and Medium-Chain Chlorinated Paraffins in Marine Mammals from the

Sep 3, 2015 - ∑SCCPs and ∑MCCPs, respectively. The repeatability of the analysis was assessed by analyzing three duplicate samples, with relative ...
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Temporal Trends and Pattern Changes of Short- and Medium-Chain Chlorinated Paraffins in Marine Mammals from the South China Sea over the Past Decade Lixi Zeng,†,‡,§ James C. W. Lam,*,† Yawei Wang,§,∥ Guibin Jiang,§ and Paul K. S. Lam*,† †

State Key Laboratory in Marine Pollution, Research Centre for the Oceans and Human Health, Shenzhen Key Laboratory for Sustainable Use of Marine Biodiversity, City University of Hong Kong, Kowloon, Hong Kong Special Administrative Region, China ‡ School of Chemistry and Chemical Engineering, University of Chinese Academy of Sciences, Beijing 100049, China § State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China ∥ Institute of Environment and Health, Jianghan University, Wuhan 430056, China S Supporting Information *

ABSTRACT: Temporal trends of short- (SCCPs) and medium-chain chlorinated paraffins (MCCPs) were examined in blubber samples of 50 finless porpoises (Neophocaena phocaenoides) and 25 Indo-Pacific humpback dolphins (Sousa chinensis) collected from the South China Sea between 2004 and 2014. Elevated levels of SCCPs and MCCPs were detected in all blubber samples of both cetacean species. Concentrations of SCCPs ranged from 280 to 3900 ng·g−1 dry weight (dw) in porpoises and from 430 to 9100 ng·g−1 dw in dolphins, while concentrations of MCCPs ranged from 320 to 8600 ng·g−1 dw in porpoises and from 530 to 23 000 ng·g−1 dw in dolphins. Significantly higher concentrations were present in dolphins than porpoises due to their exposure levels in their living habitats. Strongly linear correlations existed between SCCPs and MCCPs, but there were no significant concentration differences between the genders of the two cetacean species in the same sampling year. Significantly temporal increasing trends of ∑SCCPs and ∑MCCPs have been observed in both porpoise and dolphin samples over the past decade, which reflect the influence of histories of production and usage on the bioaccumulation of CPs in marine mammals in China. An apparent temporal shift trend from SCCPs to MCCPs was also observed in CP accumulation profiles. Complex environmental fractionation from localized sources in the study region via atmospheric transport, oceanic/offshore water transport, and trophic transfer have resulted in different CP accumulation levels and homologue patterns in the two cetacean species. This is the first report of systematic temporal trends of SCCPs and MCCPs in marine mammals.

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properties.9,10 A global regulation/ban on SCCPs as a persistent organic pollutant (POP) candidate is being reviewed under the Stockholm Convention,11 but the current information is insufficient to adequately assess the chemicals. CPs began to be produced at the end of the 1950s in China and have been manufactured since the early 2000s on a large scale. Now China is the largest producer, consumer, and exporter of CPs in the world.12 The production volume of CPs has been continuously and rapidly growing during the past decade. The annual production of CPs is estimated to have been approximately 150 kilotonnes in 2003 and then increased to about 600 kilotonnes in 2007,12 and sharply rising to about 1000 kilotonnes at present.13 CPs have been detected in various

INTRODUCTION Chlorinated paraffins (CPs), also known as polychlorinated nalkanes (PCAs), are complex industrial chemicals that have been produced in large amounts in the world for many years. Over 200 CP formulations have been widely used during the last 10 years in a variety of industrial applications, including use as high-temperature lubricants, plasticizers, flame retardants, and additives in adhesives, paint, rubber, and sealants. According to the carbon chain length, CPs are subdivided into short-chain chlorinated paraffins (SCCPs, C10−13), medium-chain chlorinated paraffins (MCCPs, C14−17), and long-chain chlorinated paraffins (LCCPs, C>17) with chlorination degree varying from 30% to 70%.1 Currently available data indicate that CPs, especially SCCPs, are persistent in the environment,2 are toxic to aquatic organisms and carcinogenic to mammals,3−5 have the potential to bioaccumulate and/or biomagnify in fresh and marine food webs,6−8 and can be prone to long-range atmospheric transport due to their semivolatile © XXXX American Chemical Society

Received: May 20, 2015 Revised: August 12, 2015 Accepted: September 3, 2015

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DOI: 10.1021/acs.est.5b02473 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology matrices in China including air,14−16 water,17 food,18 soil,19,20 sludge,21 sediment,13,22,23 and biota8,24 in recent years. However, up to now, data on SCCPs, in particular for MCCPs and LCCPs, are still scarce as compared to other POPs. Time-series investigation of contaminants is necessary to better understand trends in exposure levels, to evaluate the impacts of production and usage on emissions, and predict the future risk on the environment and on human health. Several studies have indicated the increasing trends of persistent halogenated compounds, such as polybrominated diphenyl ethers (PBDEs),25,26 polychlorinated biphenyls (PCBs),27 and perfluorinated compounds (PFCs),28 in various environmental matrices in relation to their large-scale production and usage. However, there are considerable data gaps in the current monitoring studies, such as no time-trend studies of CPs in marine mammals. Our recent papers have reported the increasing temporal trends of SCCPs in marine sediment cores from the East China Sea22 and the Chinese Yellow Sea.23 Although the two studies provided indicative information for understanding the temporal variation of SCCPs, some important factors such as bioaccumulation and/or biomagnification in halobios and spatial variation may lead to different temporal trends of CPs in marine biota. Temporal trends of CPs in halobios would be more relevant for marine ecological risk assessment when samples are available. So systematic investigation of annual temporal trends of CPs in biota samples from China is especially significant. Marine mammals are commonly used as bioindicators of marine ecosystems and human health because they are able to integrate environmental information and make a sensitive response to environmental changes across large spatial and over temporal scales.9,29−31 Indo-Pacific humpback dolphin (Sousa chinensis) and finless porpoise (Neophocaena phocaenoides) are two resident cetacean species in the South China Sea that are the top predators in the marine food chain, providing the potential to bioaccumulate CPs in their tissues. The two cetacean species have been the subjects of our previous studies, which indicated that both of them are susceptible to exposure and bioaccumulation of persistent halogenated contaminants due to their longevity, high trophic position, and body fat content.32,33 China has a region-specific production history of CPs, and Asia-Pacific countries offer the largest market demand for the industrial chemicals. To better understand the current pollution status of CPs in the marine environment, the present study aimed to identify and quantify SCCPs and MCCPs in the blubber of these two species of marine mammals from the South China Sea, to reveal the primary sources, and to assess their temporal trends and homologue pattern changes from 2004 to 2014. To our knowledge, this is the first report of systematic temporal trends of CPs in biota over the past 10 years.

adjacent to the Pearl River Delta (PRD), a highly developed industrial region of south China. The blubber of adult finless porpoises (n = 50) and adult Indo-Pacific humpback dolphins (n = 25) was sampled from stranded animals collected by the Agriculture, Fisheries and Conservation Department (AFCD) in Hong Kong, China, between 2004 and 2014 (Table S1). Blubber of stranded marine mammals is commonly used for monitoring of environmental contaminants and this sampling manner does not cause any stress or interference with the population. However, it should be noted that there are possible limitations in this collection program, including the availability of sample sizes from the two top marine predators and the possibility that use of stranded animals might skew the results to highly contaminated individuals that may be dying as a result of contaminant exposure. All samples were dissected with stainless steel tools and then wrapped in aluminum foil before being transferred to the laboratory. All the blubber samples were freeze-dried and stored at −20 °C before chemical analysis. Sample preparation was accomplished by use of our previously established procedures with minor modifications.23 Details on the extraction and cleanup procedure of CPs from the blubber samples can be found in Supporting Information. Instrumental Analysis, Identification, and Quantification. Instrumental analysis and qualitative identification of SCCPs (C10−13Cl5−10) and MCCPs (C14−17Cl5−10) were carried out on the basis of our previously developed method.7,19 Interferences from CP congeners with five carbon atoms more and two chlorine atoms less were quantitatively calculated by the chemical calculation procedure, described in detail in our early work.19 Quantifications of total SCCPs and MCCPs were conducted according to Reth et al.34 Three SCCP standards (51.5%, 55.5%, and 63.0% Cl) and three MCCP standards (42.0%, 52.0%, and 57.0% Cl), together with their respective mixtures, were used to establish a reasonably linear correlation between chlorine content and total response factor.34 The regression coefficients (R2) of five-point calibration curves for SCCP and MCCP standards were ≥0.97. Quality Assurance and Quality Control. All glassware was rinsed with dichloromethane prior to use. A procedural blank was processed with every batch of eight samples to check for possible interference or contamination. Both SCCPs and MCCPs in blanks were below or close to the limits of detection, and the reported concentration of CPs was not blank-corrected. Recoveries for surrogate standard 13C10-transchlordane and SCCP (63% Cl), and MCCP (57% Cl) standards were determined by three replicates with spiked fish oil samples (these samples were from a lake in the Tibetan Plateau, China), and the values were in the range of 83−115%, 75−99%, and 79−98%, respectively. The recoveries of 13Ctrans-chlordane in all blubber samples ranged from 70% to 104%. The chlorine contents of SCCPs and MCCPs in the samples were 61−66% and 52−56%, respectively, which were between and close to those of CP standards. Accuracy was controlled with spiked samples and deviated ≤15% from the expected values. The method detection limits (MDL) for total SCCPs and MCCPs were calculated by tripling the standard deviation of background signals from eight blank samples. The MDLs were estimated to be about 40 and 60 ng·g−1 for ∑SCCPs and ∑MCCPs, respectively. The repeatability of the analysis was assessed by analyzing three duplicate samples, with relative standard deviation ≤10%. Statistical Analysis. Statistical analysis was carried out with IBM SPSS Statistics 20.0 (IBM Corp., 1989−2011), and

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MATERIALS AND METHODS Sample Collection, Extraction, and Cleanup. Finless porpoise and Indo-Pacific humpback dolphin are two resident types of continental shelf cetacean species distributed around Hong Kong in the South China Sea. As shown in Figure S1 in Supporting Information, finless porpoises have resident populations distributed in the southern and eastern waters of Hong Kong, while Indo-Pacific humpback dolphins are commonly found in the northwestern waters of Hong Kong B

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Environmental Science & Technology Table 1. Concentrations of Short- and Medium-Chain Chlorinated Paraffins and Their Homologue Groupsa finless porpoise mean ± SD

a

median

lipid (%)

65 ± 23

67

C10 (ng·g−1 dw) C11 (ng·g−1 dw) C12 (ng·g−1 dw) C13 (ng·g−1 dw) ∑SCCPs (ng·g−1 dw)

660 ± 330 510 ± 310 380 ± 240 230 ± 160 1800 ± 1000

660 520 360 210 1800

C14 (ng·g−1 dw) C15 (ng·g−1 dw) C16 (ng·g−1 dw) C17 (ng·g−1 dw) ∑MCCPs (ng·g−1 dw)

1400 ± 910 850 ± 600 570 ± 440 360 ± 250 3200 ± 2200

1300 780 480 330 2900

range

Indo-Pacific humpback dolphin avg contribution

mean ± SD

18−93 49 ± 19 Short-Chain Chlorinated Paraffins 140−1300 37% 630 ± 530 80−1100 29% 680 ± 620 37−920 21% 590 ± 560 21−580 13% 570 ± 590 280−3900 100% 2500 ± 2300 Medium-Chain Chlorinated Paraffins 160−3700 44% 3400 ± 3600 67−2300 27% 950 ± 1000 58−1700 18% 920 ± 1000 30−960 11% 850 ± 950 320−8600 100% 6200 ± 6500

median

range

avg contribution

47

14−90

470 540 420 310 1900

140−2200 110−2600 87−2200 78−2100 430−9100

26% 27% 24% 23% 100%

2500 630 700 640 4600

300−12000 62−3300 65−3800 41−3500 530−23000

56% 15% 15% 14% 100%

In blubber samples of finless porpoises (n = 50) and Indo-Pacific humpback dolphins (n = 25) from 2004 to 2014 in Hong Kong, south China.

overall mean of 5100 ng·g−1 lw. Generally, ∑MCCPs were higher than ∑SCCPs in all porpoise blubber samples within every sampling year. C14 was the dominating homologue group that accounted for more than 40% of ∑MCCPs measured. Up to now, there have been almost no available measurements of MCCPs in marine mammals for concentration comparison. Concentrations of ∑SCCPs in finless porpoise significantly correlated with those of ∑MCCPs (R2 = 0.89, p < 0.05) (Figure S2), suggesting a similar uptake pathway/kinetics for these contaminants. Similar positive relationships between ∑SCCPs and ∑MCCPs can also be observed in air, soil, and sediment from the Pearl River Delta.13,37 It is not surprising that SCCPs and MCCPs are the two major components within CPs, and in China, commercial CP products are not strictly grouped by carbon chain length of the n-alkane feedstock used in their manufacture.38 The higher accumulation levels of MCCPs in the studied marine mammals may be due to higher levels of MCCPs in their prey, and this deserves further investigation. Concentrations of ∑SCCPs and ∑MCCPs (Figure 1) showed statistically significant increasing temporal trends in porpoises from 2004 to 2014 when linear regression analysis of yearly log concentrations was used (R2 = 0.59 for SCCPs and 0.56 for MCCPs, p < 0.05). Similar positive temporal trends were also observed for linear regression analysis of yearly log lipid-normalized concentrations (R2 = 0.29 for SCCPs and 0.31 for MCCPs, p < 0.05). Figure S3 shows the significant positive temporal trends of yearly median concentrations (nanograms per gram dry weight) in finless porpoises from log−linear regression analysis. ∑SCCP and ∑MCCP concentrations have been rising significantly from 2010 to 2014 with rates of increase of 110% and 140%, respectively. According to the linear regression equations, ∑SCCP and ∑MCCP concentrations will double from 2014 to 2018. The world market demand for CPs has increased over the past decade, while in China, CPs have been manufactured on a large scale during this period to meet both domestic demand and exports. Annual production output grew about 5 times from 2004 to 2009 (Figure S4) and reached a new high in the last three years. CPs as important additives are being widely applied to many kinds of industrial products, including rubber, paint, flame retardants, plastic, PVC, adhesives, and sealants in China (Figure S5). There is currently no restriction or control on CPs in China.

statistical significance was accepted at p < 0.05. Student′s t-test was used to assess any significant difference between two groups of data. Log transformations were applied to obtain normal distribution concentrations of individual years for data analysis. Log−linear regression was performed to evaluate temporal trends of SCCPs and MCCPs in marine mammals following the procedures described by Lam et al.,32 Park et al.,35 Okada et al.,36 and Sun et al.27

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RESULTS AND DISCUSSION SCCPs (C10−13Cl5−10) and MCCPs (C14−17Cl5−10) were detected in all blubber samples from both species of marine mammals, finless porpoise and Indo-Pacific humpback dolphin, from 2004 to 2014, suggesting that CPs are ubiquitous pollutants in the south China marine environment. No significantly gender-associated concentration differences of SCCPs and MCCPs were observed in either cetacean species (p > 0.05). Therefore, male and female samples were pooled for temporal trend analysis for dolphins and porpoises, respectively. Concentrations of CPs in this study are expressed on a dry weight basis [nanograms per gram dry weight (ng·g−1 dw)], and the lipid-normalized concentrations [lipid weight basis; nanograms per gram lipid weight (ng·g−1 lw)] are also summarized below. Accumulation Levels and Temporal Trends of Shortand Medium-Chain Chlorinated Paraffins in Finless Porpoise. Descriptive statistics of the concentrations of SCCPs, MCCPs, and their homologues in blubber samples of finless porpoises (n = 50) are summarized in Table 1. Total SCCP concentration (∑SCCPs) ranged from 280 to 3900 ng· g−1 with a mean value of 1800 ng·g−1. The lipid-normalized concentrations of ∑SCCPs were between 570 and 5800 ng·g−1 lw with a mean value of 2800 ng·g−1 lw. C10 and C11 carbon chain groups were the predominant homologue groups and accounted for more than 60% of ∑SCCPs measured, followed by C12 and C13 groups. Accumulation levels of SCCPs in the blubber of finless porpoises in this study were significantly higher than those in the blubber of beluga, ringed seal, and walrus (1978−1994) from the Arctic and the St. Lawrence River Estuary (110−1360 ng·g−1).9 Total MCCP concentration (∑MCCPs) ranged from 320 to 8600 ng·g−1 with an overall mean of 3200 ng·g−1. The lipid-normalized concentrations of ∑MCCPs were in the range 670−11 000 ng·g−1 lw with an C

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receiving exposure to CP mixtures in a similar manner from similar sources. Student’s t-test results indicated that levels of ∑SCCPs and ∑MCCPs were significantly higher in IndoPacific humpback dolphins than in finless porpoises (p < 0.05), indicating that northwestern waters of Hong Kong adjacent to the mouth of the Pearl River Estuary are more contaminated by CPs than the eastern waters. Figure 2 shows the temporal trends of ∑SCCPs and ∑MCCPs (ng·g−1 dw) in Indo-Pacific humpback dolphins

Figure 1. Temporal trends of log ∑SCCPs and log ∑MCCPs concentrations (ng·g−1 dw) in blubber samples of finless porpoise (n = 50) from the South China Sea during 2004 to 2014. The two groups of blubber samples represent males (M) and females (F).

Therefore, it can be inferred that the increasing production and usage of CPs certainly will increase the environmental release in any region with rapid economic development and industrial activities, such as in the case of the PRD.13,37 Temporal trends of both elevated SCCP and MCCP levels in finless porpoise are in good agreement with the history of CP production and usage in China over the past 10 years and also in accordance with the increasing trends of CP deposition concentrations in recent sediment layers of sediment core from the PRD.13 Accumulation Levels and Temporal Trend of Shortand Medium-Chain Chlorinated Paraffins in Indo-Pacific Humpback Dolphins. Concentrations of SCCPs, MCCPs, and their homologues in blubber samples of Indo-Pacific humpback dolphin (n = 25) are also summarized in Table 1. ∑SCCPs in dolphins ranged from 430 to 9100 ng·g−1 with a mean value of 2500 ng·g−1. The corresponding lipid-normalized concentrations of ∑SCCPs were between 920 and 24 000 ng· g−1 lw with a mean value of 5500 ng·g−1 lw. The two highest concentrations were found in the Indo-Pacific humpback dolphins stranded in 2012. ∑MCCPs in dolphins ranged from 530 to 23 000 ng·g−1 with an overall mean of 6200 ng·g−1. The lipid-normalized concentrations of ∑MCCPs were in the range 1400−56 000 ng·g−1 lw with an overall mean of 13 000 ng·g−1 lw. C14 dominates the composition profile with an average contribution of about 56% of ∑MCCPs. Significantly higher ∑MCCPs than ∑SCCPs can be observed in all dolphin blubber samples within every sampling year. Additionally, a stronger positive relationship between ∑SCCPs and ∑MCCPs was found in dolphins than in porpoises (R2 = 0.98, p < 0.05) (Figure S2), further suggesting that these marine mammals are

Figure 2. Temporal trends of log ∑SCCPs and log ∑MCCPs concentrations (ng·g−1 dw) in blubber samples of Indo-Pacific humpback dolphins (n = 25) from the South China Sea during 2004 to 2014. The two groups of blubber samples represent males (M) and females (F).

from 2004 to 2014. Both ∑SCCPs and ∑MCCPs showed statistically significant increasing trends of yearly log concentrations in dolphins (R2 = 0.82 for SCCPs and 0.84 for MCCPs, p < 0.05), which correspond well to the time trends in porpoises. Similar positive temporal trends were also observed for linear regression analysis of yearly log lipid-normalized concentrations in dolphins (R2 = 0.52 for SCCPs and 0.65 for MCCPs, p < 0.05). Significant elevating levels (ng·g−1 dw) of ∑SCCPs and ∑MCCPs in dolphin samples with rates of increase of 170% and 280% from 2010 to 2014, respectively, are shown in Figure S3. According to the linear regression equations, ∑SCCP and ∑MCCP concentrations will double from 2014 to 2022 and from 2014 to 2021, respectively, if it is assumed that the rate of usage of SCCPs and MCCPs remains constant. Temporal trends in dolphins further reflect the influence of production and usage on the bioaccumulation of CPs in marine mammals. Temporal Changes in Accumulation Profiles and Homologue Patterns. SCCP and MCCP homologue patterns in blubber samples of finless porpoise between 2004 D

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representative congener group abundance profiles of SCCPs in porpoises from different sampling years. As can be seen, a significant increase of longer-chain homologues was found in the later sampling years. C 10−11 with 8−10 chlorines predominated in different sampling years, which are similar to the compositions of a commercial CP mixture (CP52) used in China, indicating possible local sources. Coastal discharge, transport, and trophic transfer may result in accumulation of highly chlorinated congeners in finless porpoises.6 Within MCCPs, the C14 group was the most abundant homologue (range 41−51%, overall average 44%; Figure 3C), which is typical of the composition of MCCPs in technical mixtures.2 A slightly higher proportion of C14 in 2004−2010 was observed than in 2011−2014. MCCP congeners with 6−8 chlorines predominated in different sampling years. SCCP and MCCP homologue patterns in blubber samples of dolphins from 2004 to 2014 are shown in Figure 4. Different from the SCCP homologue pattern in porpoises, the dominant homologue groups within SCCPs in dolphins varied with time during the past decade. A more significant temporal shift trend from shorter- to longer-chain groups can be observed in the SCCP homologue pattern (Figure 4B). In dolphins, the relative abundance of C10 decreased with an annual change rate of 4%, while those of C12 and C13 increased with annual change rates of 2% and 6%, respectively. The congener group abundance profiles of SCCPs in dolphin from different sampling years (Figure S7) indicate that C10−11 with 7−9 chlorine atoms were predominant in 2004, whereas C12−13 with 7−9 chlorine atoms prevailed in 2014. The temporal shift trends in both cetacean species may be linked to a shift to production and usage of CP formulations containing more long-chain homologues in recent years and subsequent bioaccumulation and/or biomagnification preference or potential biotransformation in marine food webs. Similar to the MCCP homologue pattern in porpoises (Figure 3C), C14 was the most abundant homologue group in dolphins but accounted for a greater proportion (range 50−65%, overall average 56%) within MCCPs (Figure 4C). There were no significant changes in the MCCP homologue pattern observed in dolphins. A previous study13 indicated that the ratio of MCCPs/ SCCPs can serve as an effective indicator for pollution intensity and direct emission/transport of CPs in the regional environment. In the Pearl River Delta, higher MCCP/SCCP ratio was often found along with higher CP level in highly industrialized activity areas,13 while the opposite was always observed in remote surrounding areas.37 In this study, the ratio of MCCPs/ SCCPs was also used to assess whether there have been apparent changes of accumulation profiles of CPs in marine mammals between 2004 and 2014. The values of MCCP/ SCCP ratios ranged from 1.3 to 2.1 with an average value of 1.7 in porpoises and from 1.4 to 2.7 with an average value of 2.1 in dolphins, which were generally higher than those in sediments from the Pearl River Estuary.13 When it is considered that the porpoise and dolphin are top predators in the marine food webs, there is a possible change in ratios of MCCPs/SCCPs during bioaccumulation and/or biomagnification across trophic levels. C14 groups were the predominant homologue within MCCPs, which have a relatively higher octanol−water partition coefficient (Kow) than SCCP homologue (C10−13) groups.39 A recent study40 indicated that significant positive correlations were observed for MCCP concentrations versus trophic levels but not for SCCP concentrations versus trophic levels in predatory fish from the Great Lakes. An early study6 also

and 2014 are shown in Figure 3. In all porpoise blubber samples, C10 and C11 dominated the homologue profiles of

Figure 3. (A) Temporal changes in CP compositions (expressed as ratio of MCCPs to SCCPs) and (B) SCCP and (C) MCCP homologue patterns in blubber samples of finless porpoise (n = 50) over the past decade (2004−2014).

SCCPs during the whole study period, followed by C12 and C13. This is generally consistent with SCCP patterns in organisms of a marine food web from Liaodong Bay, north China.8 A stepwise temporal shift trend from shorter to longer carbon chain homologues in finless porpoise samples can be observed in SCCP homologue patterns (Figure 3B). The relative abundance of C10 decreased with an annual change rate of 4%, while those of C12 and C13 increased with annual change rates of 6% and 9%, respectively. Figure S6 shows the E

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have similar bioaccumulation and/or biomagnification abilities, the significant increasing ratios of MCCPs/SCCPs in both porpoise and dolphin samples over time could indicate an increasing trend in shifting the use of SCCPs to MCCPs during the past decade, which is in agreement with the conclusion of a shift to more use of MCCPs instead of SCCPs in recent years in the PRD13,37 and also corresponds to the temporal shift trend observed in a dated sediment core from Lake Thun (Switzerland) with a shift to more MCCPs after 2000.2 This accumulation profile could be attributed to the impacts of the regulations on SCCPs under the EU Water Framework Directive41 and the ongoing discussion on the inclusion of SCCPs in the list of POPs under the Stockholm Convention,11 resulting in more MCCPs being substituted for SCCPs as an alternative in CP technical mixtures. Additionally, significantly higher MCCP/SCCP ratios were found in dolphins than porpoises in every individual sampling year. Notwithstanding potential species−species differences, higher MCCP/SCCP ratios in dolphins than in porpoises could be mainly attributed to the different input pathway of CPs from their separate living habitats (Figure S1). This observation provides insights into the potential sources and environmental transport by the further spatiotemporal comparison below. Differences between Two Species of Marine Mammals and the Environmental Implication. Finless porpoise and Indo-Pacific humpback dolphin are two resident cetacean species around Hong Kong in the South China Sea. Both of them are apex predators that occupy many marine ecosystems and feed on a variety of aquatic prey, making them serve as representative sentinels for assessing the quality of marine environments and characterizing the contribution of anthropogenic origin contaminants. Finless porpoises generally dwell in the southern and eastern waters of Hong Kong, whereas Indo-Pacific humpback dolphins inhabit the northwest waters of Hong Kong located downstream of the PRD (Figure S1). As a highly industrialized and urbanized region of China over the last three decades, the PRD is facing accelerated environmental pollution. Dense industrial activities and e-waste dismantling/ recycling practices during the past decade have seriously deteriorated the adjacent waters of the South China Sea by industrial discharge from the PRD via the Pearl River Estuary (PRE). Meanwhile, the outflow of semivolatile organic chemicals from the PRD can also be transported to the South China Sea by Asian monsoons.42,43 As there are almost no overlapping areas of spatial distribution between porpoise and dolphin, comparisons of CP concentrations and congener profiles between the two species of marine mammals provide an indication to evaluate possible sources and transport pathways of CPs in the South China Sea. As per the results presented above, comparisons between the two species of marine mammals showed that higher ratios of MCCPs/SCCPs, along with higher SCCP accumulation levels, are present in dolphins than in porpoises. Differences in MCCP/SCCP ratios and concentrations between the two cetacean species could be attributed to species−species differences in feeding habits and biotransformation and accumulation preferences, as well as exposure levels in their living habitats. Dolphins from the northwestern waters of Hong Kong adjacent to the mouth of the PRE are thought to be affected more by direct anthropogenic sources coming from the PRD (Figure S1), while finless porpoises from the southern and eastern waters may be affected more by oceanic/offshore water from the PRE and/or atmospheric transport from the PRD.

Figure 4. (A) Temporal changes in CP compositions (expressed as ratio of MCCPs to SCCPs) and (B) SCCP and (C) MCCP homologue patterns in blubber samples of Indo-Pacific humpback dolphins (n = 25) over the past decade (2004−2014).

reported that bioaccumulation factors for MCCPs were generally higher than those for SCCPs in the Lake Ontario food webs. The results in this study suggest that MCCP/SCCP ratios could increase through multiple trophic levels in marine food webs, resulting in relatively high MCCP/SCCP ratios in marine mammals. However, the usage change of MCCP/SCCP commercial CP mixtures in recent years in China could be another important factor. As shown in Figures 3A and 4A, a significant temporal shifting trend from SCCPs to MCCPs in both porpoises and dolphins can be observed from 2004 to 2014. Given that the investigated marine mammals from different collection years F

DOI: 10.1021/acs.est.5b02473 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology Notes

Finless porpoises living further away from the PRE may show a reduction in CP concentrations in the years to come, due to the delay from long-range transport. Furthermore, SCCPs have higher vapor pressures and solubility relative to MCCPs, which make SCCPs more available for long-range transport than MCCPs. Hence, relatively lower MCCP/SCCP ratios along with relatively lower accumulation levels are expected in porpoises than in dolphins. Differences in SCCP and MCCP homologue patterns between dolphins and porpoises can be observed (Figures 3 and 4). Dolphins have greater proportions of C12−13 within SCCPs and more C14 within MCCPs compared to porpoises. This implies that a fractionation of congeners with different physicochemical properties during the complex environmental processes, including local inputs, atmospheric transport, oceanic transport, prey preference, and trophic transfer or a combination of all of these, may be attributed to differences in the CP homologue patterns. As vapor pressures decrease with increased carbon chain length and degree of chlorination,44 in general, shorter-chain and less chlorinated congeners have greater transport potential than longer-chain and more highly chlorinated congeners. Therefore, relative to commercial CP formulations,13 samples from porpoises showed a predominance of shorter-chain congeners, the more volatile components of industrial formulations. This observation is consistent with long-range atmospheric/oceanic transport of CPs to this region.37,45 The pattern of dolphins had higher proportions of the less volatile CP congeners, implying that contamination of this region is higher, probably from primary discharge from the PRD. In summary, our results filled in the current data gap in annual temporal trends of CPs in marine biota samples. The study presented here will help in understanding the current pollution state and predicting future pollution trends in marine mammals in the Asia-Pacific region. Further research is needed to track dietary sources of CPs for marine mammals. When it is considered that there are no control measures and regulatory policies on CP production and usage in most Asian countries/ regions at present, the increasing temporal trends of SCCP and MCCP accumulation levels indicate that more attention should be paid to potential environmental and health risks.

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The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the National Natural Science Foundation (21577142, 41522304, 41206080, and 41276111), Hong Kong Research Grants Council (CityU 160613 and 11100614), and Beijing NOVA Program (Z131109000413049). We thank the Agriculture, Fisheries and Conservation Department, Hong Kong SAR Government, and Ocean Park Conservation Foundation, Hong Kong (OPCFHK), for their assistance with blubber collection in Hong Kong, China.

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(1) Bayen, S.; Obbard, J. P.; Thomas, G. O. Chlorinated paraffins: A review of analysis and environmental occurrence. Environ. Int. 2006, 32 (7), 915−929. (2) Iozza, S.; Muller, C. E.; Schmid, P.; Bogdal, C.; Oehme, M. Historical profiles of chlorinated paraffins and polychlorinated biphenyls in a dated sediment core from Lake Thun (Switzerland). Environ. Sci. Technol. 2008, 42 (4), 1045−1050. (3) Fisk, A. T.; Tomy, G. T.; Muir, D. C. G. Toxicity of C-10-, C-11-, C-12-, and C-14-polychlorinated alkanes to Japanese medaka (Oryzias latipes) embryos. Environ. Toxicol. Chem. 1999, 18 (12), 2894−2902. (4) Warnasuriya, G. D.; Elcombe, B. M.; Foster, J. R.; Elcombe, C. R. A Mechanism for the induction of renal tumours in male Fischer 344 rats by short-chain chlorinated paraffins. Arch. Toxicol. 2010, 84 (3), 233−243. (5) Cooley, H. M.; Fisk, A. T.; Wiens, S. C.; Tomy, G. T.; Evans, R. E.; Muir, D. C. G. Examination of the behavior and liver and thyroid histology of juvenile rainbow trout (Oncorhynchus mykiss) exposed to high dietary concentrations of C10-, C11-, C12- and C14-polychlorinated n-alkanes. Aquat. Toxicol. 2001, 54 (1−2), 81−99. (6) Houde, M.; Muir, D. C. G.; Tomy, G. T.; Whittle, D. M.; Teixeira, C.; Moore, S. Bioaccumulation and trophic magnification of short- and medium-chain chlorinated paraffins in food webs from Lake Ontario and Lake Michigan. Environ. Sci. Technol. 2008, 42 (10), 3893−3899. (7) Zeng, L. X.; Wang, T.; Wang, P.; Liu, Q.; Han, S. L.; Yuan, B.; Zhu, N. L.; Wang, Y. W.; Jiang, G. B. Distribution and Trophic Transfer of Short-Chain Chlorinated Paraffins in an Aquatic Ecosystem Receiving Effluents from a Sewage Treatment Plant. Environ. Sci. Technol. 2011, 45 (13), 5529−5535. (8) Ma, X.; Zhang, H.; Wang, Z.; Yao, Z.; Chen, J.; Chen, J. Bioaccumulation and Trophic Transfer of Short Chain Chlorinated Paraffins in a Marine Food Web from Liaodong Bay, North China. Environ. Sci. Technol. 2014, 48 (10), 5964−5971. (9) Tomy, G. T.; Muir, D. C. G.; Stern, G. A.; Westmore, J. B. Levels of C10-C13 polychloro-n-alkanes in marine mammals from the Arctic and the St. Lawrence River estuary. Environ. Sci. Technol. 2000, 34 (9), 1615−1619. (10) Tomy, G. T.; Stern, G. A.; Lockhart, W. L.; Muir, D. C. G. Occurrence of C10-C13 polychlorinated n-alkanes in Canadian midlatitude and arctic lake sediments. Environ. Sci. Technol. 1999, 33 (17), 2858−2863. (11) Persistent Organic Pollutants Review Committee. Supporting document for the draft risk profile on short-chained chlorinated paraffins. UNEP/POPS/POPRC.6/INF/15; Sixth meeting of the Persistent Organic Pollutants Review Committee, Geneva, Switzerland, 2010. (12) Chlorinated Paraffins; De Boer, J., Ed.; The Handbook of Environmental Chemistry, Vol. 10; Springer-Verlag: Berlin and Heidelberg, Germany, 2010. (13) Chen, M.-Y.; Luo, X.-J.; Zhang, X.-L.; He, M.-J.; Chen, S.-J.; Mai, B.-X. Chlorinated Paraffins in Sediments from the Pearl River Delta, South China: Spatial and Temporal Distributions and

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.5b02473. Additional information on sample extraction and cleanup, sample information for analysis, spatial distributions of finless porpoise and dolphin, correlation analysis between SCCP and MCCP concentrations, temporal trends of yearly median concentrations, annual production and growth rate of CPs, CP industrial application profile in China, and average congener group patterns of SCCPs and MCCPs in blubber samples from different years (PDF)

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REFERENCES

AUTHOR INFORMATION

Corresponding Authors

*(J.C.W.L.) E-mail [email protected] or mail.jameslam@ gmail.com. *(P.K.S.L.) E-mail [email protected]. G

DOI: 10.1021/acs.est.5b02473 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology Implication for Processes. Environ. Sci. Technol. 2011, 45 (23), 9936− 9943. (14) Wang, Y.; Li, J.; Cheng, Z. N.; Li, Q. L.; Pan, X. H.; Zhang, R. J.; Liu, D.; Luo, C. L.; Liu, X.; Katsoyiannis, A.; Zhang, G. Short- and Medium-Chain Chlorinated Paraffins in Air and Soil of Subtropical Terrestrial Environment in the Pearl River Delta, South China: Distribution, Composition, Atmospheric Deposition Fluxes, and Environmental Fate. Environ. Sci. Technol. 2013, 47 (6), 2679−2687. (15) Li, Q.; Li, J.; Wang, Y.; Xu, Y.; Pan, X.; Zhang, G.; Luo, C.; Kobara, Y.; Nam, J.-J.; Jones, K. C. Atmospheric Short-Chain Chlorinated Paraffins in China, Japan, and South Korea. Environ. Sci. Technol. 2012, 46 (21), 11948−11954. (16) Wang, T.; Han, S. L.; Yuan, B.; Zeng, L. X.; Li, Y. M.; Wang, Y. W.; Jiang, G. B. Summer-Winter Concentrations and Gas-Particle Partitioning of Short Chain Chlorinated Paraffins in the Atmosphere of an Urban Setting. Environ. Pollut. 2012, 171, 38−45. (17) Zeng, L. X.; Li, H. J.; Wang, T.; Gao, Y.; Xiao, K.; Du, Y. G.; Wang, Y. W.; Jiang, G. B. Behavior, Fate, and Mass Loading of Short Chain Chlorinated Paraffins in an Advanced Municipal Sewage Treatment Plant. Environ. Sci. Technol. 2013, 47 (2), 732−740. (18) Harada, K. H.; Takasuga, T.; Hitomi, T.; Wang, P. Y.; Matsukami, H.; Koizumi, A. Dietary Exposure to Short-Chain Chlorinated Paraffins Has Increased in Beijing, China. Environ. Sci. Technol. 2011, 45 (16), 7019−7027. (19) Zeng, L. X.; Wang, T.; Han, W. Y.; Yuan, B.; Liu, Q. A.; Wang, Y. W.; Jiang, G. B. Spatial and Vertical Distribution of Short Chain Chlorinated Paraffins in Soils from Wastewater Irrigated Farmlands. Environ. Sci. Technol. 2011, 45 (6), 2100−2106. (20) Gao, Y.; Zhang, H. J.; Su, F.; Tian, Y. Z.; Chen, J. P. Environmental Occurrence and Distribution of Short Chain Chlorinated Paraffins in Sediments and Soils from the Liaohe River Basin, P. R. China. Environ. Sci. Technol. 2012, 46 (7), 3771−3778. (21) Zeng, L. X.; Wang, T.; Ruan, T.; Liu, Q.; Wang, Y. W.; Jiang, G. B. Levels and distribution patterns of short chain chlorinated paraffins in sewage sludge of wastewater treatment plants in China. Environ. Pollut. 2012, 160, 88−94. (22) Zeng, L.; Zhao, Z.; Li, H.; Wang, T.; Liu, Q.; Xiao, K.; Du, Y.; Wang, Y.; Jiang, G. Distribution of Short Chain Chlorinated Paraffins in Marine Sediments of the East China Sea: Influencing Factors, Transport and Implications. Environ. Sci. Technol. 2012, 46 (18), 9898−9906. (23) Zeng, L. X.; Chen, R.; Zhao, Z. S.; Wang, T.; Gao, Y.; Li, A.; Wang, Y. W.; Jiang, G. B.; Sun, L. G. Spatial Distributions and Deposition Chronology of Short Chain Chlorinated Paraffins in Marine Sediments across the Chinese Bohai and Yellow Seas. Environ. Sci. Technol. 2013, 47, 11449−11456. (24) Yuan, B.; Wang, T.; Zhu, N. L.; Zhang, K. G.; Zeng, L. X.; Fu, J. J.; Wang, Y. W.; Jiang, G. B. Short Chain Chlorinated Paraffins in Mollusks from Coastal Waters in the Chinese Bohai Sea. Environ. Sci. Technol. 2012, 46 (12), 6489−6496. (25) Hites, R. A. Polybrominated diphenyl ethers in the environment and in people: A meta-analysis of concentrations. Environ. Sci. Technol. 2004, 38 (4), 945−956. (26) Chen, D.; La Guardia, M. J.; Luellen, D. R.; Harvey, E.; Mainor, T. M.; Hale, R. C. Do Temporal and Geographical Patterns of HBCD and PBDE Flame Retardants in US Fish Reflect Evolving Industrial Usage? Environ. Sci. Technol. 2011, 45 (19), 8254−8261. (27) Jianxian, S.; Hui, P.; Jianying, H. Temporal Trends of Polychlorinated Biphenyls, Polybrominated Diphenyl Ethers, and Perfluorinated Compounds in Chinese Sturgeon (Acipenser sinensis) Eggs (1984−2008). Environ. Sci. Technol. 2015, 49 (3), 1621−1630. (28) Holmstrom, K. E.; Johansson, A. K.; Bignert, A.; Lindberg, P.; Berger, U. Temporal Trends of Perfluorinated Surfactants in Swedish Peregrine Falcon Eggs (Falco peregrinus), 1974−2007. Environ. Sci. Technol. 2010, 44 (11), 4083−4088. (29) Fair, P. A.; Adams, J.; Mitchum, G.; Hulsey, T. C.; Reif, J. S.; Houde, M.; Muir, D.; Wirth, E.; Wetzel, D.; Zolman, E.; McFee, W.; Bossart, G. D. Contaminant blubber burdens in Atlantic bottlenose dolphins (Tursiops truncatus) from two southeastern US estuarine

areas: Concentrations and patterns of PCBs, pesticides, PBDEs, PFCs, and PAHs. Sci. Total Environ. 2010, 408 (7), 1577−1597. (30) Bossart, G. D. Marine Mammals as Sentinel Species for Oceans and Human Health. Vet. Pathol. 2011, 48 (3), 676−690. (31) Ross, P. S. Marine mammals as sentinels in ecological risk assessment. Hum. Ecol. Risk Assess. 2000, 6 (1), 29−46. (32) Lam, J. C. W.; Lau, R. K. F.; Murphy, M. B.; Lam, P. K. S. Temporal Trends of Hexabromocyclododecanes (HBCDs) and Polybrominated Diphenyl Ethers (PBDEs) and Detection of Two Novel Flame Retardants in Marine Mammals from Hong Kong, South China. Environ. Sci. Technol. 2009, 43 (18), 6944−6949. (33) Zhu, B.; Lai, N. L. S.; Wai, T.-C.; Chan, L. L.; Lam, J. C. W.; Lam, P. K. S. Changes of accumulation profiles from PBDEs to brominated and chlorinated alternatives in marine mammals from the South China Sea. Environ. Int. 2014, 66, 65−70. (34) Reth, M.; Zencak, Z.; Oehme, M. New quantification procedure for the analysis of chlorinated paraffins using electron capture negative ionization mass spectrometry. J. Chromatogr. A 2005, 1081 (2), 225− 231. (35) Park, J.-S.; Holden, A.; Chu, V.; Kim, M.; Rhee, A.; Patel, P.; Shi, Y.; Linthicum, J.; Walton, B. J.; McKeown, K.; Jewell, N. P.; Hooper, K. Time-Trends and Congener Profiles of PBDEs and PCBs in California Peregrine Falcons (Falco peregrinus). Environ. Sci. Technol. 2009, 43 (23), 8744−8751. (36) Okada, E.; Kashino, I.; Matsuura, H.; Sasaki, S.; Miyashita, C.; Yamamoto, J.; Ikeno, T.; Ito, Y. M.; Matsumura, T.; Tamakoshi, A.; Kishi, R. Temporal trends of perfluoroalkyl acids in plasma samples of pregnant women in Hokkaido, Japan, 2003−2011. Environ. Int. 2013, 60, 89−96. (37) Wang, Y.; Li, J.; Cheng, Z. N.; Li, Q. L.; Pan, X. H.; Zhang, R. J.; Liu, D.; Luo, C. L.; Liu, X.; Katsoyiannis, A.; Zhang, G. Short- and Medium-Chain Chlorinated Paraffins in Air and Soil of Subtropical Terrestrial Environment in the Pearl River Delta, South China: Distribution, Composition, Atmospheric Deposition Fluxes, and Environmental Fate. Environ. Sci. Technol. 2013, 47 (6), 2679−2687. (38) Wang, Y.; Cai, Y.; Jiang, G. Research processes of persistent organic pollutants (POPs) newly listed and candidate POPs in Stockholm Convention. Sci. Sin. Chem. 2010, 40, 99−123. (39) Hilger, B.; Fromme, H.; Volkel, W.; Coelhan, M. Effects of Chain Length, Chlorination Degree, and Structure on the OctanolWater Partition Coefficients of Polychlorinated n-Alkanes. Environ. Sci. Technol. 2011, 45 (7), 2842−2849. (40) Basconcillo, L. S.; Backus, S. M.; McGoldrick, D. J.; Zaruk, D.; Sverko, E.; Muir, D. C. G. Current status of short- and medium chain polychlorinated n-alkanes in top predatory fish across Canada. Chemosphere 2015, 127, 93−100. (41) European Community. Decision No 2455/2001/EC of the European Parliament and of the Council of 20 November 2001 Establishing the list of priority substances in the field of water policy and amending Directive 2000/60/EC. Off. J. Eur. Commun. 2001, L331, 1−5. (42) Li, J.; Zhang, G.; Guo, L.; Xu, W.; Li, X.; Lee, C. S. L.; Ding, A.; Wang, T. Organochlorine pesticides in the atmosphere of Guangzhou and Hong Kong: Regional sources and long-range atmospheric transport. Atmos. Environ. 2007, 41 (18), 3889−3903. (43) Lang, C.; Tao, S.; Zhang, G.; Fu, J.; Simonich, S. Outflow of polycyclic aromatic hydrocarbons from Guangdong, Southern China. Environ. Sci. Technol. 2007, 41 (24), 8370−8375. (44) Drouillard, K. G.; Tomy, G. T.; Muir, D. C. G.; Friesen, K. J. Volatility of chlorinated n-alkanes (C10-C12): Vapor pressures and Henry’s law constants. Environ. Toxicol. Chem. 1998, 17 (7), 1252− 1260. (45) Li, Q. L.; Li, J.; Wang, Y.; Xu, Y.; Pan, X. H.; Zhang, G.; Luo, C. L.; Kobara, Y.; Nam, J. J.; Jones, K. C. Atmospheric Short-Chain Chlorinated Paraffins in China, Japan, and South Korea. Environ. Sci. Technol. 2012, 46 (21), 11948−11954.

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DOI: 10.1021/acs.est.5b02473 Environ. Sci. Technol. XXXX, XXX, XXX−XXX