Tien-Hsi Fang
email: thfang@mail.ntou.edu.tw

Jou-Yun Li

Hui-Min Feng

Hung-Yu Chen

Dr Tien -Hsi Fang

Distribution and contamination of trace metals in surface sediments of the East China Sea

Keywords: continental shelf, East China Sea, enrichment factor, trace metals, sediments, sedimentation flux)

The distributions, contamination status and annual sedimentation flux of trace metals in surface sediments of the East China Sea (ECS) were studied. Higher concentrations of the studied metals were generally found in the inner shelf and the concentrations decreased seaward. The sequences of the enrichment factor (EF) of the studied metals are Cu>Mn>Ni、Zn>Pb>Fe. The values of EF suggest that the metals contamination in the middle and outer shelves of the ECS is still minor. The annual sedimentation fluxes of trace metals in the ECS were: Fe, 3.48 x 10 7 t/y; Mn, 9.07 x 10 5 t/y; Zn, 1.08 x 10 5 t/y; Ni, 4.48 x 10 4 t/y; Pb, 4.32 x 10 4 t/y; and Cu, 3.1 x 10 4 t/y, respectively. Approximately 55-70% and 10-17% of the sedimentation fluxes of trace metals were deposited in the inner shelf and the Changjiang estuarine zone.

Introduction

The East China Sea, located between 26°-31°N and 121°-126°E, is one of the largest marginal seas in the western Pacific of the northern hemisphere, and it is also the main discharge area of the Changjiang River which is the world's fourth largest river when reviewed in terms of suspended load. The annual transportation of suspended load of the Changjiang River is approximately 4.61 x 10 8 t/y [START_REF] Zhang | Riverine composition and estuarine geochemistry of 1[END_REF]. In addition, there are another four middle size rivers, namely the Jiaojiang, the Qiantangjiang, the Jiulongjiang and the Minjiang, which together discharge 2.36 x 10 7 tons/y of suspended load into the ECS [START_REF] Zhang | Riverine composition and estuarine geochemistry of 1[END_REF]. Along the coast there are many developed cities, such as Shanghai and Ningbo, and a number of factories have also been set up there. Because of the over-emphasis on the economic development and the lack of environmental regulations since China embarked on the "Reform and Open Policy" from 1978, many studies have indicated that the Hangzhou Bay was contaminated by trace metals [START_REF] Huh | History of lead pollution recorded in East China Sea sediments[END_REF][START_REF] Yuan | Speciation of heavy metals in marine sediments from the East Chia Sea by ICP-MS with sequential extraction[END_REF] and polycyclic aromatic hydrocarbon [START_REF] Guo | High-resolution depositional record of polycyclic aromatic hydrocarbons in the central continental shelf mud of the East China Sea[END_REF]. A recent study conducted in August 2003 uncovered a hypoxic area (dissolved oxygen concentrations <2-3 mg/l) greater than 12,000 km 2 extending from the Changjiang River plume to the ECS [START_REF] Chen | Hypoxia in the East China Sea: One of largest coastal low-oxygen areas in the world[END_REF]. Thus, our current understanding is that the water quality of the ECS has been getting worse. However, the distribution and contamination status of trace metals for the whole ECS has not been established [START_REF] Shi | Methylmercury and total mercury in sediments collected from the East China Sea[END_REF]. In order to establish such a knowledge, the present study investigates the spatial distribution of trace metals in surface sediments of the ECS. In addition, based on the mass accumulation rates published in the literature for the ECS, the annual sedimentation fluxes of the studied metals in the ECS are also estimated.

Sampling and methods

Study area

Twenty-five sediment cores were collected with a box core during a cruise onboard the R/V Ocean Research-I from 6-16 November, 2006. The box core was designed to obtain undisturbed sediments and the core samples were sealed and kept frozen for subsequent processing and analyzing in the university laboratory. The sampling stations (Fig. 1) were located outside of the mouth of the Changjiang River The major source of the fine-grained sediment to the ECS continental shelf is from the Changjiang River, which discharges 4.61 x 10 8 t/y fine-grained sediment and accounts for 73% of the terrestrial export of suspended matter carried by rivers [START_REF] Zhang | Riverine composition and estuarine geochemistry of 1[END_REF]. Most of the suspended sediments consist of silt and clay. A large portion of this sediment supply is moved southward by the Jian-Su coastal current [START_REF] Accepted Manuscript Cao | Relationship between suspended sediments from the Changjiang estuary and the evolution of the embayed muddy coast of Zhejinag Province[END_REF]. A small portion of the suspended sediments is transported east and northeastwards to the ESC [START_REF] Sternberg | Tidally driven sediment transport on the East China Sea continental shelf[END_REF]. From the examination of 210 Pb profiles in sediment [START_REF] Demaster | Rates of sediment accumulation and particle reworking based on radiochemical measurements from continental shelf deposits in the East China Sea[END_REF] obtained a sedimentation rate of up to 4.5cm/y near the mouth of the Changjiang River. In a recent study based on measurements of 137 Cs throughout the ECS, [START_REF] Huh | Sedimentation dynamics in the East China Sea elucidated from 210 Pb, 137 Cs and 239, 240 Pu[END_REF] indicated that the sedimentation rates in the ECS varied by two orders of magnitude, from 2 to 0.02 cm/y, and generally decreased southwards along the inner shelf and eastwards offshore. Based on the spatial distributions of the grain size, carbonate, organic carbon contents, metals/aluminum ratios and the δC 13 content of organic carbon, the ECS continental shelf was divided into five major regions: the Delta, inner shelf, middle shelf, outer shelf and northeast outer shelf [START_REF] Lin | Sulfate reduction and iron sulfide mineral formation in the southern East China Sea continental slope sediment[END_REF]. Major types of sediments occurring there include terrigenous sediments from the Changjiang River, relict sediment from the middle shelf, biogenic carbonate from the outer shelf and sediments from the Yellow Sea [START_REF] Lin | Sulfate reduction and iron sulfide mineral formation in the southern East China Sea continental slope sediment[END_REF].

Analytical method

After thawing, the cores samples were extruded vertically with a hydraulic jack and sampled at 1 cm thickness at the surface. The outer rim (∼ 0.5cm) of each sediment slab was trimmed off to avoid contamination between layers.

Approximately 10-20 g of each surface sample (0-1 cm) was freeze-dried, ground and homogenized with a mortar and pestle. The processed sample was stored in acid-cleaned polypropylene tubes for further analysis. The bulk sediment samples were divided into two sub-samples for the determinations of total organic carbon and trace metals.

Total organic carbon analysis

Total organic carbon (TOC) contents in the sediment samples were measured by a Horbia carbon analyzer 8210 after the samples were smoked with concentrated HCl acid in a closed container for 48 hours to remove the inorganic C content. The detailed analytical procedure of TOC can be found in [START_REF] Fang | Mechanisms influencing the spatial distribution of trace metals in surficial sediments off the south-western Taiwan[END_REF].

Trace metals analysis

The trace metals contents in the surface sediments were totally digested with hydrofluoric acid (HF) in combination with aqua regia and heated on a hot plate at 200 °C for about 8 hours and evaporated to dryness. After cooling, the residue was dissolved with 0.5ml HNO 3 and the solution was made up with Milli-Q water to a volume of 25 ml in a volumetric tube. The final acidic solution was transferred into a 50ml centrifuge tube and was centrifuged at a speed of 4000 rpm for 5 minutes. The clear supernatant was stored in acid-cleaned polypropylene tubes and was analyzed for trace metals (Cu, Fe, Mn, Ni, Pb and Zn) by flame atomic absorption spectrometry using a Perkin-Elmer Analyst 800A.

Analytical quality assurance was performed by measurements of the PACS-2 reference material (National Research Council of Canada). The concentrations (n=6) of trace metals measured in the PACS-2 reference material (one standard deviation) were as follows: Cu, 286 ± 14 µg/g; Mn, 412 ± 18 µg/g; Ni, 38.8 ± 1.5 µg/g; Pb, 167 ± 3 µg/g; and Zn, 340 ± 11 µg/g, respectively. The ratio of the measured concentration to the certified value and precision (one standard deviation) was as follow: Cu, 92.6 ± 4.0%; Mn, 94.5 ± 4.4%; Ni, 98.3 ± 4.0%; Pb, 91.7 ± 1.8%; and Zn, 93.4 ± 3.4%.

RESULTS AND DISCUSSION

Spatial distribution

The concentration ranges of TOC and trace metals in surface sediments of the ECS were as follows: TOC, 0.10-0.61%; Cu, 4.3-41.5 µg/g; Mn, 152-1152 µg/g; Ni,Pb,Zn,Fe,respectively. The concentrations of TOC and trace metals found at each station are listed in Table 1. The spatial distributions of TOC and trace metals are shown in Fig. 2. Higher concentrations of TOC and trace metals were generally found on the inner shelf, especially the area off Hangzhou Bay. Away from the Hangzhou Bay area, concentrations (except for Mn) decreased in both a southerly (along the inner shelf) and south-easterly (middle and outer shelves) direction. This finding is in good agreement with TOC decreasing along transects radiating outwards from the mouth of the Changjiang River. Therefore, it supports the view that Changjiang River is a dominant factor resulting in elevated trace metals and TOC concentrations on the ECS [START_REF] Lin | Sulfate reduction and iron sulfide mineral formation in the southern East China Sea continental slope sediment[END_REF] The spatial distributions of trace metals and TOC in the ECS generally exhibited similar patterns and the concentration of TOC correlated well with trace metals (Fig. 3). It is well established that natural organic matter (NOM) has a high affinity for trace metals in the aquatic environment [START_REF] Stumm | Aquatic Chemistry[END_REF]. As a consequence, it affects the geochemical behavior of trace metal in the aquatic environment. The coupling between the cycles of TOC and trace metals is ultimately reflected in the chemical composition of marine sediments [START_REF] Basaham | Distribution and phase association of some major and trace elements in the Arabian Gulf sediments[END_REF][START_REF] Fang | Mechanisms influencing the spatial distribution of trace metals in surficial sediments off the south-western Taiwan[END_REF][START_REF] Lin | Sulfate reduction and iron sulfide mineral formation in the southern East China Sea continental slope sediment[END_REF].

In addition, the distribution of Mn showed a distinct peak situated between the middle and outer shelves at approximately located at 27° N and 123.5° E. The mechanism caused such a distribution is probably due to the sediment of this area being dominated by biogenic carbonate [START_REF] Lin | Sulfate reduction and iron sulfide mineral formation in the southern East China Sea continental slope sediment[END_REF]. Previous studies have shown that dissolved manganese can become adsorbed on, or incorporated into, freshly precipitated CaCO 3 in seawater (e.g. [START_REF] Wartel | Interaction of manganese (II) with carbonates in seawater: assessment of the solubility product of MnCO 3 and Mn distribution coefficient between the liquid phase and CaCO 3 particles[END_REF]. [START_REF] Wartel | Interaction of manganese (II) with carbonates in seawater: assessment of the solubility product of MnCO 3 and Mn distribution coefficient between the liquid phase and CaCO 3 particles[END_REF][START_REF] Wartel | Seasonal variation of Mn +2 adsorption on to calcareous surfaces in the English Channel, and its implication on the manganese distribution coefficient[END_REF] used suspended particulate matters from the English Channel, which is high in carbonate minerals, to study the interaction of Mn +2 in the CaCO 3 structure. They concluded that the adsorption on and substitution in calcite are the major mechanisms controlling the dissolved concentration of Mn in seawater along the French coast of the English Channel. Recent studies on suspended particulate matter from the Seine Estuary have also indicated that the majority of particulate Mn is bound to carbonate (Boughriet et al., 1992;[START_REF] Bougheriet | Chemical speciation of some particulate elements in the English Channel, and impact of human activities on the magnetic behavior of suspended matter[END_REF]. A good correlation between concentrations of Mn and carbonate in marine sediments has been reported off the southwestern coast of Taiwan [START_REF] Fang | Mechanisms influencing the spatial distribution of trace metals in surficial sediments off the south-western Taiwan[END_REF].

Total concentrations of trace metals in the inner shelf sediment found in the present study were in good agreement with the report by [START_REF] Yuan | Speciation of heavy metals in marine sediments from the East Chia Sea by ICP-MS with sequential extraction[END_REF] who used the four-step sequential extraction procedure to analyze coastal sediments outside of the Changjiang Estuary. Their results also indicated that more than 90% of Fe and 60-80% of Cu, Ni and Zn total concentrations were present in the residual fraction. In contrast, the concentrations of Mn and Pb were dominant in the non-residual fraction, accounting for more than 60% of the total concentrations. A comparison of trace metals concentrations in shelf sediments around the world is given in Table 2. It can be seen that the concentrations of trace metals, except Mn, found in the continental shelves, such as the Arabian Gulf, the Mediterranean Sea, the Aegean Sea and the Laptev Sea, around the world are quite comparable. However, the average concentration of Mn found in the ECS is two-three folds higher than those of the above continental shelves. Comparably high concentrations of Mn have been reported by [START_REF] Nolting | Distribution of trace and major elements in sediment and pore waters of the Lena Delta and Laptev Sea[END_REF] who indicated that Mn lateral distribution in surface sediments showed an increase from 1000 µg/g in the mouth of the Lena River to > 5000 µg/g in the eastern part of the Laptev Sea. They attributed these higher concentrations to the diagenetic process in sediments which caused large upward fluxes of Mn. The findings of [START_REF] Nolting | Distribution of trace and major elements in sediment and pore waters of the Lena Delta and Laptev Sea[END_REF] elucidate that trace metal, especial the redox sensitive metal like Fe and Mn, contents in marine sediments may increase several folds through the naturally geochemical process regardless of the anthropogenic influence.

Enrichment factor

Trace metals concentrations in marine surface sediments can vary widely [START_REF] Luoma | Processes affecting metal concentrations in estuarine and coastal marine sediments[END_REF]. As a result, it is difficult to evaluate whether the observed concentration in marine sediments is influenced by anthropogenic sources or not without normalizing the result. Some normalising procedures are widely used to compensate for differences in grain size variations and carbonate content, and thus provide a means of separating anthropogenic sources from natural inputs [START_REF] Luoma | Processes affecting metal concentrations in estuarine and coastal marine sediments[END_REF].

Normalization to a background level of metals in samples with different characteristics can be accomplished by calculating an enrichment factor (EF) relative to the reference sample. In the equation EF = (M/Al) S /(M/Al) R , (M/Al) S and (M /Al) R are the ratio of metal to Al concentrations in sample and in reference sample, respectively. It is found that the metal concentrations at stations of the outer shelf in the ECS were the least among the study areas, which may indicate that the disturbance of the outer shelf was relatively minor. In order to avoid the natural differences of sediment textures in different environments, the reference sample is taken from the data of outer shelf stations in the present study. The average concentrations of each metal and Al at all stations of outer shelf are considered as the reference values which are used to calculate the EF and assess the contamination status of the ECS. The EF range of the studied metals was as follow: Fe, 0.43-1.93 (average 1.22); Cu, 0.67-5.83 (average 1.96); Mn, 0.54-3.76 (average 1.47); Ni, 0.52-2.57 (average 1.42); Pb, 0.56-2.07(average 1.29); and Zn, 0.51-2.89 (average 1.42). Contour plots of EF distribution for each metal are shown in Fig. 4. Surprisingly, the EF values of Cu are the highest and indicate a marked anthropogenic burden, suggesting that Cu was the most contaminated metal among the studied metals. However, it can be seen in Fig. 4 that the contour values of each metal greater than 2 generally distributed in the inner shelf. While, the contour values in the middle and outer shelves are within the range of 1-2 and approache to 1, respectively. The EF values suggest the inner shelf of the ECS was mildly contaminated by trace metals. Such a metal contamination did not further extend to the middle and outer shelves.

An EF value of 1 indicates a predominantly natural origin for the element in sediment, while values greater than 1.5 indicate enrichment by either natural processes (e.g. biota contributions) or anthropogenic influences [START_REF] Zhang | Riverine composition and estuarine geochemistry of 1[END_REF]. EF values lower than 0.5 can reflect mobilization and loss of these elements relative to Al, or indicate an overestimation of the reference metal contents [START_REF] Zhang | Geochemistry of trace metals from Chinese river/estuary system: An overview[END_REF][START_REF] Mil-Homens | Heavy metal assessment for surface sediments from three areas of the Portuguese continental shelf[END_REF].

Trace metals sedimentation flux

Huh and coworker employed the radionuclide method ( 210 Pb, 137 Cs and 239,240 Pu) to comprehensively evaluate the sedimentation rates and mass accumulation rates in the East China Sea [START_REF] Huh | Sedimentation dynamics in the East China Sea elucidated from 210 Pb, 137 Cs and 239, 240 Pu[END_REF][START_REF] Su | 210 Pb, 137 Cs and 239,240 Pu in the East China Sea sediments: sources, pathways and budgets of sediments and radionuclides[END_REF]. Based on their data and trace metals concentrations in surface sediment found in the present study, an attempt is made to calculate the trace metals sedimentation fluxes in the ECS. To facilitate the calculation, the calculated area is divided into five boxes: estuary (box I), inner shelf (box II), middle shelf (box III and IV), and outer shelf (box V) (Fig. 5), according to the value of mass accumulation rate (MAR) in each box observed by Huh and coworker [START_REF] Huh | Sedimentation dynamics in the East China Sea elucidated from 210 Pb, 137 Cs and 239, 240 Pu[END_REF][START_REF] Su | 210 Pb, 137 Cs and 239,240 Pu in the East China Sea sediments: sources, pathways and budgets of sediments and radionuclides[END_REF]. The middle shelf area is divided into two boxes because the MAR in the northern middle shelf slightly differed from the southern middle shelf.

Due to the ECS being adjacent to the Yellow Sea to the north and with the North Pacific Ocean to the east, its total area is difficult to determine. Two widely accepted values are 0.74 x 10 6 km 2 for the total area of the ECS and 0.51 x 10 6 km 2 for the area with a water depth < 200m (Wong et al., 2000, and references cited therein). The calculated area of the present study is approximately 0.376 x 10 6 km 2 , which accounts for about 50% of the whole ECS area provided by [START_REF] Wong | The Kuroshio Edge Exchange Processes (KEEP) study -an introduction to hypotheses and highlights[END_REF] and about 74% of the continental shelf area. Table 3 shows the area, the concentration range of trace metals obtained in the present study and the mass accumulation rate (MAR) in each box.

There are three values for each metal-related parameter: minimum, maximum and average. The minimum value of the annual metals sedimentation flux was calculated from the minimum concentration of metals multiplied the minimum value of MAR in each box. The maximum and average values were calculated in a similar manner. The average annual sedimentation fluxes of trace metals in the calculated area were as follow: Fe, 34800 x 10 9 g/y; Mn, 907 x 10 9 g/y; Cu, 31.0 x 10 9 g/y; Ni, 44.8 x 10 9 g/y; Pb, 43.2 x 10 9 g/y; and Zn, 108 x 10 9 g/y. Most of the sedimentation fluxes of trace metals were concentrated in the inner shelf (box II), accounting for 55-70% of the total fluxes of each metal. The second important area was the estuarine zone (box I), contributing from 10 to 17% of the total fluxes of each metal. These results indicate that the suspended loads of metals exported from the Changjiang River catchment were mostly deposited on the inner shelf. It is well known that the continental shelf sediments originate primarily from the riverine suspended load. The suspended load of the Changjiang River is the major contribution and the four middle size rivers, namely the Jiaojiang, the Qiantangjiang, the Jiulongjiang and the Minjiang, contribute minor inputs to the ECS [START_REF] Zhang | Riverine composition and estuarine geochemistry of 1[END_REF]. The upper part of Table 4 summarizes the annual flux of particles to the coast and their trace metal contents.

The calculated annual chemical fluxes of particulate metals from these rivers are listed in the lower part of Table 4. These fluxes are as follows: Fe, 24456 x 10 9 g/y; Mn, 386.6 x 10 9 g/y; Cu, 29.97 x 10 9 g/y; Ni, 30.67 x 10 9 g/y; Pb, 19.87 x 10 9 g/y;

and Zn, 46.67 x 10 9 g/y.

These riverine fluxes of particulate metals are generally lower than, but with the same magnitude as, the calculated sedimentation fluxes. The reason for this phenomenon may attribute to the anthropogenic influence as indicated in the enrichment factor values. The calculation bias of sedimentation fluxes could also be another reason because the difference of maximum and minimum values may vary one order of magnitude. However, the data accuracy of the riverine sediment transportation fluxes and properties shown in literature [START_REF] Zhang | Riverine composition and estuarine geochemistry of 1[END_REF] references cited therein) should be taken into account when calculating the riverine annual transportation fluxes. Since the riverine data were established in the early 1990s. It is known that China launched its modernization campaign from 1980 and substantially increased its economic development in the last two decades [START_REF] Guo | High-resolution depositional record of polycyclic aromatic hydrocarbons in the central continental shelf mud of the East China Sea[END_REF]. The rapid economic development of China may alter the environment. One of the evidences is that the Asian dust storm which occurred since 2000 [START_REF] Mori | Change in size distribution and chemical composition of kosa (Asian dust) aerosol during long-range transport[END_REF]. Thus, in order to obtain a more accurate calculation of the riverine annual fluxes of trace metals, the updating riverine data are necessary to be used. Unfortunately, it is not able to find the updating data in the literature.

Atmospheric trace metals flux

Owing to its rapid industrial development and urbanization since 1980, the frequency and scale of dust events giving rise to dust storm aerosols has increased rapidly in the east Asian region since 2000 [START_REF] Mori | Change in size distribution and chemical composition of kosa (Asian dust) aerosol during long-range transport[END_REF]. Thus, Asian countries suffer from the dust storms which annually occur in the late winter and spring in this decade. Asian dust storms, generated when the surface soil in the arid region of the Asian continental landmass is lifted by winds, move southeastward out of the China continent, the northeasterly monsoon prevails south of 30 °N following the passage of the cold front [START_REF] Hsu | Source, solubility, and dry deposition of aerosol trace elements over the East China Sea[END_REF]. Zhang et al (1997) estimated China's annual emission of dusts to be Tg, 50% of which is subject to long-range transport to the Pacific Ocean and beyond. The East China Sea is situated the right pathway of the Asian dust storms. As a result, it is expected that the atmospheric dry deposition may provide a substantial amount of chemical constituents to the East China Sea.

Research into Asian dust storms impact on the biogeochemistry of the ECS, especially with respect to biological bloom and budget balance of nutrients and trace metals, has been conducted by several research groups [START_REF] Yuan | High correlations between Asian dust events and biological productivity in the western North Pacific[END_REF][START_REF] Hsu | Source, solubility, and dry deposition of aerosol trace elements over the East China Sea[END_REF]. A comprehensive study carried out by [START_REF] Hsu | Source, solubility, and dry deposition of aerosol trace elements over the East China Sea[END_REF] who conducted several cruises to collect the marine aerosols from the ECS during the spring of 2005 and 2007. They analyzed marine aerosol samples for both the water-soluble and the total concentration of 27 trace elements and calculated the dry deposition fluxes.

Their results for trace metals dry deposition fluxes were as follows: Fe, 39±50 µg/m 2 /d; Cu, 12±14 µg/m 2 /d; Mn, 6.7±14.3 µg/m 2 /d; Ni, 0.24±0.29 µg/m 2 /d; Pb, 2.5±6.7 µg/m 2 /d; and Zn, 19±39 µg/m 2 /d. We used these values to calculate 120-day and 180-day of the aerosol dry deposition fluxes of these metals in same area, 0.376 x 10 6 km 2 , as the calculation of metals sedimentation fluxes in the ECS, as shown above. The calculated result for the aerosol dry deposition fluxes and the riverine annual transportation fluxes of these metals are depicted together in Fig. 6. Surprisingly, the aerosol dry deposition fluxes of these metals are relatively small compared with the riverine annual fluxes. The percentage of 120-day aerosol dry deposition fluxes of these metals to the riverine annual fluxes is as follows: Cu and Zn, 1.8%; Pb, 0.56%; Mn, 0.08%; Ni, 0.035%; and Fe, 0.007%. This result may suggest that the aerosol dry deposition fluxes of Fe, Mn, Ni and Pb can be ignored, and of Cu as well as Zn contribute a small amount of fluxes to the ECS when comparing with the riverine fluxes.

Conclusions

The water quality of the ECS has been getting deleterious due to the rapid industrial development and urbanization of China since 1980. However, the results of this study find that the surface sediment of the inner shelf of the East China Sea was mildly contaminated by trace metals. Elevated concentrations of trace metals were generally found in the Hangzhou Bay and along the inner shelf of the ECS. Trace metals contamination did not extend further to the middle and outer shelves of the ECS. The combination of two effects may explain this finding. First, more than 80% the sedimentation fluxes of trace metals are deposited in the inner shelf and the Changjiang estuarine zone. Secondly, the atmospheric dry deposition fluxes of trace metals to the ECS are relatively small compared with the riverine annual fluxes.

Finally, the estimated annual sedimentation fluxes of trace metals in this study are generally higher than those of the riverine annual transportation fluxes of particulate metals. The anthropogenic source is probably the major mechanism.

However, the use of the old published data of the riverine particulate composition and flux in literature to calculate the riverine annual fluxes may cause under estimation because the environmental changes may occur substantially due to the rapid industrial development and urbanization in China.

Figures captions

  and extended to the outer shelves of the ECS with water depths < 150 m. Stations I1-I6 were located in the inner shelf and along the coast of China. Stations M1-M11 were situated in the middle shelf and extended southwards to the northern Taiwan Strait. Stations O1-O6 were located along the Okinawa Trough, through which the Kuroshio Water flows. To facilitate interpretation of the results, the sampling stations were divided into three groups based on their locations and bathymetry of the sampling sites: stations I1-I8 in the inner shelf (depth < 50 m); stations M1-M11 in the middle shelf (50 m < depth < 100 m); and stations O1-O6 in the outer shelf (100 m < depth < 150 m).

Fig. 1 .

 1 Fig.1. Map showing sampling stations in the East China Sea.

Fig. 2 .

 2 Fig.2. Spatial variation of trace metals concentrations in the surface sediment in the

Fig. 3

 3 Fig.3 Scatter plot between concentrations of TOC and trace metals and their

Fig. 5 .

 5 Fig.5. Sub-areas, as defined on the basis of sedimentation rates, and trace metal

Fig. 1

 1 Fig.1

Fig. 2

 2 Fig.2

Fig

  Fig.2 Continue

Table 1 .

 1 The concentrations of trace metals in surface sediments at the study stations

	21
	22	in the East China Sea.
	23
	Station	Long.(E)	Lat. (N)	TOC (%)	Al ( % )	Fe ( % )	Cu (µg/g )	Mn (µg/g )	Ni (µg/g )	Pb (µg/g )	Zn (µg/g )
	I1	123°8.75′	31°37.49′	0.25	5.12	1.73	8.83	251	22.4	33.8	31.8
	I2	123°55.00′ 31°20.00′	0.20	5.47	2.17	9.61	376	19.3	33.7	33.9
	I3	122°40.00′ 31°10.00′	0.44	5.67	1.67	32.1	594	39.7	33.8	96.9
	I4	123°15.00′ 30°27.50′	0.28	5.84	2.00	11.2	328	22.4	26.3	51.3
	I5	122°35.00′ 29°35.00′	0.61	8.49	3.97	41.5	730	48.6	44.8	114.2
	I6	122°2.50′	28°40.00′	0.58	5.33	3.08	40.8	1152	44.0	40.6	112.6
	I7	121°30.00′ 27°45.00′	0.43	5.83	2.70	29.0	958	33.7	26.3	86.2
	I8	120°5.00′	26°10.00′	0.51	7.44	3.19	28.9	1085	32.6	30.0	90.0
	M1	124°41.25′	31°2.50′	0.29	6.03	1.89	11.1	418	26.2	26.0	54.1
	M2	125°27.50′ 30°45.00′	0.40	5.63	2.19	13.6	436	39.7	37.5	110.4
	M3	126°13.75′ 30°27.50′	0.37	6.03	1.99	12.0	490	26.5	22.5	28.7
	M4	124°16.67′	30°4.17′	0.24	5.48	1.47	9.56	368	23.3	26.1	49.5
	M5	123°4.17′	28°16.67′	0.31	5.75	2.42	16.8	412	27.4	30.0	35.5
	M6	124°5.84′	27°53.33′	0.29	5.66	1.68	8.84	324	20.4	26.3	52.4
	M7	122°16.25′ 27°27.50′	0.26	4.75	2.18	10.4	369	22.4	22.5	56.3
	M8	123°48.75′ 26°52.50′	0.10	5.35	1.97	6.45	757	25.6	26.4	52.3
	M9	121°43.96′ 26°37.09′	0.33	5.77	2.56	16.1	488	27.5	26.3	75.9
	M10	120°47.45′ 25°55.00′	0.37	5.76	1.99	11.2	417	27.5	22.5	69.9
	M11	121°29.90′ 25°40.00′	0.30	5.65	2.25	17.7	413	27.6	22.6	66.1
	O1	127°0.01′	30°10.00′	0.27	4.35	1.42	8.82	293	19.3	26.3	44.6
	O2	126°20.00′ 29°17.50′	0.16	5.24	1.32	7.43	332	16.2	18.8	33.0
	O3	125°40.00′ 28°25.00′	0.23	5.37	2.05	7.24	389	19.4	18.8	42.2
	O4	125°7.50′	27°30.01′	0.14	5.15	1.80	6.40	360	20.3	22.4	46.4
	O5	124°35.00′ 26°35.00′	0.16	5.34	1.84	5.60	216	14.2	15.0	37.1
	O6	123°31.88′ 25°56.26′	0.15	4.87	0.62	4.29	152	8.17	10.0	18.2

Table 2 .

 2 Comparison of trace metals concentrations in surface sediment in the various continental shelves around the world. (Concentration unit is in µg/g, except Al and Fe in %)

	Location	Digested Reagent	Al	Fe	Mn	Cu	Ni	Pb	Zn	Reference
	East China Sea	HCl/HNO 3 /HF	4.4-8.5 (5.7)	0.62-4.0 (2.1)	152-1152 (484)	4.3-42 (15)	8.2-49 (26)	10-49 (27)	18-114 (60)	This study
	Arabian Gulf	HCl/HNO 3 /HF	0.1-3.5 (0.69)	0.1-2.5 (0.69)	18-415 (165)	2-21 (9)	2-101 (30)	ND	4-58 (22)	Basaham & El-Sayed, 1998
	Mediterranean, Israel coast	HNO 3	2.0-6.4	0.94-5.94	300-900	5.9-28.5	ND	9.9-20.2	22.6-88.6	Goldsmith et al., 2001
	Aegean Sea	HCl/HNO 3 /HF	2.8-5.3 (4)	0.8-2.8 (1.8)	171-323 (251)	5.3-30.5 (17)	ND	20.7-44.2 (34)	13-77 (50)	Aloupi and Angelidis, 2001
	Banc d'Arguin, Mauritania	HCl/HNO 3 /HF 1.19-4.66	0.63-2.34	27-112	2-18	5-32	2.8-8.9	19-65	Nolting et al., 1999
	Campeche shelf, Gulf of Mexico	HCl/HNO 3	ND	<0.5-7.9 (1.84)	12.5-449 (111)	3.8-18.7 (7.5)	0.56-76.9 (23.0)	0.22-20.2 (4.3)	0.04-79.6 (18.5)	Macias-Zamora et al., 1999
	Laptev Sea, Siberia	HCl/HNO 3 /HF	5.0-7.6	1.9-5.2	187-5398	2-20	16-33	12-22	56-120	Nolting et al., 1996
	Chukchi Sea, Alaska	HNO 3 /HF	1.6-8.3 (4.7)	0.7-8.1 (3)	96-610 (252)	8-31 (17)	10-38 (22)	ND	23-106 (61)	Naidu et al., 1997
	Pechora Sea, Russia	ND	2.97-6.88 (4.7)	0.51-6.88 (3)	154-684 (377)	4-25 (13)	6-47 (25)	9-22 (14)	7-97 (47)	Loring et al., 1995

ND: no data. Value in parentheses is an average.

Table 3 .

 3 The area, ranges of metals concentration, mass accumulation rate (MAR), and annual sedimentation flux for each box of the East China Sea.

	Box	Area (km 2 )	MAR* (g/cm 2 /y)	Fe	Mn	Cu	Ni	Pb	Zn
				metals concentration (Fe in %; all others in µg/g)
	I	31900	0.40-1.09(0.75)

Table 4 .

 4 The annual suspended load, the concentration of riverine particulate metals and annual transportation flux of particulate metals of the major Chinese rivers entering to the East China Sea.

	River	Suspended Load (10 6 t/yr)	Fe	Mn	Cu	Ni	Pb	Zn	Reference
		Riverine particulate metals conc. (Fe in %; all others in µg/g)
	Changjiang	461.4	5.2	811	62.3	64.2	39.9	97.7
	Qiantangjiang	4.4			89.3	92.6	76
	Jiaojiang	8.4	3.62	878	36.5	46.1	54.8	105	Zhang and Liu, 2002
	Minjiang	7.7			51.8		62.5
	Jiulongjiang	3.1	5.12	1620	39.5	81	60.6	228
				Annual flux (10 9 g/yr)
	Changjiang		23993	374.20	28.75	29.62	18.41	45.08
	Qiantangjiang				0.39	0.41	0.33
	Jiaojiang		304.1	7.38	0.31	0.39	0.46	0.88
	Minjiang				0.40		0.48
	Jiulongjiang		158.7	5.02	0.12	0.25	0.19	0.71
	Total Flux	24456	386.59	29.97	30.67	19.87	46.67

Fig.5

Acknowledgments

We wish to gratefully acknowledge the assistance provided by the captain and crew of the R/V Research-I during sampling. The authors are grateful to two anonymous referees for their constructive comments and suggestions which led to significant improvements to the manuscript. This research was financially supported by the National Science Council of the Republic of China under grants NSC 95-2611-M-019-004, 96-2611-M-019-001 and 97-2611-M-019-012.


Marie Noel

Lance Barrett-Lennard

Christophe Guinet

Neil Dangerfield

Peter S Ross
email: peter.s.ross@dfo-mpo.gc.ca

Persistent Organic Pollutants (POPs) in killer whales (Orcinus orca) from the Crozet archipelago, southern Indian Ocean

Keywords: killer whale, Crozet Archipelago, PCBs, PCDDs, PCDFs, TEQs

Persistent Organic Pollutants (POPs), including polychlorinated biphenyls (PCBs), polychlorinated dibenzo-p-dioxins (PCDDs), and dibenzofurans (PCDFs), are ubiquitous environmental contaminants of which significant concentrations are reported in upper trophic level animals. In 1998, we collected blubber biopsy samples (n=11) from killer whales (Orcinus orca) inhabiting the coastal waters around Possession Island, Crozet Archipelago, southern Indian Ocean, for contaminant analyses. Despite inhabiting an isolated region far removed from industrial activities, these killer whales can presently be considered among the most PCB-contaminated cetaceans in the southern hemisphere, with concentrations ranging from 4.4 to 20.5 mg/kg lipid weight (lw). PCDD levels ranged from below the detection limit (5 ng/kg) to 77.1 ng/kg lw and PCDF levels from below the detection limit (7 ng/kg) to 36.1 ng/kg lw. Over 70 % of our study animals had PCB concentrations which exceeded a 1.3 mg/kg PCB threshold established for endocrine disruption and immunotoxicity in free-ranging harbour seals, suggesting that organic contaminants cannot be ruled out as an additional threat to this declining population.

Introduction

Polychorinated biphenyls (PCBs) and polychlorinated dibenzo-p-dioxins / dibenzofurans (PCDDs/Fs) are persistent organic pollutants (POPs). They are hydrophobic, have moderate vapour pressure, and low reactivity that allow them to be readily transported in the environment. "Global distillation" was described as the process by which POPs evaporate in the warmer regions and are then transported in the atmosphere towards the poles where they condense and are deposited. Cold regions, such as the Arctic and the Antarctic, have thus been described as important sinks for these contaminants [START_REF] Wania | Global fractionation and cold condensation of low volatility organochlorine compounds in polar regions[END_REF].

PCBs were extensively used by industrialized nations until the late 70s when they were largely banned. They were detected for the first time in the Antarctic environment in the early 70s. Atmospheric transport is believed to be the dominant pathway for PCB contamination in Antarctica where local sources are thought to be restricted to electrical equipment at isolated research stations [START_REF] Risebrough | PCB and PCT contamination in Winter Quarters bay, Antarctica[END_REF].

PCDD/Fs are formed as by-products during different industrial and thermal processes such as emissions from metallurgical industries, municipal incinerators, pulp and paper mills, and the manufacture of chlorinated chemicals. Atmospheric transport is also thought to be the dominant pathway for the delivery of dioxins and furans to the Antarctic along with minor local sources such as incinerators at research stations [START_REF] Lugar | Results of monitoring for PCDDs and PCDFs in ambient air at McMurdo station, Antarctica[END_REF].

As long lived, high level trophic feeders, marine mammals tend to bioaccumulate POPs in lipid tissues. Marine mammals from Europe, North America, Asia, and the Arctic have been found to be particularly contaminated with PCBs [START_REF] Bergman | Renal lesions in Baltic grey seals (Halichoerus grypus) and ringed seals (Phoca hispida botnica)[END_REF][START_REF] Kajiwara | Organohalogen and organotin compounds in killer whales mass-stranded in the Shiretoko peninsula, Hokkaido, Japan[END_REF]Muir et al., 2000;[START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF]. Marine mammal-eating transient killer whales (Orcinus orca) from the Northeastern Pacific Ocean are reported as among the most PCB-contaminated marine mammals in the world [START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF] and killer whales from Norway are the most PCB-contaminated animals in the Arctic [START_REF] Wolkers | Accumulation and transfer of contaminants in killer whales (Orcinus orca) from Norway: indications for contaminant metabolism[END_REF].

The biology of killer whales from the coastal waters of Possession Island, Crozet Archipelago, southern Indian Ocean, has been studied since the late 1980s, but no information exists on their exposure to POPs. Killer whales are sighted in the area year round but some photo-identified individuals have been seen at the nearby Kerguelen Island and close to the Antarctic continent. Killer whales in the Crozet Archipelago feed on a variety of prey including fish, penguins (Eudyptes sp.), southern elephant seals (Mirounga leonina) and, occasionally, large cetaceans [START_REF] Guinet | L'orque (Orcinus orca) autour de l'archipel Crozet: comparaison avec d'autres localités[END_REF]. Between 1988 and2002, this population declined by 50% due to the decline of an important prey species (the southern elephant seal), interactions with the Patagonian toothfish (Dissostichus eleginoides) longline fishery, and/or emigration of individuals or groups from the coastal waters of the Crozet Archipelago [START_REF] Poncelet | Population dynamics of killer whales in Crozet Archipelago, southern Indian Ocean: exploiting opportunistic and protocol-based photographs in a mark recapture study[END_REF].

POPs are known to cause hormone disruption, immunosuppression, and reproductive failure in other marine mammals (Mos et al., 2007a;[START_REF] Reijnders | Reproductive failure in common seals feeding on fish from polluted coastal waters[END_REF]Ross et al., 1995;[START_REF] Tabuchi | PCB-related alteration of thyroid hormones and thyroid hormone receptor gene expression in free-ranging harbor seals (Phoca vitulina)[END_REF]. Such persistent contaminants can represent a populationlevel conservation threat to killer whales [START_REF] Ross | Fireproof killer whales: Flame retardant chemicals and the conservation imperative in the charismatic icon of British Columbia[END_REF], with heavy POP accumulation largely due to their high trophic position and long lifespan [START_REF] Hickie | Killer whales (Orcinus orca) face protracted health risks associated with lifetime exposure to PCBs[END_REF]. In analysing PCB, PCDD, and PCDF concentrations in blubber biopsies taken from the declining Crozet Archipelago population, we aimed to provide a much-needed baseline for these priority contaminants, and to characterize associated health risks.

Materials and methods

Sampling

The study was carried out in the Crozet Archipelago, southern Indian Ocean (46º25'S; 51º59'E) (Figure 1). Lightweight pneumatic darts were used to biopsy killer whales inhabiting the coastal waters of Possession Island. The variable-power dart projector and its stainless-steel, 6.4 mm diameter tip, as well as a full description of the sampling procedure, is described elsewhere [START_REF] Barrett-Lennard | A cetacean biopsy system using lightweight pneumatic darts, and its effect on the behavior of killer whales[END_REF]. This method was adapted to enable shore-based, rather than ship-based, collections.

Briefly, biopsy sampling was conducted from shore with a fine fishing line attached to the dart in order to retrieve biopsies taken posterior to, and below, the dorsal fin of the animal. Samples of epidermal, dermal, and hypodermal tissue typically weighed approximately 0.5g. Skin from the biopsy samples was preserved in dimethyl sulphoxyde and a saturated salt solution and stored at 4ºC for DNA extraction. Blubber from the biopsies was placed in pesticide grade hexane-rinsed glass vials with aluminium foilcovered caps and stored at -20ºC for contaminant analyses. 11 blubber biopsies were collected from nine different killer whales. Genetic results from the present samples, combined with the photo-identification work conducted previously [START_REF] Guinet | L'orque (Orcinus orca) autour de l'archipel Crozet: comparaison avec d'autres localités[END_REF], enabled a determination of sex as well as age class for each of the nine individuals.

Contaminant analyses

Blubber samples were analyzed for PCDDs, PCDFs, and mono-ortho, di-ortho, and non-ortho (planar) PCBs. Thawed blubber was ground in a porcelain mortar and pestle with 200 g of anhydrous sodium sulphate and spiked with a mixture of 13 C-labelled PCBs, PCDDs, and PCDFs. The blubber-sodium sulphate mixture was transferred to an extraction column and extracted with 250 mL of 1:1 dichloromethane/hexane (DCM/hex) from a glass column by gravity flow. The extract was evaporated to dryness and the lipid content of the samples was determined. Analyses of cleaned-up samples were conducted by high resolution gas chromatography / high resolution mass spectrometry (HRGC/HRMS).

Procedural blanks were analyzed along with samples to assess the integrity of the analytical procedures. Details on the sample clean-up, instrumental analysis condition used, quantification protocols, criteria used for congener identification and the quality assurance / quality control (QA/QC) measures undertaken for the HRGC/HRMS analysis of all the analytes of interest are described elsewhere [START_REF] Ikonomou | Analytical considerations when carbon-fibre fractionation is used in conjunction with HRGC/HRMS for the full congener PCBs determination in environmental samples[END_REF][START_REF] Ikonomou | A comprehensive multiresidue ultra-trace analytical method, based on HRGC/HRMS, for the determination of PCDDs, PCDFs, PCBs, PBDEs, PCDEs, and organochlorine pesticides in six different environmental matrices[END_REF][START_REF] Rantaleinen | Lipid-containing semipermeable membrane devices (SPMDs) as concentrators of toxic chemicals in the lower Fraser River, Vancouver, British Columbia[END_REF].

Data Analysis

Two killer whales were biopsied twice allowing for replicate comparison. For one of these two whales, contaminant concentrations differed between the two samples.

However, in the case of this individual, one of the biopsies was taken on the dorsal ridge just behind the dorsal fin. This sample was low in lipid content, not representative of a typical biopsy and therefore eliminated from our analysis. For the other whale, the two biopsies provided similar results (2.3% and 8.6% difference between the two samples for PCBs and PCDDs/Fs, respectively). Average contaminant concentrations were considered for this whale. Although we were unable to age sampled individuals, we were able to divide our study animals into three categories for POP comparisons: juvenile females (n = 3), adult females (n = 5) and adult male (n = 1).

All the concentrations were expressed on a lipid weight basis (lw) and were blankcorrected as well as recovery-corrected using the stable isotope dilution method based on 13 C-labelled PCB, PCDD, and PCDF spikes [START_REF] Ikonomou | A comprehensive multiresidue ultra-trace analytical method, based on HRGC/HRMS, for the determination of PCDDs, PCDFs, PCBs, PBDEs, PCDEs, and organochlorine pesticides in six different environmental matrices[END_REF] (the recovery ranges were a mean of 60% for PCBs (range 20-95%), 82% for PCDDs (50-105%), and 81% for PCDFs (60-100%)).

Many congeners were not detected. When congeners were undetected, substitutions were applied according to the following rule: 1) when congeners were detected in less than 70% of the samples, concentrations of 0 was substituted; and, 2) when congeners were detected in more than 70% of the samples, a detection limit value substitution was applied.

Total Toxic Equivalents (TEQ) to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)

were calculated for all dioxin-like PCBs measured 114,118,123,156,157,167,and 189;81,126,and 169) and2,3,7,8-Cl substituted PCDDs (n = 7) and PCDFs (n=10) using the international Toxic Equivalency Factors (TEF) [START_REF] Van Den Berg | The 2005 world health organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds[END_REF].

Statistical analysis

Differences in contaminant levels were assessed using an unpaired t-test between juvenile and adult females. The only adult male was considered separately due to evidence in the literature of sex-based differences in POP concentrations [START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF].

Results and discussion

PCB and PCDD/F data were available for 10 blubber biopsies taken from nine killer whales inhabiting the coastal waters of Possession Island, Crozet Archipelago. This represents the first information on POP contamination for this declining population of killer whales.

PCBs

Concentrations

Of the 209 PCB congeners sought, we detected 124 ± 8 (range: 119 -134) congeners in our killer whale samples. PCB levels ranged from 2.7 to 20.5 mg/kg lw (Table 1). Concentrations in juvenile and adult females did not differ (p > 0.05), in contrast to reported findings for killer whales from the Northeastern Pacific Ocean, where immature whales had higher PCB concentrations than adult females [START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF]. While the only male killer whale in the present study had the highest PCB levels of all individuals sampled in our study (Figure 2, Table 1), this could not be statistically compared with our other age/sex categories. Higher POP concentrations in males compared to females have been reported in various species of marine mammals including killer whales from the Northeastern Pacific Ocean [START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF] and in pilot whales (Globicephala melaena) [START_REF] Borrell | Age trends and reproductive transfer of organochlorine compounds in long-finned pilot whales from the Faroe Islands[END_REF]. In marine mammals, a continuous increase of POP concentrations with age is observed in immature individual of both sexes and in adult males. In adult females, concentrations start to decline when they reach sexual maturity because of the offload of fat-soluble contaminants to their young during gestation and nursing [START_REF] Borrell | Age trends and reproductive transfer of organochlorine compounds in long-finned pilot whales from the Faroe Islands[END_REF][START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF][START_REF] Ylitalo | Influence of life-history parameters on organochlorine concentrations in free-ranging killer whales (Orcinus orca) from Prince William Sound, AK[END_REF].

The Possession Island killer whales were approximately 10 times more contaminated than the type C killer whales sampled recently from the southern Ross Sea adjacent to Antarctica [START_REF] Krahn | Use of chemical tracers to assess diet and persistent organic pollutants in Antarctic type C killer whales[END_REF], likely reflecting a difference in diet and possibly the remote location of the Ross Sea. While PCB concentrations in our whales were lower than those reported in killer whales from industrialized areas (Table 2), they were similar to those observed in resident killer whales from Alaska [START_REF] Ylitalo | Influence of life-history parameters on organochlorine concentrations in free-ranging killer whales (Orcinus orca) from Prince William Sound, AK[END_REF], and only slightly lower than the levels in northern residents from the Northeastern Pacific Ocean [START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF] and Norwegian killer whales [START_REF] Wolkers | Accumulation and transfer of contaminants in killer whales (Orcinus orca) from Norway: indications for contaminant metabolism[END_REF]. As the latter killer whales are considered the most contaminated Arctic marine mammal, our results again underscore the vulnerability of high trophic level marine mammals in polar and otherwise remote regions.

However, the Norwegian killer whales and the resident killer whales of the Northeastern Pacific Ocean are fish-eating, while the Possession Island killer whales appear to consume a mixed diet of mostly marine mammals but also fish and penguins [START_REF] Guinet | L'orque (Orcinus orca) autour de l'archipel Crozet: comparaison avec d'autres localités[END_REF]. Recently, a juvenile male was found stranded on Possession Island and the stomach content revealed remains of elephant seals, fur seals (Arctocephalus sp), and king penguins but no fish. Dietary preferences are a major factor affecting contaminant concentrations in marine mammals. In the Northeastern Pacific Ocean, transient marine mammal-eating killer whales are far more contaminated than the resident fish-eating killer whales [START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF]. Based on the limited data available, the diet of the Possession Island killer whales seems trophically comparable to transient killer whales of the Northeastern Pacific Ocean and thus comparing contaminant burdens between these two populations provides at least a crude evaluation of differences in regional contamination. The present levels in the Possession Island killer whales were one fifth to one tenth of the levels recorded in transients from the Northeastern Pacific Ocean [START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF] and Alaska [START_REF] Ylitalo | Influence of life-history parameters on organochlorine concentrations in free-ranging killer whales (Orcinus orca) from Prince William Sound, AK[END_REF]. These differences could be the result of dietary preferences but may also be due to the remote nature of Possession Island.

PCB concentrations in Crozet killer whales were higher than levels reported in marine mammals from Antarctica, including southern elephant seals [START_REF] Miranda-Filho | Residues of persistent organochlorine contaminants in southern elephant seals (Mirounga leonina) from Elephant Island, Antarctica[END_REF], and minke whales (Balaenoptera acutorostrata) [START_REF] Aono | Persistent organochlorines in minke whale (Balaenoptera acutorostrata) and their prey species from the Antarctic and the North Pacific[END_REF]. The Crozet killer whales were less PCB-contaminated than only two other southern hemisphere species, namely the estuarine dolphins (Sotalia guianensis) and Atlantic spotted dolphins (Stenella frontalis) inhabiting the nearshore waters of Brazil [START_REF] Kajiwara | Contamination by persistent organochlorines in cetaceans incidentally caught along Brazilian coastal waters[END_REF]). The Crozet whales had higher PCB concentrations than Arctic belugas (Delphinapterus leucas) [START_REF] Helm | Polychlorinated naphthalenes and coplanar polychlorinated biphenyls in beluga whale (Delphinapterus leucas) and ringed seal (Phoca hispida) from the eastern Canadian Arctic[END_REF] that are at the receiving end of PCB dispersion from northern hemispheric industries.

Homologue group and congener patterns

No significant differences (p > 0.05) in PCB homologue group and congener patterns were observed between juvenile and adult females (Figure 3). The adult male also revealed a similar pattern. In all the three groups, di-ortho PCBs were highly dominant (97.5 ± 1.1 % of ∑PCBs) (Figure 2). Hexa-CBs was the dominant homologue group, accounting for 55 ± 3 % of total PCBs, followed by hepta-(23 ± 2 %) and penta-CBs (11 ± 3 %). A similar pattern was found in southern elephant seals but they had a more even contribution of hepta and penta-CBs [START_REF] Miranda-Filho | Residues of persistent organochlorine contaminants in southern elephant seals (Mirounga leonina) from Elephant Island, Antarctica[END_REF]. The six dominant congeners in our killer whales accounted for 55 ± 1 % of ∑PCBs (Table 1).

Similar to our results, PCBs-153 and 138 were among the dominant congeners in the three populations of killer whales from the Northeastern Pacific Ocean [START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF], in killer whales from Alaska [START_REF] Ylitalo | Influence of life-history parameters on organochlorine concentrations in free-ranging killer whales (Orcinus orca) from Prince William Sound, AK[END_REF], and Norway [START_REF] Wolkers | Accumulation and transfer of contaminants in killer whales (Orcinus orca) from Norway: indications for contaminant metabolism[END_REF]. In addition, PCB 153 and 138 dominated PCB patterns in southern elephant seals [START_REF] Miranda-Filho | Residues of persistent organochlorine contaminants in southern elephant seals (Mirounga leonina) from Elephant Island, Antarctica[END_REF] as well as in lower trophic levels of the Antarctic killer whale food web [START_REF] Goerke | Increasing levels and biomagnification of persistent organic pollutants (POPs) in Antarctic biota[END_REF]. This is likely due to the fact that PCB-153 was a major component of the most heavily used PCB technical mixture, and, as it has no vicinal hydrogen and is Cl-substituted at both para positions, is resistant to metabolism [START_REF] Boon | The possible role of metabolism in determining patterns of PCB congeners in species from the Dutch Wadden Sea[END_REF].

Dioxins and furans

Concentrations

Dioxin and furan concentrations were very low with many congeners being undetected. Out of the 75 possible dioxin congeners, only up to 3 congeners were detected.

The total PCDD concentrations ranged from below the mean detection limit (6.8 ± 2.3 ng/kg) to 77.1 ng/kg lw with a mean concentration of 17.5 ± 7.8 ng/kg lw (Table 2). Out of the 135 possible furan congeners, only up to two congeners were detected in our whales and the total PCDF concentrations ranged from below the mean detection limit (3.4 ± 1.4 ng/kg) to 113.1 ng/kg lw with a mean concentration of 5.1 ± 3.6 ng/kg lw.

There were no significant differences in PCDD/F concentrations between juvenile and adult female killer whales from Possession Island (Table 2). The adult male was the most PCDD/F contaminated, as observed in killer whales from the Northeastern Pacific Ocean [START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF], but the small sample size precluded statistical evaluation. The apparently higher dioxin and furan concentrations in adult females compared to juvenile females were not supported statistically (p > 0.05). The high standard error reported for adult females was due to only one highly PCDD contaminated individual. Due to our limited sample size and therefore lack of strong statistical basis, it was not clear whether or not the higher concentrations reported in adult females compared to the juveniles could be an indication that dioxins and furans are not transferred as efficiently as PCBs from mother to calf.

Data on dioxins and furans in killer whales are limited (Table 2). PCDD/F concentrations in our study were higher than those reported for killer whales from Japan [START_REF] Kajiwara | Organohalogen and organotin compounds in killer whales mass-stranded in the Shiretoko peninsula, Hokkaido, Japan[END_REF], but lower than levels reported for the three different communities of killer whales living in the Northeastern Pacific Ocean [START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF]. The higher PCDD/F concentrations observed in the latter killer whales may reflect local contamination by pulp and paper mills [START_REF] Ross | Harbour seals (Phoca vitulina) in British Columbia, Canada, and Washington, USA, reveal a combination of local and global polychlorinated biphenyl, dioxin, and furan signals[END_REF]. Despite these observations, however, PCDD/F concentrations in all killer whales are relatively low, something that has been attributed to the minimal biomagnification of planar "dioxin-like" compounds in aquatic food webs as a consequence of metabolism and excretion [START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF]. The duality of distance from source (remote location) and limited biomagnification in aquatic food webs likely explains the low levels of dioxins and furans in Crozet killer whales.

Total PCDD/F concentrations in killer whales from Possession Island were higher than levels previously reported for other Antarctic marine mammals such as Weddell seals [START_REF] Corsolini | Polychloronaphthalenes and other dioxin-like compounds in Arctic and Antarctic marine food webs[END_REF] and Antarctic fur seals (Arctocephalus gazella) [START_REF] Oehme | Polychlorinated Dibenzo-p-Dioxins, dibenzofurans and coplanar biphenyls in Antarctic fur seal blubber[END_REF]. However, they were lower than levels reported for south polar skuas (Catharacta maccomicki) which migrate to more contaminated areas in lower latitudes [START_REF] Senthilkumar | Polychlorinated dibenzo-pdioxins, dibenzofurans and polychlorinated biphenyls in polar bear, penguin and south polar skua[END_REF]. Compared to Arctic marine mammals, our observed concentrations were in the same range as reported in ringed seals (Pusa hispida) [START_REF] Norstrom | Polychlorinated dibenzo-p-dioxins and dibenzofurans in marine mammals in the Canadian north[END_REF], but higher than levels in belugas from Baffin Island (Norstrom et al., 1992).

Homologue group and congener patterns

Only congeners from the hexa and octa homologue groups were detected, accounting for 30 ± 35 % and 56 ± 37 % of ∑PCDD, respectively. 1,2,3,6,7,8 HxCDD accounted on average for 65 ± 15 % of ∑HxCDD. This particular congener was previously reported as being dominant in several species of marine mammals including killer whales from Japan [START_REF] Kajiwara | Organohalogen and organotin compounds in killer whales mass-stranded in the Shiretoko peninsula, Hokkaido, Japan[END_REF], Weddell seals from Antarctica [START_REF] Senthilkumar | Polychlorinated dibenzo-pdioxins, dibenzofurans and polychlorinated biphenyls in polar bear, penguin and south polar skua[END_REF], harbour seals (Phoca vitulina) from British Columbia [START_REF] Addison | PCDD/F and PCB in harbour seals (Phoca vitulina) from British Columbia: response to exposure from pulp mill effluents[END_REF]. This congener has, in part, been attributed to the historical use of elemental chlorine by pulp mills, and to woodchips contaminated by pentachlorophenol [START_REF] Addison | PCDD/F and PCB in harbour seals (Phoca vitulina) from British Columbia: response to exposure from pulp mill effluents[END_REF]. OCDD was also detected in Arctic ringed seals [START_REF] Norstrom | Polychlorinated dibenzo-p-dioxins and dibenzofurans in marine mammals in the Canadian north[END_REF]. OCDD originates from pulp mills, combustion, or high temperature industrial processes in which there is a chlorine source [START_REF] Norstrom | Polychlorinated dibenzo-p-dioxins and dibenzofurans in marine mammals in the Canadian north[END_REF]). The remote nature of Possession Island thus suggests that PCDD contamination is most likely due to long range atmospheric transport but could also be in part due to small-scale combustion-related activities nearby, such as shipping or research operations [START_REF] Lugar | Results of monitoring for PCDDs and PCDFs in ambient air at McMurdo station, Antarctica[END_REF].

No PCDF congeners were detected in juvenile females. 1,2,3,4,7,8 HxCDF,1,2,3,4,6,7,8 HpCDF,1,2,3,4,7,8,9 HpCDF, and OCDF were the only congeners detected in the adult females. 2,3,7,8 TCDF was the only congener detected in the adult male. Even though the patterns appeared different among the three groups, no clear trend can be concluded as the sample size was small and the number of analytes detected very limited.

Toxic Equivalents (TEQ)

Consistent with the POP concentration patterns, juvenile females had similar TEQ to adult females (76.5 ± 5.0 ng/kg lw and 44.2 ± 8.4 ng/kg lw, respectively) (p > 0.05), while the adult male had the highest TEQ (109.1 ng/kg lw) (Table 3). Again, however, the small sample size precluded statistical interpretation of the single male sample. PCBs contributed up to 99.9% of the total TEQ in the killer whale samples, underscoring the recalcitrance of this contaminant class. The adult male appeared to have a proportionately lower contribution of PCBs to TEQ (88.3%) than did the immature (99.8 ± 0.1%) and adult females (97.3 ± 1.7%), although the limited sample size precludes a rigorous evaluation.

Non-ortho PCB congeners contributed to most of the PCB TEQ (Table 3). This pattern differed to those previously reported for other cetaceans species including killer whales from the Northeastern Pacific Ocean [START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF], in which non-ortho and monoortho PCBs contributed more equally to the ∑PCB TEQ. However, our use of new TEF values (2005) partly explains this difference in observations; similar non-ortho and monoortho PCB contributions to the ∑PCB TEQ was observed when we applied TEFs from 1998 to this dataset. 169,126,and 105 were the dominant contributors to the total TEQ, consistent with previous studies of cetaceans [START_REF] Corsolini | Persistent organic pollutants in some species of a Ross Sea pelagic trophic web[END_REF][START_REF] Focardi | Isomer-specific analysis and toxic potential evaluation of polychlorinated biphenyls in Antarctic fish, seabirds and Weddell seals from Terra Nova Bay (Ross Sea)[END_REF][START_REF] Ylitalo | Influence of life-history parameters on organochlorine concentrations in free-ranging killer whales (Orcinus orca) from Prince William Sound, AK[END_REF].

Toxicological implications

Organic contaminants are a concern to the health of marine mammals, with observations of impaired reproduction, skeletal lesions, kidney damage, tumors, premature birth and skin lesions in populations inhabiting contaminated areas [START_REF] Beckmen | Clinical and pathological characterization of northern elephant seal skin disease[END_REF][START_REF] Béland | Toxic compounds and health and reproductive effects in St. Lawrence beluga whales[END_REF][START_REF] Bergman | Renal lesions in Baltic grey seals (Halichoerus grypus) and ringed seals (Phoca hispida botnica)[END_REF][START_REF] Delong | Premature births in California sea lions: Association with high organochlorine pollutant residue levels[END_REF][START_REF] Olsson | Contaminants and diseases in seals from Swedish waters[END_REF]. High PCB concentrations have been linked to decreased immune function in field studies of harbour seals [START_REF] Mos | Chemical and biological pollution contribute to the immunological profiles of freeranging harbor seals[END_REF], bottlenose dolphins (Tursiops truncatus) [START_REF] Lahvis | Decreased lymphocyte responses in free-ranging bottlenose dolphins (Tursiops truncatus) are associated with increased concentrations of PCBs and DDT in peripheral blood[END_REF] and polar bears [START_REF] Lie | Does high organochlorine (OC) exposure impair the resistance to infection in polar bears (Ursus maritimus)? Part 2: possible effect of OCs on mitogen-and antigen-induced lymphocyte proliferation[END_REF], as well as captive feeding studies of harbour seals [START_REF] De Swart | Impairment of immune function in harbor seals (Phoca vitulina) feeding on fish from polluted waters[END_REF][START_REF] Ross | Contaminant-induced immunotoxicity in harbour seals: wildlife at risk?[END_REF]. Contaminant-related immunotoxicity has been, in part, blamed for serious outbreaks of infectious disease outbreaks in marine mammals [START_REF] Osterhaus | Morbillivirus infections of aquatic mammals: newly identified members of the genus[END_REF]. In addition, PCBs have been implicated in the disruption of vitamin A and thyroid hormone systems in harbour seals, which could lead to adverse effects on growth and development (Mos et al., 2007a;[START_REF] Tabuchi | PCB-related alteration of thyroid hormones and thyroid hormone receptor gene expression in free-ranging harbor seals (Phoca vitulina)[END_REF].

Different thresholds for adverse health effects have been established for PCBs in marine mammals. Immunotoxicity and endocrine disruption were observed in harbour seals at a concentration of 209 ng/kg total TEQ [START_REF] De Swart | Impairment of immune function in harbor seals (Phoca vitulina) feeding on fish from polluted waters[END_REF][START_REF] Ross | Contaminant-related suppression of delayed-type hypersensitivity and antibody responses in harbor seals fed herring from the Baltic Sea[END_REF]. This value was adjusted to 255 ng/kg TEQ for killer whales from the Northeastern Pacific Ocean owing to a broader analytical evaluation [START_REF] Ross | High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference[END_REF]. None of our Crozet killer whales surpass this threshold.

Thresholds have also been determined for PCBs in marine mammals. A threshold value of 17 mg/kg lw was established for immunotoxicity in captive harbour seals [START_REF] Ross | Contaminant-induced immunotoxicity in harbour seals: wildlife at risk?[END_REF], while a 10 mg/kg lw threshold was associated with an increase in calf mortality in bottlenose dolphins [START_REF] Hall | Individual-based model framework to assess population consequences of polychlorinated biphenyl exposure in bottlenose dolphins[END_REF]. Recently, a more protective value of 1.3 mg/kg was proposed for the protection of marine mammal health based on the 95% confidence interval for endocrine disruption and immunotoxicity in multiple studies of free-ranging harbour seals (Mos et al., 2007b). Even though the PCB concentrations in killer whales from Possession Island were among the lowest reported in killer whales world-wide, 70% of our study animals surpassed this latter threshold level, suggesting that contaminants cannot be excluded as a possible risk factor in the decline of this population.

Conclusion

Despite our limited number of samples, this study provided baseline organic contaminant data for the Possession Island killer whales. While these killer whales were less contaminated than some of their northern hemispheric counterparts, they can be counted among the most PCB-contaminated marine mammals in the southern hemisphere.

Despite a PCB ban in the industrialized world in the 1970s, the dispersion of this chemical has attained the far reaches of the planet, including the killer whales that ply the remote waters around Possession Island. While concentrations of POPs are decreasing in the industrialized regions and in the Arctic, the global PCB distribution has not yet reached a steady state and concentrations are expected to increase in the Antarctic before reaching a state of equilibrium [START_REF] Goerke | Increasing levels and biomagnification of persistent organic pollutants (POPs) in Antarctic biota[END_REF]). While we did not measure the organochlorine pesticide dichloro diphenyl trichloroethane (DDT), other studies of marine mammals from the southern hemisphere have found their concentrations to exceed that of PCBs by 2 -9 times [START_REF] Krahn | Use of chemical tracers to assess diet and persistent organic pollutants in Antarctic type C killer whales[END_REF][START_REF] Aono | Persistent organochlorines in minke whale (Balaenoptera acutorostrata) and their prey species from the Antarctic and the North Pacific[END_REF]. The results of our study provide another reminder that POPs know no borders, and can significantly contaminate wildlife inhabiting remote corners of the world.

FIGURE CAPTIONS

ACCEPTED MANUSCRIPT

Figure 1 :

 1 Figure 1: Killer whales were sampled around Possession Island, Crozet Archipelago, in the

Figure 2 :

 2 Figure 2: Juvenile and adult females have similar PCB (total, di-ortho, mono-ortho and

Figure 3 :

 3 Figure 3: The homologue group contribution to the total PCB concentrations was similar across

  Figure 1:

Table 1 :

 1 The PCB composition was generally similar across age/sex categories as evidenced by the top six PCB congeners (concentrations in mg/kg lw). The percentage contribution to the total PCB contamination is added in brackets.

		Juvenile Females		Adult Females		Adult male
			(n = 3)		(n = 5)		(n = 1)
	∑ PCBs		11.4 ± 1.2		10.1 ± 3.1		19.5
		153 a	2.2 ± 0.2 (19.3 ± 0.4%)	153 a	2.0 ± 0.6 (19.9 ± 0.2%)	153 a	3.8 (19.2%)
		138 a	1.5 ± 0.1 (12.9 ± 0.8%)	138 a	1.4 ± 0.4 (13.1 ± 0.2%)	138 a	2.7 (13.8%)
		180	0.9 ± 0.2 (7.5 ± 1.2%)	149	0.8 ± 0.3 (7.4 ± 0.3%)	180	1.5 (7.8%)
		149	0.8 ± 0.2 (7.2 ± 0.6%)	180	0.7 ± 0.2 (7.2 ± 0.1%)	149	1.3 (6.9%)
		187 a	0.7 ± 0.1 (5.8 ± 0.6%)	187 a	0.6 ± 0.2 (5.8 ± 0.2%)	187 a	1.1 (5.6%)
		201	0.5 ± 0.2 (3.9 ± 1.0%)	201	0.4 ± 0.1 (3.4 ± 0.1%)	118 a	0.6 (3.1%)
	∑ top 6	6.5 ± 0.3 (57.4 ± 0.6%)		5.9 ± 0.3 (54.6 ± 0.2%)		11.0 (56.4%)
		a : dominant congener of a co-eluting group (CB-153 was co-eluting with 132; 138 with
		163 and 164; 187 with 182; 118 with 106)

Table 2 :

 2 PCB concentrations in the largely marine mammal-eating Crozet killer whales exceed concentrations in the fish-eating Antarctic killer whales. PCB levels approach those observed in the relatively contaminated northern resident killer whales from the Northeastern Pacific Ocean.

	Location	Year	Type	Sex	Lifestage	PCBs (mg/kg lw)	PCDDs (ng/kg lw)	PCDFs (ng/kg lw)	TEQ (ng/kg lw)	Reference
	Crozet Archipelago	1998		F	Juvenile	11.4 ± 1.1	3.9 ± 1.8	ND a	76.5 ± 5.0	Our study
				F	Adult	10.1 ± 3.0 20.6 ± 12.1	6.6 ± 5.9	44.2 ± 8.4
				M	Adult	19.5	38.79	11.4	120.4
	Ross Sea, Antarctica	2005-2006	Type C b	M	Adult	1.6 ± 1.1	n.a c	n.a	n.a	Krahn et al.,2008
				M	Subadult	2.1 ± 2.3	n.a	n.a	n.a
				F	Adult	0.6 ± 0.4	n.a	n.a	n.a
	Norway	2002		M	Adult/Juvenile	16-44	n.a	n.a	n.a	Wolkers et al., 2007
	Japan	2005		M	Calf	47	0.62	0.77	300	Kajiwara et al., 2006
				F	Calf	51	N.D	0.96	405
				M	Adult	57	1.50	3.90	350
				F	Adult	30	3.50	5.80	220
	British Columbia,	1993-1996	Northern Resident	M	Adult	37 ± 6			435 ± 60	Ross et al., 2000
	Canada			F	Adult	9 ± 3			111 ± 29
			Southern Resident	M	Adult	146 ± 33	1050 ± 258	55 ± 6	845 ± 195
				F	Adult	55 ± 19			456 ± 27
			Transient	M	Adult	251 ± 55			699 ± 142
				F	Adult	59 ± 21			338 ± 53
		2004-2006	Southern Resident	M	Adult	66 ± 26	n.a	n.a	n.a	Krahn et al.,2007
				F	Adult	45	n.a	n.a	n.a
	Alaska, USA	1994-1999	Resident	M/F	Adult/Juvenile	14 ± 13	n.a	n.a	100 ± 98	Ylitalo et al., 2001
			Transient	M/F	Adult/Juvenile	230 ± 130	n.a	n.a	860 ± 640

a : Non detected b : Type C killer whales are thought to prey mainly on marine fish c : Non available

Table 3 :

 3 In juvenile female, adult female and adult male killer whales, PCBs are the dominant contributor to the total toxic equivalents to 2,3,7,8-TCDD.

			Mean TEQ ± st error (pg/g lw)
		PCB	Juvenile Female	Adult female	Adult male
		congeners	(n=3)	(n=6)	(n=1)
	Non-ortho PCBs	77	0.01 ± 0.00	0.01 ± 0.00	0.02
		81	0.01 ± 0.00	0.01 ± 0.00	0.01
		126	10.61 ± 2.53	7.69 ± 1.11	16.63
		169	53.39 ± 7.07	31.38 ± 7.02	60.56
	∑ non-ortho PCBs	64.01 ± 8.72	39.07 ± 7.65	77.21
	% of ∑PCB TEQ	83.42 ± 8.71%	87.30 ± 2.06%	70.82%
	Mono-ortho PCBs	105	1.17 ± 0.25	0.81 ± 0.18	4.74
		114	0.09 ± 0.02	0.06 ± 0.01	0.32
		118	3.77 ± 0.74	2.71 ± 0.66	17.89
		123	0.04 ± 0.01	0.02 ± 0.01	0.20
		156	0.57 ± 0.03	0.38 ± 0.09	2.16
		157	0.15 ± 0.01	0.11 ± 0.03	0.69
		167	0.51 ± 0.04	0.39 ± 0.12	2.68
		189	0.08 ± 0.02	0.06 ± 0.02	0.40
	∑ mono-ortho PCBs	6.38 ± 0.98	4.55 ± 1.12	29.08
	% of ∑PCB TEQ	8.28 ± 0.97%	9.97 ± 1.17%	26.68%
	Sum PCB TEQ		76.26 ± 4.88	43.62 ± 8.66	106.29
			99.77 ± 0.15%	97.27 ± 1.70%	88.31%
	Sum PCDD TEQ		0.19 ± 0.13	0.45 ± 0.34	1.59
			0.23 ± 0.15%	1.99 ± 1.56%	1.46%
	Sum PCDF TEQ		ND	0.17 ± 0.14	1.14
			-	0.72 ± 0.66%	1.04%
	TOTAL TEQ		76.45 ± 5.00	44.24 ± 8.37	109.02

Acknowledgements

This work was conducted in part under the Program 109 of the Institut Polaire Paul Emile Victor. We would like to thank Terres Australes et Antarctiques Francaises (TAAF), the Killer Whale Adoption Program of the Vancouver Aquarium, and the staff of the regional contaminant laboratory at the Institute of Ocean Sciences, Fisheries and Oceans Canada.


S Prasanna Kumar

Raj P Roshin

Jayu Narvekar

P K Dinesh Kumar

E Vivekanandan

S Prasanna Kumar

Response of the Arabian Sea to global warming and associated regional climate shift

Keywords: Climate change, Arabian Sea, sea surface temperature, cyclones, rainfall, winter temperature, wheat production, food quantity, vegetation cover

The response of the Arabian Sea to global warming is the disruption in the natural decadal cycle in the sea surface temperature (SST) after 1995, followed by a secular warming. The Arabian Sea is experiencing a regional climate-shift after 1995, which is accompanied by a 5-fold increase in the occurrence of "most intense cyclones". Signatures of this climate-shift are also perceptible over the adjacent landmass of India as: (1) progressively warmer winters, and (2) decreased decadal monsoon rainfall. The warmer winters are associated with a 16-fold decrease in the decadal wheat production after 1995, while the decreased decadal rainfall was accompanied by a decline of vegetation cover and increased occurrence of heat spells. We propose that in addition to the oceanic thermal inertia, the upwelling-driven cooling provided a mechanism that offset the CO 2 -driven SST increase in the Arabian Sea until 1995.

Introduction

Global warming and human-induced climate change are the immediate threats to mankind and tropical regions are the most vulnerable to them.

Global warming has different manifestations, such as increase in the number and severity of tropical cyclones [START_REF] Emanuel | Increasing destructiveness of tropical cyclones over the past 30 years[END_REF][START_REF] Webster | Changes in tropical cyclone number, duration, and intensity in a warming environment[END_REF], changing pattern of precipitation and increase of extreme rain events [START_REF] Goswami | Increasing trend of extreme rains over India in a warming environment[END_REF]Zhang et al., 2007), melting of glaciers [START_REF] Oerlemans | Quantifying global warming from the retreat of glaciers[END_REF] and associated sea level rise [START_REF] Church | How fast are sea levels rising?[END_REF]Meehl et al., 2005). In addition to these changes in the physical climate, the terrestrial as well as the aquatic ecosystem will also experience great pressure and undergo change [START_REF] Meyer | Impacts of climate change on aquatic ecosystem functioning and health[END_REF][START_REF] Cramer | Global response of terrestrial ecosystem structure and function to CO 2 and climate change: results from six dynamic global vegetation models[END_REF]. For example, variation in the length of a season may lead to mismatches between the key elements in an ecosystem such as flowering and nesting times, feeding period of young birds [START_REF] Both | Climate change and population declines in a long-distance migratory bird[END_REF]. Similarly, a warming environment driven by rapid increase in the concentration of atmospheric carbon dioxide and ocean acidification may lead to coral bleaching [START_REF] Hughes | Climate, human impacts, and the resilience of coral reefs[END_REF][START_REF] Hoegh-Guldberg | Coral reefs under rapid climate change and ocean acidification[END_REF], while increased land temperature may lead to an increase in the tropical vector-borne diseases [START_REF] Rogers | The global spread of malaria in a future, warmer world[END_REF]Hopp and Foley, 2003) thus causing concern for human health. Recent studies showed that not only are the oceans becoming warmer at the surface, but there is penetration of the human induced warming into the deeper parts of the oceans [START_REF] Barnett | Penetration of human-induced warming into the world's oceans[END_REF]. However, it is presently unclear how the Arabian Sea is responding, except that it has warmed by about 0.5 o C during 1904[START_REF] Oerlemans | Quantifying global warming from the retreat of glaciers[END_REF][START_REF] Rupakumar | Climate change in India: Observations and model projections[END_REF]. In this paper we explore the response of the Arabian Sea to global warming and its possible impact on frequency and intensity of cyclones, summer monsoon rainfall, wheat production, land vegetation cover and frequency of heat spells.

Material and methods

Study area

The Arabian Sea is a tropical basin situated in the western part of the northern Indian Ocean (0-25 o N and 45-80 o E) which is land locked in the north. It is forced by a semi-annually reversing wind system called monsoon. During winter (December-February), the weak (~5m s -1 ) northeast trade winds bring cool, dry continental air into the Arabian Sea, while during summer (June-September), the strong (~15m s -1 ) southwest winds brings moisture-laden maritime air into the Arabian Sea. In response to this wind reversal, the upper ocean circulation of the Arabian Sea also undergoes seasonal reversal. The Arabian Sea is biologically one of the most productive regions of the worlds' oceans [START_REF] Ryther | Primary organic production in relation to the chemistry and hydrography of the western Indian Ocean[END_REF] due to the summer and winter blooms. The summer phytoplankton bloom occurs due to wind-driven upwelling [START_REF] Smith | Southwest monsoon of 1979: chemical and biological response of Somali coastal waters[END_REF][START_REF] Banse | Seasonality of phytoplankton chlorophyll in the central and northern Arabian Sea[END_REF][START_REF] Brock | Interannual variability in phytoplankton blooms observed in the northwestern Arabian Sea during the southwest monsoon[END_REF] along the coast of Somalia, Arabia and southern part of the west coast of India, while the winter bloom driven by winter-cooling and convective mixing [START_REF] Madhupratap | Mechanismof the biological response to winter cooling in the northeastern Arabian Sea[END_REF]Prasanna Kumar et al., 2001a) occurs in the northern Arabian Sea.

Data and Analysis

We used a variety of multi-disciplinary data from the Arabian Sea and the adjacent landmass of India to elucidate the signature of global warming and Comprehensive Ocean-Atmosphere Data Set (ICOADS) [START_REF] Woodruff | Early ship observational data and ICOADS[END_REF] (http://www.cdc.noaa.gov/cdc/data.coads.1deg.html), (2) NOAA SST data [START_REF] Reynolds | An inproved in situ and satellite SST analysis for climate[END_REF] and (3) Kaplan SST data [START_REF] Kaplan | Analyses of global sea surface temperature 1856-1991[END_REF], both provided by the NOAA/OAR/ERSL PSD, Boulder, Colorado, USA from their website http://www.cdc.noaa.gov/in [START_REF] Reynolds | An inproved in situ and satellite SST analysis for climate[END_REF]. From the monthly mean SST annual mean SST anomaly was computed for further analysis. The strong El Nino years (1972-73, 1982-83, 1991-92 and 1997-98) (see http://ggweather.com/enso/oni.htm) as well as Indian Ocean Dipole climatology of wind was obtained from NCEP/NCAR reanalysis [START_REF] Kalnay | The NCEP/NCAR 40-year reanalysis project[END_REF] data (http://www.cdc.noaa.gov/cdc/data.ncep.reanalysis.html).

Fig.1 Location

The February temperature in northwestern India and western Himalayas (see

Results and discussion

The analysis of all the three basin- The decadal cycle seen in the SST anomaly closely followed the solar irradiance cycle until the year 1995, which underscored the importance of the decade after 1995. Note that when the solar activity was declining after the year 2000, and subsequently was at its lowest (Fig. 2), the SST anomaly did not show any decreasing trend.

Fig. 2 Location

On the contrary, SST anomaly was the highest. This indicated that the solar activity was not responsible for the deviation of the natural decadal cycle in SST anomaly after 1995. To understand this, we examined the atmospheric Table 1). Note that the Kaplan SST did not show significant correlation with atmospheric CO 2 concentration prior to 1995.

Similarly, though the correlation of all the three SSTs with global CO 2 emission was not significant during the period 1960 and 1995, a stronger and significant correlation was noticed during the period 1960 and 2006 (Table 1).

Table 1 Location

Both To understand the effect of this regional climate-shift on the oceanatmospheric processes, we analyzed the cyclone data available for the past 2.

Table 2 Location

For the present study, the cyclones with wind speed greater than 100 km per hour were designated as "most intense cyclones". The analysis showed a 5fold increase in the occurrence of intense cyclones in the Arabian Sea during the past 12 years (1995)(1996)(1997)(1998)(1999)(2000)(2001)(2002)(2003)(2004)(2005)(2006)(2007), compared to the previous 25 years , when there was only one in 1976. In addition to the increase in the "number" of occurrence of severe cyclones the "intensity" of these cyclones also showed an increase with time as can be discerned from the T-number in Table 2. Such increase in the intensity and occurrence of severe cyclones in the tropics, especially in the Atlantic and Indian Oceans are reported in a warming environment [START_REF] Emanuel | Increasing destructiveness of tropical cyclones over the past 30 years[END_REF][START_REF] Webster | Changes in tropical cyclone number, duration, and intensity in a warming environment[END_REF]Elsner et al., 10 2008). However, we would like to point out that the length of our data is only 25 years.

In order to decipher further, the impact of the regional climate-shift on the adjacent landmass, we analyzed the monthly mean air temperature and rainfall over India. The air temperature during February in the regions of northwestern India and western Himalayas (see Fig. 1 for location) did not show any trend during 1960 and 1995, but after 1995 it showed a rapid warming of about 1.5 o C (Fig. 3a).

Fig. 3 Location

Since wheat is a winter crop and a major portion of the wheat-producing region falls within northwestern India, we analyzed the annual wheat yield (kg hectare -1 ) (Fig. 3b) which showed a steady increase in the decadal yield Next we analyzed the all India summer monsoon (June to September) rainfall data. The integrated decadal anomaly showed a decline of 70.9 mm during 1995 and 2004 (Fig. 4a). Hence, the negative decadal anomaly in the all India summer monsoon rainfall during late 1995 appears to be linked to the weakening of land-ocean thermal-gradient under the secular warming of the Arabian Sea (Fig. 2).

Since more than 80% of the rainfall over India occurs during summer monsoon, it is expected to have a major influence on the vegetation cover.

We analyzed the Normalized Difference Vegetation Index (NDVI) for the homogeneous Indian monsoon rainfall region (see Fig. 1 for location). The NDVI showed an increasing trend from 1982 to 1995 and after 1995, the trend reversed showing a general decrease (Fig. 4b). We attribute a major part of this declining vegetation cover to declining summer monsoon rainfall. Though human induced changes such as deforestation could also alter the vegetation cover, its contribution is presumably much smaller.

Since it is generally known that changes in the land cover can magnify the effect of extreme climate events, we examined the data on the occurrence of heat spells over India during the period 1978 to 2005. The number of heat spells during 1978 to 1995 was below 20, but after 1995 it showed a sudden increase up to 35 (Fig. 4c).

Thus, we see a close link between the disruption of the natural decadal cycle of SST in the Arabian Sea after 1995 and the events such as increased occurrence of "most intense" cyclones, warming winters, decreased decadal monsoon rain fall, decreased vegetation cover and increased number of heat spells. Some of these changes may be interacting to strengthen/weaken the others through positive/negative feedbacks in the ocean-atmosphere-land system. We attribute these changes to warming driven by increased CO 2 emission. The obvious question is why the Arabian Sea showed a climate change response only after 1995, though the global CO 2 emission and atmospheric CO 2 concentrations showed an increasing trend from 1958

onwards. The answer may lie in the geographic location of the Arabian Sea and its special oceanographic feature. As mentioned earlier, this tropical basin experiences strong wind-driven upwelling during summer monsoon [START_REF] Swallow | Some aspects of the physical oceanography of the Indian Ocean[END_REF]Smith and Botterro, 1977;Smith and Codispoti, 1890) along the coasts of Somalia, Arabia and the southwest coast of India.

Upwelling supplies cold and nutrient-rich subsurface waters to the surface which subsequently moves offshore under the influence of prevailing currents (Prasanna Kumar et al., 2001b). For example, the temperature of the upwelled water in the Somali region is about 17-22 o C (Smith and Codispoti, 1890) and advection carries these waters to the central Arabian Sea. Thus, the upwelling of cold subsurface waters and its advetion to offshore region cools a large part of the Arabian Sea. It is this upwelling-driven cooling that was able to offset the increased SST and maintain the natural decadal cycle until 1995. But after 1995, the basin-wide winds in the Arabian Sea showed a decline (Fig. 5).

Fig. 5 Location

However, after 1995 the CO 2 driven radiative forcing showed a 20% increase during 1995 and 2005 (IPCC, 2007) and the upwelling-driven cooling in the Arabian Sea was unable to compensate the oceanic response of warming in the Arabian Sea. This led to the observed disruption in the natural decadal cycle of SST and subsequent secular warming.

Summary and conclusion

Using a suite of multi-disciplinary data from the Arabian Sea and the adjacent landmass, we explored the signature of global warming and showed that the disruption in the natural decadal cycle of SST after 1995 is a manifestation of regional climate-shift. Concurrent with this, a 5-fold increase in the occurrence of most intense cyclones as well as an increase in their intensity was noticed. The winters over the northern part of the Indian landmass showed a rapid warming consistent with the increase in SST which resulted in a 16-fold decrease in the decadal wheat production after 1995.

The all India summer monsoon rainfall anomaly showed a sharp decline after 1995, which was linked to the decline in vegetation cover. Concomitant with this, the number of heat spells showed a sharp increase after 1995. We propose that the upwelling-driven cooling in the Arabian Sea was able to maintain the natural decadal cycle in the SST until 1995, in spite of the oceanic thermal inertia as well as increased global CO 2 emission and atmospheric CO 2 concentrations. After 1995 the upwelling-driven cooling was unable to offset the CO 2 -driven warming seen in the SST.

The present study illustrate the correlation between components in the ocean-atmosphere-land processes and indicates complicated feedbacks in the Arabian Sea and the adjacent landmass, which has implications for the food and water security of this region. The quantification of these changes is a big challenge. We do not know as yet, how long the observed trend will continue. There is an urgent need to assemble more data and follow a multidisciplinary approach to analyze them. 3660 1960 1965 1970 1975 1980 1985 1990 1995 ) 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 Year

  regional climate-shift. The monthly mean sea surface temperature (SST) data in the Arabian Sea (0-25 o N and 45-80 o E) were extracted for the period 1960-2006 from three different sources -(1) the International

Fig. 1

 1 Fig.1 for the geographic location) was computed by averaging the air

  averaged annual mean SST (ICOADS, NOAA & Kaplan) anomaly of the Arabian Sea (0-25 o N and 45-80 o E) showed dominant decadal scale variability during the period 1960 to 1995 (Fig.2) with a slow warming trend. Beyond 1995, a disruption in the natural decadal cycle of SST anomaly was noticed. Since the natural decadal cycle is known to arise from solar activity (White, 2006) we examined the measured as well as reconstructed solar irradiance. It showed a smooth decadal cycle without any abrupt change during the study period (Fig.2).

  CO 2 concentration measured at Mauna Loa, Hawaii, and global CO 2 emission. The correlation of atmospheric CO 2 concentration with all the three basin-averaged SSTs (ICOADS, NOAA, Kaplan) in the Arabian Sea was larger and highly significant during the period 1960 to 2006 compared to the period 1960 to 1995 (

  these results indicated the role of human-induced warming in the disruption of natural decadal cycle and subsequent secular warming of SST after 1995. It may be noted that the CO 2 driven radiative forcing during 1995 and 2005 showed a 20% increase, the largest change for any decade in at least the last 200 years (IPCC, 2007). The observed disruption of the natural decadal cycle of SST after 1995 can thus be attributed to intrinsic ocean response, in the form of regional climate-shift, to external forcing by greenhouse gases.

  37 years. In the Arabian Sea, cyclones are formed mainly during two periods: May-June (spring-summer transition) and October-November (fall-winter transition). The cyclones during May and June are formed within the Arabian Sea itself, while during October and November they are mostly formed over the Bay of Bengal and cross over to the Arabian Sea. Hence, we analyzed the data during May and June to identify the occurrence of the most intense cyclones in the Arabian Sea and presented the results in Table

  during 1965 and 1995 (from 425 kg hectare -1 during 1965-1975 to 689 kg hectare -1 during 1985-1995). However, during 1995 and 2005 the decadal yield dramatically decreased to 42 kg hectare -1 in synchrony with increasing February temperature (Fig.3a). A correlation of annual wheat yield with air temperature in February during 1960-2005 showed a significant negative correlation (r = -0.30 & p-value = 0.05). The critical period for the wheat crop is its growth and reproductive stages which occur during February[START_REF] Kumar | Indian agriculture and climate sensitivity[END_REF]. Higher temperatures during this period lead to stress on the growth and reduce yield. It has been shown that for every 1 o C increase in temperature, the kernel weight of wheat declined up to 4.5% of the maximum predicted kernel weight at 16 o C[START_REF] Saini | Thermal and photoperiodic effects on phase durations of four wheat varieties grown on different sowing dates[END_REF]. Hence, we attribute a significant portion of this 16-fold reduction in the wheat production after 1995 to the warmer winters (~1.5 o C). There also could be other factors responsible for the observed reduction such as change in the land area under wheat cultivation, availability of water resources, change in the usage of fertilizers, for which we do not have data.

Fig. 4 Location

 4 Fig. 4Location

  manuscript and suggesting language corrections. We thank Dr. Ragu Murtugudde of University of Maryland, USA for his constructive criticism of the manuscript and suggestions, Mr. O.P. Sreejith, IMD, Pune for making available the data on Disastrous Weather Events, Mr. Byju for processing the wind data, Dr. P. Vethamony and Dr. G.N. Swamy of NIO, Goa for discussions, Mr. Shyam and Mr. Uchil for the help in preparing the diagrams. We also wish to acknowledge Director NIO Goa and Council of Scientific and Industrial Research (CSIR), New Delhi for all the support and encouragement. Authors Roshin and Jayu acknowledge CSIR for their fellowships. The authors thank the anonymous reviewers for their constructive criticism which helped to improve the manuscript. This is NIO contribution number xxxx.

Fig. 1

 1 Fig. 1 Map showing geographical regions used in the study for computing spatial averages of various parameters. Region with vertical lines represent Western Himalayas and slanting lines represent the northwestern Indian region over which winter temperature data were used. The dotted region indicates the homogeneous rainfall region. The data on Normalized Difference Vegetation Index (NDVI) were used for the homogeneous rainfall region.

Fig. 2

 2 Fig.2The annual mean of sea surface temperature (SST, °C) anomaly of the Arabian Sea from ICOADS, NOAA and Kaplan averaged over the basin (0°-25°N, 45°-80°E) and the reconstructed as well as measured solar irradiance.See text for details.

Fig. 4

 4 Fig.4 (a) All India summer-monsoon rainfall anomaly (red curve), 5-year running mean (black curve), integrated decadal rainfall anomaly (bar diagram), (b) Normalized Difference Vegetation Index (NDVI) for the homogeneous Indian rainfall region, and (c) number of heat spells over India. The broken line indicates the linear trend line.

Fig. 5

 5 Fig. 5 Basin-averaged annual mean winds in the Arabian Sea during 1995 to 2008 from NCEP/NCAR reanalysis data. See text for details. The solid line is the linear trend line with r = -0.83 and p-value of 0.0002.

Fig. 2

 2 Fig.2The annual mean of sea surface temperature (SST, °C) anomaly of the Arabian Sea from ICOADS, NOAA and Kaplan averaged over the basin (0°-25°N, 45°-80°E) and the reconstructed as well as measured solar irradiance. See text for details.

Fig. 3 .

 3 Fig.3. (a) February mean air temperature (°C) for the northwestern India and western Himalayas , and (b) all India decadal wheat yield (kg hectre -1 ). The broken line indicates the linear trend line. The broken line is the linear trend line.

  Figure3

Figure 4

 4 Figure 4

Table 2

 2 Number of intense cyclones in the ArabianSea during 1970Sea during -2007. .

	A cyclone is categorized as "intense" when the wind speed associated with
	the cyclone exceeds 100 km h -1 . 'T-Number' is a measure of the intensity of
	a cyclone (For details, see http://www.ssd.noaa.gov/PS/TROP/CI-
	chart.html). n.a: 'data not available'.
	Year	Duration	Wind speed	Intensity
			(km h -1 )	T-Number
	1976	May 31-June05	167	n.a
	1996	June 17-June 20	111	3.5
	1998	June 05-June 09	167	5.0
	1999	May 16-May 22	195	5.5
	2001	May 21-May 28	210	5.5
	2007	May 31-June 07	315	7.0

Acknowledgements. The authors wish to express their gratitude to Lucy James, Professor, Department of English, Government College of Arts, Science and Commerce, Sanquelim, Goa for meticulously going through the

) while that during 2000 and 2007 were taken from the Joint Typhoon Warning Center (JTWC) https://metocph.nmci.navy.mil/jtwc/best_tracks/2001/2001 sbio/ bio012001.txt. The data for air temperature and rainfall over India (Fig.1) during 1960 and 2005 (Parthasarathy et al., 2001; Kothwale and RupaKumar, 2005) were taken from Indian Institute of Tropical Meteorology (IITM) (http://www.tropmet.res.in). The monthly mean

//ftp.ncdc.noaa.gov/pub/data/paleo/climate_forcing/solar_variability/lean 2000_irradiance.txt. The data

 Solomon, S., Stott, P.A., Nozawa, T., 2007. Detection of human influence on twentieth-century precipitation Trends, Nature 448, 461-465 1960-1995 1960-2006 1960-1995 1960