Research High Percentage of Butyltin Residues in Total Tin in the Livers of Cetaceans from Japanese Coastal Waters LE THI HAI LE,† SHIN TAKAHASHI,† KAZUTOSHI SAEKI,‡ NOBUTAKE NAKATANI,† S H I N S U K E T A N A B E , * ,† NOBUYUKI MIYAZAKI,§ AND YOSHIHIRO FUJISE# Department of Environment Conservation, Ehime University, Tarumi 3-5-7, Matsuyama 790-8566, Japan, Faculty of Education, Oita University, Dannoharu 700, Oita 870-1192 Japan, Otsuchi Marine Research Center, Ocean Research Institute, The University of Tokyo, Iwate 028-1102, Japan, and The Institute of Cetacean Research, 4-8 Toyomi-cho, Tokyo 104-0055, Japan
There have been few reports on quantitative discussion of organic tin compounds based on total tin in environmental media and biota. The present study determined concentrations of total tin (∑Sn ) organic + inorganic) and butyltin compounds (∑BTs ) MBT + DBT + TBT) in the livers of cetaceans collected from Japanese coastal waters in order to estimate the ratio of ∑BTs:∑Sn and to elucidate the role of anthropogenic butyltins in the view of total tin accumulation in these higher trophic organisms. Additionally, some cetacean species from open seas and oceans were also subjected to analyses for comparison purposes. Higher concentrations of ∑Sn and ∑BTs were found in coastal species than in offshore species, indicating greater input of tin compounds in coastal waters surrounding Japan. ∑Sn concentrations increased with an increase in ∑BTs residues in all species analyzed (r ) 0.95, p < 0.001). Furthermore, ∑BTs made up considerably higher percentages of the hepatic ∑Sn in coastal species, with up to 74% in finless porpoise (Neophocaena phocaenoides) and 90% in bottlenose dolphin (Tursiops truncatus). These findings suggest that hepatic tin in coastal cetaceans predominantly exists in organic form such as butyltin compounds, implying that tin residues in marine mammals reflect mostly the input from anthropogenic sources. Despite some similar features expected between the residues of tin and mercury, anthropogenic exposure to tin compounds seems to be more apparent than exposure to mercury, which generally originates from natural exposure.
Introduction During the past several decades, butyltin compounds (BTs) have been widely used as an antifouling agent in paints for boats, ships, and aquaculture nets (1, 2); thus, these compounds have been found in a variety of marine organisms, often at concentrations exceeding the acute and chronic toxicity levels (3, 4). Consequently, the serious pollution and 10.1021/es980624t CCC: $18.00 Published on Web 04/10/1999
1999 American Chemical Society
hazardous effects of antifouling paints containing butyltins on marine ecosystems has become a great environmental issue all over the world (5-8). To prevent the destruction of marine ecosystems, usage of antifouling paints on small boats and fish farming equipment has been banned or regulated in developed nations since the late 1980s (6, 7). Nevertheless, significant accumulation of BTs including monobutyltin (MBT), dibutyltin (DBT), and tributyltin (TBT) has been noted in cetaceans, pinnipeds, and seabirds (8-15), indicating that BTs’ impact remains in higher trophic marine organisms. Because marine mammals have a low capacity of drugmetabolizing enzyme systems (16-18), high accumulation of BTs has been observed. Monitoring studies on the accumulation of BTs in marine mammals have clearly demonstrated significant residues and worldwide distribution (8-14). Although the relationship between organic and inorganic mercury has been well documented in a variety of animals (20-28), to date, few investigations have been done regarding total tin (sum of inorganic and organic tin). To our knowledge, only a recent study of fish, mussels, and algae from the German coast has been reported concerning total tin (19). Determination of total tin may lead to a further understanding of anthropogenic effect of organotins in the ecosystem and could provide an important insight into the whole spectrum of environmental behavior of this element. Moreover, studies for the interpretation of organotin data, as part of total tin analysis, have not been done in higher trophic marine organisms, such as dolphins and whales. The present study attempts to understand the current status of contamination and the specific accumulation and behavior of ∑Sn (organic + inorganic) and ∑BTs (MBT + DBT + TBT) in cetaceans, which are representatives of higher trophic organisms in the aquatic ecosystem. Earlier studies indicated that marine mammals retained the highest concentration of BTs in the liver (10-13). Recently, we also found the highest concentration of ∑Sn in the liver of finless porpoises among the various organs/tissues analyzed (data not published), suggesting that the liver of marine mammals is the target organ for tin accumulation. Hence, we investigated total tin residues in the liver of various cetaceans. In addition, some previous data on BTs in cetacean species reported by our research team (8, 10-12, 14) were used for evaluating the ∑BTs-∑Sn relationship in these animals.
Materials and Methods Sampling. Cetaceans were collected from 1983 to 1996 in different localities along the coastal waters of Japan, The Philippines, India, the Black Sea, and the North Pacific Ocean (Figure 1). About 120 samples from 16 species of cetaceans (Table 1) were analyzed for ∑Sn and ∑BTs concentrations. Hepatic samples of cetaceans used in this study were obtained from three sources: (1) fresh strandings along the coasts; (2) accidental catches by fishermen; and (3) specimens collected by Whaling for Commercial and Scientific Purposes that were accepted by an International Convention for the Regulation of Whaling. In the course of our research work, species of a larger number of populations were collected, and endangered * Author to whom correspondence should be addressed. Phone: +81 89 946 9904; fax: +81 89 946 9904; e-mail:
[email protected]. † Ehime University. ‡ Oita University. § The University of Tokyo. # The Institute of Cetacean Research, Tokyo. VOL. 33, NO. 11, 1999 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 1. Sampling location of cetaceans for the present study. species were ruled out. Finless porpoise (Nephocaena phocaenoides), bottlenose dolphin (Tursiops truncatus), harbor porpoise (Phonica phonica), and Indo-Pacific humpback dolphin (Sousa chinensis) caught from inshore areas were recognized as coastal species. The other cetaceans including a variety of dolphins, porpoises, and whales were considered to be offshore species (29). Cetaceans in the maturity stage were selectively employed for the present study. Immediately after dissection, hepatic samples were frozen in clean bags and then transported to the laboratory and stored at -20 °C until chemical analysis. Chemical Analysis. (a) Total tin (∑Sn) Analysis. The analytical procedure for ∑Sn was based on the method described elsewhere (30). Briefly, liver samples were dried at 80 °C for 12 h. After drying, samples were homogenized into a powder state. About 0.1 g of the powdered sample was weighed in an 8 mL PTFE tube and 1 mL of purified HNO3 (∼63%) was added. The digestion was carried out in a microwave oven (model Toshiba ER-V11) for 6 min at 200 W. After cooling, 0.5 mL of purified HNO3 and ∼1 mL of Milli-Q water were added into the sample tube and again heated in the microwave oven for 40 s. When digestion was complete, the sample was transferred into a measuring flask and diluted with Milli-Q water. Tin concentrations in samples were determined by measuring tin isotope 120Sn, using inductively coupled plasma mass spectrometry (Perkin-Elmer Elan 5000 ICP-MS). Accuracy of the analytical method was checked using a certified reference biological material (NIES 11), and the recovery of ∑Sn obtained was 96.4 (1.5 (n ) 3). Detection limits were ∼10 ng/g on a dry weight basis for ∑Sn. (b) Butyltin (BTs) Analysis. The analytical procedure for ∑BTs, including MBT, DBT, and TBT, has been described elsewhere (8-10). About 1-2 g (wet weight) of liver sample was homogenized with 70 mL of 0.1% tropolone-acetone and 5 mL of 2 N HCl. The homogenate was centrifuged, and BTs in the supernatant were transferred to 0.1% tropolonebenzene. After elimination of the moisture in the organic layer with anhydrous Na2SO4, the extract was concentrated to near dryness using a rotary evaporator (40 °C) and made up to 5 mL with benzene. BTs in the extract were propylated by adding 5 mL of n-propylmagnesium bromide (∼2 mol/L in THF solution), and the mixture was shaken at 40 °C for 1 h. After decomposition of excess Grignard reagent with 1 N H2SO4, the derivatized extract was transferred to 20 mL of 1782
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10% benzene-hexane and concentrated to near dryness; the volume was made up to 5 mL with hexane. The extract was then passed through an 8 g Florisil-packed wet column for cleanup. The final hexane eluate from the cleanup column was concentrated to 5 mL and subjected to GC quantification. BTs concentrations in samples were measured using capillary gas chromatography with flame photometric detection (GCFPD) and a tin mode filter (610 nm). A fused silica capillary column (DB-1; 30 m length × 0.25 mm i.d., 0.25 µm film thickness) was used for separation. Detection limits of BTs as MBT, DBT, and TBT in liver tissues were 15, 4.0, and 2.0 ng/g wet wt, respectively. Average recovery rates for monobutyltin trichloride, dibutyltin dichloride, and tributyltin monochloride spiked into the liver of an Antarctic minke whale were 104 ( 19.6, 117 ( 14.3, and 108 ( 5.2% (n ) 4), respectively, throughout the analytical procedure. These recovery rates were similar to those reported in our previous studies (8, 10-12, 14), of which data were combined with those obtained in this study and are shown in Table 1. Hexyltributyltin was added as an internal standard. The concentrations of ∑BTs (TBT + DBT + MBT) reported in this study were normalized as micrograms of Sn per gram on a dry weight basis to compare with the data of ∑Sn concentrations. Statistical Analysis. The relationship between concentrations of ∑BTs and ∑Sn in the livers of cetaceans was evaluated by two-tailed significance of Sperman’s correlation coefficient. Significant difference between the data sets was analyzed using the Mann-Whitney U-test. These statistical analyses were done using SPSS 6.1 for Macintosh software.
Results and Discussion ∑Sn was found in the liver of all cetaceans analyzed, with significant levels of ∑BTs (Table 1). The highest hepatic concentrations of ∑Sn and ∑BTs were found in a finless porpoise stranded along the Seto-Inland Sea, Japan, at 47 and 18 µg/g of dry wt, respectively. Relatively high levels of ∑BTs were detected in coastal species such as finless porpoises, caught from Ise Bay (up to 14 µg/g of dry wt) and Nagasaki (up to 8.9 µg/g of dry wt), and bottlenose dolphins from Taiji (up to 8.8 µg/g of dry wt). Concentrations of ∑Sn and ∑BTs found in offshore species such as rough-toothed dolphin from Tori Island (0.22 and 0.050 µg/g of dry wt, respectively) and minke whale of the northwestern North
TABLE 1. Mean and Range Concentrations of Total Tin (∑Sn) and Butyltins (∑BTs) in the Livers of Cetaceans Collected from the North Pacific and Coastal Waters of Japan, The Philippines, India, and the Black Sea country/region North Pacific
Japan
species scientific name
Black Sea
∑Sn (µg/g of Sn dry wt)
∑BTsb (µg/g of Sn dry wt)
2 187 (172-196)d 5 13 7587 (5910-8400)
1.1 (0.48-2.0) 0.55 (0.25-1.1)
0.17 (8) (0.081-0.31) 0.2 (8) (0.11-0.37)
19 (15-24) 41 (18-82)
2.0 (0.86-2.6) 1.7 (0.78-2.9) 1.0 (0.45-1.6) 3.1
1.2 (8) (0.54-1.6) 1.2 (0.88-2.4) 0.40 (8) (0.17-0.56) 1.1 (8)
59 (52-63) 67 (45-90) 35 (31-37) 36
na year
/ 1
?
body length (cm)
∑BTs/∑Sn (%)
Dall’s porpoisec Phocoenoides dalli minke whalec Balaenoptera acutorostrata
northwest
1992
northwest
1995
Dall’s porpoisec Phocoenoides dalli minke whalec Balaenoptera acutorostrata Baird’s beaked whalec Berardius bairdii dwarf sperm whalec Kogia simus Stejneger’s beaked whalec Mesoplodon stejnegeri ginkgo-toothed beaked whalec Mesoplodon ginkgodens short-finned pilot whalec Globicephala macrorhynchus Risso’s dolphinc Grampus griseus killer whalec Orcinus orca rough-toothed dolphinc Steno bredanensis bottlenose dolphine Tursiops truncatus finless porpoisee Neophocaena phocaenoides
Sanriku
1995
1
Ayukawa
1987
8
Ayukawa
1988
1
Toyohashi
1993
2 183 (163-195) 6 5435 (2800-7300) 2 9900 (930-1060) 1 188
Niigata
1993
1 429
2.6
0.72 (8)
27
Yamagata
1993
1 479
1.6
0.32 (11)
20
Ayukawa
1985
3
Taiji
1991
12
Taiji
1986
2
Tori Island
1983
3
Taiji
1986
3
Seto-Inland Sea 1985 Nagasaki 1992
2
Ise Bay
19921995
2
3 482 (355-368) 7 269 (210-287) 1 613 (598-636) 3 211 (205-216) 3 289 (282-316) 1 162 2 119 (103-161) 1 166 (139-187)
6.0 (5.1-7.2) 7.0 (1.2-15) 5.9 (5.4-6.3) 0.22 (0.20-0.27) 11 (7.0-16) 47 7.1 (2.9-16) 13 (8.9-15)
4.3 (8) (3.7-5.8) 5.8 (12) (0.90-10) 4.8 (8) (4.3-5.2) 0.050 (8) (0.040-0.070) 8.0 (7.3-8.8) 18 (10) 6.7 (2.4-8.9) 8.3 (4.7-14)
74 (58-110) 80 (48-110) 82 (74-94) 21 (15-30) 90 (68-110) 38 74 (55-90) 64 (34-91)
Sulu Sea
1996
1
Sulu Sea
1996
1
1 187 (182-192) 1 223 (221-225)
0.82 (0.44-1.2) 0.92 (0.54-1.3)
0.18 (8) (0.10-0.26) 0.14 (8) (0.11-0.17)
23 (22-23) 17 (13-20)
Indo-Pacific humpback dolphine Bay of Bengal Sousa chinensis bottlenose dolphine Bay of Bengal Tursiops truncatus long-snouted spinner dolphinc Bay of Bengal Stenella longirostris
19881992 19881992 19881992
2
2 210 (194-225) 1 200 (169-230) 2 143 (117-170)
1.6 (0.57-1.9) 0.93 (0.38-1.6) 0.27 (0.17-0.32)
0.51 (8) (0.27-0.90) 0.27 (8) (0.13-0.32) 0.10 (8) (0.050-0.20)
47 (39-53) 29 (20-35) 38 (28-59)
harbor porpoisee Phocoena phocoena
1993
5
8 121 (112-139)
0.37 0.31 (14) (0.24-0.65) (0.22-0.40)
The Philippines long-snouted spinner dolphinc Stenella longirostris Fraser’s dolphinc Lagenodelphis hosei India
sampling location
Turkey
3 2
82 (50-95)
a n, number of samples: /, male; ?, female. b ∑BTs ) MBT + DBT + TBT. The data were normalized into units of µg/g of Sn dry wt. c Offshore species. d Figures in parentheses indicate the range of body length, concentrations of ∑Sn or ∑BTs, or % ∑BTs/∑Sn. e Coastal species.
Pacific (0.55 and 0.20 µg/g of dry wt, respectively) were lower than those in coastal species by 1 or 2 orders of magnitude. Although concentrations of BTs were detected at low levels in cetaceans from open sea areas, these observations clearly indicate that tin compounds, including butyltins, were distributed worldwide in higher trophic marine animals. The detectable levels of ∑BTs in coastal species of cetaceans further indicate that, despite control in the usage of butyltin compounds as antifouling paints in several developed countries such as Japan, contamination by these compounds is continuing in the marine ecosystems. The relationship between ∑BTs and ∑Sn concentrations was examined in the livers of cetaceans collected from Japanese coastal waters and northwestern North Pacific. As seen in Figure 2, hepatic concentrations of ∑BTs and ∑Sn positively correlated with highly significant coefficient values (r ) 0.95; p < 0.001). These observations indicate that butyltin residues detected have a major role in view of total tin accumulation in cetaceans. Nevertheless, as revealed by the different lines shown in Figure 2, concentration ratios of ∑BTs and ∑Sn varied in the range of 1:1 to 1:10 depending
on the cetacean species. ∑BTs/∑Sn values in coastal species were closer to 1:1. Although most offshore species revealed lower ratios (closer to 1:10), some species such as Risso’s dolphin and killer whale revealed higher ratios. This pattern suggests that cetaceans with higher ∑Sn tend to have higher ∑BTs levels. To elucidate the anthropogenic input of tin compounds, the percentages of ∑BTs in hepatic ∑Sn concentrations (∑BTs/∑Sn × 100) were estimated for all cetacean species analyzed (Table 1). Although the mean percentages of ∑BTs were not over a value of 100%, the maximum values were up to 110% in some specimens. Such is not surprising should we consider some unavoidable uncertainties in the analytical procedure for both BTs and ∑Sn, which may be due to different recoveries and sample forms (wet or dry mass) employed between these two analyses (see Materials and Methods). The mean percentage of ∑BTs estimated varied widely. This might be attributable to the different degradation capacities among species and/or input from local anthropogenic tin sources. Comparing the same species collected from various locations, a significantly higher ∑BTs percentage VOL. 33, NO. 11, 1999 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 2. Relationship between ∑BTs and ∑Sn concentrations in the livers of cetaceans from Japanese coastal waters and northwestern North Pacific. The data shown in this figure were based on the individual values of ∑BTs and ∑Sn concentrations given in Table 1, which include those cited from refs 8 and 10-12. (p < 0.001) was found in minke whales collected from Japanese coastal waters (Ayukawa) than in those from offshore waters (northwestern North Pacific) (Table 1). Similar difference in the percentages of ∑BTs (p < 0.02) between sampling locations was observed in bottlenose dolphins, which were collected from Japanese and Indian coastal waters (Table 1). These results suggest that high constituents of manmade BTs in total tin residues accumulated in the cetaceans is attributable to their local anthropogenic input around Japan. Considering the cetaceans from Japanese coastal waters and northwestern North Pacific, such a difference in the percentages of ∑BTs were also observed between coastal and offshore species (Figure 3). Apparently higher percentages of ∑BTs were found in most coastal cetaceans such as bottlenose dolphins (up to 90%) and finless porpoises (up to 74%). Interestingly, in contrast to the above coastal cetaceans, a finless porpoise collected in the Seto-Inland Sea showed very low percentages of ∑BTs (38%), even though the highest concentrations of ∑BTs and ∑Sn were found in this animal. Although the definitive reason is still unclear due to the small number of samples, the following possibilities may be considered: (1) The Seto-Inland Sea is situated in the western Japan, where heavy pollution by maritime traffic and industrial and agricultural activities is ongoing. It could imply that in this location the contamination by tin compounds is not only from butyltins but also from other organotins (e.g., methyl-, octyl-, and phenyltins) for antifouling paints and other applications. (2) The elevated accumulation of some toxic organochlorines including coplanar PCBs has been found in the finless porpoise (31), which is the same specimen analyzed in this study. On the basis of toxic equivalency factors (TEFs) suggested by the World Health Organization (32), a 2,3,7,8-tetrachlorodibenzo-p-dioxin toxic equivalent (T4CDD-TEQ) was estimated at 1400 pg/g wet wt in the blubber of this animal. It has been well documented that planar halogenated aromatic hydrocarbons (PHAHs) including coplanar PCBs induce the cytochrome P-450-related activities (32, 33). Hepatic cytochrome P-450 plays an important role in the degradation of BTs in mammals (34). 1784
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FIGURE 3. Mean percentages of ∑BTs in ∑Sn concentrations in the livers of cetaceans from Japanese coastal waters and northwestern North Pacific. The data shown in this figure were based on the mean values of ∑BTs percentages given in Table 1. Therefore, metabolic capacity to degrade BTs can be enhanced by exposure to coplanar PCBs, which may cause a lower percentage of ∑BTs in this animal. These possibilities should be examined by further study with more detailed approach on the speciation of organotins and biochemical analysis on P-450-related activities. Except for this animal and some offshore species, ∑BTs made up considerably high percentages (>50%) of the hepatic ∑Sn in these cetaceans (Table 1 and Figure 3). This pattern may be explained by the following two reasons: (1) BTs are more stable and bioaccumulative than inorganic tin and/or other organic tin compounds, and/or (2) the usage and input of butyltin compounds in the environment have been larger, overwhelming other organic tin and inorganic tin including natural backgrounds. Therefore, the abundance of ∑BTs may have a greater share among other tin compounds in the liver of marine mammals. This accumulation pattern of tin seems to be partly similar to that of mercury because organic mercury (mostly methylmercury) is found to be the main form of mercury compounds in fish (20-23) and also an important one in the muscle tissue of marine mammals (2427). As in the case of mercury, it can be expected that organotins including BTs have higher bioavailability and, thus, are more easily assimilated in the animal body than inorganic tin. Despite such an analogy expected in their accumulation feature, some different points between the cases of tin and mercury can also be suggested. The major part of mercury accumulated in the liver of marine mammal is inorganic (80-90%) (24-27), whereas cetaceans analyzed in this study, particularly coastal species, showed the high ∑BTs portion in their livers (>50%). Such a different proportion of organic fraction between hepatic tin and mercury may be due to more stable retention of inorganic mercury than of inorganic tin. It has been suggested that long-term accumulation of inorganic mercury in the liver of marine mammals is due to the mercury-selenium interaction, which forms mercuric selenide (HgSe) that leads to the detoxification of meth-
ylmercury (27, 35, 36). Alternatively, it is noteworthy that cytochrome P-450 monooxygenases, which play an important role in the degradation of BTs as previously mentioned, showed apparently lower activities in cetaceans than in other mammals (16-18). This fact suggests slower metabolic kinetics for BTs in cetaceans, which can induce higher ∑BTs portion of ∑Sn accumulated in their liver. Further difference between the cases of tin and mercury can be found in their sources. Man-made BTs have been introduced only from anthropogenic sources. Therefore, the high butyltin portion of hepatic ∑Sn observed in this study clearly suggests that anthropogenic tin input considerably contributes to the total tin accumulation in the cetaceans. With regard to the accumulation of mercury as well as other toxic metals such as cadmium, cetaceans can be affected by both anthropogenic and natural background exposures. Although accumulation of mercury derived from anthropogenic input cannot be ignored in some marine mammals inhabiting polluted coastal and semiclosed waters (37-39), elevated mercury accumulations have been found in the various marine mammals and seabirds collected from offshore waters, far from any human/industry activity (20, 28, 41-44). Thus, it can be expected that these animals generally represent natural exposure levels. Taking all of these facts into consideration, the anthropogenic exposure to tin compounds seems to be more apparent than exposure to mercury. Despite the high percentages (∼50-90%) of ∑BTs in ∑Sn found in the livers of coastal cetaceans, the actual anthropogenic portion of total tin compounds would be greater than those estimated only from butyltin derivatives. Occurrence of other organotin species such as methyltins, octyltins, and phenyltins has been also reported in aquatic ecosystems (19), although methyltins can be environmentally induced by the microbial methylation of inorganic tin (45-49). A recent study that analyzed organotins such as butyltins and methyltins and total tin in several fish species, mussels, and algae also noted that BTs made up a higher percentage (6090%) of the total tin (19). With these observations, the present results suggest a bioaccumulative nature of organic tin as compared with inorganic tin in various aquatic organisms. Further investigations to make clear the relationship among butyltins, other organotins, and total tin residues should be carried out in pinnipeds, seabirds, fish, bivalves, and other organisms.
Acknowledgments We thank Dr. Annamalai Subramanian (Annamalai University, India), Ms. Pauline Suarez (Silliman University, Philippines), Dr. A. Amaha Oztu ¨ rk (Istanbul University, Turkey), Dr. Tadasu K. Yamada (National Science Museum, Tokyo, Japan), Mr. Atsushi Yamato (Niigata City Aquarium, Japan), Dr. Toshio Kasuya (Mie University, Japan), and Dr. Hiroyuki Tanaka (National Research Institute of Far Seas Fisheries, Japan) for their help in the collection of samples. We thank Dr. K. Kannan (Michigan State University) and Dr. M. Prudente (De La Salle University System, Phillippines) for critical reading of the manuscript. This research was supported by Grants-in-Aid from the Scientific Research Program (Grants 10559015 and 09460086) of the Ministry of Education, Science and Culture of Japan, and the 2nd Toyota High-tech Research Grant Program.
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Received for review June 17, 1998. Revised manuscript received March 2, 1999. Accepted March 9, 1999. ES980624T
