ± SD and range on lg g
0.0389 ± 0.0275 (0.00648–0.135) n = 53 0.0332 ± 0.0207 (0.00631–0.158) n = 47 0.0473 ± 0.0547 (0.0145–0.197) n = 10
Rb
S. Horai et al. / Chemosphere 65 (2006) 657–665
659
Fig. 1a shows that as T-Hg levels were higher, the O/THg concentration ratios were lower. This result was consistent with some reports about marine mammals (Caurant et al., 1996; Meador et al., 1999; Cardellicchio et al., 2000, 2002). Significant correlations of T-Hg with V, Se, Cd and O-Hg in livers, O-Hg with Cu in kidneys and T-Hg with O-Hg in brains were observed in the Javan mongoose (Table 2). Significant correlations of T-Hg with Se (Caurant et al., 1996; Wagemann et al., 1998; Meador et al., 1999; Fant et al., 2001; Woshner et al., 2001; Cardellicchio et al., 2002; Endo et al., 2002; Decataldo et al., 2004), Cd (Woshner et al., 2001) and O-Hg (Honda et al., 1983; Andre´ et al., 1991; Leonzio et al., 1992; Woshner et al., 2001; Chen et al., 2002) in the livers of marine mammals were studied. The molar ratio of T-Hg and Se concentrations in the livers of the Javan mongoose was almost 1 (Fig. 1b). This result was consistent with some studies of marine mammals. The marine mammals may have adapted so as to tolerate high Hg levels because of a detoxification mechanism involved in Se metabolism in the liver (Wagemann et al., 1998; Cardellicchio et al., 2000; Endo et al., 2002; Arai et al., 2004). Javan mongooses may also tolerate Hg toxicity because they have an efficient detoxification system of methyl Hg in their livers as with marine mammals. The correlation of Hg with Ag similar to Se was observed in the livers of the marine mammals (Mackey et al., 1996; Saeki et al., 2001; Woshner et al., 2001). Moreover, Saeki et al. (1999) has reported that there were not only the correlations of Hg with Ag and Se but also V in livers of marine mammals and that V could behave similarly to Hg and Ag, therefore V might accumulate in tissues as a contaminant similar to Hg and Ag. In contrast to the marine mammals, however, there were no significant correlations of Hg–Ag and V–Ag in the livers of Javan mongoose (p = 0.131 and p = 0.259, respectively). Amami rabbits are endemic and rare species which inhabit only Amamioshima and Tokunoshima Islands in the Amamioshima Archipelago. They were the first species designated as a natural monument and are now designated as species in danger of extinction 1B in Japan. The trace element concentrations in the livers of Amami rabbits are shown in Table 3. Mean T-Hg concentration in the livers of Amami rabbits was 0.032 lg g 1 wet wt. This value was the same level as in caribou, reindeer (Aastrup et al., 2000) and hares (Poole et al., 1998), which are also herbivores, and lower than raccoons (Burger et al., 2002), an omnivore, arctic wolves (Gamberg and Braune, 1999) and minks (Poole et al., 1998), which are carnivores. Taken together, it is suggested that the accumulation of T-Hg in the livers of Amami rabbits was affected by diet, and much higher T-Hg concentrations in the livers of the Javan mongoose might be a specific accumulation. Most of the hepatic metal concentrations measured were higher in the Javan mongoose than in the Amami rabbit except for Co, Sr, Mo and Ba. Relatively higher Mo concentrations found in the livers of moose (Frank et al.,
660
S. Horai et al. / Chemosphere 65 (2006) 657–665 T-Hg concentration (μmol g -1 wet wt.)
Persent O-Hg (of T-Hg)
120 Liver
100
Kidney Brain
80 60 40 20 0
0
20
(a)
40
60
Total Hg concentration (μg g-1 wet wt.)
0.3
0.2
1:1 0.1
Liver Kidney Brain
0.0 0.0
(b)
0.1
0.2
0.3
Se concentration (μmol g-1 wet wt.)
Fig. 1. Relationships between (a) T-Hg and percent organic Hg , and (b) Se and T-Hg concentrations in three organs of Javan mongoose.
Furthermore, as described above, the hepatic T-Hg level of the Amami rabbit was similar to that of some herbivorous mammals living in other areas, indicating that the hepatic T-Hg accumulation of the Javan mongoose is specific. Mercury enters the water as a natural process of off-gassing from the earth’s crust and as a result of industrial pollution, then methylated by algae and bacteria in the water and moving up the food chain to its highest concentrations in large predatory fish such as swordfish, sharks and tuna (Quig, 1998), which can contain high levels of methyl Hg (Bridges and Zalups, 2005). Mercury accumulation of marine mammals is dependent upon biomagnifications (Monaci et al., 1998; Fant et al., 2001; Cardellicchio et al., 2002; Endo et al., 2002). Although the hepatic T-Hg level of the Javan mongoose is at the same level as those of marine mammals, it is not dependent upon an aquatic food system. The major diet of the Javan mongoose is insects, such as crickets and grasshoppers, and non-insect invertebrates (Rodda et al., 1999). Mammalian and avian preys, mostly rodents, have also been found in Javan mongoose gastrointestinal tracts (Rodda et al., 1999). This information indicates that T-Hg accumulation in the Javan mongoose may be caused by unique biomagnifications, which are involved in the physiological mechanisms such as high Hg absorbent ability, high Hg accumulation and/or low Hg excretion.
Table 2 Spearman’s rank correlation coefficient between Hg and other element concentrations in the three organs of Javan mongoose
Liver THg-V THg-Se THg-Cd THg-OHg Kidney OHg-Cu Brain THg-OHg
r
p
0.297 0.916 0.677 0.802
0.032 <0.001 <0.001 <0.001
0.366
0.013
0.988
0.003
2004) and feral pigeons (unpublished data), which are herbivores, may support that the these element contents in herbivores is higher than in carnivores. 3.2. Area difference We compared hepatic T-Hg concentrations in the Javan mongoose from Amamioshima Island with those from Okinawa Island (mean of 23.1 lg g 1 wet wt., minimum and maximum were 0.465 lg g 1 wet wt. and 112 lg g 1 wet wt., respectively, n = 10) to clarify whether the high T-Hg accumulation in the Javan mongoose is affected by their habitat, and no significant area difference of T-Hg concentrations was subsequently observed (p = 0.679).
Table 3 Heavy metal concentrations (range on lg g
1
wet wt.) in the liver of Amami Rabbit collected from Amamioshima Island
Sample ID
Mg
V
Cr
Mn
Fe
Co
Ni
Cu
Zn
As
Se
04-0412 04-0421 Mean
200 188 194
0.0332 0.0166 0.0249
0.0462 0.0371 0.0417
3.54 3.67 3.61
348 347 348
0.0618 0.0569 0.0593
0.0119 0.0254 0.0186
4.26 4.21 4.24
26.5 32.7 29.6
0.0298 0.0212 0.0255
0.213 0.342 0.278
Rb
Sr
Mo
Ag
Cd
Sb
Cs
Ba
T-Hg
Tl
Pb
2.86 11.6 7.24
0.399 0.250 0.325
1.18 0.983 1.08
ND ND –
0.0479 0.171 0.109
0.00922 0.00740 0.00831
0.0302 0.0872 0.0587
0.147 0.0708 0.109
0.00967 0.0543 0.0320
0.00803 0.00860 0.00831
0.0977 0.109 0.103
04-0412 04-0421 Mean
ND; not detected.
S. Horai et al. / Chemosphere 65 (2006) 657–665
661
Table 4 Marine mammal and terrestrial mammal species Species
n
Sampling site
Marine mammals Bikal seal (Phoca sibirica) Bottlenose dolphin (Tursiops truncatus) Caspian seal (Phoca caspica) Dall’s porpoise (Phocoenoides dalli) Dugong (Dugong dugong) Habour seal (Phoca vitulina largha) Harbour porpoise (Phocoena phocoena) Melon headed whale (Peponocephala electra) Minke whale (Balaenoptera acutorostrata) Northern fur seal (Callorhinus ursinus) Pacific white-sided dolphin (Lagenorhynchus obliquidens) Rough-toothed dolphin (Steno bredanensis) Short-finned pilot whale (Globicephala macrorhynchus) Short-finned pilot whale (Globicephala melas) Sperm whale (Physeter macrocephalus) Spotted seal (Phoca largha) Striped dolphin (Stenella coeruleoalba) Weddell seal (Leptonychotes weddelli)
40 3 42 130 3 31 47 18 37 4 19 13 47 28 1 20 22 3
Lake Baikal Japanese waters Caspian Sea Japanese waters Okinawa and Indonesia Japanese waters Black Sea Japanese waters Antarctic Sea Japanese waters Japanese waters Japanese waters Japanese waters Japanese waters Japanese waters Japanese waters Japanese waters Antarctic Sea
Terrestrial mammals Asiatic black bear (Selenarctos thibetanus) Japanese weasel (Mustela itatsi) Japanese badger (Meles meles) Japanese macaque (Maccaca fuscata) Japanese raccoon dog (Nyctereutes procyonoides) Japanese red fox (Vulpes vulpes) Japanese serow (Capricornis crispus) Japanese wild boar (Sus leucomustax) Large Japanese field mice (Apodemus speciosus) Masked palm civet (Paguma larvata) Racoon (Procyon lotor) Siberian weasel (Mustela sibirica) Sika deer (Cervus nippon)
3.3. Comparison of terrestrial and marine mammals High T-Hg accumulation was found in the liver of the Javan mongoose, which is a terrestrial mammal. Next, the T-Hg concentrations of terrestrial mammals, including Javan mongoose, were compared with those of marine mammals to characterize the Hg accumulation of the Javan mongoose. The marine and terrestrial mammalian species used for this comparative study are shown in Table 4 (Unpublished data). Fig. 2a shows a comparison of hepatic T-Hg levels between the terrestrial mammals including the Javan mongoose and the marine mammals except dugongs which are herbivores. No significant difference was observed between the T-Hg levels of the Javan mongoose and marine mammals which contain relatively higher T-Hg than other organisms (p = 0.204). A significant difference of hepatic Pb levels between the terrestrial mammals, including the Javan mongoose, and the marine mammals including the Baikal seal inhabiting freshwater was observed (p < 0.001) (Fig. 2b). The Pb level is higher in fresh water and terrestrial realms than in the marine realm (Bowen, 1979), indicating a significant difference of hepatic Pb levels between terrestrial and marine mammals is dependent on their habitats. Therefore, marine
4 16 3 2 3 3 1 4 1 9 5 5 5
Japan Japan Japan Japan Japan Japan Japan Japan Japan Japan Japan Japan Japan
mammals may be weaker against Pb toxicity than terrestrial mammals, although the marine mammals possess a tolerance of Hg toxicity. In regard to a comparison of the relationship between hepatic and renal T-Hg concentrations of terrestrial and marine groups, T-Hg concentrations were similarly distributed in the livers of the Javan mongoose, the Baikal seal and the marine mammals (Fig. 3). However, T-Hg accumulation patterns of the Javan mongoose and the Baikal seal inhabiting freshwater showed that the distribution levels were higher in the kidneys than those of the marine mammals. The relationship between hepatic T-Hg concentrations and ratios of renal and cerebral to hepatic T-Hg concentrations is shown in Fig. 4. As hepatic T-Hg level increases, the transition rate of T-Hg from liver to kidney and brain decreases. The kidney/liver (K/L) ratio of the Javan mongoose was similar to that of marine mammals. The brain/ liver (B/L) ratio was lower than K/L ratio in the Javan mongoose. It has been reported that marine mammals concentrate Hg from the food web system, and they can thus tolerate it with no apparent symptoms of poisoning (Augier et al., 1993; Cardellicchio et al., 2000). The Javan mongoose may also show no symptom of Hg poisoning.
S. Horai et al. / Chemosphere 65 (2006) 657–665
1 0.1 0.01
(a)
1
0.1
0.01
Javan mongoose
Marine mammals
Other terrestrial mammals
Javan mongoose
0.001
10
(b)
Marine mammals
-1
10
Baikal seal
100
100
Other terrestrial mammals
Pb concentration (μg g wet wt.)
1000
-1
T-Hg concentration (μg g wet wt.)
662
Fig. 2. Comparison of (a) T-Hg and (b) Pb concentrations in the liver of terrestrial and marine mammals.
Renal concentration (μg g -1 dry wt.)
1000 100 10 1 0.1 0.01 0.001
0.0001 0.001
0.01
0.1
1
10
100
1000
10000
Hepatic concentration (μg g-1 dry wt.) Javan mongoose
Japan weasel
Siberian weasel
Japanese badger
Racoon
Asiatic black bear
Masked palm civet
Japanese red fox
Japanese racoon dog
Japanese wild boar
Sika deer
Japanese serow
Japanese macaque Large Japanese field mouse
Melon headed whale
Pacific white-sided dolphin
Rough-toothed dolphin
Short-finned pilot whale
Striped dolphin
Globicephala melas
Bottlenose dolphin
Weddell seal
Spotted seal
Harbor seal
Minke whale
Northern fur seal
Baikal seal
Harbour porpoise
Caspian seal
Dall's porpoise
Fig. 3. Relationship between hepatic and renal Hg concentrations of terrestria and marine mammals.
The Hg accumulation pattern of the Javan mongoose and marine mammals which appear to tolerate Hg toxicity were compared with those of a human (National Institute for Minamata Disease, 2005) and a cat (Eto et al., 2001) causing methyl mercury toxicity (Fig. 4). The K/L ratios of the Javan mongoose and the marine mammals were much less than that of human who was diagnosed with Minamata disease, although hepatic T-Hg levels of the Javan mongoose and marine mammals were higher than that of human. The B/L ratio was lower than the K/L ratio in the Javan mongoose, indicating the transition rate from
liver was lower to the brain than to the kidneys. The B/L ratio was the same the K/L ratio in the cat which caused methyl Hg toxicity, whereas the K/L ratio of the cat was similar to those of the Javan mongoose and the marine mammals which show no symptom of Hg toxicity (Fig. 4). In contrast, the B/L ratio of the Javan mongoose (proximate equation; y = 0.435x 0.718) was about 30-fold lower than that of the cat (proximate equation; y = 3.13x 0.423) (Fig. 4). The brain and central nervous system are the primary target sites where the adverse affects of methyl Hg are manifested (Bridges and Zalups, 2005).
Ratio of T-Hg concentrationin the organs
S. Horai et al. / Chemosphere 65 (2006) 657–665
663
100
10 -0.428
y = 3.13x
1 0.1
- 0.430
y = 0.307x
y = 0.435x-0.718
0.01 y = 0.0063x-0.4
0.001 0.001
0.01
0.1
1
10
100
1000
Hepatic T-Hg concentration (μg g-1 wet wt.) Dugong Short-finned pilot whale Tappanaga Weddell seal Fur seal Harbor porpoise Javan mongoose B/L Human K/L(b)
Dall's porpoise Rough-toothed dolphin Common dolphin Largha seal Minke whale Caspian seal Cat K/L(a) Human B/L(b)
Pacific white-sided dolphin Striped dolphin Sperm whale Harbor seal Baikal seal K/L Javan mongoose K/L Cat B/L(a)
Fig. 4. Relationship between hepatic T-Hg concentrations and ratio of renal and cerebral to hepatic T-Hg concentrations of terrestrial and marine mammals. K/L: kidney/liver ratio; B/L: brain/liver ratio. Only K/L ratios are plotted in marine mammals including Baikal seal. B/L ratios of a human and a cat are pointed with arrows. (a) Eto et al. (2001), (b) National Institute for Minamata Disease (2005).
Taken together, the transition rate of Hg from the liver to the brain and methyl Hg, not T-Hg, content in tissues seem to be crucial factors as the cause of methyl Hg toxicity. Mercury is released and absorbed as methyl Hg in the gastrointestinal tract of animals, then the transport of methyl Hg from hepatocytes into the biliary canaliculus is dependent on GSH (Bridges and Zalups, 2005). The amount of methyl Hg excretion in bile is inhibited with the existence of Se (Urano et al., 1997). It may concluded that methyl Hg taken up into the livers of the Javan mongoose and marine mammals induces an increase of Se in their livers, the methyl Hg excretion to bile is then depleted by Se, subsequently a large amount of Hg accumulates in the livers of these species. Moreover, instead of a detoxification mechanism as methyl Hg excretion, the Javan mongoose and the marine mammals might possess more efficient detoxification systems, in which most of hepatic Se forms complexes with inorganic Hg (Koeman et al., 1973; Ping et al., 1986; Palmisano et al., 1995), followed by methyl Hg being converted to inorganic Hg in the liver. Even if a portion of Hg in the livers of the Javan mongoose and the marine mammals enters into the hepatic vein, most of the Hg would pass less through blood-brain barrier because most of Hg is composed of the inorganic form. The transition rate to the brain from the liver, therefore, may be lower. In regard to Hg distribution of in humans, one of the reasons for the lower accumulation of Hg in the liver may be that methyl Hg metabolism taken up in the human
body may be depend upon excretion mainly through bile, and not demethylation of methyl Hg to inorganic form in the liver. An hypothesis that a part of methyl Hg taken up in the human body may be converted to inorganic Hg mainly in the kidney, and not in the liver, may be derived from a report that the major organ in which Hg was detected was the kidney in human beings (Barrega˚rd et al., 1999). On the other hand, methyl Hg excretion is inhibited by the presence of Se, which relatively increased Hg content in the liver, subsequently methyl Hg, as methyl Hg-GSH complex, may be transported to various organs such as the kidneys and the brain. The facts that distribution of renal Hg concentrations were higher in the terrestrial mammals than in marine mammals (Fig. 3), T-Hg level distributed relatively higher in the liver of the cat caused methyl Hg toxicity was as same level as in the kidney and in the brain (Fig. 4), and Hg accumulates mainly in the kidneys of humans (Barrega˚rd et al., 1999) can be interpreted that Hg metabolism and the efficiency of demethylation in the livers of terrestrial mammals are below those of marine mammals. In this study, however, the molar ratio of T-Hg and Se concentrations in the livers of the Javan mongoose was approximately 1 (Fig. 1b), the transition rate of T-Hg from the liver to the kidneys in the Javan mongoose was similar degree to that of the marine mammals, and the transition rate of T-Hg from the liver to the brain was lower (Fig. 4), indicating the Javan mongoose possesses efficient Hg metabolic potential in the liver as with the marine mammals.
664
S. Horai et al. / Chemosphere 65 (2006) 657–665
References Aastrup, P., Riget, F., Dietz, R., Asmund, G., 2000. Lead, zinc, cadmium, mercury, selenium and copper in Greenland caribou and reindeer (Rangifer tarandus). Sci. Total. Environ. 245, 149–159. Anan, Y., Kunito, T., Watanabe, I., Sakai, H., Tanabe, S., 2001. Trace element accumulation in hawksbill turtles (Eretmochelys imbricata) and green turtles (Chelonia mydas) from Yaeyama Island, Japan. Environ. Toxicol. Chem. 20 (12), 2802–2814. Andre´, J.M., Ribeyre, F., Boudou, A., 1991. Mercury accumulation in Delphinidae. Water Air Soil Pollut. 56, 187–201. Arai, T., Ikemoto, T., Hokura, A., Terada, Y., Kunito, T., Tanabe, S., Nakai, I., 2004. Chemical forms of mercury and cadmium accumulated in marine mammals and seabirds as determined by XAFS analysis. Environ. Sci. Technol. 38, 6468–6474. Augier, H., Benkoel, L., Chamlian, A., Park, W.K., Ronneau, C., 1993. Mercury, zinc and selenium bioaccumulation in tissues and organs of Mediterranean striped dolphins Stenella coeruleoalba meyen. Toxicological result of their interaction. Cell Mol. Biol. 39, 621–634. Barrega˚rd, L., Sa¨llsten, G., Conradi, N., 1999. Tissue levels of mercury determined in a deceased worker after occupational exposure. Int. Arch. Occup. Environ. Health 72, 169–173. Bowen, H.J.M., 1979. Environmental Chemistry of the elements. Asami, T., Chino, M., 1983. Hakuyusya, Tokyo, p. 369 (in Japanese). Bridges, C.C., Zalups, R.K., 2005. Molecular and ionic mimicry and the transport of toxic metals. Toxicol. Appl. Pharmcol. 204, 274–308. Burger, J., Trivedi, C.D., Gochfeld, M., 2000. Metals in herring and great black-blacked gulls from the New York bight: the role of salt gland in excretion. Environ. Monit. Assess. 64, 569–581. Burger, J., Gaines, K.F., Lord, C.G., Brisbin Jr., I.L., Shukla, S., Gochfeld, M., 2002. Metal levels in racoon tissues: differences on and off the department of energy’s savannah river site in South Carolina. Environ. Monit. Assess. 74, 67–84. Cardellicchio, N., Giandomenico, S., Ragone, P., Di Leo, A., 2000. Tissue distribution of metals in striped dolphins (Stenella coeruleoalba) from the Apulian coasts, Southern Italy. Mar. Environ. Res. 49, 55–66. Cardellicchio, N., Decataldo, A., Di Leo, A., Misino, A., 2002. Accumulation and tissue distribution of mercury and selenium in striped dolphins (Stenella coeruleoalba) from the Mediterranean Sea (southern Italy). Environ. Pollut. 116, 265–271. Caurant, F., Navarro, M., Amiard, J.C., 1996. Mercury in pilot whales: possible limits to the detoxification process. Sci. Total Environ. 186, 95–104. Chen, M.H., Shih, C.C., Chou, C.L., Chou, L.S., 2002. Mercury, organicmercury and selenium in small cetaceans in Taiwanese waters. Mar. Pollut. Bull. 45, 237–245. Decataldo, A., Di Leo, A., Giandomenico, S., Cardellicchio, N., 2004. Association of metals (mercury, cadmium and zinc) with metallothionein-like proteins in storage organs of stranded dolphins from the Mediterranean sea (Southern Italy). J. Environ. Monit. 6, 361–367. Elliott, J.E., Scheuhammer, A.M., Leighton, F.A., Pearce, P.A., 1992. Heavy metal and metallothionein concentrations in Atlantic Canadian seabirds. Arch. Environ. Contam. Toxicol. 22, 63–73. Endo, T., Haraguchi, K., Sakata, M., 2002. Mercury and selenium concentrations in the internal organs of toothed whales and dolphins marketed for human consumptions in Japan. Sci. Total Environ. 300, 15–22. Eto, K., Yasutake, A., Nakano, A., Akagi, H., Tokunaga, H., Kojima, T., 2001. Reappraisal of the Historic 1959 cat experiment in Minamata by the Chisso Factory. Tohoku J. Exp. Med. 194, 197–203. Fant, M.L., Nyman, M., Helle, E., Rudba¨ck, E., 2001. Mercury, cadmium, lead and selenium in ringed seals (Phoca hispida) from the Baltic Sea and from Svalbard. Environ. Pollut. 111, 493–501. Frank, A., Danielsson, R., Selinus, O., 2004. Comparison of two monitoring systems for Cu and Mo in the Swedish environment. Sci. Total Environ. 330, 131–143.
Gamberg, M., Braune, B.M., 1999. Contaminant residue levels in arctic wolves (Canis lupus) from the Yukon territory, Canada. Sci. Total Environ. 243/244, 329–338. Honda, K., Tatsukawa, R., Itano, K., Miyazaki, N., Fujiyama, T., 1983. Heavy metal concentrations in muscle, liver and kidney tissue of striped dolphins, Stenella coeruleoalba, and their variations with body length, weight, age and sex. Agr. Biol. Chem. 49, 515–517. Ikemoto, T., Kunito, T., Tanaka, H., Baba, N., Miyazaki, N., Tanabe, S., 2004a. Detoxification mechanism of heavy metals in marine mammals and seabirds: interaction of selenium with mercury, silver, copper, zinc, and cadmium in liver. Arch. Environ. Contam. Toxicol. 47, 402– 413. Ikemoto, T., Kunito, T., Watanabe, I., Yasunaga, G., Baba, N., Miyazaki, N., Petrov, E.A., Tanabe, S., 2004b. Comparison of trace element accumulation in Baikal seals (Pusa sibirica), Caspian seal (Pusa caspica) and northern fur seals (Callorhinus ursinus). Environ. Pollut. 127, 83–97. Japan Wild Research Center, 2000. Toshochiikinoinyusyukujo seigyomoderujigyo (Amamioshima: mongoose) chosahoukokusyo, p. 115 (in Japanese). Kim, E.Y., Ichihashi, H., Saeki, K., Arrashkevich, G., Tanabe, S., Tatsukawa, R., 1996a. Metal accumulation in tissues of sea birds from Chaun, Northest Siberia. Russia Environ. Pollut. 92 (3), 247–252. Kim, E.Y., Murakami, T., Saeki, K., Tatsukawa, R., 1996b. Mercury levels and its chemical form in tissues and organic of seabirds. Arch. Environ. Contam. Toxicol. 30, 259–266. Kim, E.Y., Goto, R., Tanabe, S., Tanaka, H., Tatsukawa, R., 1998. Distribution of 14 elements in tissues and organs of oceanic seabirds. Arch. Environ. Contam. Toxicol. 35, 638–645. Koeman, J.H., Peeters, W.H.M., Koudstaal-Hol, C.H.M., Tjioe, P.S., de Goeij, J.J.M., 1973. Mercury–selenium correlations in marine mammals. Nature 254, 385–386. Leonzio, C., Focardi, S., Fossi, C., 1992. Heavy metals and selenium in stranded dolphins of the Northern Tyrrhenian (NW Mediterranean). Sci. Total Environ. 119, 77–84. Mackey, E.A., Becker, P.R., Demiralp, R., Greenberg, R.R., Koster, B.J., Wise, S.A., 1996. Bioaccumulation of vanadium and other trace elements in livers of Alaskan cetaceans and pinniped. Arch. Environ. Contam. Toxicol. 30, 503–512. Meador, J.P., Ernest, D., Hohn, A.A., Tilbury, K., Gorzelany, J., Worthy, G., Stein, J.E., 1999. Comparison of elements in bottlenose dolphins stranded on the beaches of Texas and Florida in the gulf of Mexico over a one-year period. Arch. Environ. Contam. Toxicol. 36, 87–98. Monaci, F., Borrel, A., Leonzio, C., Marsili, L., Calzada, N., 1998. Trace elements in striped dolphins (Stenella coeruleoalba) from the western Mediterranean. Environ. Pollut. 99, 61–68. Monteiro-Neto, C., Itavo, R.V., de Souza Moraes, L.E., 2003. Concentrations of heavy metals in Sotalia fluviatilis (Cetacea: Delphinidae) off the coast of Ceara´, northeast Brazil. Environ. Pollut. 123, 319–324. National Institute for Minamata Disease, 2005. Clinical research for Minamata disease. In: Eto, T., Takahashi, H., Kakita, A., Tokunaga, H., Yasutake, A., Nakano, A. (Eds.), pp. 4–8 (in Japanese). Palmisano, F., Cardellicchio, N., Zambonin, P.G., 1995. Speciation of mercury in dolphin liver: a two-stage mechanism for the demethylation accumulation process and role of selenium. Mar. Environ. Res. 40, 109–121. Ping, L., Nagasawa, H., Matsumoto, K., Suzuki, A., Fuwa, K., 1986. Extraction and purification of a new compound containing selenium and mercury accumulated in dolphin liver. Biol. Trace Elem. Res. 11, 185–199. Poole, K.G., Elkin, B.T., Bethke, R.W., 1998. Organochlorine and heavy metal contaminants in wild mink in western northwest territories, Canada. Arch. Environ. Contam. Toxicol. 34, 406–413. Quig, D., 1998. Cysteine metabolism and metal toxicity. Alt. Med. Rev. 3, 262–270. Rodda, G.H., Sawai, Y., Chiszar, D., Tanaka, H., 1999. Problem snake management. In: Abe, S., Handa, Y., Abe, Y., Takatsuki, Y., Nigi, H.
S. Horai et al. / Chemosphere 65 (2006) 657–665 (Eds.), Food Habits of Feral Mongoose (Herpestes sp.) on Amamioshima, Japan. Cornell University Press, Ithaca and London, pp. 372– 383. Saeki, K., Nakajima, M., Noda, K., Loughlin, T.R., Baba, N., Kiyota, M., Tatsukawa, R., Calkins, D.G., 1999. Vanadium accumulation in pinnipeds. Arch. Environ. Contam. Toxicol. 36, 81–86. Saeki, K., Nakajima, M., Loughlin, T.R., Calkins, D.G., Baba, N., Kiyota, M., Tatsukawa, R., 2001. Accumulation of silver in the liver of three species of pinnipeds. Environ. Pollut. 112, 19–25. Takekawa, J.Y., de La Cruz, S.E.W., Hothem, R.L., Yee, J., 2002. Relating body condition to inorganic contaminant concentrations of diving ducks wintering in coastal California. Arch. Environ. Contam. Toxicol. 42, 60–70. Urano, T., Imura, N., Naganuma, A., 1997. Inhibitory effect of selenium on biliary secretion of methyl mercury in rats. Biochem. Biophys. Res. Com. 239, 862–867. Uthe, J.F., Solomon, J., Grift, B., 1972. Rapid semimicro method for the determination of methyl mercury in fish tissue. J. Assoc. Off. Anal. Chem. 55 (3), 583–589.
665
Wagemann, R., Trebacz, E., Lockhart, W.L., 1998. Methylmercury and total mercury in tissues of arctic marine mammals. Sci. Total Environ. 218, 19–31. Watanabe, I., Horai, S., Arai, Y., Kuno, K., Hayashi, T., Yachimori, S., Kunito, T., Tanabe, S., 2003. Trace element accumulation in gray starling died by local mortality happened in Tochigi Prefecture in July of 2000. Environ. Sci. 16 (4), 317–328 (in Japanese). Wayland, M., Garcia-Fernandez, A.J., Neugebauer, E., Gilchrist, H.G., 2001. Concentrations of cadmium, mercury and selenium in blood, liver and kidney of common eider ducks from the Canadian Arctic. Environ. Monit. Assess. 71, 255–267. Woshner, V.M., O’Hara, T.M., Bratton, G.R., Suydam, R.S., Beasley, V.R., 2001. Concentrations and interactions of selected essential and non-essential elements in bowhead and beluga whales of Arctic Alaska. J. Wildlife Dis. 37 (4), 693–710. Wren, C.D., 1986. A review of metal accumulation and toxicity in wild mammals. I. Mercury. Environ. Res. 40, 210–244. Yanai, H., 2004. Statcel—The useful Addin Forms on Excel, second ed. Seiunsya, Tokyo, p. 270 (in Japanese).
Accumulation of Hg and other heavy metals in the Javan mongoose (Herpestes javanicus) captured on Amamioshima Island, Japan Sawako Horai a,d, Mikiko Minagawa b, Hirokazu Ozaki c, Izumi Watanabe b,*, Yasuo Takeda d, Katsushi Yamada d, Tetsuo Ando d, Suminori Akiba d, Shintaro Abe e, Katsuji Kuno b a
Department of Environmental Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo 183-8509, Japan b Department of Environmental and Natural Resource Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo 183-8509, Japan c Ocean Research Institute, The University of Tokyo, 1-15-1 Minamidai, Nakano, Tokyo 164-8639, Japan d Graduate School of Medical and Dental Sciences, Kagoshima University, 8-35-1 Sakuragaoka, Kagoshima 890-8520, Japan e Amami Wildlife Conservation Center, Ministry of the Environment, 551 Onsyojikosinohata, Yamato-son, Oshima-gun, Kagoshima 894-3104, Japan Received 5 September 2005; received in revised form 6 January 2006; accepted 26 January 2006 Available online 23 March 2006
Abstract Concentrations of 22 elements (Mg, V, Cr, Mn, Fe, Co, Ni, Cu, Zn, As, Se, Rb, Sr, Mo, Ag, Cd, Sb, Cs, Ba, Tl, total Hg (T-Hg), Pb) and organic Hg (O-Hg) were examined in the liver, kidney and brain of the Javan mongoose (Herpestes javanicus) and in liver of the Amami rabbit (Pentalagus furnessi) from Amamioshima Island in Japan. Relatively high levels of T-Hg levels (from 1.75 to 55.5 lg g 1 wet wt.) were found in the Javan mongoose. As for a comparison of hepatic T-Hg concentrations between the two areas, there was no significant difference between the Javan mongoose in Amamioshima and those in the Okinawa islands. In addition, T-Hg levels in the livers of the Amami rabbit were the same as in the livers of other herbivorous mammals. Taken together, it suggested that T-Hg accumulation in the livers of the Javan mongoose was not affected by the environment but by a specific physiological mechanism. The comparison of Hg and other heavy metal accumulations between terrestrial mammals (13 species, 61 individuals) including the Javan mongoose and marine mammals (18 species, 508 individuals) were also discussed. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Mercury; Organic mercury; Selenium; Javan mongoose; Terrestrial mammals; Marine mammals
1. Introduction As animals are at higher trophic levels, toxic effects of bioaccumulative contaminants such as some heavy metals through biomagnification are more severe (Burger et al., *
Corresponding author. Tel./fax: +81 42 367 5736. E-mail addresses: [email protected] (S. Horai), [email protected] (I. Watanabe). 0045-6535/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2006.01.078
2000). While toxic heavy metals such as Cd and Hg cause weight loss, organ damage, metabolic disorders and behavioral disorders (Takekawa et al., 2002), high specific accumulations of these metals have been found in sea turtles (Anan et al., 2001), marine mammals (Wagemann et al., 1998; Cardellicchio et al., 2000, 2002; Fant et al., 2001; Woshner et al., 2001; Chen et al., 2002; Monteiro-Neto et al., 2003; Ikemoto et al., 2004a,b) and sea birds (Elliott et al., 1992; Kim et al., 1996a,b; Kim et al., 1998; Wayland
658
S. Horai et al. / Chemosphere 65 (2006) 657–665
et al., 2001). Hence, although bioaccumulation of metals via aquatic food webs has been extensively studied, there is much less information regarding terrestrial systems. A database for heavy metal concentrations in some organs of various animals from Japan, is need to allow an analysis of heavy metal accumulation in the species and an understanding of heavy metal pollution in the country. The Javan mongoose lives in Amamioshima and the Okinawa islands in Japan. Amamioshima Island is almost 570 km in circumference and an area of approximately 719 km2. The area of this island is third largest island next to Okinawa and Sado. Because an island is isolated, there are endemic and rare organisms, which have formed peculiar biota in Amamioshima and Okinawa. The Javan mongoose could be useful as an indicator for heavy metal monitoring in a terrestrial system because it is a carnivorous terrestrial mammal and a top predator on Amamioshima Island. In this study, the heavy metal concentrations in Javan mongooses and Amami rabbits from Amamioshima Island were determined. 2. Material and methods 2.1. Samples Fifty four Javan mongooses, Herpestes javanicus, were collected from Amamioshima Island during 2004 and 2005 as part of a control of harmful wildlife. The specimens of 54 livers, 47 kidneys and 10 brains were analyzed in this study. Two Amami rabbits, Pentalagus furnessi, were collected from the same area in 2004. The deaths of the Amami rabbits were road accidents. Ten Javan mongooses were collected from Okinawa Island as part of a control of harmful wildlife in 2004. The 10 hepatic samples were used to compare the Hg level in livers with those from Amamioshima Island. All samples in this study were frozen at 80 °C until chemical analysis. Around 1979, Javan mongooses were introduced to Amamioshima Island from Okinawa Island, where the species was introduced from India as a countermeasure against bites by the habu, a species of very poisonous snake inhabiting the Amamioshima and Okinawa Islands, and also to prevent crop damage due to rodents. However, the danger of bites by the habu has been already decreasing remarkably before the Javan mongooses were introduced. This decrease has been a result of the capture of habu by human and the maintenance of the surroundings, for what the introduction of the Javan mongoose has contributed very little to the decrease in the problems (Japan Wild Research Center, 2000). In addition, excrement analysis of the Javan mongoose demonstrated that Javan mongooses have killed endemic rare species on Amamioshima Island such as the Amami rabbit, Pentalagus furnessi, and the Ryukyu robin, Erithacus komadori (Japan Wild Research Center, 2000). Extermination and control of invasive alien species are needed to protect the rare species
in the areas where unique ecosystems remain (Japan Wild Research Center, 2000). 2.2. Chemical analysis The livers, kidneys and brains were dried for 16 h at 90 °C. About 0.10 g of powdered samples were digested with 2.0 ml of nitric acid in a microwave. The concentrations of 20 elements (Mg, V, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Rb, Sr, Mo, Ag, Cd, Sb, Cs, Ba, Tl, Pb) were determined by inductively coupled plasma-mass spectrometry (ICP-MS; Hewlett-Packard, HP-4500) (Watanabe et al., 2003). Iron concentrations were measured by atomic absorption spectrometry (AAS; Hitachi, Z-5310). Mercury levels were determined by cold vapor technique using a mercury analyzer (Hiranuma, Model HG-300). Concentration of organic Hg (O-Hg) was determined with CV-AAS with the modifying Uthe et al. (1972) method. Briefly, powdered samples were mixed with CuSO4 and acidic sodium bromide to release O-Hg followed by extraction of O-Hg into the toluene phase. Part of the toluene phase was removed, and sodium thiosulfate solution was added to it. A sample of the thiosulfate solution was removed and digested with a mixture of acids (HNO3:H2SO4:HClO4 = 2 ml:2.5 ml:2 ml). The accuracy of the methods was assessed using standard reference materials DORM2 (National Research Council Canada) and SRM1577b (National Institute of Standards and Technology). The recoveries of the metals ranged from 85% to 106%. In this study, all metal concentrations were expressed on a wet wt. basis (lg g 1 wet weight [wet wt.]). Conversion of concentrations from wet weight to dry weight basis using percent of water content in the tissues was done as to requirement. 2.3. Statistical analysis Correlation between the metal concentrations in tissues was examined using the Spearman rank test. The different sets of data were compared regarding location and species using the Mann–Whitney U-test. A p-value < 0.05 was considered statistically significant. All of the statistical analyses were executed by the Statcel2 program (Yanai, 2004). 3. Results and discussion 3.1. Heavy metal concentrations in tissues Heavy metal concentrations in the tissues of the Javan mongoose collected from Amamioshima Island are shown in Table 1. Most elements were highest in the livers, the Cd concentration was highest in the kidneys and the Cr concentration was highest in the brains. Mean T-Hg concentration was 12.7 lg g 1 wet wt. in livers of the Javan mongoose and the maximum was 55.5 lg g 1 wet weight. This level was the highest compared with some terrestrial mammals studied by Wren (1986).
0.339 ± 0.235 (0.0612–1.32) n = 53 0.121 ± 0.0890 (0.0138–0.435) n = 47 0.0126 ± 0.00521 (0.00814–0.0226) n = 10 0.0141 ± 0.0107 0.000872–0.0691 n = 53 0.00615 ± 0.00327 (0.00125–0.0202) n = 47 0.00241 ± 0.00238 (0.000392–0.00673) n = 10 ND; not detected. Minimum and maximum values are in parentheses. T-Hg; Total mercury. O-Hg; Organic mercury.
Brain
Kidney
Tl O-Hg
2.45 ± 1.61 (0.610–8.61) n = 53 2.00 ± 0.872 (0.667–4.64) n = 47 0.864 ± 0.448 (0.309–1.73) n = 10 12.7 ± 10.6 (1.75–55.5) n = 53 5.12 ± 2.68 (1.26–12.6) n = 47 1.27 ± 0.807 (0.383–2.90) n = 10
T-Hg Ba
0.0183 ± 0.0130 (ND–0.0610) n = 51 0.0163 ± 0.0126 (ND–0.0507) n = 27 0.00613 ± 0.00459 (ND–0.0160) n=9 0.0540 ± 0.0279 (0.0139–0.134) n = 53 0.0501 ± 0.0274 (0.0111–0.121) n = 47 0.0346 ± 0.0181 (0.0177–0.0734) n = 10
Cs Sb
0.0186 ± 0.0125 (ND–0.0673) n = 52 0.00532 ± 0.000951 (ND–0.00685) n=5 0.00309 ± 0.00135 (ND–0.00442) n=4 0.477 ± 0.416 (0.103–2.04) n = 53 1.10 ± 1.38 (0.176–9.14) n = 47 0.00532 ± 0.00278 (ND–0.00850) n=7
Cd Ag
0.143 ± 0.194 (0.0128–1.29) n = 53 0.00156 ± 0.00168 (ND–0.00761) n = 30 0.0108 ± 0.00283 (ND–0.0139) n=4 0.409 ± 0.0848 (0.277–0.657) n = 53 0.121 ± 0.0439 (0.0315–0.326) n = 47 0.0118 ± 0.00288 (ND–0.0145) n=4
Mo Sr
Brain
Kidney
0.0759 ± 0.0252 (0.0318–0.125) n = 53 0.0809 ± 0.0432 (0.0325–0.220) n = 47 0.0899 ± 0.0394 (0.0403–0.151) n = 10
Pb
8.32 ± 3.43 (3.00–18.8) n = 53 5.87 ± 2.63 (1.01–12.8) n = 47 3.56 ± 1.04 (2.30–5.55) n = 10
Liver
Se
4.60 ± 3.27 (1.07–18.5) n = 53 1.63 ± 0.485 (0.466–3.62) n = 47 0.249 ± 0.0586 (0.184–0.377) n = 10 0.0510 ± 0.0512 (0.0129–0.385) n = 53 0.0283 ± 0.0232 (0.00740–0.105) n = 47 0.0162 ± 0.0124 (ND–0.0359) n=7
As Zn
79.1 ± 41.4 (35.3–211) n = 53 21.4 ± 7.67 (4.94–42.5) n = 47 12.8 ± 2.59 (9.82–17.1) n = 10 10.3 ± 3.25 (4.77–19.5) n = 53 3.14 ± 0.871 (0.950–6.84) n = 47 3.44 ± 0.609 (2.56–4.28) n = 10
Cu Ni
0.0201 ± 0.0217 (ND–0.0862) n = 47 0.0121 ± 0.0185 (ND–0.116) n = 42 0.00674 ± 0.00148 (ND–0.00569) n=2 0.0493 ± 0.0209 (0.0184–0.109) n = 53 0.0205 ± 0.00675 (0.00559–0.0380) n = 47 0.00832 ± 0.00425 (0.00238–0.0142) n = 10
Co Fe
216 ± 86.4 (77.5–476) n = 53 131 ± 38.0 (62.8–210) n = 47 34.4 ± 7.95 (25.3–46.2) n = 10 4.38 ± 1.72 (2.23–10.4) n = 53 0.794 ± 0.218 (0.230–1.70) n = 47 0.392 ± 0.0748 (0.288–0.507) n = 10
wet wt.) in the three organs of Javan mongoose captured at Amamioshima Island
Mn
0.0275 ± 0.0193 (ND–0.00808) n = 52 0.0118 ± 0.00610 (ND–0.0343) n = 46 0.00602 ± 0.00210 (ND–0.00742) n=4 170 ± 41.3 (101–257) n = 53 110 ± 30.5 (38.4–258) n = 47 143 ± 11.6 (133–168) n = 10 Liver
V Mg Organs
Cr
1
Table 1 Heavy metal concentrations (mean ± SD and range on lg g
0.0389 ± 0.0275 (0.00648–0.135) n = 53 0.0332 ± 0.0207 (0.00631–0.158) n = 47 0.0473 ± 0.0547 (0.0145–0.197) n = 10
Rb
S. Horai et al. / Chemosphere 65 (2006) 657–665
659
Fig. 1a shows that as T-Hg levels were higher, the O/THg concentration ratios were lower. This result was consistent with some reports about marine mammals (Caurant et al., 1996; Meador et al., 1999; Cardellicchio et al., 2000, 2002). Significant correlations of T-Hg with V, Se, Cd and O-Hg in livers, O-Hg with Cu in kidneys and T-Hg with O-Hg in brains were observed in the Javan mongoose (Table 2). Significant correlations of T-Hg with Se (Caurant et al., 1996; Wagemann et al., 1998; Meador et al., 1999; Fant et al., 2001; Woshner et al., 2001; Cardellicchio et al., 2002; Endo et al., 2002; Decataldo et al., 2004), Cd (Woshner et al., 2001) and O-Hg (Honda et al., 1983; Andre´ et al., 1991; Leonzio et al., 1992; Woshner et al., 2001; Chen et al., 2002) in the livers of marine mammals were studied. The molar ratio of T-Hg and Se concentrations in the livers of the Javan mongoose was almost 1 (Fig. 1b). This result was consistent with some studies of marine mammals. The marine mammals may have adapted so as to tolerate high Hg levels because of a detoxification mechanism involved in Se metabolism in the liver (Wagemann et al., 1998; Cardellicchio et al., 2000; Endo et al., 2002; Arai et al., 2004). Javan mongooses may also tolerate Hg toxicity because they have an efficient detoxification system of methyl Hg in their livers as with marine mammals. The correlation of Hg with Ag similar to Se was observed in the livers of the marine mammals (Mackey et al., 1996; Saeki et al., 2001; Woshner et al., 2001). Moreover, Saeki et al. (1999) has reported that there were not only the correlations of Hg with Ag and Se but also V in livers of marine mammals and that V could behave similarly to Hg and Ag, therefore V might accumulate in tissues as a contaminant similar to Hg and Ag. In contrast to the marine mammals, however, there were no significant correlations of Hg–Ag and V–Ag in the livers of Javan mongoose (p = 0.131 and p = 0.259, respectively). Amami rabbits are endemic and rare species which inhabit only Amamioshima and Tokunoshima Islands in the Amamioshima Archipelago. They were the first species designated as a natural monument and are now designated as species in danger of extinction 1B in Japan. The trace element concentrations in the livers of Amami rabbits are shown in Table 3. Mean T-Hg concentration in the livers of Amami rabbits was 0.032 lg g 1 wet wt. This value was the same level as in caribou, reindeer (Aastrup et al., 2000) and hares (Poole et al., 1998), which are also herbivores, and lower than raccoons (Burger et al., 2002), an omnivore, arctic wolves (Gamberg and Braune, 1999) and minks (Poole et al., 1998), which are carnivores. Taken together, it is suggested that the accumulation of T-Hg in the livers of Amami rabbits was affected by diet, and much higher T-Hg concentrations in the livers of the Javan mongoose might be a specific accumulation. Most of the hepatic metal concentrations measured were higher in the Javan mongoose than in the Amami rabbit except for Co, Sr, Mo and Ba. Relatively higher Mo concentrations found in the livers of moose (Frank et al.,
660
S. Horai et al. / Chemosphere 65 (2006) 657–665 T-Hg concentration (μmol g -1 wet wt.)
Persent O-Hg (of T-Hg)
120 Liver
100
Kidney Brain
80 60 40 20 0
0
20
(a)
40
60
Total Hg concentration (μg g-1 wet wt.)
0.3
0.2
1:1 0.1
Liver Kidney Brain
0.0 0.0
(b)
0.1
0.2
0.3
Se concentration (μmol g-1 wet wt.)
Fig. 1. Relationships between (a) T-Hg and percent organic Hg , and (b) Se and T-Hg concentrations in three organs of Javan mongoose.
Furthermore, as described above, the hepatic T-Hg level of the Amami rabbit was similar to that of some herbivorous mammals living in other areas, indicating that the hepatic T-Hg accumulation of the Javan mongoose is specific. Mercury enters the water as a natural process of off-gassing from the earth’s crust and as a result of industrial pollution, then methylated by algae and bacteria in the water and moving up the food chain to its highest concentrations in large predatory fish such as swordfish, sharks and tuna (Quig, 1998), which can contain high levels of methyl Hg (Bridges and Zalups, 2005). Mercury accumulation of marine mammals is dependent upon biomagnifications (Monaci et al., 1998; Fant et al., 2001; Cardellicchio et al., 2002; Endo et al., 2002). Although the hepatic T-Hg level of the Javan mongoose is at the same level as those of marine mammals, it is not dependent upon an aquatic food system. The major diet of the Javan mongoose is insects, such as crickets and grasshoppers, and non-insect invertebrates (Rodda et al., 1999). Mammalian and avian preys, mostly rodents, have also been found in Javan mongoose gastrointestinal tracts (Rodda et al., 1999). This information indicates that T-Hg accumulation in the Javan mongoose may be caused by unique biomagnifications, which are involved in the physiological mechanisms such as high Hg absorbent ability, high Hg accumulation and/or low Hg excretion.
Table 2 Spearman’s rank correlation coefficient between Hg and other element concentrations in the three organs of Javan mongoose
Liver THg-V THg-Se THg-Cd THg-OHg Kidney OHg-Cu Brain THg-OHg
r
p
0.297 0.916 0.677 0.802
0.032 <0.001 <0.001 <0.001
0.366
0.013
0.988
0.003
2004) and feral pigeons (unpublished data), which are herbivores, may support that the these element contents in herbivores is higher than in carnivores. 3.2. Area difference We compared hepatic T-Hg concentrations in the Javan mongoose from Amamioshima Island with those from Okinawa Island (mean of 23.1 lg g 1 wet wt., minimum and maximum were 0.465 lg g 1 wet wt. and 112 lg g 1 wet wt., respectively, n = 10) to clarify whether the high T-Hg accumulation in the Javan mongoose is affected by their habitat, and no significant area difference of T-Hg concentrations was subsequently observed (p = 0.679).
Table 3 Heavy metal concentrations (range on lg g
1
wet wt.) in the liver of Amami Rabbit collected from Amamioshima Island
Sample ID
Mg
V
Cr
Mn
Fe
Co
Ni
Cu
Zn
As
Se
04-0412 04-0421 Mean
200 188 194
0.0332 0.0166 0.0249
0.0462 0.0371 0.0417
3.54 3.67 3.61
348 347 348
0.0618 0.0569 0.0593
0.0119 0.0254 0.0186
4.26 4.21 4.24
26.5 32.7 29.6
0.0298 0.0212 0.0255
0.213 0.342 0.278
Rb
Sr
Mo
Ag
Cd
Sb
Cs
Ba
T-Hg
Tl
Pb
2.86 11.6 7.24
0.399 0.250 0.325
1.18 0.983 1.08
ND ND –
0.0479 0.171 0.109
0.00922 0.00740 0.00831
0.0302 0.0872 0.0587
0.147 0.0708 0.109
0.00967 0.0543 0.0320
0.00803 0.00860 0.00831
0.0977 0.109 0.103
04-0412 04-0421 Mean
ND; not detected.
S. Horai et al. / Chemosphere 65 (2006) 657–665
661
Table 4 Marine mammal and terrestrial mammal species Species
n
Sampling site
Marine mammals Bikal seal (Phoca sibirica) Bottlenose dolphin (Tursiops truncatus) Caspian seal (Phoca caspica) Dall’s porpoise (Phocoenoides dalli) Dugong (Dugong dugong) Habour seal (Phoca vitulina largha) Harbour porpoise (Phocoena phocoena) Melon headed whale (Peponocephala electra) Minke whale (Balaenoptera acutorostrata) Northern fur seal (Callorhinus ursinus) Pacific white-sided dolphin (Lagenorhynchus obliquidens) Rough-toothed dolphin (Steno bredanensis) Short-finned pilot whale (Globicephala macrorhynchus) Short-finned pilot whale (Globicephala melas) Sperm whale (Physeter macrocephalus) Spotted seal (Phoca largha) Striped dolphin (Stenella coeruleoalba) Weddell seal (Leptonychotes weddelli)
40 3 42 130 3 31 47 18 37 4 19 13 47 28 1 20 22 3
Lake Baikal Japanese waters Caspian Sea Japanese waters Okinawa and Indonesia Japanese waters Black Sea Japanese waters Antarctic Sea Japanese waters Japanese waters Japanese waters Japanese waters Japanese waters Japanese waters Japanese waters Japanese waters Antarctic Sea
Terrestrial mammals Asiatic black bear (Selenarctos thibetanus) Japanese weasel (Mustela itatsi) Japanese badger (Meles meles) Japanese macaque (Maccaca fuscata) Japanese raccoon dog (Nyctereutes procyonoides) Japanese red fox (Vulpes vulpes) Japanese serow (Capricornis crispus) Japanese wild boar (Sus leucomustax) Large Japanese field mice (Apodemus speciosus) Masked palm civet (Paguma larvata) Racoon (Procyon lotor) Siberian weasel (Mustela sibirica) Sika deer (Cervus nippon)
3.3. Comparison of terrestrial and marine mammals High T-Hg accumulation was found in the liver of the Javan mongoose, which is a terrestrial mammal. Next, the T-Hg concentrations of terrestrial mammals, including Javan mongoose, were compared with those of marine mammals to characterize the Hg accumulation of the Javan mongoose. The marine and terrestrial mammalian species used for this comparative study are shown in Table 4 (Unpublished data). Fig. 2a shows a comparison of hepatic T-Hg levels between the terrestrial mammals including the Javan mongoose and the marine mammals except dugongs which are herbivores. No significant difference was observed between the T-Hg levels of the Javan mongoose and marine mammals which contain relatively higher T-Hg than other organisms (p = 0.204). A significant difference of hepatic Pb levels between the terrestrial mammals, including the Javan mongoose, and the marine mammals including the Baikal seal inhabiting freshwater was observed (p < 0.001) (Fig. 2b). The Pb level is higher in fresh water and terrestrial realms than in the marine realm (Bowen, 1979), indicating a significant difference of hepatic Pb levels between terrestrial and marine mammals is dependent on their habitats. Therefore, marine
4 16 3 2 3 3 1 4 1 9 5 5 5
Japan Japan Japan Japan Japan Japan Japan Japan Japan Japan Japan Japan Japan
mammals may be weaker against Pb toxicity than terrestrial mammals, although the marine mammals possess a tolerance of Hg toxicity. In regard to a comparison of the relationship between hepatic and renal T-Hg concentrations of terrestrial and marine groups, T-Hg concentrations were similarly distributed in the livers of the Javan mongoose, the Baikal seal and the marine mammals (Fig. 3). However, T-Hg accumulation patterns of the Javan mongoose and the Baikal seal inhabiting freshwater showed that the distribution levels were higher in the kidneys than those of the marine mammals. The relationship between hepatic T-Hg concentrations and ratios of renal and cerebral to hepatic T-Hg concentrations is shown in Fig. 4. As hepatic T-Hg level increases, the transition rate of T-Hg from liver to kidney and brain decreases. The kidney/liver (K/L) ratio of the Javan mongoose was similar to that of marine mammals. The brain/ liver (B/L) ratio was lower than K/L ratio in the Javan mongoose. It has been reported that marine mammals concentrate Hg from the food web system, and they can thus tolerate it with no apparent symptoms of poisoning (Augier et al., 1993; Cardellicchio et al., 2000). The Javan mongoose may also show no symptom of Hg poisoning.
S. Horai et al. / Chemosphere 65 (2006) 657–665
1 0.1 0.01
(a)
1
0.1
0.01
Javan mongoose
Marine mammals
Other terrestrial mammals
Javan mongoose
0.001
10
(b)
Marine mammals
-1
10
Baikal seal
100
100
Other terrestrial mammals
Pb concentration (μg g wet wt.)
1000
-1
T-Hg concentration (μg g wet wt.)
662
Fig. 2. Comparison of (a) T-Hg and (b) Pb concentrations in the liver of terrestrial and marine mammals.
Renal concentration (μg g -1 dry wt.)
1000 100 10 1 0.1 0.01 0.001
0.0001 0.001
0.01
0.1
1
10
100
1000
10000
Hepatic concentration (μg g-1 dry wt.) Javan mongoose
Japan weasel
Siberian weasel
Japanese badger
Racoon
Asiatic black bear
Masked palm civet
Japanese red fox
Japanese racoon dog
Japanese wild boar
Sika deer
Japanese serow
Japanese macaque Large Japanese field mouse
Melon headed whale
Pacific white-sided dolphin
Rough-toothed dolphin
Short-finned pilot whale
Striped dolphin
Globicephala melas
Bottlenose dolphin
Weddell seal
Spotted seal
Harbor seal
Minke whale
Northern fur seal
Baikal seal
Harbour porpoise
Caspian seal
Dall's porpoise
Fig. 3. Relationship between hepatic and renal Hg concentrations of terrestria and marine mammals.
The Hg accumulation pattern of the Javan mongoose and marine mammals which appear to tolerate Hg toxicity were compared with those of a human (National Institute for Minamata Disease, 2005) and a cat (Eto et al., 2001) causing methyl mercury toxicity (Fig. 4). The K/L ratios of the Javan mongoose and the marine mammals were much less than that of human who was diagnosed with Minamata disease, although hepatic T-Hg levels of the Javan mongoose and marine mammals were higher than that of human. The B/L ratio was lower than the K/L ratio in the Javan mongoose, indicating the transition rate from
liver was lower to the brain than to the kidneys. The B/L ratio was the same the K/L ratio in the cat which caused methyl Hg toxicity, whereas the K/L ratio of the cat was similar to those of the Javan mongoose and the marine mammals which show no symptom of Hg toxicity (Fig. 4). In contrast, the B/L ratio of the Javan mongoose (proximate equation; y = 0.435x 0.718) was about 30-fold lower than that of the cat (proximate equation; y = 3.13x 0.423) (Fig. 4). The brain and central nervous system are the primary target sites where the adverse affects of methyl Hg are manifested (Bridges and Zalups, 2005).
Ratio of T-Hg concentrationin the organs
S. Horai et al. / Chemosphere 65 (2006) 657–665
663
100
10 -0.428
y = 3.13x
1 0.1
- 0.430
y = 0.307x
y = 0.435x-0.718
0.01 y = 0.0063x-0.4
0.001 0.001
0.01
0.1
1
10
100
1000
Hepatic T-Hg concentration (μg g-1 wet wt.) Dugong Short-finned pilot whale Tappanaga Weddell seal Fur seal Harbor porpoise Javan mongoose B/L Human K/L(b)
Dall's porpoise Rough-toothed dolphin Common dolphin Largha seal Minke whale Caspian seal Cat K/L(a) Human B/L(b)
Pacific white-sided dolphin Striped dolphin Sperm whale Harbor seal Baikal seal K/L Javan mongoose K/L Cat B/L(a)
Fig. 4. Relationship between hepatic T-Hg concentrations and ratio of renal and cerebral to hepatic T-Hg concentrations of terrestrial and marine mammals. K/L: kidney/liver ratio; B/L: brain/liver ratio. Only K/L ratios are plotted in marine mammals including Baikal seal. B/L ratios of a human and a cat are pointed with arrows. (a) Eto et al. (2001), (b) National Institute for Minamata Disease (2005).
Taken together, the transition rate of Hg from the liver to the brain and methyl Hg, not T-Hg, content in tissues seem to be crucial factors as the cause of methyl Hg toxicity. Mercury is released and absorbed as methyl Hg in the gastrointestinal tract of animals, then the transport of methyl Hg from hepatocytes into the biliary canaliculus is dependent on GSH (Bridges and Zalups, 2005). The amount of methyl Hg excretion in bile is inhibited with the existence of Se (Urano et al., 1997). It may concluded that methyl Hg taken up into the livers of the Javan mongoose and marine mammals induces an increase of Se in their livers, the methyl Hg excretion to bile is then depleted by Se, subsequently a large amount of Hg accumulates in the livers of these species. Moreover, instead of a detoxification mechanism as methyl Hg excretion, the Javan mongoose and the marine mammals might possess more efficient detoxification systems, in which most of hepatic Se forms complexes with inorganic Hg (Koeman et al., 1973; Ping et al., 1986; Palmisano et al., 1995), followed by methyl Hg being converted to inorganic Hg in the liver. Even if a portion of Hg in the livers of the Javan mongoose and the marine mammals enters into the hepatic vein, most of the Hg would pass less through blood-brain barrier because most of Hg is composed of the inorganic form. The transition rate to the brain from the liver, therefore, may be lower. In regard to Hg distribution of in humans, one of the reasons for the lower accumulation of Hg in the liver may be that methyl Hg metabolism taken up in the human
body may be depend upon excretion mainly through bile, and not demethylation of methyl Hg to inorganic form in the liver. An hypothesis that a part of methyl Hg taken up in the human body may be converted to inorganic Hg mainly in the kidney, and not in the liver, may be derived from a report that the major organ in which Hg was detected was the kidney in human beings (Barrega˚rd et al., 1999). On the other hand, methyl Hg excretion is inhibited by the presence of Se, which relatively increased Hg content in the liver, subsequently methyl Hg, as methyl Hg-GSH complex, may be transported to various organs such as the kidneys and the brain. The facts that distribution of renal Hg concentrations were higher in the terrestrial mammals than in marine mammals (Fig. 3), T-Hg level distributed relatively higher in the liver of the cat caused methyl Hg toxicity was as same level as in the kidney and in the brain (Fig. 4), and Hg accumulates mainly in the kidneys of humans (Barrega˚rd et al., 1999) can be interpreted that Hg metabolism and the efficiency of demethylation in the livers of terrestrial mammals are below those of marine mammals. In this study, however, the molar ratio of T-Hg and Se concentrations in the livers of the Javan mongoose was approximately 1 (Fig. 1b), the transition rate of T-Hg from the liver to the kidneys in the Javan mongoose was similar degree to that of the marine mammals, and the transition rate of T-Hg from the liver to the brain was lower (Fig. 4), indicating the Javan mongoose possesses efficient Hg metabolic potential in the liver as with the marine mammals.
664
S. Horai et al. / Chemosphere 65 (2006) 657–665
References Aastrup, P., Riget, F., Dietz, R., Asmund, G., 2000. Lead, zinc, cadmium, mercury, selenium and copper in Greenland caribou and reindeer (Rangifer tarandus). Sci. Total. Environ. 245, 149–159. Anan, Y., Kunito, T., Watanabe, I., Sakai, H., Tanabe, S., 2001. Trace element accumulation in hawksbill turtles (Eretmochelys imbricata) and green turtles (Chelonia mydas) from Yaeyama Island, Japan. Environ. Toxicol. Chem. 20 (12), 2802–2814. Andre´, J.M., Ribeyre, F., Boudou, A., 1991. Mercury accumulation in Delphinidae. Water Air Soil Pollut. 56, 187–201. Arai, T., Ikemoto, T., Hokura, A., Terada, Y., Kunito, T., Tanabe, S., Nakai, I., 2004. Chemical forms of mercury and cadmium accumulated in marine mammals and seabirds as determined by XAFS analysis. Environ. Sci. Technol. 38, 6468–6474. Augier, H., Benkoel, L., Chamlian, A., Park, W.K., Ronneau, C., 1993. Mercury, zinc and selenium bioaccumulation in tissues and organs of Mediterranean striped dolphins Stenella coeruleoalba meyen. Toxicological result of their interaction. Cell Mol. Biol. 39, 621–634. Barrega˚rd, L., Sa¨llsten, G., Conradi, N., 1999. Tissue levels of mercury determined in a deceased worker after occupational exposure. Int. Arch. Occup. Environ. Health 72, 169–173. Bowen, H.J.M., 1979. Environmental Chemistry of the elements. Asami, T., Chino, M., 1983. Hakuyusya, Tokyo, p. 369 (in Japanese). Bridges, C.C., Zalups, R.K., 2005. Molecular and ionic mimicry and the transport of toxic metals. Toxicol. Appl. Pharmcol. 204, 274–308. Burger, J., Trivedi, C.D., Gochfeld, M., 2000. Metals in herring and great black-blacked gulls from the New York bight: the role of salt gland in excretion. Environ. Monit. Assess. 64, 569–581. Burger, J., Gaines, K.F., Lord, C.G., Brisbin Jr., I.L., Shukla, S., Gochfeld, M., 2002. Metal levels in racoon tissues: differences on and off the department of energy’s savannah river site in South Carolina. Environ. Monit. Assess. 74, 67–84. Cardellicchio, N., Giandomenico, S., Ragone, P., Di Leo, A., 2000. Tissue distribution of metals in striped dolphins (Stenella coeruleoalba) from the Apulian coasts, Southern Italy. Mar. Environ. Res. 49, 55–66. Cardellicchio, N., Decataldo, A., Di Leo, A., Misino, A., 2002. Accumulation and tissue distribution of mercury and selenium in striped dolphins (Stenella coeruleoalba) from the Mediterranean Sea (southern Italy). Environ. Pollut. 116, 265–271. Caurant, F., Navarro, M., Amiard, J.C., 1996. Mercury in pilot whales: possible limits to the detoxification process. Sci. Total Environ. 186, 95–104. Chen, M.H., Shih, C.C., Chou, C.L., Chou, L.S., 2002. Mercury, organicmercury and selenium in small cetaceans in Taiwanese waters. Mar. Pollut. Bull. 45, 237–245. Decataldo, A., Di Leo, A., Giandomenico, S., Cardellicchio, N., 2004. Association of metals (mercury, cadmium and zinc) with metallothionein-like proteins in storage organs of stranded dolphins from the Mediterranean sea (Southern Italy). J. Environ. Monit. 6, 361–367. Elliott, J.E., Scheuhammer, A.M., Leighton, F.A., Pearce, P.A., 1992. Heavy metal and metallothionein concentrations in Atlantic Canadian seabirds. Arch. Environ. Contam. Toxicol. 22, 63–73. Endo, T., Haraguchi, K., Sakata, M., 2002. Mercury and selenium concentrations in the internal organs of toothed whales and dolphins marketed for human consumptions in Japan. Sci. Total Environ. 300, 15–22. Eto, K., Yasutake, A., Nakano, A., Akagi, H., Tokunaga, H., Kojima, T., 2001. Reappraisal of the Historic 1959 cat experiment in Minamata by the Chisso Factory. Tohoku J. Exp. Med. 194, 197–203. Fant, M.L., Nyman, M., Helle, E., Rudba¨ck, E., 2001. Mercury, cadmium, lead and selenium in ringed seals (Phoca hispida) from the Baltic Sea and from Svalbard. Environ. Pollut. 111, 493–501. Frank, A., Danielsson, R., Selinus, O., 2004. Comparison of two monitoring systems for Cu and Mo in the Swedish environment. Sci. Total Environ. 330, 131–143.
Gamberg, M., Braune, B.M., 1999. Contaminant residue levels in arctic wolves (Canis lupus) from the Yukon territory, Canada. Sci. Total Environ. 243/244, 329–338. Honda, K., Tatsukawa, R., Itano, K., Miyazaki, N., Fujiyama, T., 1983. Heavy metal concentrations in muscle, liver and kidney tissue of striped dolphins, Stenella coeruleoalba, and their variations with body length, weight, age and sex. Agr. Biol. Chem. 49, 515–517. Ikemoto, T., Kunito, T., Tanaka, H., Baba, N., Miyazaki, N., Tanabe, S., 2004a. Detoxification mechanism of heavy metals in marine mammals and seabirds: interaction of selenium with mercury, silver, copper, zinc, and cadmium in liver. Arch. Environ. Contam. Toxicol. 47, 402– 413. Ikemoto, T., Kunito, T., Watanabe, I., Yasunaga, G., Baba, N., Miyazaki, N., Petrov, E.A., Tanabe, S., 2004b. Comparison of trace element accumulation in Baikal seals (Pusa sibirica), Caspian seal (Pusa caspica) and northern fur seals (Callorhinus ursinus). Environ. Pollut. 127, 83–97. Japan Wild Research Center, 2000. Toshochiikinoinyusyukujo seigyomoderujigyo (Amamioshima: mongoose) chosahoukokusyo, p. 115 (in Japanese). Kim, E.Y., Ichihashi, H., Saeki, K., Arrashkevich, G., Tanabe, S., Tatsukawa, R., 1996a. Metal accumulation in tissues of sea birds from Chaun, Northest Siberia. Russia Environ. Pollut. 92 (3), 247–252. Kim, E.Y., Murakami, T., Saeki, K., Tatsukawa, R., 1996b. Mercury levels and its chemical form in tissues and organic of seabirds. Arch. Environ. Contam. Toxicol. 30, 259–266. Kim, E.Y., Goto, R., Tanabe, S., Tanaka, H., Tatsukawa, R., 1998. Distribution of 14 elements in tissues and organs of oceanic seabirds. Arch. Environ. Contam. Toxicol. 35, 638–645. Koeman, J.H., Peeters, W.H.M., Koudstaal-Hol, C.H.M., Tjioe, P.S., de Goeij, J.J.M., 1973. Mercury–selenium correlations in marine mammals. Nature 254, 385–386. Leonzio, C., Focardi, S., Fossi, C., 1992. Heavy metals and selenium in stranded dolphins of the Northern Tyrrhenian (NW Mediterranean). Sci. Total Environ. 119, 77–84. Mackey, E.A., Becker, P.R., Demiralp, R., Greenberg, R.R., Koster, B.J., Wise, S.A., 1996. Bioaccumulation of vanadium and other trace elements in livers of Alaskan cetaceans and pinniped. Arch. Environ. Contam. Toxicol. 30, 503–512. Meador, J.P., Ernest, D., Hohn, A.A., Tilbury, K., Gorzelany, J., Worthy, G., Stein, J.E., 1999. Comparison of elements in bottlenose dolphins stranded on the beaches of Texas and Florida in the gulf of Mexico over a one-year period. Arch. Environ. Contam. Toxicol. 36, 87–98. Monaci, F., Borrel, A., Leonzio, C., Marsili, L., Calzada, N., 1998. Trace elements in striped dolphins (Stenella coeruleoalba) from the western Mediterranean. Environ. Pollut. 99, 61–68. Monteiro-Neto, C., Itavo, R.V., de Souza Moraes, L.E., 2003. Concentrations of heavy metals in Sotalia fluviatilis (Cetacea: Delphinidae) off the coast of Ceara´, northeast Brazil. Environ. Pollut. 123, 319–324. National Institute for Minamata Disease, 2005. Clinical research for Minamata disease. In: Eto, T., Takahashi, H., Kakita, A., Tokunaga, H., Yasutake, A., Nakano, A. (Eds.), pp. 4–8 (in Japanese). Palmisano, F., Cardellicchio, N., Zambonin, P.G., 1995. Speciation of mercury in dolphin liver: a two-stage mechanism for the demethylation accumulation process and role of selenium. Mar. Environ. Res. 40, 109–121. Ping, L., Nagasawa, H., Matsumoto, K., Suzuki, A., Fuwa, K., 1986. Extraction and purification of a new compound containing selenium and mercury accumulated in dolphin liver. Biol. Trace Elem. Res. 11, 185–199. Poole, K.G., Elkin, B.T., Bethke, R.W., 1998. Organochlorine and heavy metal contaminants in wild mink in western northwest territories, Canada. Arch. Environ. Contam. Toxicol. 34, 406–413. Quig, D., 1998. Cysteine metabolism and metal toxicity. Alt. Med. Rev. 3, 262–270. Rodda, G.H., Sawai, Y., Chiszar, D., Tanaka, H., 1999. Problem snake management. In: Abe, S., Handa, Y., Abe, Y., Takatsuki, Y., Nigi, H.
S. Horai et al. / Chemosphere 65 (2006) 657–665 (Eds.), Food Habits of Feral Mongoose (Herpestes sp.) on Amamioshima, Japan. Cornell University Press, Ithaca and London, pp. 372– 383. Saeki, K., Nakajima, M., Noda, K., Loughlin, T.R., Baba, N., Kiyota, M., Tatsukawa, R., Calkins, D.G., 1999. Vanadium accumulation in pinnipeds. Arch. Environ. Contam. Toxicol. 36, 81–86. Saeki, K., Nakajima, M., Loughlin, T.R., Calkins, D.G., Baba, N., Kiyota, M., Tatsukawa, R., 2001. Accumulation of silver in the liver of three species of pinnipeds. Environ. Pollut. 112, 19–25. Takekawa, J.Y., de La Cruz, S.E.W., Hothem, R.L., Yee, J., 2002. Relating body condition to inorganic contaminant concentrations of diving ducks wintering in coastal California. Arch. Environ. Contam. Toxicol. 42, 60–70. Urano, T., Imura, N., Naganuma, A., 1997. Inhibitory effect of selenium on biliary secretion of methyl mercury in rats. Biochem. Biophys. Res. Com. 239, 862–867. Uthe, J.F., Solomon, J., Grift, B., 1972. Rapid semimicro method for the determination of methyl mercury in fish tissue. J. Assoc. Off. Anal. Chem. 55 (3), 583–589.
665
Wagemann, R., Trebacz, E., Lockhart, W.L., 1998. Methylmercury and total mercury in tissues of arctic marine mammals. Sci. Total Environ. 218, 19–31. Watanabe, I., Horai, S., Arai, Y., Kuno, K., Hayashi, T., Yachimori, S., Kunito, T., Tanabe, S., 2003. Trace element accumulation in gray starling died by local mortality happened in Tochigi Prefecture in July of 2000. Environ. Sci. 16 (4), 317–328 (in Japanese). Wayland, M., Garcia-Fernandez, A.J., Neugebauer, E., Gilchrist, H.G., 2001. Concentrations of cadmium, mercury and selenium in blood, liver and kidney of common eider ducks from the Canadian Arctic. Environ. Monit. Assess. 71, 255–267. Woshner, V.M., O’Hara, T.M., Bratton, G.R., Suydam, R.S., Beasley, V.R., 2001. Concentrations and interactions of selected essential and non-essential elements in bowhead and beluga whales of Arctic Alaska. J. Wildlife Dis. 37 (4), 693–710. Wren, C.D., 1986. A review of metal accumulation and toxicity in wild mammals. I. Mercury. Environ. Res. 40, 210–244. Yanai, H., 2004. Statcel—The useful Addin Forms on Excel, second ed. Seiunsya, Tokyo, p. 270 (in Japanese).