Environ. Sci. Technol. 2010, 44, 2675–2681
Stable Isotope Ratios of Carbon and Nitrogen and Mercury Concentrations in 13 Toothed Whale Species Taken from the Western Pacific Ocean off Japan T E T S U Y A E N D O , * ,† Y O H S U K E H I S A M I C H I , † OSAMU KIMURA,† KOICHI HARAGUCHI,‡ SHANE LAVERY,§ MEREL L. DALEBOUT,| NAOKO FUNAHASHI,⊥ AND C. SCOTT BAKER# Faculty of Pharmaceutical Sciences, Health Sciences University of Hokkaido, 1757 Ishikari-Tobetsu, Hokkaido 061-0293, Japan, Daiichi College of Pharmaceutical Sciences, 22-1 Tamagawa-Cho, Minami-Ku, Fukuoka 815-8511, Japan, School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales 2052, Australia, International Fund for Animal Welfare, 1-6-10-203, Saiwaicho, Higashikurume, Tokyo 203-0052, Japan, and Marine Mammal Institute and Department of Fisheries and Wildlife, Oregon State University, Newport, Oregon 97365
Received November 27, 2009. Revised manuscript received January 29, 2010. Accepted February 17, 2010.
Stable isotope ratios of carbon (∂13C) and nitrogen (∂15N) and total mercury (T-Hg) concentrations were measured in red meat samples from 11 odontocete species (toothed whales, dolphins, and porpoises) sold in Japan (n ) 96) and in muscle samples from stranded killer whales (n ) 6) and melonheaded whales (n ) 15), and the analytical data for these species were classified into three regions (northern, central, and southern Japan) depending on the locations in which they were caught or stranded. The ∂15N in the samples from southern Japan tended to be lower than that in samples from the north, whereas both ∂13C and T-Hg concentrations in samples from the south tended to higher than those in samples from northern Japan. Negative correlations were found between the ∂13C and ∂15N values and between the ∂15N value and T-Hg concentrations in the combined samples all three regions (γ) -0.238, n ) 117, P < 0.01). The ∂13C, ∂15N, and T-Hg concentrations in the samples varied more by habitat than by species. Spatial variations in ∂13C, ∂15N, and T-Hg concentrations in the ocean may be the cause of these phenomena.
feeding ecology of marine species (1-4). The ∂13C value is used to indicate the relative contribution to the diet of potential primary sources and can demonstrate differences between pelagic and benthic prey species (5-7). Furthermore, the ∂13C value in marine phytoplankton decreases slightly from the equatorial regions toward the North Pole at about 0.015 ‰ per 1° (8), and this decrease is consequently reflected in the ∂13C values in marine predators. On the other hand, the ∂15N value shows a stepwise increase in the trophic level of a food chain. A significant increase in ∂15N of 3.4 ( 1.1‰ has been shown to occur between consumer and prey (9), whereas only a small enrichment of about 1‰ is found in the ∂13C value (10). Variations in ∂15N also reflect the regional characteristics of nitrogen metabolism such as denitrification and N2 fixation (6, 11). The main islands of Japan are surrounded by a number of both warm and cold ocean currents (Figure 1). Tanaka et al. (7) analyzed the ∂13C and ∂15N in Japanese anchovy (Engraulis japonicus) samples from the Pacific coast: They reported higher values from inshore samples than from offshore samples and lower values from anchovies taken from the Kuroshio (warm current) extension and Kuroshio-Oyashio (cold current) transition zones. However, little is known about the ∂13C and ∂15N in marine samples taken from northern Japan (cold current region). According to a worldwide survey of squid (6), the ∂13C ranges from -19.9 ‰ to -13.8 ‰ and the ∂15N ranges from 8.3 ‰ to 16.8 ‰, with the lowest ∂13C values found in squid caught in the Sea of Japan. The Japanese archipelago stretches for more than 3000 km from north to south, and many species of toothed whales, including dolphins and porpoises, are known to inhabit the coastal waters. About 20,000 of those cetaceans are annually caught off the coast of Japan for human consumption. The main species of small cetaceans taken are Dall’s porpoise (Phocoenoides dalli), Baird’s beaked whale (Berardius bairdii), short-finned pilot whale (Globicephala macrorhynchus), pantropical spotted dolphin (Stenella attenuata), Risso’s dolphin (Grampus griseus), rough-toothed dolphin (Steno bredanensis), striped dolphin (Stenella coeruleoalba), common bottlenose dolphin (Tursiops truncatus), and false killer whale (Pseudorca crassidens) (12). Baird’s beaked whales are caught off Abashiri, Hakodate, Ayukawa (Ishinomaki), and Wada (Minamiboso), northern form short-finned pilot whales are caught off Ayukawa, and southern form short-finned pilot whales are caught off Wada, Taiji, and Nago (Figure 1). Dall’s
1. Introduction Stable isotope analyses have been used as an alternative to stomach content analysis to obtain information on the * Corresponding author phone and fax: +81-133-23-3902; e-mail:
[email protected]. † Health Sciences University of Hokkaido. ‡ Daiichi College of Pharmaceutical Sciences. § University of Auckland. | University of New South Wales. ⊥ International Fund for Animal Welfare. # Oregon State University. 10.1021/es903534r
2010 American Chemical Society
Published on Web 03/10/2010
FIGURE 1. Map of Japan and South Korea showing warm and cold currents and whaling towns. VOL. 44, NO. 7, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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porpoises are mainly caught off Otsuchi, and other cetacean species are mainly caught off Taiji and/or Nago. Abashiri (N44° and E144°) is the northernmost and Nago (N26° and E128°) is the southernmost of these whaling towns. As small cetaceans are long-lived and occupy the top of the marine food web, they biomagnify marine pollutants such as heavy metals and organochlorine compounds (12-15). Among these pollutants, accumulation of mercury (Hg) is prominent, and high levels of Hg are found in red meat products from small cetaceans sold in Japan. To date, the highest and second highest concentrations of total mercury (T-Hg) found in our laboratory were 98.9 and 81.0 µg/wet g in red meat products from a bottlenose dolphin (15) and a false killer whale (12), respectively. These products were purchased in Nago, the southernmost whaling town in Japan. The T-Hg contamination levels in small cetaceans caught off the coast of Japan vary markedly by the species (12, 15, 16) and by habitat (12, 17). The level of Hg accumulation is generally correlated with trophic level as determined by ∂15N value (18). However, there are often wide intraspecific and/or interspecific variations in ∂15N within a similar trophic level, and it has been suggested that this results from geographical variations as mentioned above (6, 7, 11). We previously reported the contamination level of T-Hg in red meat products from nine species of odontocetes (12, 15). However, little is known about the ∂13C and ∂15N values in those species or the correlation between T-Hg concentration and ∂15N in those species. Killer whales (Orcinus orca) represent the top of marine food web and have the most diverse diet, ranging from fish/ squid of all sizes to seals and other cetacean species (19). In the eastern North Pacific Ocean, three sympatric forms of killer whales, referred to as “residents”, “transients” and “offshore”, with fundamentally different dietary preferences have been described (3). Resident killer whales principally consume marine fish while transient killer whales generally hunt marine mammals (3). Reflecting their dietary preferences, contamination level of organohalogen compounds in the blubber and the ∂15N value in the skin of transients were higher than those of residents, respectively (3). In contrast to killer whales in the eastern North Pacific Ocean, information about the feeding habits and migration of killer whales in the western North Pacific Ocean is very limited. Available data for killer whales in this area are limited to the T-Hg distribution in the organs of killer whales stranded on the coast of Hokkaido, in the north of Japan (17). From stomach content analysis, these killer whales appear to correspond to the transient form. However, the contamination level of T-Hg in these killer whales was low compared to that in other odontocetes caught off the coast of Japan (17). In 2006, a pod of melon-headed whales (Peponocephala electra) was massstranded on the coast of Chiba Prefecture, in central Japan. We analyzed heavy metals in the organs of the stranded whales and reported that the T-Hg concentrations in the organs increased with their body lengths (20). To our knowledge, however, stable isotopes ratios in the muscle of neither killer whales nor melon-headed whales around the coast of Japan have yet been reported. Here, we reported on the stable isotope ratios of carbon (∂13C) and nitrogen (∂15N) and the T-Hg concentration in the red meat products from 11 species of odontocetes purchased from several Japanese whaling towns and their environs as published previously. Furthermore, we analyzed stable isotope ratios and T-Hg concentration in muscle samples from stranded killer whales and melon-headed whales. We compared the ∂13C, ∂15N, and the T-Hg concentration in the red meat (muscle) samples among whaling towns by area (northern, central, and southern Japan) and among species and investigated the correlation among the ∂15N and ∂13C values and T-Hg concentration. 2676
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2. Materials and Methods 2.1. Red Meat Products and Muscle Samples Originating from Odontocetes. As reported previously (12, 14, 15), 88 samples of red meat products were purchased from retail outlets in Japan from 2000 to 2004 and analyzed for total mercury (T-Hg) concentration as well as species identification using molecular taxonomy. These samples were analyzed for determination of ∂13C and ∂15N (see below). Eight samples of red meat products purchased in 2004 and 2005 were analyzed for the determination of ∂13C, ∂15N, and T-Hg concentration and identification of species origin. Muscle samples from mature killer whales stranded on the coast of Hokkaido Prefecture, in northern Japan (n ) 6) (17), and mature melon-headed whales stranded on the coast of Chiba Prefecture, in central Japan (n ) 15) (20), were also analyzed for ∂13C and ∂15N. All products were stored at -20 °C prior to analyses. 2.2. Chemical Analyses. The T-Hg concentrations in the odontocete products were determined using a flameless atomic absorption spectrophotometer (Hiranuma Sangyo, HG-1, Japan) after digestion by a mixture of HNO3, HClO4, and H2SO4 (12, 21). The species of origin of odontocete products was identified from the mitochondrial DNA sequences (22). After the removal of lipid using chloroform/methanol, the stable isotope ratios of carbon and nitrogen (∂13C and ∂15N) in the dried red meat (muscle) samples were analyzed using a mass spectrometer (Delta S, Finnigan Co., Germany) coupled with an elemental analyzer (EA1108, Fisons Co., Italy) (4). 2.3. Statistical Analyses. The data were analyzed using the Statcell 12 program, and the level of significance was set at P < 0.05. All data were expressed as the mean ( standard deviation (S.D.).
3. Results Measurements of ∂13C and ∂15N were obtained from 88 samples of red meat products from 11 cetacean species and 21 muscle samples from stranded mature killer whales and mature melon-headed whales. These samples, representing 13 species, were stratified into northern, central, and southern regions on the basis of the locations of the whaling towns and stranding areas from which they were obtained (Table 1). The northern and southern form pilot whales were stratified by the area in which the samples were purchased. Although the southern form short-finned pilot whales are caught off Wada and Taiji (central Japan) as well as Nago (southern Japan) (Figure 1), we classified all samples from southern form short-finned pilot whale in the central region. As the northern form short-finned pilot whales are caught off Ayukawa, samples from this type were classified into the northern region. As Baird’s beaked whales are caught off Abashiri, Hakodate, and Ayukawa (northern Japan) as well as Wada (central Japan) and striped dolphins are caught off Taiji (central Japan) and Nago (southern Japan), we classified the samples from these whales into the northern and central regions, respectively, based on purchase location. Among the 13 species shown in Table 1, the four lowest average T-Hg concentrations were found in Baird’s beaked whale, the northern form short-finned pilot whale, Dall’s porpoise, and killer whale. All those species were found in the northern region, and average values of T-Hg concentrations were about 1.3 µg/wet g. In contrast, all average T-Hg concentrations in the red meat (muscle) samples of whales and dolphins found in the central and southern regions exceeded 3.0 µg/wet g. High but variable concentrations of T-Hg were found in the red meat products of bottlenose dolphins and false killer whales. The highest and second highest concentrations in the red meat products summarized
TABLE 1. Stable Isotope Ratios of Carbon and Nitrogen and Total Mercury Concentration in the Red Meat Products and Muscle Samples of Odontocetes Caught off the Coast of Japan mean ( SD group
killer whale (n ) 6) Baird’s beaked whale (n ) 19b) short-finned pilot whale, northern form (n ) 5) Dall’s porpoise (n ) 8) striped dolphin (n ) 11b) Risso’s dolphin (n ) 8) short-finned pilot whale, southern form (n ) 18b) melon-headed whalea (n ) 15) bottlenose dolphin (n ) 10) pygmy killer whale (n ) 2) false killer whale (n ) 5) pantropical spotted dolphin (n ) 4) rought-toothed dolphin (n ) 6) a
Northern
Central
Southern
δ13C (‰)
species
-17.1 -17.8 -18.3 -18.8 -17.7 -16.7 -16.9 -16.8 -17.2 -17.6 -16.2 -17.3 -16.9
( ( ( ( ( ( ( ( (
0.1 0.6 0.6 0.2 0.6 0.3 0.5 0.2 0.3
( 0.6 ( 0.3 ( 0.5
δ15N (‰) 16.5 16.3 13.3 13.2 12.3 13.1 12.2 12.7 13.1 14.1 12.8 12.1 11.6
( ( ( ( ( ( ( ( (
0.3 0.8 0.8 0.3 0.9 0.5 0.7 0.3 0.6
( 0.6 ( 0.8 ( 0.5
total mercury (µg/wet g) 1.27 1.30 1.30 1.27 5.91 3.84 12.4 4.89 38.3 13.1 20.7 5.33 5.33
( ( ( ( ( ( ( ( (
0.13 0.99 0.41 0.33 4.07 1.52 8.6 2.32 28.3
( 10.6 ( 1.75 ( 1.75
a Muscle from stranded animals. b Sum of Baird’s beaked whales purchased in and around Abashiri, Hakodate, Ayukawa, and Wada, sum of short-finned pilot whales (southern form) purchased from in and around Taiji and Nago, or sum of striped dolphins purchased in and around Taiji and Nago.
in Table 1 were 65.3 µg/wet g in sample from bottlenose dolphins and 32.3 µg/wet g in sample from false killer whales purchased in Nago (southern Japan). Among the 13 species, excluding the pygmy killer whale (n ) 2), the average ∂15N in the four species from the northern region was the four highest (Table 1). In contrast, the average ∂13C values from the species in the northern region, excluding the killer whale, were the three lowest. The ∂13C-∂15N map of four species in the northern region appeared to be different from that of nine species in the central and southern regions (Figure 2). The ∂13C tended to increase with increases in the ∂15N among the four species from the northern region (P < 0.01), whereas no correlation was found between the ∂15N and T-Hg concentration (P > 0.05). The ∂15N of nine species from the central and southern regions tended to be lower than that of the four species from the northern region, whereas the ∂13C of the former region tended to be higher (Figure 2). No correlations (P > 0.05) were found between the ∂13C and ∂15N values and between the ∂15N and T-Hg concentration in the whales and dolphins from the central and southern regions. It is noteworthy that negative correlations were found between the ∂13C and ∂15N values (γ ) -0.223, P < 0.05) and the ∂15N value and T-Hg concentration (γ ) -0.238, P < 0.01) in the combined samples from all three regions (n ) 117), while positive correlation was found between the ∂13C value and T-Hg concentration (γ ) 0.219, n ) 117, P < 0.05). These correlations were weak but statistically significant. The T-Hg concentration and the ∂13C and ∂15N in the Baird’s beaked whale products purchased in and around Abashiri, Hakodate, Ayukawa, and Wada were compared (Table 2, see Figure S1). In agreement with the results shown in a previous report (12), the T-Hg concentrations in Baird’s beaked whale products purchased in and around Abashiri were significantly lower than those in products purchased in and around Ayukawa and Wada (P < 0.05). The ∂15N value from beaked whale products purchased in and around Hakodate was significantly lower than those in products purchased in and around Ayukawa and Wada (P < 0.05), and the ∂13C values from whale products purchased in and around Abashiri and in and around Hakodate were significantly lower than those from the products purchased in and around Ayukawa and Wada (P < 0.05). The T-Hg concentration, ∂13C and ∂15N in the short-finned pilot whales caught off Ayukawa (northern form), and Taiji and Nago (southern form) were also compared (Table 2, see Figure S2). Again, in agreement with the results of a previous
report (12), the T-Hg concentrations in red meat products of pilot whales purchased in and around Ayukawa were significantly lower than that in the products purchased in and around Nago (P < 0.05). Correspondingly, the ∂15N values of the products purchased in and around Nago were significantly lower than those from the products purchased in and around Ayukawa (P < 0.05), and the ∂13C values of the products purchased in and around Ayukawa were significantly lower than those of products purchased in and around Taiji and Nago (P < 0.05). On the other hand, no differences were found in the ∂13C and ∂15N values or T-Hg concentrations in red meat products from striped dolphins caught off Taiji and Nago (Table 2).
4. Discussion 4.1. Geographical Differences in D13C, D15N, and Hg Contamination. The ∂13C and ∂15N values of red meat (muscle) samples of four species from the northern area of Japan were apparently lower and higher than those of other species from the central and southern areas, respectively (Figure 2). The ∂13C values in the combined samples of northern, central, and southern regions tended to decrease with an increase in ∂15N (γ) -0.223, n ) 117, P < 0.05). To explain this negative correlation, we considered whether ∂15N and ∂13C values from animals inhibiting in the cold current ocean regions of Japan may be higher and lower than those in the warm current region, respectively. The marked differences in ∂13C between samples from the northern and southern region (Table 1) cannot be fully explained by the effect of latitude (8), as the expected difference in ∂13C calculated from the difference in latitude between Abashiri and Nago (18°) is only 0.27‰. Unfortunately, little information is available regarding geographical variations in ∂13C and ∂15N in marine biota around Japan. Takai et al. (6) reported lower ∂13C values in squid samples from the northwest of the Sea of Japan. Similarly, ∂13C in Baird’s beaked whales hunted in this area was lower than in whales from other areas (see Figure S1). Tanaka et al. (7) suggested lower ∂13C and ∂15N values in the Kuroshio extension and Kuroshio-Oyashio transition zones. To precisely estimate the trophic position of toothed whales, dolphins, and porpoise around Japan and compare with the trophic level from different areas, measurements of ∂13C and ∂15N in primary producers (the base of the food web) around Japan are necessary (11). On the other hand, T-Hg concentrations in the samples from southern Japan were apparently higher than those from northern Japan (Figure 2). As suggested previously (12, 17), VOL. 44, NO. 7, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 2. Comparison of δ13C, δ15N, and total mercury concentration in toothed whales, dolphins, and porpoises taken from northern, central, and southern Japan. KW: killer whale, BBW: Barid’s beaked whale, SPW (N): short-finned pilot whale (northern form), DP: Dall’s porpoise, RD: Risso’s dolphin, MHW: melon-headed whale, SD: striped dolphin, SPW (S): short-finned pilot whale (southern form), BD: bottlenose dolphin, FKW: false killer whale, PKW: pygmy killer whale, PSD: pantropical spotted dolphin, RTD: rough-toothed dolphin. See Table 1.
TABLE 2. Spatial Differences in δ13C, δ15N, and Total Mercury in Baird’s Beaked Whales, Short-Finned Pilot Whales, and Striped Dolphinsa
Baird’s beaked whale
short-finned pilot whale striped dolphin
purchase area
δ13C (‰)
δ15N (‰)
total mercury (µg/wet g)
Abashiri (northern Japan), n ) 5 Hakodate (northern Japan), n ) 6 Ayukawa (northern Japan) and Wada (central Japan), n ) 8 Ayukawa, northern form (northern Japan), n ) 5 Taiji, southern form (central Japan), n ) 9 Nago, southern form (southern Japan), n ) 9 Taiji (central Japan), n ) 6 Nago (southern Japan), n ) 5
-18.1 ( 0.2a -18.3 ( 0.2a
16.5 ( 0.7a,b 15.6 ( 0.4a
0.62 ( 0.30a 1.03 ( 0.29a,b
-17.2 ( 0.3b
16.8 ( 0.9b
1.98 ( 0.43b
-18.3 -16.8 -17.0 -18.0 -17.4
( ( ( ( (
a
0.6 0.4b 0.8b 0.4 0.5
13.3 12.6 11.7 12.0 12.7
( ( ( ( (
a
0.8 0.4b 0.6b 0.4 1.2
1.30 ( 0.41a 10.81 ( 4.47a,b 12.71 ( 11.20b 5.20 ( 5.27 6.76 ( 2.22
a The data represent the mean ( S.D. The data were analyzed by Tukey-Kramer or Scheffe’s F test. Different superscript letters indicate a significant difference (P < 0.05).
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TABLE 3. Comparison between This Study and Previously Reported Data Regarding δ13C, δ15N, and Total Mercury δ13C (‰)
δ15N (‰)
-17.1 ( 0.1
16.5 ( 0.3 1.27 ( 0.13b
n)6
N.D.
N.D.
striped dolphin Risso’s dolphin a
62.2 ( 21.9
17.8 ( 0.8 N.D.
n ) 13 -17.0 ( 1.9
16.4 ( 1.7 N.D.
n)1 n)1
N.D. N.D.
N.D. N.D.
n ) 10 -17.2 ( 0.3
88 13.3
13.1 ( 0.6 38.3 ( 28.3
n)2 -18.6, -17.1 13.5, 12.6 2.57a, 166a n ) 10 -17.7 ( 0.6 12.3 ( 0.9 5.91 ( 4.07 n ) 27 -17.2 ( 0.5
11.1 ( 0.6 N.D.
n)3
-18.3 ( 0.1
9.1 ( 0.3
n)8
-16.7 ( 0.3
13.1 ( 0.5 3.84 ( 1.52
n)3
-17.2 ( 0.3
11.4 ( 0.9 91.0 ( 73.9
Expressed by µg/g dry weight.
b
28.0 ( 27.5
organ (type)
area
n)6
killer whale n ) 23 -17.2 ( 1.0
bottlenose dolphin
T-Hg (µg/wet g)
west North Pacific Ocean west North Pacific Ocean east North Pacific Ocean east North Pacific Ocean U.K. Japan Sea west North Pacific Ocean
muscle
this study and Endo et al. (17)
liver
Endo et al. (17)
skin (transient) Krahan et al. (3) skin (resident)
Krahan et al. (3)
liver red meat
Law et al. (19) Endo et al. (23)
red meat
this study
Mediterranean Sea muscle west North Pacific Ocean red meat a
a
reference
Mediterranean Sea
blubber
Mediterranean Sea west North Pacific Ocean Mediterranean Sea
muscle
Capelli et al. (24) this study Borrell and Aguilar (25) Capelli et al. (24)
red meat
this study
muscle
Capelli et al. (24)
Data from Endo et al (17).
Hg concentrations in the Kuroshio region may be higher due to natural and anthropogenic inputs. We expected to find a positive correlation between ∂15N value and T-Hg concentration, as the level of Hg accumulation in biota is generally correlated with trophic level as reflected in ∂15N value (18). However, a negative correlation between the ∂15N value and T-Hg concentration was found in the combined samples of three areas (γ ) -0.238, n ) 117, P < 0.01), probably reflecting geographical variations of ∂15N (6, 7, 11) and T-Hg concentration (12, 17) in the seawater around Japan. In contrast, a positive correlation was found between the ∂13C value and T-Hg concentration in the combined samples (γ ) 0.219, n ) 117, P < 0.05). As mentioned above, the measurements of ∂13C and ∂15N in primary producers are necessary. The contamination levels of T-Hg in the toothed whales, dolphins, and porpoises caught off the coast of Japan appear to be determined mainly by the Hg concentration in their habitat rather than by species. In agreement with the present results, the T-Hg concentrations and ∂13C found in the muscle of yellowfin tuna and albacore caught off southern Japan were found to be higher than in those caught off central Japan, whereas the ∂15N found in the former was lower (our unpublished data). 4.2. Species and Spatial Differences in D13C, D15N, and Hg Contamination in the Northern Region. Table 3 summarizes the data from the present study together with that obtained from the literature regarding ∂13C and ∂15N values and T-Hg concentration in killer whales, bottlenose dolphins, striped dolphins, and Risso’s dolphins. We assumed that the killer whales stranded on the coast of Japan corresponded to the transient form because the major items found in stomach contents were an assortment of seal tissues (21). However, the present results for ∂13C and ∂15N in the stranded killer whales correspond closely to those in observed in the resident form (primary fish eaters) rather than the transient form (primary mammal eaters) of killer whales in the eastern North Pacific Ocean (Table 3) (3), and the contamination level of T-Hg in the stranded killer whales was the lowest among the 13 species studied (Table 1). As most recent studies of killer whales have been undertaken using biopsy sample of skin with blubber, contamination data for Hg are lacking. The available data for Hg listed in Table 3 were obtained from liver sample of a killer whale stranded in the United Kingdom (88 µg/wet g) (19) and a red
meat product sold in Busan, South Korea (13.3 µg/wet g) (23). The T-Hg concentration in the liver is compatible with that found in the killer whales stranded in northern Japan (17), whereas the concentration in the red meat sample is markedly higher. Baird’s beaked whales inhabit the North Pacific Ocean and adjacent waters, where they prefer deep water, feeding on squid, octopus, and skate (26). The average ∂15N in the red meat samples from Baird’s beaked whales was almost the same as that in muscle samples from killer whales (Table 1), although the trophic position of Baird’s beaked whales was expected to be lower than that of killer whales. Hobson et al. (5) reported a higher ∂15N in benthic biota. The higher ∂15N value in the Baird’s beaked whales may reflect their preference for deeper water. Around Japan, this species is found in the southern Okhotsk Sea, the eastern Sea of Japan, and off the Pacific coast (27) and is hunted at Abashiri, Hakodate, Ayukawa, and Wada, respectively. In agreement with the existence of separate populations, some significant differences in ∂13C, ∂15N, and T-Hg concentration were found among the three regional samples (Table 2, see Figure S1). The higher level of T-Hg contamination in the Pacific coast population may result from higher Hg level in the southern sea region, as we previously suggested (12, 17). The lower ∂13C in the Baird’s beaked whales purchased in and around Hakodate and Abashiri may be explained by the lower ∂13C in the cold current regions. Takai et al. (6) reported the lowest level of ∂13C in squid caught off the Sea of Japan near the hunting area of the eastern Sea of Japan population. Dall’s porpoises are found in the North Pacific Ocean and adjacent seas. The average ∂13C value in Dall’s porpoises was the lowest, and the average ∂15N was higher in our analysis among the 13 species (Table 1). In the eastern North Pacific Ocean, Dall’s porpoises are a prey item of the killer whale. Interestingly, the average differences in ∂13C and ∂15N between killer whales and Dall’s porpoises were 1.7 ‰ and 3.3‰, respectively, which correspond approximately to one tropic level (9). However, in spite of apparent differences in tropic level, the average T-Hg concentration in the red meat samples from Dall’s porpoises was very similar to that in the muscle samples from killer whales (Table 1). The average ∂13C, ∂15N, and T-Hg concentrations in the northern form short-finned pilot whales were similar to those in Dall’s porpoises, respectively. No correlation was found VOL. 44, NO. 7, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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between the T-Hg concentration and ∂15N values from muscle samples of the four species from the northern region (Figure 2). As Hg is distributed preferentially in liver relative to muscle of mammals (17, 20), the hepatic concentrations of T-Hg were compared among the four species. The average T-Hg concentration in the liver from the Dall’s porpoises (8.75 ( 2.54 µg/wet g, n ) 5; our unpublished data) was markedly lower than that from the northern form of short-finned pilot whales (60.0 ( 40.1 µg/wet g, n ) 20) (16), Baird’s beaked whales (37.7 ( 44.1 µg/wet g, n ) 37) (16), and killer whales (57.7 ( 22.5 µg/wet g, n ) 6) (17). The hepatic concentrations of T-Hg in these species might not be well correlated with their ∂15N values. 4.3. Species and Spatial Differences in D13C, D15N, and Hg Contamination in the Central and Southern Regions. In the western North Pacific, off the coast of Japan, shortfinned pilot whales have been morphologically, genetically, and ecologically discriminated into southern and northern forms (28), and these forms of whales are hunted for consumption in Nago, Taiji, Wada, and in Ayukawa, respectively. Higher levels of T-Hg contamination in the southern form pilot whales were observed (see Figure S2), probably reflecting the higher concentration of T-Hg in the Kuroshio Current region (12, 17). The ∂13C in the northern form pilot whales was significantly lower than that in the southern form pilot whales, probably reflecting lower ∂13C in the cold current areas. The ∂15N in the southern form pilot whales purchased in and around Nago was significantly lower than that in the southern form pilot whales purchased in and around Taiji and in the northern form pilot whales purchased in and around Ayukawa, probably reflecting the lower ∂15N in Kuroshio Current region. Little is known regarding the migration of short-finned pilot whales, and it is unclear whether the southern form short-finned pilot whales caught off Taiji and Nago are from the same population. The present results for ∂13C and ∂15N in the red meat products of bottlenose dolphins, striped dolphins, and Risso’s dolphins were similar to those found in the muscle of three dolphin species (24) and in the blubber of striped dolphins (25), respectively (Table 3). The T-Hg concentrations reported by Capelli et al. (24) were expressed in “µg/g dry weight”. As the T-Hg concentrations expressed in “µg/g dry weight” are about four times higher than those expressed in “µg/g wet weight” (21), the present data regarding T-Hg concentrations expressed in “µg/g wet weight” are compatible with those reported by Capelli et al (24). Contamination levels of T-Hg in the samples from the five species from southern Japan were markedly higher than those from northern Japan (Table 1) and tended to increase with increases in ∂15N. According to Honda (16), the contamination level of T-Hg in the liver of striped dolphins caught off Taiji (central Japan) was 205 ( 139 µg/wet g (n ) 59). Another report showed that the average T-Hg concentrations in the liver of southern form short-finned pilot whales and Risso’s dolphins caught off Taiji were 230 µg/wet g (n ) 7) and 406 µg/wet g (n ) 2), respectively (14). These hepatic levels of T-Hg in the whales and dolphins from central Japan were markedly higher than those from northern species of Dall’s porpoises, northern form short-finned pilot whales, Baird’s beaked whales and killer whales as mentioned above, which is in agreement with the T-Hg concentrations in the red meat (muscle) samples (Table 1). Unfortunately, little is known about hepatic T-Hg concentrations in whales and dolphins in southern Japan.
Acknowledgments This work was supported by Grants-in-Aid from the Japan Society of for the Promotion of Science (B20404006 and C21590135) and from the International Fund for the Animal Welfare (IFAW). Stable isotope analyses were conducted using 2680
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Cooperative Research Facilities (Isotope Ratio Mass Spectrometers) of Center for Ecological Research, Kyoto University.
Supporting Information Available Figures S1 and S2. This material is available free of charge via the Internet at http://pubs.acs.org.
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